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	�:	Comparative analysis of nuclear and cytoplasmic p21 expression with p53 and cdk2 expression in canine tumours
Zahoor Ahmad War, Sreelekshmy Mohandas, Rahul Kadam, M. Karikalan, Pawan Kumar, Abhijit Motiram Pawde and Anil Kumar Sharma
Addresses of authors
Zahoor Ahmad WAR, Ph.D. Scholar, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India

Sreelekshmy MOHANDAS, Ph.D. Scholar, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India

Rahul KADAM, Ph.D. Scholar, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India

M. KARIKALAN, Scientist, Wildlife Section, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India 

Pawan KUMAR, Scientist, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India

Abhijeet M. PAWDE, Principal Scientist, Division of Surgery and Radiology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India

Anil Kumar SHARMA, Principal Scientist, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India
Corresponding Author: Zahoor Ahmad WAR, Ph.D. Scholar, Division of Pathology, Indian Veterinary Research Institute, Izatnagar- 243 122, Uttar Pradesh, India
E Mail: drzahoorahmadwar@gmail.com

Abstract
          The present study was undertaken to evaluate the comparative expression of cell cycle regulators- p53, p21 and cdk2 in spontaneous canine tumours. Out of 46 cases diagnosed as tumour by histopathology, 19 were benign and 27 were malignant. Expression of p53, p21 and cdk2 was analyzed by employing immunohistochemical staining technique and their expression detected in 84.62%, 69.23% and 69.23% cases, respectively. The per cent expressions of p53, p21 and cdk2 showed variation among different histopathological types of tumours. Visceral/mucosal tumours exhibited higher expression of p53 when compared to cutaneous tumours. Expression of p21 was found to be 62.5% and 80% whereas cdk2 was 68.75% and 70% in skin and visceral/mucosal tumours, respectively. Analysis of individual cases for the expression and localization of these three biomarkers revealed seven different patterns. Out of the 15 tumours which showed both p53 and p21 overexpression, 11 tumours showed cytoplasmic expression of p21 along with overexpression of cdk2, which indicated that cytoplasmic p21 was not able to perform its normal function of blocking the expression of cdk2. Overexpression of p53 along with cdk2 was observed in 5 cases where p21 expression was totally absent indicating overexpression of abnormal or mutated p53 which was not able to induce the expression  of p21 leading to overexpression of cdk2. From present study it can be concluded that cytoplasmic or abnormal p21 expression is induced by either the abnormal/mutated p53 or any other pathway independent of p53.
Key words: p53, p21, cdk2, Immunohistochemistry, Tumour
Introduction
          Cancer is considered as the most frequent cause of deaths in canines and felines [1]. Diagnosis and prognosis of canine tumours represents the major challenge to veterinary oncologists as it is very difficult to assess the likely nature of a tumour by observing its site, gross appearance, history and histopathology. Tumour markers comprise a wide spectrum of biomolecules, either synthesized in excess or reduced concentration as a result of neoplastic cells [2]. The search for better prognostic markers and predictive factors is now focused on molecular mechanism which underlies tumour behaviour such as altered cell cycle progression and proliferation. 
          Uncontrolled proliferation of the cells is a hallmark of neoplastic cells. Therefore, genes and proteins regulating the transition of the GI to S phase of the cell cycle have been implicated in the development of various types of human and animal cancers. Disregulation of the cell cycle in carcinogenesis is prerequisite which enables the cell to divide uncontrollably as the mechanisms for the cell cycle regulation are disrupted. Most important among these G1 to S phase cell cycle regulators is the p53 and the downstream regulators like p21 and cdk2 [3]. Alterations in p53 function can result in loss of p21 expression and may be one of the mechanisms by which altered p53 influences tumour progression [4]. Similarly, mutated p53 will disturb the pathway leading to accumulation of cdk2 and failure of G1 arrest.
Expression of p21 protein in the cells is mainly induced by p53 in response to several cellular insults but many other stimuli can induce p21 expression and cell cycle arrest independent of p53 [5].  P53 independent induction of p21 expression in various neoplastic cells in human breast cancer and the canine MDCK cell line  was reported in earlier studies [6,7]. Therefore, the present investigation was targeted to evaluate the expression and localization of p21 in relation with p53 and cdk2 in canine tumours.
Materials and methods
Tissue samples: Tissue samples were collected from 57 dog cases suspected for tumourous growths presented to the RVP, Indian Veterinary Research Institute (IVRI) and other pet clinics in India. Three tumour samples were collected from post mortem cases at Division of Pathology, IVRI. The tumour masses were collected in 10% neutral buffered formalin (NBF) for histological and immunohistochemical studies. 
Histopathology: After fixation in 10% NBF, tissue samples were cut to 1.5 mm thickness and given overnight washing under running tap water. The tissue samples were then dehydrated by passing through ascending grades of ethyl alcohol, cleared in xylene and embedded in paraffin blocks. The sections were cut at 4-5� thickness and stained by Haematoxylin & Eosin (H&E) stain as per standard procedure [8].
Immunohistochemical staining: The duplicate sections were taken on 3-aminopropyl-triethoxysilane (Sigma Chemicals, USA) coated slides [9]. Deparaffinization and rehydration of tissue sections was done by immersing in xylene and descending grades of ethanol for 5 minute each at room temperature, respectively. Antigen unmasking was performed by subjecting the tissue sections to microwave heating in a couplin jar containing trisodium citrate buffer, pH 6.0, for 5x3 minutes. Quenching of endogenous peroxidases was done in 3% hydrogen peroxide in absolute methanol for 30 minutes. Then sections were covered with blocking serum (Santa Cruz, USA) and incubated in humidified chamber for 1 hour at room temperature. Slides were then rinsed in PBS for 15 min (thrice, 5 min each). Then sections were incubated with primary antibodies viz.  rabbit polyclonal anti-p53 (1:50 dilution; Sigma, USA),  rabbit polyclonal anti-p21 (1:50 dilution; Santa Cruz, USA) and rabbit polyclonal anti cdk2 (1:50 dilution; Sigma, USA) for overnight in humidified chamber. The negative controls were covered with PBS only. Goat anti-rabbit HRPO conjugated IgG (1:40 dilution, Santa Cruz, USA) was applied to moist sections and incubated for 1 hour in humidified chamber. DAB (Sigma, USA) was used as substrate and sections were then counterstained lightly for 3-5 min with Mayer�s haematoxylin (Sigma, MHS-16).
IHC Scoring:  The immunostaining was evaluated by counting positive nuclei and/or cytoplasm in ten representative high-power fields (hpf). The proportion of positive neoplastic cells to total number of cells in each field was calculated to be expressed as percentage and scored [10]. Briefly, sections with 0 to 5 percent positive cells were scored as �0�,  5 to 20 percent positive cells scored as �1�, 20 to 50 percent positive cells scored as �2� and 50 to 100 percent positive cells scored as �3�.
Results
Histopathological evaluation
Histopathological examination revealed that 46/57 tissue samples were showing presence of neoplastic cells, of which 31 were skin tumours and 15 were visceral/mucosal tumours. Among them 19 cases were benign and 27 were malignant. Out of 19 benign tumours 13 (68.42%) were skin tumours and 6 (31.58%) were visceral tumours. Skin benign tumours included perianal gland adenoma (4), sebaceous adenoma (3), cutaneous fibroma (2), ceruminous gland cystadenoma (1), leiomyoma (1), cutaneous haemangioma (1) and cutaneous melanoma (1) while visceral/mucosal benign tumours includes  fibromatous epulis (2), acanthomatous epulis (1), sertoli cell tumour (1), seminoma (1) and parasitic fibroma of aorta (1).
Out of the total 27 malignant tumours,  18 (66.67%) were skin tumours comprising of  mast cell tumour  (3), perianal gland carcinoma (3), cutaneous fibrosarcoma (3), basal cell carcinoma (3), squamous cell carcinoma (2), malignant histiocytoma (1), cutaneous haemangiosarcoma (1), cutaneous liposarcoma (1) and  cutaneous malignant melanoma (1). The 9 malignant   (33.33%) visceral/mucosal tumours were transmissible venereal tumour  (6), oral malignant melanoma (2) and lymphosarcoma (1).
Expression of p53, p21 and cdk2 biomarkers
Immunohistochemical staining for p53, p21 and cdk2 in different tumours revealed different expression patterns. p53 expression was observed only in the nucleus whereas p21 and cdk2 showed expression in cytoplasm and/or nucleus.  A total of 26 representative tumour cases were studied for the immunohistochemical expression of these biomarkers. Expression of p53, p21 and cdk2 was observed in 84.62%, 69.23% and 69.23% cases, respectively. The details of scoring of expression of p53, p21 and cdk2 is given in table 1. In skin tumours, p53 over expression was reported in 75% of the cases, p21 in 62.5% cases and cdk2 in 68.75% cases while in visceral/mucosal tumours p53 over expression was reported in 100% of the cases, p21 in 80% cases and cdk2 in 70% cases. 
The immunohistochemical staining revelaed different patterns of expression of these biomarkers in individual cases. Seven different patterns of expression were identified based on the expression of p53, p21 and cdk2 and the localization of these biomarkers in the neoplastic cells (Table 2). 
Discussion
In the present study, the expression patterns of p53, p21 and cdk2, which regulate the transition of G1 to S phase of cell cycle, were evaluated.  The expression of p53 was detected in 22 (84.62%) whereas p21 and cdk2 expressions were observed in 18 (69.23%) cases each. p53 expression was recorded mainly in the nucleus whereas p21 and cdk2 showed expression in cytoplasm and/or nucleus. Different patterns of expressions of p53, p21 and cdk2 emerged when they were evaluated as individual cases. Expression pattern of p53+p21+ was detected in 15 cases whereas in 3 cases no association between p21 and p53 expression levels could be detected. p21 has been implicated in mechanisms of cell-cycle arrest that allow cellular DNA repair, differentiation and apoptosis by the interaction with cyclin A-cdk2 and cyclin D-cdk4 complexes [11]. Expression of p21 is mainly induced by p53 in response to many cellular stress stimuli but several other factors can induce p21 expression and cell cycle arrest independent of p53 [12].
Out of the 15 cases which showed p53+p21+ expression pattern in present study, 11 showed cytoplasmic expression of p21 (p21C+) along with increased cdk2 expression (cdk2+) whereas other 4 showed nuclear expression of p21 (p21N+) with absence of cdk2 expression (cdk2-). It was reported in earlier studies that cytoplasmic p21 might inhibit apoptotic death by binding and inhibiting the apoptosis signal-regulating kinase 1 or it might be unable to inhibit nuclear cdk2, which leads to over expression of cdk2 [13,14]. Further, the accumulation of cytosolic p21 could lead this protein to act as an oncogene that promoted cell survival and thus tumour development [15,16]. High p21C+ expression associated with high levels of p53 expression suggested that either p21C+ was presumably expressed independently of p53 or p53 was mutated which was not able to induce the expression of p21N+. The other 4 cases which showed nuclear expression of p21 and absence of cdk2 staining indicated the normal functioning of p53 in which the cell cycle progression is arrested. 
Expression of cdk2 in cancer has been reported based on the nuclear and cytoplasmic expression of the protein. Cytoplasmic expression of cdk2 was correlated with the increasing tumour grade [17]. The oncogenic forms of cyclin E in complex with cdk2 are preferentially mislocalized to the cytoplasm. Although the expression of cdk2 in present study was detected in both the benign and malignant tumours but its cytoplasmic localization in the benign tumours indicated that it might become malignant in later course of the disease.
Expression patterns with p53+ p21- cdk2+, p53+ p21- cdk2-, p53- p21+ cdk2+, p53-p21+cdk2-  and p53- p21- cdk2- were also observed in present investigation. Cases showing p53+ p21- cdk2+ were suspected for expressing the mutated form of p53 since the later is not able to activate the expression of normal p21N and thus the levels of cdk2 will be increased. It was reported that the function of p21 might not be retained after the mutation of p53 in cancers and hence its expression might be absent or reduced [18,19].  Mechanism for the development of p53+ p21- cdk2-, p53- p21+ cdk2+, p53- p21+ cdk2- and p53-p21- cdk2- expression patterns indicated the involvement of some other genes or pathways which were independent of p53. The absence of cdk2 expression in p53+p21-cdk2- might be due to the activation of some other factors by mutated p53 or mutant p53 protein itself which can inhibit normal p53 [20].
From present study it can be concluded that cytoplasmic or abnormal p21 expression is induced by the abnormal/mutated p53 and this cytoplasmic p21 is unable to inhibit cdk2 leading to failure of cell cycle arrest. Further, it suggests several other pathways associated with p21 expression in the canine tumour genesis which are independent of p53 expression.
Acknowledgments
The authors are thankful to the Director, Indian Veterinary Research Institute, Izatnagar, for providing the necessary facilities for carrying out the present research work. The first author is grateful to the Indian Council of Agricultural Research, New Delhi, for providing financial assistance in the form of scholarship during the course of the study.

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TABLES

Table 1: Immunohistochemistry scoring from 0-3 (based on percentage of stained cells) for p53, p21 and cdk2.
S. no.Sample IdentificationHistopathological diagnosisp53p21cdk21.ZT-1Fibroma203 N+C2.ZT-3TVT32 C1 C3.ZT-4Haemangiosarcoma2004.ZT-6Liposarcoma01 C1 C5.ZT-7Basal cell carcinoma31 C3 N+C6.ZT-8Sebaceous adenoma32 C1 N+C7.ZT-9TVT32N08.ZT-11Malignant histiocytoma3009.ZT-12Lymphosarcoma31 C1C10.ZT-15Mast cell tumour22 C1 N+C11.ZT-16Acanthomatous epulis32 C1 C12.ZT-20TVT31 N013.ZT-21TVT31 C1 N+C14.ZT-22Mebomian gland adenoma31 C2 C15.ZT-24Seminoma31 C1 C16.ZT-25Fibromatous epulis32 N017.ZT-27TVT301 N+C18.ZT- 29Leomyoma101 N+C19.ZT-30Fibrosarcoma21 C2 N+C20.ZT-32Perianal gland adenoma203 N+C21.ZT-37Perianal gland carcinoma02 N022.ZT-42Mast cell tumour31 N023.ZT-45Basal cell carcinoma03 C2 C24.ZT-46Fibrosarcoma00025.ZT-50Sertoli cell tumour202 C26.ZT-51Perianal gland adenoma22 C1 CNote: N= nuclear staining, C= cytoplasmic staining, (N+C)= Both







Table 2: Different patterns of expression of p53, p21 and cdk2 observed.   
S. No.p53p21cdk2No. of cases1.+-+52.+     + (c)+113.+    +(n)-44.+--25.-++26.-+-17.---1













FIGURE LEGENDS

Figure 1: Sebaceous adenoma: Very high nuclear expression of p53. (DAB �400) 
Figure 2: Malignant histiocytoma:  Moderate nuclear expression of p53. (DAB �400) 
Figure 3: TVT:  Increased nuclear expression of p53. (DAB �400)
Figure 4: Sebaceous adenoma: Moderate cytoplasmic expression of p21 (DAB �400) 
Figure 5: TVT:  Moderate p21 expression in both  cytoplasm as well as nucleus. (DAB0?DL\mn����	6	7	N	h	�	�	�	�	�	�	�	
 
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Figure7: Sebaceous adenoma : Mild expression of CDK2 in cytoplasm and nucleus.    
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Figure 8: TVT:  Mild CDK2 expression in both cytoplasm as well as nucleus. (DAB �400) 
Figure 9: Basal cell carcinoma: Moderate expression of CDK2 in nucleus as well as 
                 cytoplasm, (DAB �400)























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