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Leucine-rich diet and light aerobic training modulate GLUT4 expression and increase the glycogen content in the gastrocnemius muscle of Walker-256 tumour-bearing rats



Emilianne M. Salom�o, Aline T. Toneto, Gisele O. Silva and Maria Cristina C.
Gomes-Marcondes*


Laboratory of Nutrition and Cancer, Department of Structural and Functional Biology, Institute of Biology, University of Campinas -
UNICAMP, Campinas, 13083862, Sao Paulo, Brazil



*Corresponding author: Maria Cristina C. Gomes-Marcondes
Telephone number: 55-19-3521-6194
Fax number: 55-19-3521-6185
E-mail address: cintgoma@unicamp.br




ABSTRACT
 The intense mobilisation of substrates during cancer induces the loss of body mass, which mainly results from the depletion of muscle protein due to increased proteolysis and/or decreased protein synthesis, leading to cachexia. Leucine is also used as an energy source and as a cell-signalling molecule by skeletal muscle. Additionally, physical activity increases glucose consumption, which reduces the levels of circulating glucose and insulin. This work investigated the effects of leucine supplementation and light aerobic-exercise (swimming) on muscle carbohydrate metabolism in Walker tumour-bearing rats.  Trained adult rats were fed a leucine-rich diet and implanted with Walker-256 tumour cells. We assessed the levels of serum glucose, cytokine and hormone and muscle glycolytic gene expression, glycogen content and fibre size. The data presented here clearly show that tumour growth produced deleterious effects on tumour-bearing rats, increasing the levels of serum cytokines (pro-inflammatory TNF-(, INF-( and IL-6, anti-inflammatory IL-4 and IL-10 and the IL-10/TNF-( ratio) and reducing serum glucose and insulin levels. Tumour growth induced a decrease in muscle GLUT4 expression and increased muscle pyruvate dehydrogenase (PDH), lactate dehydrogenase (LDH), and monocarboxylic acid transporter 1 (MCT1) expression; it also reduced muscle glycogen content and muscle fibre size. Leucine supplementation alone or combined with exercise benefited the host tissues, improving the muscle glucose metabolism, as illustrated by the reduction of serum pro-inflammatory cytokine levels and the maintenance of GLUT4, hexokinase, PDH, LDH and MCT1 expression. These changes all increased the muscle glycogen content, which consequently benefited the tumour-bearing host.


Keywords: leucine; exercise; Walker-256 tumour; glucose metabolism; cachexia.
INTRODUCTION
Cachexia syndrome is a comorbid state that occurs with many types of cancers and is the most important factor leading to the premature death of cancer patients. This syndrome is characterised by a complex network of several factors, including significant weight loss and decreased quality of life and life expectancy  ADDIN EN.CITE <EndNote><Cite><Author>Tisdale</Author><Year>1997</Year><RecNum>829</RecNum><DisplayText>[1]</DisplayText><record><rec-number>829</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">829</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tisdale, M. J.</author></authors></contributors><auth-address>Pharmaceutical Sciences Institute, Aston University, Birmingham, United Kingdom.</auth-address><titles><title>Cancer cachexia: metabolic alterations and clinical manifestations</title><secondary-title>Nutrition</secondary-title></titles><periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></periodical><pages>1-7</pages><volume>13</volume><number>1</number><edition>1997/01/01</edition><keywords><keyword>Animals</keyword><keyword>Anorexia/complications</keyword><keyword>Cachexia/etiology/*metabolism</keyword><keyword>Carbohydrate Metabolism</keyword><keyword>Cytokines/*physiology</keyword><keyword>Energy Metabolism</keyword><keyword>Humans</keyword><keyword>Lipid Metabolism</keyword><keyword>Muscle, Skeletal/metabolism</keyword><keyword>Neoplasms/*complications</keyword></keywords><dates><year>1997</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0899-9007 (Print)&#xD;0899-9007 (Linking)</isbn><accession-num>9058439</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9058439</url></related-urls></urls><electronic-resource-num>S0899900796003139 [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_1" \o "Tisdale, 1997 #829" 1].
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Experimental tumour-bearing animals often suffer from hypoglycaemia, which is associated with low glucose metabolism in tissues. However, the anaerobic glycolysis that occurs in neoplastic cells, which is mainly, but not exclusively, due to high glucose metabolism, leads to increased energy expenditure in host tissues  ADDIN EN.CITE <EndNote><Cite><Author>Sauer</Author><Year>1994</Year><RecNum>831</RecNum><DisplayText>[3]</DisplayText><record><rec-number>831</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">831</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Sauer, L. A.</author><author>Dauchy, R. T.</author></authors></contributors><auth-address>Sauer, La&#xD;Mary Imogene Bassett Hosp,Med Res Inst,Cooperstown,Ny 13326, USA&#xD;Mary Imogene Bassett Hosp,Med Res Inst,Cooperstown,Ny 13326, USA</auth-address><titles><title>Lactate Release and Uptake in Hepatoma 7288ctc Perfused in-Situ with L-[(U)-C-14]Lactate or D-[(U)-C-14]Glucose</title><secondary-title>Metabolism-Clinical and Experimental</secondary-title><alt-title>Metabolism</alt-title></titles><pages>1488-1497</pages><volume>43</volume><number>12</number><keywords><keyword>metastatic breast-cancer</keyword><keyword>lactic-acidosis</keyword><keyword>rat-tumors</keyword><keyword>local hyperthermia</keyword><keyword>ketone-body</keyword><keyword>amino-acid</keyword><keyword>blood-flow</keyword><keyword>invivo</keyword><keyword>glucose</keyword><keyword>metabolism</keyword></keywords><dates><year>1994</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0026-0495</isbn><accession-num>ISI:A1994PW06200006</accession-num><urls><related-urls><url>&lt;Go to ISI&gt;://A1994PW06200006</url></related-urls></urls><electronic-resource-num>Doi 10.1016/0026-0495(94)90006-X</electronic-resource-num><language>English</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_3" \o "Sauer, 1994 #831" 3]. Lactate, alanine and glycerol are converted to glucose by hepatic gluconeogenesis and the Cori cycle, which increases the host energy deficit and results in a cachectic state  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Tisdale, 1997 #829" 1,  HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4-6]. Studies have also observed an association between hypoglycaemia and lactic acidosis in patients with lymphoma  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_2" \o "Inui, 1999 #620" 2,  HYPERLINK \l "_ENREF_7" \o "Glasheen, 2005 #841" 7]; however, this association is more frequent in animal models  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_8" \o "Gomes-Marcondes, 2003 #732" 8-11]. Reduced protein synthesis and increased protein degradation, which result in an increase in total body protein turnover, are commonly observed in cancer patients  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_2" \o "Inui, 1999 #620" 2,  HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4]. The loss of body mass, especially skeletal muscle, leads to fatigue, weakness and muscle atrophy  ADDIN EN.CITE <EndNote><Cite><Author>Mulligan</Author><Year>1998</Year><RecNum>832</RecNum><DisplayText>[12]</DisplayText><record><rec-number>832</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">832</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Mulligan, K.</author><author>Bloch, A. S.</author></authors></contributors><auth-address>Mulligan, K&#xD;San Francisco Gen Hosp, Div Endocrinol, Bldg 100,Room 321,1001 Potrero Ave, San Francisco, CA 94110 USA&#xD;San Francisco Gen Hosp, Div Endocrinol, Bldg 100,Room 321,1001 Potrero Ave, San Francisco, CA 94110 USA&#xD;San Francisco Gen Hosp, Div Endocrinol, San Francisco, CA 94110 USA&#xD;Univ Calif San Francisco, Dept Med, San Francisco, CA 94143 USA&#xD;Mem Sloan Kettering Canc Ctr, Dept Med, GI Nutr Serv, New York, NY 10021 USA</auth-address><titles><title>Energy expenditure and protein metabolism in human immunodeficiency virus infection and cancer cachexia</title><secondary-title>Seminars in Oncology</secondary-title><alt-title>Semin Oncol</alt-title></titles><pages>82-91</pages><volume>25</volume><number>2</number><keywords><keyword>total parenteral-nutrition</keyword><keyword>body-composition</keyword><keyword>weight-loss</keyword><keyword>hiv-infection</keyword><keyword>carbohydrate-metabolism</keyword><keyword>impedance analysis</keyword><keyword>host metabolism</keyword><keyword>aids patients</keyword><keyword>survival</keyword><keyword>turnover</keyword></keywords><dates><year>1998</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>0093-7754</isbn><accession-num>ISI:000074056800014</accession-num><urls><related-urls><url>&lt;Go to ISI&gt;://000074056800014</url></related-urls></urls><language>English</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_12" \o "Mulligan, 1998 #832" 12]. Fatigue is one of the most severe symptoms in cancer patients and compromises strength and endurance, which leads to a subsequent decrease in the quality of life  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_13" \o "al-Majid, 2001 #834" 13-16]. Aerobic exercise can improve physical performance and may increase the quality of life of cancer patients  ADDIN EN.CITE <EndNote><Cite><Author>Crevenna</Author><Year>2003</Year><RecNum>838</RecNum><DisplayText>[17]</DisplayText><record><rec-number>838</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">838</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Crevenna, R.</author><author>Schmidinger, M.</author><author>Keilani, M.</author><author>Nuhr, M.</author><author>Fialka-Moser, V.</author><author>Zettinig, G.</author><author>Quittan, M.</author></authors></contributors><auth-address>Department of Physical Medicine and Rehabilitation, Vienna University, General Hospital of Vienna, Waehringer Guertel 18-20, 1090 Vienna, Austria. richard.crevenna@univie.ac.at</auth-address><titles><title>Aerobic exercise for a patient suffering from metastatic bone disease</title><secondary-title>Support Care Cancer</secondary-title></titles><periodical><full-title>Support Care Cancer</full-title><abbr-1>Supportive care in cancer : official journal of the Multinational Association of Supportive Care in Cancer</abbr-1></periodical><pages>120-2</pages><volume>11</volume><number>2</number><edition>2003/02/01</edition><keywords><keyword>Bone Neoplasms/complications/*rehabilitation/*secondary</keyword><keyword>Breast Neoplasms/*pathology/*rehabilitation</keyword><keyword>*Exercise Therapy</keyword><keyword>Female</keyword><keyword>Humans</keyword><keyword>Middle Aged</keyword><keyword>Oxygen Consumption</keyword><keyword>Palliative Care</keyword><keyword>Physical Fitness</keyword><keyword>Quality of Life</keyword><keyword>Treatment Outcome</keyword></keywords><dates><year>2003</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0941-4355 (Print)&#xD;0941-4355 (Linking)</isbn><accession-num>12560941</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/12560941</url></related-urls></urls><electronic-resource-num>10.1007/s00520-002-0400-1</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_17" \o "Crevenna, 2003 #838" 17]. In animals, moderate exercise reduces the incidence of tumours and neoplastic symptoms as well as the incidence of metastases and tumour growth  ADDIN EN.CITE <EndNote><Cite><Author>Shewchuk</Author><Year>1997</Year><RecNum>839</RecNum><DisplayText>[18]</DisplayText><record><rec-number>839</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">839</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Shewchuk, L. D.</author><author>Baracos, V. E.</author><author>Field, C. J.</author></authors></contributors><auth-address>Department of Agricultural, Food and Nutritional Sciences, University of Alberta, Edmonton, Canada.</auth-address><titles><title>Dietary L-glutamine supplementation reduces the growth of the Morris Hepatoma 7777 in exercise-trained and sedentary rats</title><secondary-title>J Nutr</secondary-title></titles><periodical><full-title>J Nutr</full-title><abbr-1>The Journal of nutrition</abbr-1></periodical><pages>158-66</pages><volume>127</volume><number>1</number><edition>1997/01/01</edition><keywords><keyword>Amino Acids/blood</keyword><keyword>Animals</keyword><keyword>*Diet</keyword><keyword>Female</keyword><keyword>Glucose/metabolism</keyword><keyword>Glutamine/*administration &amp; dosage/*metabolism</keyword><keyword>Liver Neoplasms, Experimental/immunology/*metabolism/*therapy</keyword><keyword>*Physical Conditioning, Animal</keyword><keyword>Rats</keyword><keyword>Rats, Sprague-Dawley</keyword><keyword>Spleen/immunology/metabolism</keyword></keywords><dates><year>1997</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0022-3166 (Print)&#xD;0022-3166 (Linking)</isbn><accession-num>9040560</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9040560</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_18" \o "Shewchuk, 1997 #839" 18]. Physical activity promotes an increased consumption of glucose, reducing the levels of circulating glucose and insulin, which leads to a lower supply of these molecules for tumour cells  ADDIN EN.CITE <EndNote><Cite><Author>Anthony</Author><Year>1999</Year><RecNum>840</RecNum><DisplayText>[19]</DisplayText><record><rec-number>840</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">840</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Anthony, J. C.</author><author>Anthony, T. G.</author><author>Layman, D. K.</author></authors></contributors><auth-address>Division of Nutritional Sciences and the Department of Food Science and Human Nutrition, University of Illinois, Urbana, IL 61801, USA.</auth-address><titles><title>Leucine supplementation enhances skeletal muscle recovery in rats following exercise</title><secondary-title>J Nutr</secondary-title></titles><periodical><full-title>J Nutr</full-title><abbr-1>The Journal of nutrition</abbr-1></periodical><pages>1102-6</pages><volume>129</volume><number>6</number><edition>1999/06/04</edition><keywords><keyword>Animals</keyword><keyword>Blood Glucose/analysis</keyword><keyword>Diet</keyword><keyword>Dietary Carbohydrates/pharmacology</keyword><keyword>Glycogen/metabolism</keyword><keyword>Insulin/blood</keyword><keyword>Leucine/administration &amp; dosage/*pharmacology</keyword><keyword>Male</keyword><keyword>Muscle Proteins/biosynthesis</keyword><keyword>Muscle, Skeletal/*drug effects/metabolism/*physiology</keyword><keyword>Physical Conditioning, Animal/*physiology</keyword><keyword>Rats</keyword><keyword>Rats, Sprague-Dawley</keyword></keywords><dates><year>1999</year><pub-dates><date>Jun</date></pub-dates></dates><isbn>0022-3166 (Print)&#xD;0022-3166 (Linking)</isbn><accession-num>10356072</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/10356072</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_19" \o "Anthony, 1999 #840" 19]. Additionally, high concentrations of corticosteroid hormones and cytokines, which are induced by physical activity, increase the immune response, which is usually depressed during tumour development  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_20" \o "Bacurau, 2000 #211" 20]. Conversely, the positive effect produced by physical activity improves insulin sensitivity, altering the balance between anabolic and catabolic hormones  ADDIN EN.CITE <EndNote><Cite><Author>Daneryd</Author><Year>1995</Year><RecNum>842</RecNum><DisplayText>[21]</DisplayText><record><rec-number>842</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">842</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Daneryd, P.</author><author>Westin, T.</author><author>Edstrom, S.</author><author>Soussi, B.</author></authors></contributors><auth-address>Department of Surgery, Sahlgrenska University Hospital, Goteborg, Sweden.</auth-address><titles><title>Tumour purine nucleotides and cell proliferation in response to exercise in rats</title><secondary-title>Eur J Cancer</secondary-title></titles><pages>2309-12</pages><volume>31A</volume><number>13-14</number><edition>1995/12/01</edition><keywords><keyword>Adenosine Monophosphate/analysis</keyword><keyword>Animals</keyword><keyword>*Cell Division</keyword><keyword>Female</keyword><keyword>*Physical Conditioning, Animal</keyword><keyword>Purine Nucleotides/*analysis</keyword><keyword>Rats</keyword><keyword>Rats, Inbred WF</keyword><keyword>Sarcoma, Experimental/*chemistry/pathology/physiopathology</keyword></keywords><dates><year>1995</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>0959-8049 (Print)&#xD;0959-8049 (Linking)</isbn><accession-num>8652261</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/8652261</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_21" \o "Daneryd, 1995 #842" 21]. Therefore, when properly supervised, physical activity can be a co-adjuvant alternative to improve the treatment and rehabilitation of patients with cancer  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_22" \o "Segal, 2001 #843" 22,  HYPERLINK \l "_ENREF_23" \o "Segar, 1998 #845" 23].
The branched chain amino acids (BCAAs), especially leucine, are essential substrates and important regulators of protein synthesis. Additionally, they represent the largest source of nitrogen for the synthesis of glutamine and alanine in muscle  ADDIN EN.CITE <EndNote><Cite><Author>Holecek</Author><Year>2002</Year><RecNum>380</RecNum><DisplayText>[24]</DisplayText><record><rec-number>380</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">380</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Holecek, M.</author></authors></contributors><auth-address>Department of Physiology, Charles University School of Medicine, Hradec Kralove, Czech Republic. holecek@fhk.cuni.cz</auth-address><titles><title>Relation between glutamine, branched-chain amino acids, and protein metabolism</title><secondary-title>Nutrition</secondary-title></titles><periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></periodical><pages>130-3</pages><volume>18</volume><number>2</number><edition>2002/02/15</edition><keywords><keyword>Alanine/*biosynthesis/metabolism</keyword><keyword>Amino Acids, Branched-Chain/*metabolism</keyword><keyword>Animals</keyword><keyword>Critical Illness</keyword><keyword>Glutamine/*biosynthesis/metabolism</keyword><keyword>Humans</keyword><keyword>Liver/metabolism</keyword><keyword>Muscle, Skeletal/metabolism</keyword><keyword>Proteins/*metabolism</keyword><keyword>Rats</keyword></keywords><dates><year>2002</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0899-9007 (Print)&#xD;0899-9007 (Linking)</isbn><accession-num>11844643</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/11844643</url></related-urls></urls><electronic-resource-num>S0899900701007675 [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Holecek, 2002 #380" 24]. The increased oxidation rate of leucine in skeletal muscle, which commonly occurs during the inflammation induced by cancer, produces acetyl-CoA, contributing to muscle loss  ADDIN EN.CITE <EndNote><Cite><Author>Holecek</Author><Year>2002</Year><RecNum>380</RecNum><DisplayText>[24]</DisplayText><record><rec-number>380</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">380</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Holecek, M.</author></authors></contributors><auth-address>Department of Physiology, Charles University School of Medicine, Hradec Kralove, Czech Republic. holecek@fhk.cuni.cz</auth-address><titles><title>Relation between glutamine, branched-chain amino acids, and protein metabolism</title><secondary-title>Nutrition</secondary-title></titles><periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></periodical><pages>130-3</pages><volume>18</volume><number>2</number><edition>2002/02/15</edition><keywords><keyword>Alanine/*biosynthesis/metabolism</keyword><keyword>Amino Acids, Branched-Chain/*metabolism</keyword><keyword>Animals</keyword><keyword>Critical Illness</keyword><keyword>Glutamine/*biosynthesis/metabolism</keyword><keyword>Humans</keyword><keyword>Liver/metabolism</keyword><keyword>Muscle, Skeletal/metabolism</keyword><keyword>Proteins/*metabolism</keyword><keyword>Rats</keyword></keywords><dates><year>2002</year><pub-dates><date>Feb</date></pub-dates></dates><isbn>0899-9007 (Print)&#xD;0899-9007 (Linking)</isbn><accession-num>11844643</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/11844643</url></related-urls></urls><electronic-resource-num>S0899900701007675 [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_24" \o "Holecek, 2002 #380" 24]. Leucine also induces transcription and can inhibit protein degradation and/or stimulate protein synthesis in cachetic animals. Therefore, leucine prevents body deterioration by preserving protein mass, as observed in tumour-bearing rats  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_10" \o "Ventrucci, 2004 #36" 10,  HYPERLINK \l "_ENREF_25" \o "Pitkanen, 2003 #848" 25]. In previous studies, a leucine-supplemented diet improved the nitrogen balance, restored lean body mass through the preservation of muscle protein and increased the intestinal absorption in Walker tumour-bearing rats  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_11" \o "Ventrucci, 2001 #70" 11]. 
To determine whether nutritional supplementation with leucine can also support muscle energy expenditure and whether physical activity can divert the energy substrate and increase muscle glucose uptake, we investigated muscle carbohydrate metabolism by assessing the glycolytic pathway within muscle cells by analysing the key enzymes and glucose receptor expression and their relationships to the pro-inflammatory and anti-inflammatory host responses. 

METHODS
Animals and diets
Male Wistar rats (21 days old) were obtained from the animal facilities at the State University of Campinas, UNICAMP, Brazil, and were housed in collective cages for the entire experimental period. The rats received food and water ad libitum in a controlled light/dark (12-12 hours) and temperature (22 � 2(C) environment. The semi-purified diets were in accordance with AIN-93M formula from the American Institute of Nutrition  ADDIN EN.CITE <EndNote><Cite><Author>Reeves</Author><Year>1993</Year><RecNum>850</RecNum><DisplayText>[26]</DisplayText><record><rec-number>850</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">850</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Reeves, P. G.</author><author>Nielsen, F. H.</author><author>Fahey, G. C., Jr.</author></authors></contributors><auth-address>United States Department of Agriculture, Grand Forks Human Nutrition Research Center, ND 58202-9034.</auth-address><titles><title>AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet</title><secondary-title>J Nutr</secondary-title></titles><periodical><full-title>J Nutr</full-title><abbr-1>The Journal of nutrition</abbr-1></periodical><pages>1939-51</pages><volume>123</volume><number>11</number><edition>1993/11/01</edition><keywords><keyword>Animals</keyword><keyword>Antioxidants</keyword><keyword>Carbohydrates</keyword><keyword>Diet/*standards</keyword><keyword>Female</keyword><keyword>Mice</keyword><keyword>Minerals</keyword><keyword>*Nutritional Requirements</keyword><keyword>Rats</keyword><keyword>Rodentia</keyword><keyword>Vitamins</keyword></keywords><dates><year>1993</year><pub-dates><date>Nov</date></pub-dates></dates><isbn>0022-3166 (Print)&#xD;0022-3166 (Linking)</isbn><accession-num>8229312</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/8229312</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_26" \o "Reeves, 1993 #850" 26]. The normoprotein diet (C) comprised 18% protein in the form of casein, containing 1.1% leucine. The leucine-rich diet (L) contained 18% protein and 3% L-leucine, resulting in a total of 4.1% leucine.
An adjustment in the amino acid-rich diet was made to reduce the amount of carbohydrates. The diets were isocaloric and had similar quantities of cornstarch (39.7%), dextrin (13.2%) and sugar (10.0%). Additionally, the C and L diets contained the same amount of fat (7% soy oil), fibre (5% cellulose micro fibre), salt (3.5%) and vitamin mix (1.0%). The diets were also supplemented with cystine and choline. The amino acid L-leucine and cornstarch were provided by Ajinomoto Interamericana Ind. and Com. Ltd. and Corn Products Brazil Ingredients, respectively.
Experimental protocol
Young rats (21 days old) were fed the leucine-rich diet or the normoproteic diet and were or were not submitted to physical activity. The rats were distributed into the following groups: C � control; L � leucine-rich diet; TC � trained rats on control diet; TL � trained rats on leucine-rich diet. After 60 days of these interventions (exercise and/or diet), the rats were redistributed into 8 groups based on whether they received Walker-256 tumour cells (W). The first four groups received the control diet and were defined as the control (C), trained (TC), tumour-bearing (W) and trained tumour-bearing (TW) groups. The second four groups were fed the leucine-rich diet, and these groups were defined as rats fed the leucine-rich diet (L), trained rats fed the leucine-rich diet (TL), tumour-bearing rats fed the leucine-rich diet (LW) and trained tumour-bearing rats fed the leucine-rich diet (TWL). The body weights were recorded three times per week. Twenty-one days after tumour implantation, the animals were sacrificed. The sacrifices occurred 24 hours after the final exercise protocol, to avoid acute inflammatory stimulus, and also during a no fasting period. Serum samples were collected for the assessment of glucose, hormone and cytokine content, while gastrocnemius muscles were quickly collected and stored at -80(C for RT-PCR analyses of various genes related to glucose metabolism. A small sample from the lateral portion of the gastrocnemius muscle of rats that were selected at random was collected to histochemically determine the single-fibre cross-sectional area and the muscle glycogen content. 
Exercise protocol
Rats were submitted to non-strenuous swim training for 11 weeks (60 days + 21 days after tumour implantation) in a 1-m3 container with 30 � 2�C circulating water to produce continuous motion, which prevented the rats from floating. The training was performed 5 days a week in the morning. The training sessions were initially performed for 5 minutes and were progressively increased to 45 minutes per day of exercise without body weight overload, which was maintained until the end of the experiment. To avoid thermal stress after swimming, the animals were gently dried and kept in a warm room. Body temperature was monitored. Cardiac rhythm was recorded by electrocardiogram analysis, and low cardiac frequency was observed, especially in the leucine-treated rats (data not shown), confirming the exercise adaptation.
Tumour implantation
Tumour-bearing rats received approximately 2.5 � 105 Walker-256 carcinoma cells subcutaneously implanted into the right flank  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_27" \o "Gomes-Marcondes, 1998 #72" 27]. The rats without tumours were injected with 0.5 mL of 0.9% (w/v) NaCl solution without anaesthesia. The general animal welfare guidelines of the UKCCCR (United Kingdom Coordinating Committee on Cancer Research, 1998) were followed, and the experimental protocols were approved by the Institutional Committee for Ethics in Animal Research (CEEA.IB/UNICAMP, protocol # 465-4)  ADDIN EN.CITE <EndNote><Cite><Author>Vale</Author><Year>2005</Year><RecNum>875</RecNum><DisplayText>[28]</DisplayText><record><rec-number>875</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">875</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Vale, C.</author><author>Stewart, L.</author><author>Tierney, J.</author></authors></contributors><auth-address>Meta-analysis Group, MRC Clinical Trials Unit, 222 Euston Road, London NW1 2DA, UK. claire.vale@ctu.mrc.ac.uk</auth-address><titles><title>Trends in UK cancer trials: results from the UK Coordinating Committee for Cancer Research National Register of Cancer Trials</title><secondary-title>Br J Cancer</secondary-title></titles><periodical><full-title>Br J Cancer</full-title><abbr-1>British journal of cancer</abbr-1></periodical><pages>811-4</pages><volume>92</volume><number>5</number><edition>2005/03/10</edition><keywords><keyword>Great Britain</keyword><keyword>Humans</keyword><keyword>Multicenter Studies as Topic/trends</keyword><keyword>Neoplasms/*epidemiology/*therapy</keyword><keyword>Patient Selection</keyword><keyword>Randomized Controlled Trials as Topic/*trends</keyword><keyword>Registries</keyword><keyword>Research/*trends</keyword></keywords><dates><year>2005</year><pub-dates><date>Mar 14</date></pub-dates></dates><isbn>0007-0920 (Print)&#xD;0007-0920 (Linking)</isbn><accession-num>15756251</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/15756251</url></related-urls></urls><custom2>2361907</custom2><electronic-resource-num>6602425 [pii]&#xD;10.1038/sj.bjc.6602425</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_28" \o "Vale, 2005 #875" 28].
Glucose metabolism in the gastrocnemius muscle
Reverse transcription-polymerase chain reaction (RT-PCR)
RT-PCR was performed to determine the gene expression of glycolytic enzymes and transporters in the muscle samples from different animals.
mRNA was extracted using TRIzol reagent (Sigma, USA) according to the manufacturer's instructions. The RNA quality was determined by spectrophotometry at 260 nm, and the purity was determined by gel electrophoresis (1% agarose, Tris borate, pH 8.3) and stained with ethidium bromide  ADDIN EN.CITE <EndNote><Cite><Author>Meadus</Author><Year>2003</Year><RecNum>623</RecNum><DisplayText>[29]</DisplayText><record><rec-number>623</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">623</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Meadus, W. J.</author></authors></contributors><auth-address>Meat Research Section, Agriculture and Agri-Food Canada, Lacombe Research Center. 6000 C&amp;E Trail, Lacombe, Alberta, T4l 1W1. Canada.</auth-address><titles><title>A semi-quantitative RT-PCR method to measure the in vivo effect of dietary conjugated linoleic acid on porcine muscle PPAR gene expression</title><secondary-title>Biol Proced Online</secondary-title></titles><pages>20-28</pages><volume>5</volume><edition>2003/05/08</edition><dates><year>2003</year></dates><isbn>1480-9222 (Print)&#xD;1480-9222 (Linking)</isbn><accession-num>12734559</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/12734559</url></related-urls></urls><custom2>150388</custom2><electronic-resource-num>10.1251/bpo43</electronic-resource-num><language>Eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_29" \o "Meadus, 2003 #623" 29]. cDNA was produced using the primers for hexokinase (NM_012734.1: 5'-GAC CAA GTC AAA AAG ATT GA-3' (sense), 5'-TCT TCT CGT GGT TCA CCT GC-3' (antisense))  ADDIN EN.CITE <EndNote><Cite><Author>Schuit</Author><Year>1999</Year><RecNum>877</RecNum><DisplayText>[30]</DisplayText><record><rec-number>877</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">877</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Schuit, F.</author><author>Moens, K.</author><author>Heimberg, H.</author><author>Pipeleers, D.</author></authors></contributors><auth-address>Diabetes Research Center, Vrije Universiteit Brussel, Brussels, B-1090 Belgium. fschuit@minf.vub.ac.be</auth-address><titles><title>Cellular origin of hexokinase in pancreatic islets</title><secondary-title>J Biol Chem</secondary-title></titles><periodical><full-title>J Biol Chem</full-title><abbr-1>The Journal of biological chemistry</abbr-1></periodical><pages>32803-9</pages><volume>274</volume><number>46</number><edition>1999/11/07</edition><keywords><keyword>Animals</keyword><keyword>Deoxyglucose/pharmacology</keyword><keyword>Flow Cytometry</keyword><keyword>Gene Expression Regulation, Enzymologic</keyword><keyword>Glucokinase/analysis</keyword><keyword>Glucose/metabolism</keyword><keyword>Hexokinase/classification/genetics/*metabolism</keyword><keyword>Insulin/metabolism</keyword><keyword>Islets of Langerhans/*enzymology</keyword><keyword>Isoenzymes/analysis/metabolism</keyword><keyword>Kinetics</keyword><keyword>Male</keyword><keyword>Mannoheptulose/pharmacology</keyword><keyword>Proinsulin/biosynthesis</keyword><keyword>RNA, Messenger/analysis</keyword><keyword>Rats</keyword><keyword>Rats, Wistar</keyword><keyword>Reverse Transcriptase Polymerase Chain Reaction</keyword></keywords><dates><year>1999</year><pub-dates><date>Nov 12</date></pub-dates></dates><isbn>0021-9258 (Print)&#xD;0021-9258 (Linking)</isbn><accession-num>10551841</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/10551841</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_30" \o "Schuit, 1999 #877" 30], pyruvate dehydrogenase (PDH) (NM_001004072.2: 5'-GTG ATG GTG CTG CTA ACC A-3' (sense), 5'-AAC TGG GCA GCA TCC TCG AT-3' (antisense))  ADDIN EN.CITE <EndNote><Cite><Author>Lucia</Author><Year>2003</Year><RecNum>836</RecNum><DisplayText>[15]</DisplayText><record><rec-number>836</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">836</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Lucia, A.</author><author>Earnest, C.</author><author>Perez, M.</author></authors></contributors><auth-address>Physiology Department, Faculty of Health Sciences, European University of Madrid, Spain. alejandro.lucia@mfrs.cisa.uem.es</auth-address><titles><title>Cancer-related fatigue: can exercise physiology assist oncologists?</title><secondary-title>Lancet Oncol</secondary-title></titles><pages>616-25</pages><volume>4</volume><number>10</number><edition>2003/10/14</edition><keywords><keyword>Bone and Bones/physiopathology</keyword><keyword>Child</keyword><keyword>Cost-Benefit Analysis</keyword><keyword>Exercise/*physiology</keyword><keyword>*Exercise Therapy/contraindications/methods</keyword><keyword>Fatigue/*therapy</keyword><keyword>Humans</keyword><keyword>Muscles/physiopathology</keyword><keyword>Neoplasms/*therapy</keyword><keyword>Nutritional Physiological Phenomena</keyword><keyword>Quality of Life</keyword></keywords><dates><year>2003</year><pub-dates><date>Oct</date></pub-dates></dates><isbn>1470-2045 (Print)&#xD;1470-2045 (Linking)</isbn><accession-num>14554239</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/14554239</url></related-urls></urls><electronic-resource-num>S147020450301221X [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_15" \o "Lucia, 2003 #836" 15], lactate dehydrogenase (LDH) (NM_017025.1: 5�-TGG GGT TGG TGC TGT TGG CAT G-3� (sense), 5�-ACG TTT CGC TGG ACC AAA TTG AGC C-3� (antisense))  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_31" \o "Nakai, 2000 #878" 31], monocarboxylic acid transporter 4 (MCT4) (NM_030834.1: 5�- ATG GGA GGA GCT GTG GTG GAC G-3� (sense), 5�-GCT GTG TCG CTG TAG CCA ATC CC-3� (antisense)) [31], monocarboxylic acid transporter 1 (MCT1) (NM_012716.2: 5�-CTT GTG GCG TGA TCC T-3� (sense), 5�-GTT TCG GAT GTC TCG GG -3� (antisense)) [31] and glucose transporter 4 (GLUT-4) (NM_012751.1: 5'-GGT TCC ATC CAT GAG TTA TGT GTC-3' (sense), 5'-CTA AGA GAG AAG GTG TTC CGT CG-3' (antisense))  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_32" \o "Asada, 1998 #879" 32].
cDNA was amplified by RT-PCR  ADDIN EN.CITE <EndNote><Cite><Author>Khal</Author><Year>2005</Year><RecNum>132</RecNum><DisplayText>[33]</DisplayText><record><rec-number>132</rec-number><foreign-keys><key app="EN" db-id="090r9eexov0zfyearetvspea00fe5055rd2f">132</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Khal, J.</author><author>Wyke, S. M.</author><author>Russell, S. T.</author><author>Hine, A. V.</author><author>Tisdale, M. J.</author></authors></contributors><auth-address>Pharmaceutical Sciences Research Institute, Aston University, Birmingham, UK.</auth-address><titles><title>Expression of the ubiquitin-proteasome pathway and muscle loss in experimental cancer cachexia</title><secondary-title>Br J Cancer</secondary-title><alt-title>British journal of cancer</alt-title></titles><periodical><full-title>Br J Cancer</full-title><abbr-1>British journal of cancer</abbr-1></periodical><alt-periodical><full-title>Br J Cancer</full-title><abbr-1>British journal of cancer</abbr-1></alt-periodical><pages>774-80</pages><volume>93</volume><number>7</number><keywords><keyword>Animals</keyword><keyword>Base Sequence</keyword><keyword>Blotting, Western</keyword><keyword>Cachexia/complications/enzymology/metabolism/*physiopathology</keyword><keyword>DNA Primers</keyword><keyword>Mice</keyword><keyword>Muscle, Skeletal/enzymology/metabolism/*physiopathology</keyword><keyword>Neoplasms, Experimental/complications/enzymology/metabolism/*physiopathology</keyword><keyword>Proteasome Endopeptidase Complex/*metabolism</keyword><keyword>Reverse Transcriptase Polymerase Chain Reaction</keyword><keyword>Ubiquitin/*metabolism</keyword></keywords><dates><year>2005</year><pub-dates><date>Oct 3</date></pub-dates></dates><isbn>0007-0920 (Print)&#xD;0007-0920 (Linking)</isbn><accession-num>16160695</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/16160695</url></related-urls></urls><custom2>2361629</custom2><electronic-resource-num>10.1038/sj.bjc.6602780</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_33" \o "Khal, 2005 #132" 33] using a reaction mixture that included 1.5 mM MgCl2, 40 pmol of each primer, 4 pmol of each nucleotide and 0.5 U of Taq DNA polymerase. The reaction was performed using a Mastercycler thermocycler gradient (Eppendorf, Wien, Austria) with an initial denaturation at 95�C for 5 minutes followed by 40 cycles of denaturation at 95�C for 30 seconds, hybridisation at 65�C for 30 seconds and extension at 72�C for 30 seconds. The negative control was a mixture containing all reagents except the RNA sample. The positive control included primers for the constitutively expressed �-actin gene (NM_031144: 5'-GGA CTT CGA GCA GGA GAT GG-3' (sense) and 5'-GCA CCG TGT TGG CGT AGA GG-3' (antisense)). All amplification products were evaluated by 3% agarose gel electrophoresis using 5 �L of each PCR product diluted (1:4) in sample buffer. The gels were visualised under UV light, photographed and quantified using Gel-Pro Plus software (1.0 version, Silver Spring, Cybernetics USA). The data are expressed as the percentage relative to group C normalised to �-actin expression.
Histology and morphometry
The gastrocnemius muscle of the rats was dissected. Portions of the tissue were fixed in paraformaldehyde and cut into 3-�m-thick paraffin sections. These sections were stained in periodic acid-Schiff (PAS) to detect and quantify the glycogen content  ADDIN EN.CITE <EndNote><Cite><Author>Junqueira</Author><Year>1979</Year><RecNum>886</RecNum><DisplayText>[34]</DisplayText><record><rec-number>886</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">886</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Junqueira, L. C.</author><author>Bignolas, G.</author><author>Brentani, R. R.</author></authors></contributors><titles><title>Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections</title><secondary-title>Histochem J</secondary-title></titles><pages>447-55</pages><volume>11</volume><number>4</number><edition>1979/07/01</edition><keywords><keyword>Animals</keyword><keyword>Cartilage/analysis</keyword><keyword>Collagen/*analysis</keyword><keyword>Coloring Agents</keyword><keyword>Histocytochemistry</keyword><keyword>Intestines/analysis</keyword><keyword>Staining and Labeling</keyword><keyword>Vertebrates</keyword></keywords><dates><year>1979</year><pub-dates><date>Jul</date></pub-dates></dates><isbn>0018-2214 (Print)&#xD;0018-2214 (Linking)</isbn><accession-num>91593</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/91593</url></related-urls></urls><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_34" \o "Junqueira, 1979 #886" 34]. Glycogen-positive cells were quantified using Image-Pro Plus software after capturing the image on a Leica microscope using 200x magnification.
Morphometric analysis was performed on 6 different 500-(m2 fields in 8 different muscle lamina per group (n = 8 rats per group). The measurement was calibrated using a Zeiss lamina reticule expressing the values in micrometres. The images were analysed using Image-Pro Plus Software (1.0 version for Windows, Cybernetics, Silver Spring, USA).
Biochemical analysis of cytokines, hormones and glucose
Analyses of serum interleukins 4, 6 and 10 (IL-4, IL-6 and IL-10, respectively), tumour necrosis factor alpha (TNF-(), interferon gamma (INF-() and the hormones insulin and glucagon were performed using immunoassay kits (Linco/Millipore), with 1�10,000 pg of detection range, and fluorescent flow cytometry with Luminex equipment (Millipore, USA).
Serum aliquots were also analysed for glucose content using an enzyme-based kit according to the manufacturer�s instructions.
Statistical analysis
The data are expressed as the mean � SEM. The data were statistically analysed by two-way ANOVA to determine the effects of diet and exercise on tumour growth, muscle parameters and gene expression. Comparisons among the groups were assessed by a post-hoc Bonferroni multiple comparison test (Graph Pad Prism software, v3.00 for Windows 98, USA). The results were considered statistically significant when the P value was less than 5% [35].

RESULTS
Cytokines
The level of TNF-( (Figure 1A) changed significantly during tumour growth and was greatly increased in the tumour-bearing groups W, TW, LW and TWL when compared to the respective control groups C, TC, L and TL. INF-( (Figure 1B) showed a significant increase in group W compared to the control and experimental groups TW, LW and TWL. With the exception of the TW and LW groups, the other groups (TWL and non-tumour-bearing groups TC, L and TL) showed a decrease of approximately 30% in the serum INF-( content when compared to the C group. The serum concentration of IL-6 (Figure 1C) increased by 26.5-fold in group W compared to the other groups. This cytokine was also enhanced in the TW, LW, and TWL groups but only by 3.0-fold in comparison to the C group. IL-6 is also a �myokine�, or a cytokine produced by muscle, particularly during contraction. IL-6 expression increased 3.0-fold in the trained and leucine-fed groups compared to the control group (C); these data showed that the interaction between diet and exercise accounted for 10.3% of the total variance, which can be considered significant (P=0.0434). The serum concentration of IL-4 (Figure 1D) was significantly increased in group W compared to the control and other tumour-bearing groups. The anti-inflammatory cytokine IL-10 (Figure 1E) increased in each group with tumours; higher IL-10 expression was observed in the W and TWL groups when compared to the respective control groups (C, TC, L and TL). In the L and TL groups, IL-10 expression decreased in comparison to the rats in groups C and TC. As suggested by some studies  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_35" \o "Lira, 2009 #887" 35-38], increased IL-10 may inhibit the release of TNF-( and other cytokines. However, our results showed an increase in pro-inflammatory and anti-inflammatory cytokines, suggesting a possible anti-inflammatory response, which could be suppressed by the pro-inflammatory response. This process is depicted in Figure 1F, as the IL-10/TNF-( ratio increased in each of the tumour-bearing groups, mainly in the W group, which displayed an even greater ratio than the LW and TWL groups; these data showed that diet accounted for 52% of the total variation, which was considered extremely significant (P<0.0001). 
Glucose metabolism
The serum glucose level (Figure 2A) was reduced in the tumour-bearing groups W, LW and TWL by 32% compared to the control groups C and TC. Despite having cancer, the TW group had a similar level of glycaemia as the control group. A significant reduction in plasma insulin (approximately 60%; Figure 2B) and a significant increase in glucagon levels (Figure 2C) were also observed in each of the tumour-bearing groups when compared to the control groups; however, this increase was lower in the LW and TWL groups. These results suggest that a compensatory balance between anabolic and catabolic hormones exists because glycaemia in the TW group was maintained near normal values.
Expression of GLUT-4 mRNA in the gastrocnemius muscle (Figure 3A) was significantly reduced in the tumour-bearing groups W and TW, implying less translocation of this transporter to the cell membrane, which may result in lower glucose uptake. mRNA expression of hexokinase was significantly increased in the trained groups and in each tumour-bearing group, with the exception of the TWL group (Figure 3B). A significant reduction in pyruvate dehydrogenase expression was observed in the TWL group when compared to the controls TC and L (Figure 3C); the two-way analysis showed that diet and exercise accounted for 51% of the total variation, which represented a significant difference (P=0.0013). According to our results, LDH expression increased in the trained groups (TC and TL) and in the tumour-bearing group (W) (Figure 3D); however, a similar expression pattern was not observed in the TW, LW and TWL groups, which had similar values to the control group (Figure 3D); these data showed that exercise accounted for 25.6% of the total variation (P=0.046). The serum lactate content increased in all tumour-bearing groups (W = 27.3 ( 1.3; TW = 35.0 ( 0.8; LW = 27.4 ( 3.5 mg/dL) in comparison to the other groups (C = 20.6 ( 2.9; TC = 16.9 ( 0.6; L = 16.6 ( 0.2; TL = 24.8 ( 3.4; TWL = 24.5 ( 5.5 mg/dL). Transport of lactate across the plasma membrane is performed by proton-linked monocarboxylate transporters (MCTs), primarily MCT1 and MCT4, in skeletal muscle. In the present work, we found that MCT1 expression increased in the W and LW groups, and its expression was reduced in the TW and TWL groups (Figure 3E) when compared to the control group, where exercise accounted for this significance (40.9% for total variation; P=0.027). However, MCT4 expression did not change among the groups (Figure 3F). 
Morphology of the gastrocnemius muscle
Muscle weight was significantly reduced only in the W and TWL groups (W=1.26+0.05 and TWL=1.19+0.11 g), and the TW and WL groups exhibited muscle mass reduction (TW=1.45+0.14; WL= 1.37+0.19 g) compared to the C and L groups (, C=1.82+0.09; TC= 1.85+0.11; L=1.79+0.11; TL= 1.59+0.14 g)  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_39" \o "Salomao, 2010 #29" 39]. Additionally, morphological analysis showed a significant reduction in fibre diameter within the gastrocnemius muscle (Figure 4A) in the W and LW groups compared to the control groups C, TC, L and TL. The trained rats from the TC and TL groups tended to have an increased muscle fibre diameter, similar to the TW and TWL groups, despite accelerated tumour growth. These data showed that exercise accounted for 72.4% of the total variation, which was extremely significant (P<0.0001).
Additionally, the glycogen content of the gastrocnemius muscle (Figures 4B and 4C) was reduced in the sedentary tumour-bearing rats (W and LW). However, the muscle glycogen content was maintained in the trained groups, despite the presence of tumours. The leucine-treated groups L and TL had a higher muscle glycogen content compared to the C group (Figures 4B and 4C); diet and exercise accounted for this difference (P<0.0001). 

DISCUSSION
This work demonstrated that the leucine-rich diet with or without exercise affected skeletal muscle and improved glucose metabolism. Despite the presence of a tumour, some parameters related to glucose metabolism were improved by a leucine-rich diet or exercise alone and others were only improved by the combination of a leucine-rich diet and exercise. Exercise can improve the quality of life of cancer patients  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_22" \o "Segal, 2001 #843" 22,  HYPERLINK \l "_ENREF_23" \o "Segar, 1998 #845" 23], and it can minimise the deterioration of lean body mass  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_21" \o "Daneryd, 1995 #842" 21,  HYPERLINK \l "_ENREF_39" \o "Salomao, 2010 #29" 39,  HYPERLINK \l "_ENREF_40" \o "Salomao, 2012 #24" 40]. Our findings suggest that these effects may result from the alteration of key genes related to glucose metabolism. As observed in our previous studies, Walker-256 tumour growth altered both protein synthesis (inhibition) and protein degradation (stimulation)  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_8" \o "Gomes-Marcondes, 2003 #732" 8,  HYPERLINK \l "_ENREF_10" \o "Ventrucci, 2004 #36" 10,  HYPERLINK \l "_ENREF_39" \o "Salomao, 2010 #29" 39,  HYPERLINK \l "_ENREF_40" \o "Salomao, 2012 #24" 40]. However, this tumour also altered glucose metabolism in the gastrocnemius muscle in rats. Despite the presence of tumours, these changes could be partially attenuated with aerobic exercise and/or leucine supplementation. 
The pathophysiology of cancer cachexia is not fully understood. However, studies have shown that cytokines affect carbohydrate, lipid, and protein metabolism. Numerous cytokines, including tumour necrosis factor-�, interleukins 1 and 6, interferon gamma and leukaemia-inhibitory factor, are thought to mediate the cachectic process  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Tisdale, 1997 #829" 1,  HYPERLINK \l "_ENREF_41" \o "Inui, 2002 #619" 41,  HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42]. High plasma concentrations of cytokines were observed in patients with cancer  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_41" \o "Inui, 2002 #619" 41,  HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42] and in tumour-bearing mice  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_43" \o "Singh, 2009 #894" 43,  HYPERLINK \l "_ENREF_44" \o "Verma, 2009 #893" 44], where these cytokines are thought to be involved in weight loss by a mechanism not related to anorexia. 
In accordance with data from the literature, a significant increase in the serum levels of the pro-inflammatory cytokines IL-6, TNF-( and INF-( was observed in the tumour-bearing group (W) compared to the control groups. This increase may directly impact lean body mass wasting  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_45" \o "Al-Majid, 2008 #895" 45-47], and it may be related to changes in carbohydrate metabolism. TNF-( induces IL-6 secretion, and these molecules have a synergistic effect that results in the stimulation of other cytokines in a cascade, which has both pro- and anti-inflammatory components  ADDIN EN.CITE <EndNote><Cite><Author>Tisdale</Author><Year>2009</Year><RecNum>97</RecNum><DisplayText>[42]</DisplayText><record><rec-number>97</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">97</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tisdale, M. J.</author></authors></contributors><auth-address>Nutritional Biomedicine, School of Life and Health Sciences, Aston University, Birmingham, UK. m.j.tisdale@aston.ac.uk</auth-address><titles><title>Mechanisms of cancer cachexia</title><secondary-title>Physiol Rev</secondary-title><alt-title>Physiological reviews</alt-title></titles><periodical><full-title>Physiol Rev</full-title><abbr-1>Physiological reviews</abbr-1></periodical><alt-periodical><full-title>Physiol Rev</full-title><abbr-1>Physiological reviews</abbr-1></alt-periodical><pages>381-410</pages><volume>89</volume><number>2</number><keywords><keyword>Adipose Tissue/metabolism/pathology</keyword><keyword>Atrophy</keyword><keyword>Cachexia/drug therapy/*physiopathology</keyword><keyword>Energy Metabolism/physiology</keyword><keyword>Humans</keyword><keyword>Muscle, Skeletal/metabolism/pathology</keyword><keyword>Neoplasms/*physiopathology</keyword></keywords><dates><year>2009</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>0031-9333 (Print)&#xD;0031-9333 (Linking)</isbn><accession-num>19342610</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/19342610</url></related-urls></urls><electronic-resource-num>10.1152/physrev.00016.2008</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42]. In contrast, IL-6 seems to be beneficial for insulin-regulated glucose metabolism in muscle during exercise; serum levels of IL-6 are elevated during muscle contraction, preceding the appearance of other cytokines. In our study, this elevation was observed in trained rats. Meanwhile, acute and chronic elevation of IL-6 has different effects. During cancer development  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_48" \o "Kim, 2012 #282" 48,  HYPERLINK \l "_ENREF_49" \o "Kim, 2009 #898" 49], IL-6 is associated with insulin resistance and reduced insulin levels, and this association was observed in the tumour-bearing rats, particularly in the W group. Although they had decreased insulin levels, the TW, LW and TWL groups had a similar lNF-( content and a similar IL-6 increase as the trained groups, which could suggest a modulatory effect induced by the leucine-rich diet and/or exercise. 
Alteration of the balance between pro- and anti-inflammatory cytokines may cause or exacerbate health complications due to cancer, such as cachexia  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_35" \o "Lira, 2009 #887" 35,  HYPERLINK \l "_ENREF_50" \o "Argiles, 2003 #529" 50]. Although cytokines alone are unable to explain the complex mechanism of mass wasting in cancer during cachexia  ADDIN EN.CITE <EndNote><Cite><Author>Tisdale</Author><Year>2009</Year><RecNum>97</RecNum><DisplayText>[42]</DisplayText><record><rec-number>97</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">97</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tisdale, M. J.</author></authors></contributors><auth-address>Nutritional Biomedicine, School of Life and Health Sciences, Aston University, Birmingham, UK. m.j.tisdale@aston.ac.uk</auth-address><titles><title>Mechanisms of cancer cachexia</title><secondary-title>Physiol Rev</secondary-title><alt-title>Physiological reviews</alt-title></titles><periodical><full-title>Physiol Rev</full-title><abbr-1>Physiological reviews</abbr-1></periodical><alt-periodical><full-title>Physiol Rev</full-title><abbr-1>Physiological reviews</abbr-1></alt-periodical><pages>381-410</pages><volume>89</volume><number>2</number><keywords><keyword>Adipose Tissue/metabolism/pathology</keyword><keyword>Atrophy</keyword><keyword>Cachexia/drug therapy/*physiopathology</keyword><keyword>Energy Metabolism/physiology</keyword><keyword>Humans</keyword><keyword>Muscle, Skeletal/metabolism/pathology</keyword><keyword>Neoplasms/*physiopathology</keyword></keywords><dates><year>2009</year><pub-dates><date>Apr</date></pub-dates></dates><isbn>0031-9333 (Print)&#xD;0031-9333 (Linking)</isbn><accession-num>19342610</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/19342610</url></related-urls></urls><electronic-resource-num>10.1152/physrev.00016.2008</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42], Argil�s and colleagues  ADDIN EN.CITE <EndNote><Cite><Author>Argiles</Author><Year>1997</Year><RecNum>539</RecNum><DisplayText>[37]</DisplayText><record><rec-number>539</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">539</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Argiles, J. M.</author><author>Alvarez, B.</author><author>Lopez-Soriano, F. J.</author></authors></contributors><auth-address>Department de Bioquimica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona, Spain. argiles@porthos.bio.ub.es</auth-address><titles><title>The metabolic basis of cancer cachexia</title><secondary-title>Med Res Rev</secondary-title></titles><pages>477-98</pages><volume>17</volume><number>5</number><edition>1997/09/01</edition><keywords><keyword>Adipose Tissue/metabolism</keyword><keyword>Cachexia/*etiology/physiopathology</keyword><keyword>Carbohydrate Metabolism</keyword><keyword>Energy Metabolism</keyword><keyword>Humans</keyword><keyword>Insulin Resistance/physiology</keyword><keyword>Muscle, Skeletal/physiopathology</keyword><keyword>Neoplasms/*complications/physiopathology</keyword></keywords><dates><year>1997</year><pub-dates><date>Sep</date></pub-dates></dates><isbn>0198-6325 (Print)&#xD;0198-6325 (Linking)</isbn><accession-num>9276862</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9276862</url></related-urls></urls><electronic-resource-num>10.1002/(SICI)1098-1128(199709)17:5&lt;477::AID-MED3&gt;3.0.CO;2-R [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_37" \o "Argiles, 1997 #539" 37] proposed the adoption of the balance between pro- and anti-in�ammatory cytokines as a marker of cancer cachexia severity. Recently, the IL-10/TNF-( ratio has been adopted as a marker of the in�ammatory process  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_35" \o "Lira, 2009 #887" 35,  HYPERLINK \l "_ENREF_36" \o "Lira, 2012 #889" 36,  HYPERLINK \l "_ENREF_51" \o "Argiles, 2009 #86" 51,  HYPERLINK \l "_ENREF_52" \o "Gould, 2013 #911" 52]. In the present work, the IL-10/TNF-( ratio increased in all tumour-bearing groups, especially in the W group. Although the other tumour groups, LW and TWL, had higher ratios, they were less pronounced than in the W group. This result suggests that nutritional supplementation alone or in combination with physical activity could affect the INF-( and IL-6 serum levels.
Importantly, marked alterations in carbohydrate metabolism are observed in the tumour-free tissue of patients with cancer  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4,  HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42,  HYPERLINK \l "_ENREF_53" \o "Tisdale, 2007 #105" 53]. Neoplastic cells preferentially use 10- to 50-fold more glucose as an energy substrate than normal cells  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_5" \o "Tisdale, 1999 #194" 5,  HYPERLINK \l "_ENREF_6" \o "Cori, 1925 #830" 6,  HYPERLINK \l "_ENREF_53" \o "Tisdale, 2007 #105" 53]. As a consequence, a decrease in serum glucose was observed in each tumour-bearing group, as it is common observed hypoglycaemia in experimental cachexia models  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Tisdale, 1997 #829" 1,  HYPERLINK \l "_ENREF_54" \o "Togni, 2003 #899" 54]. However, the tumour-bearing group subjected to exercise (TW) tended to maintain its glucose level; this level of glycaemia is similar to that observed in the control group, most likely because of the effects of exercise, which diverts this substrate from the tumour cells to the muscle tissue. As a consequence of this, in a previous study, we observed a lower tumour growth rate in the trained rats, which was independent of nutritional supplementation  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_40" \o "Salomao, 2012 #24" 40]. The elevated level of pro-inflammatory cytokines observed in the W group may have led to an inflammatory process, which could cause oxidative stress and muscle wasting. The W group had smaller diameter muscle fibres and a low glycogen content. However, these parameters may be improved by the effects of leucine and exercise in the TW and TWL groups, which even showed a tendency of reduced muscle weight. This hypothesis is consistent with our previous report that long-term exercise training may benefit protein synthesis rather than protein degradation, particularly when associated with leucine treatment  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_40" \o "Salomao, 2012 #24" 40]. The metabolic changes in muscle responses found in the W group, dependent or independent of the inflammatory process, led to increased gene expression of hexokinase, pyruvate dehydrogenase (increasing the conversion of pyruvate to acetyl-CoA) and lactate dehydrogenase (increasing the conversion of pyruvate to lactate); these effects induced the glycolytic process and most likely enhanced energy expenditure. In contrast, the other tumour-bearing rat groups (TW, LW and TWL) showed partial recovery of these parameters, possibly due to exercise and/or leucine supplementation. Several studies point to the processes of peripheral resistance to insulin in cancer  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_55" \o "el Razi Neto, 1996 #900" 55,  HYPERLINK \l "_ENREF_56" \o "Fernandes, 1990 #901" 56]. Physical activity, however, improves tissue responsiveness to insulin  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_19" \o "Anthony, 1999 #840" 19,  HYPERLINK \l "_ENREF_21" \o "Daneryd, 1995 #842" 21], especially in diabetic patients subjected to physical activity or in experimental animals harbouring tumours  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_55" \o "el Razi Neto, 1996 #900" 55,  HYPERLINK \l "_ENREF_56" \o "Fernandes, 1990 #901" 56].
Hepatic gluconeogenesis provided by muscle substrate waste  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4,  HYPERLINK \l "_ENREF_42" \o "Tisdale, 2009 #97" 42] through the Cori cycle  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4,  HYPERLINK \l "_ENREF_6" \o "Cori, 1925 #830" 6] is 2- to 3-fold higher in patients with advanced cancer and progressive weight loss than in patients without weight loss or in healthy volunteers  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Tisdale, 1997 #829" 1,  HYPERLINK \l "_ENREF_4" \o "Tisdale, 2000 #181" 4,  HYPERLINK \l "_ENREF_5" \o "Tisdale, 1999 #194" 5,  HYPERLINK \l "_ENREF_57" \o "Tisdale, 2002 #165" 57]. 
According to some studies, pyruvate has potential anti-oxidant and anti-inflammatory activities and also inhibits the production of tumour necrosis factor-alpha and IL-6 mRNA expression in the liver  ADDIN EN.CITE <EndNote><Cite><Author>Das</Author><Year>2006</Year><RecNum>902</RecNum><DisplayText>[58]</DisplayText><record><rec-number>902</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">902</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Das, U. N.</author></authors></contributors><auth-address>UND Life Sciences, Shaker Heights, OH, USA.</auth-address><titles><title>Pyruvate is an endogenous anti-inflammatory and anti-oxidant molecule</title><secondary-title>Med Sci Monit</secondary-title></titles><pages>RA79-84</pages><volume>12</volume><number>5</number><edition>2006/04/28</edition><keywords><keyword>Animals</keyword><keyword>Anti-Inflammatory Agents, Non-Steroidal/*metabolism</keyword><keyword>Antioxidants/*metabolism</keyword><keyword>Cytokines/metabolism</keyword><keyword>Free Radicals/metabolism</keyword><keyword>Glucose/metabolism</keyword><keyword>Humans</keyword><keyword>Insulin/metabolism</keyword><keyword>Macrophage Migration-Inhibitory Factors/metabolism</keyword><keyword>Pyruvates/pharmacology</keyword><keyword>Pyruvic Acid/*metabolism</keyword><keyword>Sepsis/drug therapy/metabolism</keyword><keyword>Tumor Necrosis Factor-alpha/metabolism</keyword></keywords><dates><year>2006</year><pub-dates><date>May</date></pub-dates></dates><isbn>1234-1010 (Print)&#xD;1234-1010 (Linking)</isbn><accession-num>16641887</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/16641887</url></related-urls></urls><electronic-resource-num>8737 [pii]</electronic-resource-num><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_58" \o "Das, 2006 #902" 58]. Because insulin influences the production of pyruvate through its action on glucose metabolism, pyruvate may be oxidised in the tricarboxylic acid cycle; in this way, the higher pyruvate dehydrogenase gene expression found in the W and LW groups could be related to higher pyruvate levels. Our data suggest that similar expression of PDH together with changes in the serum levels of TNF-(, IL-6 and INF-( could be related to the lesser increase in lactate levels in the TWL group. However, in the TW and TWL groups, we observed similar expression of LDH, which is associated with lower gene expression of MCT1, which could not prevent the changes in serum lactate content. The gastrocnemius muscle expresses the largest amount of MCT1, which has a greater affinity for lactate than MCT4  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_59" \o "Gladden, 2004 #903" 59,  HYPERLINK \l "_ENREF_60" \o "Gladden, 2000 #905" 60]. Therefore, these data suggest that the muscle of TW and TWL rats has adapted to the chronic stimulation imposed by exercise, as these rats maintained the glycogen content in the gastrocnemius muscle and also showed, in our previous data, lower muscle wasting when compared to the W group  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_39" \o "Salomao, 2010 #29" 39]. 
 Non-tumour-bearing trained animals showed an increase in the gene expression of hexokinase, PDH and LDH, which suggests increased energy production in the muscle tissue. Conversely, the leucine-treated animals showed higher gene expression of PDH and LDH and similar gene expression of GLUT-4 and hexokinase, suggesting an improvement in energy production in these groups. In parallel, the nutritional supplementation with leucine also led to an increase in the energy storage, as these animals demonstrated increased glycogen storage in skeletal muscle. These two processes likely improved the energy balance in the muscle tissue in these groups (TC, L and TL), which could be extended to the tumour-bearing groups (TW and TWL), likely benefiting the host under the cachexia state.
As mentioned above, several studies using experimental tumours, including Walker- 256 tumours, have shown decreased insulin secretion, which we verified in all tumour-bearing groups  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_32" \o "Asada, 1998 #879" 32,  HYPERLINK \l "_ENREF_55" \o "el Razi Neto, 1996 #900" 55,  HYPERLINK \l "_ENREF_61" \o "Piffar, 2003 #906" 61]. Additionally, hormonal changes related to the effects of tumour growth can be observed, such as an increase in the serum glucagon level. These hormonal changes are likely related to the increased anaerobic glucose utilisation in tumour cells and the reduction in translocation of glucose transporters in peripheral tissues, such as skeletal muscle. Thus, the reduced gene expression of GLUT-4 in the W and TW groups may exacerbate the metabolic imbalance observed during the advanced stages of the neoplastic process  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_19" \o "Anthony, 1999 #840" 19,  HYPERLINK \l "_ENREF_21" \o "Daneryd, 1995 #842" 21], as observed in our study. Furthermore, the increased glucagon levels in the W, TW, LW and TWL groups corroborates the results of other studies in the literature, suggesting that counter-regulatory hormones increase the availability of nutrients to neoplastic tissue  ADDIN EN.CITE <EndNote><Cite><Author>Argiles</Author><Year>2009</Year><RecNum>86</RecNum><DisplayText>[51]</DisplayText><record><rec-number>86</rec-number><foreign-keys><key app="EN" db-id="090r9eexov0zfyearetvspea00fe5055rd2f">86</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Argiles, J. M.</author><author>Busquets, S.</author><author>Toledo, M.</author><author>Lopez-Soriano, F. J.</author></authors></contributors><auth-address>Cancer Research Group, Departament de Bioquimica i Biologia Molecular, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, Barcelona 08028, Spain. jargiles@ub.edu</auth-address><titles><title>The role of cytokines in cancer cachexia</title><secondary-title>Curr Opin Support Palliat Care</secondary-title><alt-title>Current opinion in supportive and palliative care</alt-title></titles><periodical><full-title>Curr Opin Support Palliat Care</full-title><abbr-1>Current opinion in supportive and palliative care</abbr-1></periodical><alt-periodical><full-title>Curr Opin Support Palliat Care</full-title><abbr-1>Current opinion in supportive and palliative care</abbr-1></alt-periodical><pages>263-8</pages><volume>3</volume><number>4</number><keywords><keyword>Cachexia/etiology/*physiopathology</keyword><keyword>Cytokines/*physiology</keyword><keyword>Humans</keyword><keyword>Inflammation/physiopathology</keyword><keyword>Metabolism/physiology</keyword><keyword>Neoplasms/*complications</keyword><keyword>Transcription Factors/physiology</keyword></keywords><dates><year>2009</year><pub-dates><date>Dec</date></pub-dates></dates><isbn>1751-4266 (Electronic)&#xD;1751-4258 (Linking)</isbn><accession-num>19713854</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/19713854</url></related-urls></urls><electronic-resource-num>10.1097/SPC.0b013e3283311d09</electronic-resource-num></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_51" \o "Argiles, 2009 #86" 51]. Currently, attenuation of the metabolic decline associated with cancer is an important area of research, and the present work demonstrated that leucine and exercise interventions minimised some of the deleterious effects of tumour burden on indices of glucose metabolism and muscle morphometry. We have previously shown the beneficial effects of leucine in tumour-bearing animals, and in this work, we extended these observations to serum cytokines and muscle glycolytic gene expression, glycogen content and fibre size. Further studies are being conducted in our laboratory to determine if and how leucine supplementation in combination with exercise could counteract the tumour effects on carbohydrate metabolism in parallel with body mass wasting during cancer-induced cachexia. 
COMPETING INTERESTS
The authors declare that there are no competing interests.
AUTHORS� CONTRIBUTIONS
EMS and MCCGM conceived of the study and participated in its design, data collection, analysis and writing of the manuscript. ATT and GOS collected data and analysed the results. All authors read and approved the final manuscript.
ACKNOWLEDGMENTS
The authors are grateful for financial support from the Funda��o de Amparo a Pesquisa do Estado de S�o Paulo (FAPESP; #2006/00974-1, #2006/04645-2, #2010-00260-9, #2010/11328-9) and Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq; #304000/2007-8 and #502915/2007-2). The authors also thank Dr. J Marcondes for computational support and Dr. M. A. R. Mello for insightful discussion. The manuscript was edited for proper English language by American Journal Experts (Editorial Certificate # 1968-B203-DE04-ED60-3A08).


Figures Legends
Figure 1. Serum levels of the cytokines TNF-( (A), INF-( (B), IL-6 (C), IL-4 (D), and IL-10 (E) and the IL-10/TNF-( ratio (F) in tumour-bearing rats fed a leucine-rich diet with or without aerobic exercise. The minimum number of animals per group was eight. Legend: C � control rats, TC � trained rats, W � tumour-bearing rats, TW � trained tumour-bearing rats, L � rats fed a leucine-rich diet, TL � trained rats fed a leucine-rich diet, LW � tumour-bearing rats fed a leucine-rich diet, TWL � trained tumour-bearing rats fed a leucine-rich diet. The columns represent the mean � SEM. * P < 0.05 versus the C and L groups. a P < 0.05 versus the C group. b P < 0.05 versus the W group. Significant differences were assessed by two-way ANOVA analysis, followed by the Bonferroni post-hoc test.

Figure 2. Blood glucose concentration (A) and serum levels of insulin (B) and glucagon (C) in tumour-bearing rats fed a leucine-rich diet with or without aerobic exercise. The minimum number of animals per group was eight. Legend: C � control rats, TC � trained rats, W � tumour-bearing rats, TW � trained tumour-bearing rats, L � rats fed a leucine-rich diet, TL � trained rats fed a leucine-rich diet, LW � tumour-bearing rats fed a leucine-rich diet, TWL � trained tumour-bearing rats fed a leucine-rich diet. The columns represent the mean � SEM. * P < 0.05 versus the C group. 

Figure 3. Gene expression of GLUT-4 (A), hexokinase (B), pyruvate dehydrogenase (C), lactate dehydrogenase (D), monocarboxylate transporter 1 (MCT1; E) and monocarboxylate transporter 4 (MCT4; F) in the gastrocnemius muscle of tumour-bearing rats fed a leucine-rich diet with or without aerobic exercise. The minimum number of animals per group was eight. Gene expression was measured in eight muscle samples per group, and the image is representative of all experimental groups. Legend: C � control rats, TC � trained rats, W � tumour-bearing rats, TW � trained tumour-bearing rats, L � rats fed a leucine-rich diet, TL � trained rats fed a leucine-rich diet, LW � tumour-bearing rats fed a leucine-rich diet, TWL � trained tumour-bearing rats fed a leucine-rich diet. The columns represent the percentage value in relation to the C group. * P < 0.05 versus the C group.

Figure 4. Measurement of the diameter of the gastrocnemius muscle ((m; A), quantification of the muscle glycogen content in histological sections (3 �m) (B) and images of glycogen staining of histological sections of the gastrocnemius muscle (purple dye) (C) in tumour-bearing rats fed a leucine-rich diet with or without exercise. The minimum number of animals per group was eight. The magnification is 200x and scale bar is 10�m. Legend: C � control rats, TC � trained rats, W � tumour-bearing rats, TW � trained tumour-bearing rats, L � rats fed a leucine-rich diet, TL � trained rats fed a leucine-rich diet, LW � tumour-bearing rats fed a leucine-rich diet, TWL � trained tumour-bearing rats fed a leucine-rich diet. The columns represent the mean � SEM. * P < 0.05 versus the C, TC, L and TL groups. a P < 0.05 versus the W and LW groups.

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J.</author></authors></contributors><auth-address>Pharmaceutical Sciences Institute, Aston University, Birmingham, United Kingdom.</auth-address><titles><title>Cancer cachexia: metabolic alterations and clinical manifestations</title><secondary-title>Nutrition</secondary-title></titles><periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></periodical><pages>1-7</pages><volume>13</volume><number>1</number><edition>1997/01/01</edition><keywords><keyword>Animals</keyword><keyword>Anorexia/complications</keyword><keyword>Cachexia/etiology/*metabolism</keyword><keyword>Carbohydrate Metabolism</keyword><keyword>Cytokines/*physiology</keyword><keyword>Energy Metabolism</keyword><keyword>Humans</keyword><keyword>Lipid Metabolism</keyword><keyword>Muscle, Skeletal/metabolism</keyword><keyword>Neoplasms/*complications</keyword></keywords><dates><year>1997</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0899-9007 (Print)&#xD;0899-9007 (Linking)</isbn><accession-num>9058439</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9058439</url></related-urls></urls><electronic-resource-num>S0899900796003139 [pii]</electronic-resource-num><language>eng</language></record></Cite><Cite><Author>Tisdale</Author><Year>2000</Year><RecNum>181</RecNum><record><rec-number>181</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">181</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tisdale, M. J.</author></authors></contributors><auth-address>Pharmaceutical Sciences Research Institute, Aston University, Birmingham, UK. m.j.tisdale@aston.ac.uk</auth-address><titles><title>Metabolic abnormalities in cachexia and anorexia</title><secondary-title>Nutrition</secondary-title><alt-title>Nutrition</alt-title></titles><periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></periodical><alt-periodical><full-title>Nutrition</full-title><abbr-1>Nutrition</abbr-1></alt-periodical><pages>1013-4</pages><volume>16</volume><number>10</number><keywords><keyword>Anorexia/*metabolism</keyword><keyword>Cachexia/*metabolism</keyword><keyword>*Carbohydrate Metabolism</keyword><keyword>Eicosanoic Acids/therapeutic use</keyword><keyword>Humans</keyword><keyword>*Lipid Metabolism</keyword><keyword>Proteins/*metabolism</keyword></keywords><dates><year>2000</year><pub-dates><date>Oct</date></pub-dates></dates><isbn>0899-9007 (Print)&#xD;0899-9007 (Linking)</isbn><accession-num>11054609</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/11054609</url></related-urls></urls></record></Cite><Cite><Author>Tisdale</Author><Year>1999</Year><RecNum>194</RecNum><record><rec-number>194</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">194</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Tisdale, M. J.</author></authors></contributors><auth-address>Pharmaceutical Sciences Institute, Aston University, Birmingham B4 7ET, United Kingdom.</auth-address><titles><title>Wasting in cancer</title><secondary-title>J Nutr</secondary-title><alt-title>The Journal of nutrition</alt-title></titles><periodical><full-title>J Nutr</full-title><abbr-1>The Journal of nutrition</abbr-1></periodical><alt-periodical><full-title>J Nutr</full-title><abbr-1>The Journal of nutrition</abbr-1></alt-periodical><pages>243S-246S</pages><volume>129</volume><number>1S Suppl</number><keywords><keyword>Anorexia/metabolism</keyword><keyword>Energy Metabolism/physiology</keyword><keyword>HIV Wasting Syndrome/*metabolism/pathology</keyword><keyword>Humans</keyword><keyword>Lipid Metabolism</keyword><keyword>Muscles/metabolism</keyword><keyword>Weight Loss/physiology</keyword></keywords><dates><year>1999</year><pub-dates><date>Jan</date></pub-dates></dates><isbn>0022-3166 (Print)&#xD;0022-3166 (Linking)</isbn><accession-num>9915907</accession-num><urls><related-urls><url>http://www.ncbi.nlm.nih.gov/pubmed/9915907</url></related-urls></urls></record></Cite><Cite><Author>Cori</Author><Year>1925</Year><RecNum>830</RecNum><record><rec-number>830</rec-number><foreign-keys><key app="EN" db-id="xa0zfpfpudrptpetwdpppx9wra0swft00atp">830</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Cori, C. F.</author><author>Cori, G. T.</author></authors></contributors><titles><title>The carbohydrate metabolism of tumors. II. 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