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:The effects of salidrosid on DIABLO and XAF1 gene expression in PC3 prostat cancer cells
Ugur Uyeturk1, Zeynep Ocak2, Muradiye Acar3, Isa Ozbey4, Vildan Tekelioglu5

1-Department of Urology, Abant Izzet Baysal Medical Faculty, Bolu, Turkey
2-Department of Medical Genetics, Abant Izzet Baysal Medical Faculty, Bolu, Turkey
3-Department of Urology, Turgut Ozal Medical Faculty, Ankara, Turkey
4-Department of Urology, Ataturk Medical Faculty, Erzurum, Turkey
5-Department of Internal Medicine, Abant Izzet Baysal Medical Faculty, Bolu, Turkey
Experimental Study
Conflict of interest: The authors declare that they have no conflict of interest
Key words:Salidrosid, prostat cancer, anti-tumor effect
This study was supported by the Abant Izzet Baysal University, Scientific Research Projects Fund (Project No. BAP- 2013.08.02.593).

Correspondence author: 
Assist. Prof. Ugur UYETURK, MD
Abant Izzet Baysal University, Medical Faculty
Department of Urology, 14280, Bolu, Turkey.
E-mail: uguruyeturk@yahoo.com
Telephone number: +903742534618
Fax number: +903742534615

ABSTRACT
Aim:Our objective was to determine the effects of salidroside on androgen-independent prostate cancer (PC-3) and nonmalignant transformed PNT1a prostate cells.
Methods:PC3 and PNT1a cells were cultivated and treated separately with 1,5 or 20 �g/mL salidroside. After 24 h, RNA was isolated and transcribed into cDNA. Expression analysis was performed using real-time reverse-transcription polymerase chain reaction, and cell survival was determined using the 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay and enzyme-linked immunosorbent assay.
Results:Our gene expression study revealed that, compared with the PNT1a control group, a statistically significant decrease was found in the expression of the DIABLO and XAF1 genes in PC3 cells(p=0.021). However, a statistically significant change was not found in the expression levels of these genes in either cell line following salidroside therapy. 
Conclusion:However, when considering salidroside for cancer therapy, it should be noted that this agent not only causes cancer cell death but also damages normal tissue.

Key words:Salidrosid, prostat cancer, anti-tumor effect





INTRODUCT0ON
Prostate cancer is the second most common type of cancer and the second leading cause of cancer mortality, after lung cancer, worldwide  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_1" \o "Kiratli, 2001 #2" 1, HYPERLINK \l "_ENREF_2" \o "Wilt, 2008 #1" 2]. The incidence of prostate cancer increases with age. The process of cancer development involves the production of androgens, estrogens, growth factors, and neurotransmitters, which can function alone or in combination. Thus, hormonal therapy remains one of the most used therapeutic modalities for prostate cancer. Conversely, long-term hormonal therapy increases the risk of osteoporosis and fracture, particularly in the geriatric population  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_3" \o "Andriole, 2010 #3" 3].
Due to the frequency of prostate cancer and the undesirable effects of long-term hormonal therapy, the discovery of new drugs for prostate cancer therapy and the search for novel findings regarding prostate cancer are increasing  ADDIN EN.CITE <EndNote><Cite><Author>Yu</Author><Year>2014</Year><RecNum>16</RecNum><DisplayText>(4)</DisplayText><record><rec-number>16</rec-number><foreign-keys><key app="EN" db-id="xtsfrrzd2tfv9gewarvvte9jf2zpwaps990v">16</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Yu, X. L.</author><author>Jing, T.</author><author>Zhao, H.</author><author>Li, P. J.</author><author>Xu, W. H.</author><author>Shang, F. F.</author></authors></contributors><auth-address>Department of Pathophysiology, Medical College of Qingdao University, Qingdao, China E-mail : xiaoling_yu2004@163.com.</auth-address><titles><title>Curcumin inhibits expression of inhibitor of DNA binding 1 in PC3 cells and xenografts</title><secondary-title>Asian Pac J Cancer Prev</secondary-title><alt-title>Asian Pacific journal of cancer prevention : APJCP</alt-title></titles><periodical><full-title>Asian Pac J Cancer Prev</full-title><abbr-1>Asian Pacific journal of cancer prevention : APJCP</abbr-1></periodical><alt-periodical><full-title>Asian Pac J Cancer Prev</full-title><abbr-1>Asian Pacific journal of cancer prevention : APJCP</abbr-1></alt-periodical><pages>1465-70</pages><volume>15</volume><number>3</number><edition>2014/03/13</edition><dates><year>2014</year></dates><isbn>1513-7368 (Print)&#xD;1513-7368 (Linking)</isbn><accession-num>24606484</accession-num><urls></urls><remote-database-provider>NLM</remote-database-provider><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_4" \o "Yu, 2014 #16" 4]. Thus, therapeutic modalities that provide an alternative major therapy are warranted. One strategy is the use of extracts obtained from plants. Many studies concerning the anticancer activities of medicinal plant extracts have been performed. One of these plants is Rhodiola rosea  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_3" \o "Andriole, 2010 #3" 3, HYPERLINK \l "_ENREF_5" \o "Felici, 2012 #4" 5]. 
R. rosea, a plant used in traditional and modern medical science, inhibits the production of free radicals and has strong antioxidant properties. In the literature, anti-aging, anti-inflammatory, anti-hypoxic properties of R. rosea have been reported. Additionally, because of the presence of salidroside in this plant, it has been shown to exert strong antidepressant and antioxidant effects, as well as a protective role against neural cell death  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_6" \o "Qian, 2012 #5" 6, HYPERLINK \l "_ENREF_7" \o "Zhang, 2012 #6" 7]. The effects of salidroside have not been evaluated in prostate cancer cells, and existing studies are limited in number. XIAP-associated factor 1 (XAF1) is a new candidate tumor suppressor that exerts proapoptotic effects by interfering with the caspase-inhibiting activity of XIAP. The 17p13 region harboring the XAF1 gene undergoes frequent alleic losses in various human malignancies, including bladder cancer, and the tumor-specific loss or downregulation of XAF1 expression suggests a possible role for XAF1 in the suppression of malignancy. However, the mechanism by which XAF1 is downregulated in human cancers is poorly characterized  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_8" \o "Lee, 2006 #7" 8, HYPERLINK \l "_ENREF_9" \o "Qiu, 2014 #8" 9]. Smac/DIABLO is a proapoptotic protein. Its release from the mitochondria causes it to interact with and sequester inhibitor of apoptosis proteins (IAPs), thereby maintaining the activation of caspases during apoptotic induction  ADDIN EN.CITE <EndNote><Cite><Author>Qiu</Author><Year>2014</Year><RecNum>8</RecNum><DisplayText>(9)</DisplayText><record><rec-number>8</rec-number><foreign-keys><key app="EN" db-id="xtsfrrzd2tfv9gewarvvte9jf2zpwaps990v">8</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Qiu, W.</author><author>Zhou, J.</author><author>Zhu, G.</author><author>Zhao, D.</author><author>He, F.</author><author>Zhang, J.</author><author>Lu, Y.</author><author>Yu, T.</author><author>Liu, L.</author><author>Wang, Y.</author></authors></contributors><auth-address>Department of Microbiology and Immunology, Nanjing Medical University, Nanjing, People&apos;s Republic of China.</auth-address><titles><title>Sublytic C5b-9 triggers glomerular mesangial cell apoptosis via XAF1 gene activation mediated by p300-dependent IRF-1 acetylation</title><secondary-title>Cell Death Dis</secondary-title><alt-title>Cell death &amp; disease</alt-title></titles><periodical><full-title>Cell Death Dis</full-title><abbr-1>Cell death &amp; disease</abbr-1></periodical><alt-periodical><full-title>Cell Death Dis</full-title><abbr-1>Cell death &amp; disease</abbr-1></alt-periodical><pages>e1176</pages><volume>5</volume><edition>2014/04/20</edition><dates><year>2014</year></dates><isbn>2041-4889 (Electronic)</isbn><accession-num>24743731</accession-num><urls></urls><custom2>PMC4001307</custom2><electronic-resource-num>10.1038/cddis.2014.153</electronic-resource-num><remote-database-provider>NLM</remote-database-provider><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_9" \o "Qiu, 2014 #8" 9].
In the present study, we investigated the protective effects of salidroside on prostate cancer cells as well as the potential time-dependency of salidroside�s toxic effects in a series of primary and secondary cell lines. Additionally, changes in the expression levels of the XAF1 and DIABLO genes in these cell lines, the role these genes play in the etiopathogenesis of prostate cancer, and changes in their expression following salidroside treatment were investigated.
MATERIALS AND METHODS
Cell culture
PC3 and PNT1a cells were obtained from the American Type Culture Collection (ATCC).  Both cell lines were cultured in Dulbecco�s modified Eagle�s medium (DMEM) containing 10% fetal bovine serum and 1% penicillin/streptomycin at 37(C in a humidified atmosphere of 5% CO2. The medium was changed every 2 days. Sixth passage cells were used in all experiments. 
Salidroside stimulation
All cells were incubated initially in 2 mL medium containing 10% fetal bovine serum. After 72 h, the medium was changed to serum-free DMEM, and the cells were incubated for another 24 h. The cells were then exposed to 1, 5 and 20 �g/mL salidroside in dimethysulfoxide or to phosphate-buffered saline (PBS) containing 0.1% bovine serum albumin as a control (n=6 each) as described previously  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_10" \o "Ocak, 2013 #9" 10].
Total RNA isolation and cDNA synthesis 
Total RNA was extracted using TRIzol (Ambion Life Technologies/Invitrogen, Carlsbad, CA, USA) according to methods described previously  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_10" \o "Ocak, 2013 #9" 10]. One microgram of RNA was reverse transcribed using reverse transcriptase (Thermo Scientific) with oligo (dT) primers according to the manufacturer�s instructions (Table 1). Mouse �-actin was amplified as a control for polymerase chain reaction (PCR). To control for the presence of genomic DNA contamination, samples lacking reverse transcriptase were amplified by PCR.
3-(4,5-Dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) cell viability assay
The effects of salidroside on cell viability were evaluated using a Vybrant� MTT Cell Proliferation Assay Kit (V-13154) (MTT) (Vybrant, Leiden, The Netherlands). PC3 and PNT1a cells were cultivated at 1(104 per well in 96-well culture plates. The cells were exposed to 0.5, 1, 5, 10, 20 and 30 �g/mL salidroside for 1, 8, 17 and 24 h, respectively. Cells that were not exposed to salidroside were used as the control, and the assay was repeated three times per salidroside concentration. After culturing, MTT was added, and the cells were cultured for an additional 4 h. The absorbance was then measured at 490 nm using an ELx800 Absorbance Microplate Reader (BioTek, Winooski, VT, USA). The absorbance values relative to those of the control were calculated, and the cytotoxicity was determined.
Caspase 3 activity
The activity of caspase 3 was determined using a fluorometric immunosorbent enzyme assay (Roche Molecular Biochemicals, Roche Diagnostics, Basel, Switzerland), in which caspase 3 derived from cellular lysates is captured by a monoclonal antibody, and the amount of activated caspase 3 cleaved is proportional to the amount of substrate added. Due to proteolytic cleavage of the substrate, free fluorescent AFC (7-amino-4-trifluoromethylcoumarin) is generated and determined fluorometrically at a maximum wavelength of 505 nm. Briefly, cultured vascular smooth muscle cells were treated with vehicle or docosahexaenoic acid for the times indicated in the figure legends. Cells were washed twice with ice-cold PBS, harvested, and suspended in lysis buffer. After incubation on ice for 1 min, the homogenate was centrifuged at 4�C for 30 min. The cleared lysate was stored at "70�C until ready for assay. The caspase 3 assay was carried out according to the manufacturer�s instructions.
Next, intracellular caspase 3 levels, which are indicative of apoptosis, were measured by enzyme-linked immunosorbent assay using the Roche Caspase 3 Activity Assay kit according to the manufacturer�s instructions.  The increase or decrease in caspase 3 levels compared with the control group was calculated. 
Real-time PCR (XAF1 and Smac/DIABLO)
Real-time PCR was performed on the cDNA samples (Thermo Scientific Revert Aid First Strand cDNA Synthesis Kit) as described previously. The PCR mixture consisted of the cDNA samples plus SYBR Green PCR Master Mix, comprising DNA polymerase, SYBR Green I Dye, dNTPs, PCR buffer, and forward and reverse primers, in a total volume of 50 �l/mL. The amplification of XAF1 and DIABLO genes was used to normalize the efficiency of cDNA synthesis and the amount of RNA added. PCR was performed with an initial denaturation step at 95�C for 15 min, followed by amplification for 35 cycles, each cycle consisting of denaturation at 95�C for 15 seconds, primer annealing at 58�C for 30 seconds, and primer extension at 72�C for 30 seconds, followed by a final primer extension at 72�C for 5 min. 
Statistical analysis
Between group comparisons were performed using the Student�s t-test. A p-value less than 0.05 was indicative of statistical significance. For these calculations, SPSS version 11 was used. The expression levels of XAF1 and Smac/DIABLO RNA were determined in PC3 and PNT1a cells. The bars represent the mean XAF1 and Smac/DIABLO expression levels (gene/�-actin ratio). The error bars represent the standard errors of the means.
RESULTS
The MTT viability assays revealed proliferation in both cell lines when treated with 5 �g/mL salidroside for 1 and 17 h. When the salidroside concentration was increased, particularly to 20 �g/ml, both cell lines exhibited cell death (Figs. 1 and 2). In contrast to the PNT1a cell control group, treatment of PC3 cells with 5 or 20 �g/ml of salidroside showed no statistically significant differences in proliferation or the range of cell death (p=0.773). Salidroside caused various morphological changes in PC3 cells depending on the concentration applied (Fig. 3).
Caspase 3 was not activated in PC3 or PNT1a cells treated with 5 �g/ml salidroside (p>0.1) compared with untreated controls (Fig. 4).
Our gene expression analysis showed that, compared with the PNT1a cell control group, statistically significant decreases were found in DIABLO and XAF1 gene expression in PC3 cells (p=0.021). Statistically significant increases were found in DIABLO and XAF1 gene expression in both PC3 (p=0.016) and PNT1a cells (p=0.024) treated with 5 �g/ml salidroside, compared with their respective untreated control groups. Compared with the PNT1a control group, a statistically significant increase could not be determined in DIABLO and XAF1 gene expression in PC3 cells treated with 5 �g/ml salidroside.

DISCUSSION
In this study, due to the decrease in DIABLO and XAF1 gene expression in PC3 cells compared with PNT1a cells, these genes were expected to be important apoptotic pathway components. A recent study showed that down-regulation of Smac/DIABLO expression contributed to the potent anti-atherosclerotic effect induced by shear stress via prevention of endothelial cells from entering apoptosis. Conversely, no statistically significant differences in Smac/DIABLO expression levels were found in either cell type after salidroside therapy. 
This study raises doubts about the anticancer effects of salidroside in prostate cancer. Thus, when considering salidroside for cancer therapy, it should be noted that this agent not only targets cancer cells but can also damage normal tissue. However, we did not evaluate other genes involved in the apoptotic pathway, indicating a limitation in our study. Recent studies have shown that salidroside can inhibit the growth of stomach adenocarcinoma cells, leukemia cells, bladder carcinoma cells, breast carcinoma cells and parotid carcinoma cells in vitro. In those studies, the anticancer effects of salidroside were reported to change according to the dose, time, and surface receptor status of cancer cells.  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_11" \o "Hu, 2010 #10" 11]. Interestingly, hormone-resistant cells were more sensitive to the inhibitory action of lower salidroside concentrations than were hormone-sensitive cells, indicating a possible interaction of salidroside with steroid receptors  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_12" \o "Hu, 2010 #11" 12,  HYPERLINK \l "_ENREF_13" \o "Zhang, 2007 #12" 13]. PC3 cells do not express the androgen receptor or prostate-specific antigen and are androgen independent  ADDIN EN.CITE <EndNote><Cite><Author>Atala</Author><Year>2012</Year><RecNum>13</RecNum><DisplayText>(14)</DisplayText><record><rec-number>13</rec-number><foreign-keys><key app="EN" db-id="xtsfrrzd2tfv9gewarvvte9jf2zpwaps990v">13</key></foreign-keys><ref-type name="Journal Article">17</ref-type><contributors><authors><author>Atala, A.</author></authors></contributors><titles><title>Re: PC3 is a cell line characteristic of prostatic small cell carcinoma</title><secondary-title>J Urol</secondary-title><alt-title>The Journal of urology</alt-title></titles><periodical><full-title>J Urol</full-title><abbr-1>The Journal of urology</abbr-1></periodical><alt-periodical><full-title>J Urol</full-title><abbr-1>The Journal of urology</abbr-1></alt-periodical><pages>325</pages><volume>188</volume><number>1</number><edition>2012/06/12</edition><dates><year>2012</year><pub-dates><date>Jul</date></pub-dates></dates><isbn>1527-3792 (Electronic)&#xD;0022-5347 (Linking)</isbn><accession-num>22682868</accession-num><urls></urls><electronic-resource-num>10.1016/j.juro.2012.03.074</electronic-resource-num><remote-database-provider>Nlm</remote-database-provider><language>eng</language></record></Cite></EndNote>[ HYPERLINK \l "_ENREF_14" \o "Atala, 2012 #13" 14]. Another prostate cell line, PNT1a, is a good model for the analysis of cellular processes, such as prostate epithelium proliferation, in response to androgens and growth factors  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_15" \o "Avances, 2001 #14" 15]. Another explanation for the discrepant results among studies could be due to the cells used in our study and the hormone receptor status of the cells. Subsequent studies should be repeated using a larger sample number and more cell lines expressing different hormone receptor types. 
A recent study showed that salidroside could significantly inhibit tumor-induced angiogenesis in mice, suggesting angiogenic effects as another important parameter for defining the anticancer effect of an agent  ADDIN EN.CITE  ADDIN EN.CITE.DATA [ HYPERLINK \l "_ENREF_16" \o "Skopinska-Rozewska, 2008 #15" 16]. Another limitation in our study was that the effect on angiogenesis could not be evaluated. To determine the suitability of salidroside for prostate cancer therapy, its effects on angiogenesis in tumor tissues should be evaluated by a subsequent study. 
We believe that the effects of salidroside on other genes related to the apoptosis pathway should be investigated to obtain clearer results concerning the anticarcinogenic effects of this agent. The incidence of prostate cancer is high, and hormonal therapy can cause unwanted and long-term effects. Identifying an efficient target molecule (gene/protein) for prostate cancer and understanding the effective mechanisms are important for defining alternative, less toxic therapies. Thus, constructing in vitro models for testing agents in the clinic is important. Cells with genetic backgrounds differing from those of normal cell lines should be evaluated in studies concerning anti-carcinogenic agents. In regard to methods, expression assays of apoptosis-related genes and micro-RNA studies should be used in conjunction with the evaluation of cell viability and apoptosis, thus allowing the effects of the test agent and its associated signaling pathways to be evaluated more appropriately.

Conflict of interest: The authors declare that they have no conflict of interest
This study was supported by the Abant Izzet Baysal University, Scientific Research Projects Fund (Project No. BAP- 2013.08.02.593).


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10. Ocak Z, Acar M, Gunduz E, Gunduz M, Demircan K, et al. (2013) Effect of hypericin on the ADAMTS-9 and ADAMTS-8 gene expression in MCF7 breast cancer cells. European review for medical and pharmacological sciences 17:1185-1190.
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$d�a$gd	��]�]�]�]�]�^�^a_b_``�`�`�`�`oapabb�b�b�c�c�d�d�e�edfef"g#g�g�gphqh�h�h�i�i�i�������䵝��������������������������������������U)h	�CJOJQJaJmHnHsH	tH	u/h	�h\CJOJQJaJmHnHsH	tH	u/h	�h�?�CJOJQJaJmHnHsH	tH	u,h	�h\CJOJQJaJmH	nH	sH	tH	5jh	�h\CJOJQJUaJmH	nH	sH	tH	+ et al. (2008) The influence of Rhodiola quadrifida 50% hydro-alcoholic extract and salidroside on tumor-induced angiogenesis in mice. Polish journal of veterinary sciences 11:97-104.
Figure and Table Legends 
Table 1. The forward and reverse primers used in real-time PCR analyses of the XAF1, DIABLO and �-actin genes.
Figure 1:  Effects of salidroside on the viability of PC3 and PNT1a cells after 1 h of salidroside treatment.
Figure 2:  Effects of salidroside on the viability of PC3 and PNT1a cells after 17 h of salidroside treatment.
Figure 3: Morphological changes in PC3 cells treated with 5 or 20 �g/mL salidroside for 24 h, as viewed under an inverted phase-contrast microscope (200 �) (arrows indicate the apoptotic cells).
Figure 4: Changes in intracellular caspase 3 levels in PC3 and PNT1a cells after treatment with salidroside for 24 h.


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