Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis

Sahu, S K; Chakrabarti, S; Roy, S D; Baishya, N; Reddy, R R; Suklabaidya, S; Kumar, A; Mohanty, S; Maji, S; Suryanwanshi, A; Rajasubramaniam, S; Asthana, M; Panda, A K; Singh, S P; Ganguly, S; Shaw, O P; Bichhwalia, A K; Sahoo, P K; Chattopadhyay, N R; Chatterjee, K; Kundu, C N; Das, A K; Kannan, R; Zorenpuii; Zomawia, E; Sema, S A; Singh, Y I; Ghosh, S K; Sharma, K; Das, B S; Choudhuri, T

doi:10.1038/oncsis.2016.31

Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis

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Published: 09 May 2016

Volume 5, page e225, (2016)
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Oncogenesis

Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis

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S K Sahu¹,
S Chakrabarti¹,
S D Roy²,
N Baishya³,
R R Reddy¹,
S Suklabaidya¹,
A Kumar¹,
S Mohanty¹,
S Maji¹,
A Suryanwanshi¹,
S Rajasubramaniam⁴,
M Asthana¹,
A K Panda^1,5,
S P Singh⁶,
S Ganguly⁷,
O P Shaw⁷,
A K Bichhwalia⁷,
P K Sahoo⁷,
N R Chattopadhyay⁷,
K Chatterjee⁷,
C N Kundu^1,8,
A K Das³,
R Kannan⁹,
Zorenpuii¹⁰,
E Zomawia¹⁰,
S A Sema²,
Y I Singh¹¹,
S K Ghosh¹²,
K Sharma¹³,
B S Das¹ &
…
T Choudhuri^1,7

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Abstract

Tumor suppressor p53 is a critical player in the fight against cancer as it controls the cell cycle check point, apoptotic pathways and genomic stability. It is known to be the most frequently mutated gene in a wide variety of human cancers. Single-nucleotide polymorphism of p53 at codon72 leading to substitution of proline (Pro) in place of arginine (Arg) has been identified as a risk factor for development of many cancers, including nasopharyngeal carcinoma (NPC). However, the association of this polymorphism with NPC across the published literature has shown conflicting results. We aimed to conduct a case–control study for a possible relation of p53 codon72 Arg>Pro polymorphism with NPC risk in underdeveloped states of India, combine the result with previously available records from different databases and perform a meta-analysis to draw a more definitive conclusion. A total of 70 NPC patients and 70 healthy controls were enrolled from different hospitals of north-eastern India. The p53 codon72 Arg>Pro polymorphism was typed by polymerase chain reaction, which showed an association with NPC risk. In the meta-analysis consisting of 1842 cases and 2330 controls, it was found that individuals carrying the Pro allele and the ProPro genotype were at a significantly higher risk for NPC as compared with those with the Arg allele and the ArgArg genotype, respectively. Individuals with a ProPro genotype and a combined Pro genotype (ProPro+ArgPro) also showed a significantly higher risk for NPC over a wild homozygote ArgArg genotype. Additionally, the strength of each study was tested by power analysis and genotype distribution by Hardy–Weinberg equilibrium. The outcome of the study indicated that both allele frequency and genotype distribution of p53 codon72 Arg>Pro polymorphism were significantly associated with NPC risk. Stratified analyses based on ethnicity and source of samples supported the above result.

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Introduction

Nasopharyngeal carcinoma (NPC) arises from the epithelial cells that cover the upper part of the throat behind the nose and near the base of the skull. The disease is treatable at an early stage but the majority of NPC patients are diagnosed at a late stage because of the exhibition of nonspecific symptoms related to other head and neck illnesses.^{1, 2} General symptoms of NPC include trismus, otitis media, hearing loss, nasal regurgitation, cranial nerve palsies, nasal twang, bleeding and pain.³ The World Health Organization histopathological grading system classifies NPC into three types: keratinizing squamous cell carcinoma; non-keratinizing differentiated carcinoma; and undifferentiated carcinoma.⁴ The American joint committee on cancer established tumor, node and metastasis classification to determine the different stages of NPC.

Epidemiological studies suggest the association of food habits (alcohol, intake of salted fish containing nitrosamine, herbal tea and herbal medicine), lifestyle (occupational exposure to formaldehyde, chlorophenol, wood dust, tobacco users) and viral infection (Epstein–Barr virus and human papilloma virus) in the etiology of NPC.^{5, 6, 7, 8, 9} However, many individuals exposed to these parameters do not develop NPC, which indicates the involvement of genetic factors. To establish a link between genetic factors and NPC development, study of single-nucleotide polymorphism (SNP) in tumor suppressor genes has been the focus of many researchers.

p53 is a well-established tumor suppressor gene located on chromosome 17p13.1. It plays a critical role in response to genotoxic stress and tries to maintain genomic stability and control proper execution of the cell cycle and apoptotic pathways.^{10, 11, 12} Deregulated function of p53 may result in loss of this regulation, resulting in uncontrolled cell proliferation and cancer development.^{13, 14, 15} Polymorphisms in p53 or target genes impair the function of the p53 signaling pathway.¹⁶ The most studied polymorphism in p53 is located in exon 4 at codon72. It carries either the CGC sequence that encodes arginine or the CCC sequence that encodes proline due to G/C transversion.^{17, 18} As a result, two allelic forms (Arg and Pro) and three genotypes (ArgArg, ArgPro and ProPro) have evolved. These allelic variants and genotypes oscillate in their binding capacity to the transcriptional factors, induction of apoptosis and repression of transformation of human cells.^{7, 18, 19, 20} Arg variants induce apoptosis more efficiently than do the Pro variants, which may be due to their ability to localize into mitochondria and regulate the release of cytochrome C into cytosol.¹⁸ The released cytochrome C in turn activates caspase-3, one of the key executioners of apoptosis.^{21, 22} This difference between Arg and Pro variants may provide the plausible cause for Pro allele’s involvement in increased susceptibility to NPC. Earlier, several studies including our present study among the populations of north-eastern India have investigated the relation between p53 codon72 Arg>Pro polymorphism and NPC risk.^{23, 24, 25, 26, 27, 28, 34} In India, this rate is comparable to that of the United Kingdom with the younger age peak in the second decade.^{35, 36} Several susceptible genes have been implicated for NPC risk, such as tumor suppressor p53, TGFβ1, IL-12 p40 and DNA repair genes.^{28, Full size table}

The p53 codon72 SNP has been studied by many groups across the world. In the Chinese population Birgander et al., in 1996, and Yung WC et al., in 1997 demonstrated no association between the mutant p53 codon72 and the risk for NPC.²³ Subsequently, Tsai et al.,²⁴ in 2002, reported that the p53 ProPro homozygote was a risk factor for NPC development. In the Thai population, Tiwawech et al.,²⁵ in 2003, reported that the p53 gene polymorphism may be associated with NPC susceptibility, particularly the Pro/Pro genotype carriers in subjects older than 40 years. In Portugal, Sousa et al.²⁶ in 2006 reported similar findings linking the susceptibility of the P53 codon72 polymorphism to NPC. Further, Hadhri-Guiga et al.,²⁷ in 2007, found that individuals carrying the ProPro homozygote carried an elevated risk for NPC in Tunisia. Similarly, ** data with previous publications, and review articles.

Full size image

The distribution of genotype frequency among controls in all these studies did not deviate from Hardy–Weinberg equilibrium since P>0.05, except the study in the north-eastern Indian population (Table 3).

Table 3 Main characteristics of studies included in the meta-analysis

Full size table

It is worth noting that the small size of samples from the north-eastern population may be due to the low incidence of NPC.

Significant associations between p53 codon72 Arg>Pro polymorphism and NPC risk were observed in the combined analysis of overall studies (Pro vs Arg: OR=1.28, 95% CI=1.17–1.40, P_OR <0.001; ProPro vs ArgArg: OR=1.70, 95% CI=1.41–2.04, P_OR<0.001; ArgPro vs ArgArg: OR=1.24, 95% CI=1.07–1.43, P_OR=0.004; ProPro+ArgPro vs ArgArg: OR=1.35, 95% CI=1.17–1.55, P_OR<0.001; ProPro vs ArgArg+ProPro: OR=1.54, 95% CI=1.18–2.01, P_OR=0.002) (Figure 2). Stratified analysis was performed according to ethnicity (Asian, Caucasian), source of sample (hospital-based and population-based studies) and in Chinese studies. The pooled ORs (Table 4) and forest plots (figures not shown) indicated that the p53 codon72 polymorphism among Asians and population-based studies was associated with the development of NPC in all five comparison models (Pro vs Arg, ProPro vs ArgArg, ArgPro vs ArgArg, ProPro+ArgPro vs ArgArg and ProPro vs ArgArg+ProPro). In Caucasian and hospital-based studies a similar risk was noted in three comparison models (Pro vs Arg, ProPro vs ArgArg and ProPro vs ArgArg+ProPro). In the overall Chinese studies NPC risk was found for all comparison models except for the recessive model. Sensitivity analyses were carried out to assess the stability of the results in the overall and stratified analysis by sequential omission of individual study each time. It was observed that the influence of individual data sets on the significance of pooled ORs was not markedly influenced by any single study (data not shown). Funnel plot and Egger’s test were conducted in five comparison models to assess the publication bias in the overall combined meta-analyses. The shape of funnel plots did not reveal any evidence of asymmetry (Figure 3). Stratified analysis in Asian, population-based and Chinese studies also showed similar trends in the shape of the funnel plots (figures not shown). Furthermore, Egger’s test in overall, Asian, population-based and Chinese studies did not show evidence of publication bias in any of the comparison models as P-values were larger than 0.05 (Table 4). However, publication bias (Funnel plot and Egger’s test) was not possible in Caucasian and hospital-based studies because the numbers of studies were less than three. Heterogeneity within and among different studies were tested with Q-value, P-value of heterogeneity (P_H) and I² statistics (Table 4). The random-effects model was used for meta-analysis if the Q-statistic was significant (P_H<0.05), which indicates heterogeneity across studies. The fixed-effect model was employed when P_H⩾0.05. In the overall population, the fixed-effect model was employed for meta-analysis of the p53 codon72 Arg>Pro polymorphism in four comparison models (Pro vs Arg, ProPro vs ArgArg, ArgPro vs ArgArg and ProPro+ArgPro vs ArgArg). However, the ProPro vs ArgArg+ArgPro comparison model showed heterogeneity among studies in the overall population and the random-effect model was used.

Table 4 Summary of overall and stratified meta-analysis results

Full size table

In the stratified analysis, the fixed-effect model was employed in all comparison models of Asian studies except the Pro vs Arg comparison, in which the random-effect model was used. In Caucasian studies the fixed-effect model was employed in all comparison models. In population-based and Chinese studies the fixed-effect model was employed in all comparison models except in the ProPro vs ArgArg+ArgPro comparison model, which reflects the combined results of the overall study. In hospital-based studies the fixed-effect model was employed in three comparison models (Pro vs Arg, ProPro vs ArgArg and ProPro vs ArgArg+ProPro) and the random-effect model in two comparison models (ArgPro vs ArgArg and ProPro+ArgPro vs ArgArg). The overall pooled results indicate that the p53 codon72 polymorphism is a significant risk factor in the pathogenesis of NPC. Stratified analyses in Asian, Caucasian, hospital-based, population-based and Chinese case–control studies corroborate this association. This meta-analysis supports the findings in north-eastern Indian populations. To our knowledge, the current study is the first to analyze the p53 codon72 polymorphism and association with NPC in the Indian population.

In conclusion, our case–control study in North Indian populations and meta-analysis results as evidenced from five genetic models suggest that the p53 codon72 Arg>Pro polymorphism could be employed as a risk factor for NPC. However, some limitations exist in the current meta-analysis. Association of p53 codon72 polymorphism with susceptibility to the histological and clinical grade of NPC patients has not been investigated because of lack of available data on the subject.

The p53 Arg form is more susceptible to degradation than the Pro form by human papilloma virus E6 protein.⁴⁹ Notably, Epstein–Barr virus infection modulates the effect of the p53 family²² and is a well-nown risk factor for NPC. Nevertheless, whether the p53 Arg or the Pro form is also susceptible to degradation by viruses or by other infectious agents needs to be investigated. Further, as there are a large number of SNPs for p53, the SNP studied in the present analysis was limited only to the functionally important one. In future, screening of all p53 and related polymorphisms in larger samples based on ethnicity in view of confounding factors such as age, sex, cigarette smoke, tobacco use, alcohol intake, dietary habit, stages of NPC and socioeconomic status is required to validate the findings.

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Acknowledgements

This work was supported by a DBT, Government of India-sponsored project (Sanction No: BT/01/NE/TBP/204(Med)/3/2011) and from an intramural grant from the Institute of Life Sciences, Bhubaneswar, India. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

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Division of Infectious Disease Biology, Institute of Life Sciences, Bhubaneswar, India
S K Sahu, S Chakrabarti, R R Reddy, S Suklabaidya, A Kumar, S Mohanty, S Maji, A Suryanwanshi, M Asthana, A K Panda, C N Kundu, B S Das & T Choudhuri
Department of Radiation Oncology, Civil Hospital, Dimapur, Nagaland, India
S D Roy & S A Sema
Dr B. Borooah Cancer Institute, ENT Department, Guwahati, Assam, India
N Baishya & A K Das
Department of Biotechnology, Regional Medical Research Centre for Tribals, Jabalpur, India
S Rajasubramaniam
Central University of Jharkhand, Brambe, Ranchi, India,
A K Panda
Department of Gastroentrology, Shri Ramachandra Bhanj Medical College, Cuttack, Odisha, India
S P Singh
Department of Biotechnology, Siksha Vhabana, Visva Bharati, Santiniketan, Bolpur, India
S Ganguly, O P Shaw, A K Bichhwalia, P K Sahoo, N R Chattopadhyay, K Chatterjee & T Choudhuri
School of Biotechnology, KIIT University, Bhubaneswar, India
C N Kundu
Cachar Cancer Hospital & Research Centre, Silchar, Assam, India
R Kannan
Civil Hospital, Aizawl, Mizoram, India
Zorenpuii & E Zomawia
Regional Institute of Medical Sciences, Department of Radiotherapy, Imphal, Manipur, India
Y I Singh
Department of Biotechnology, Assam Central University, Silchar, India
S K Ghosh
Guwahati Medical College & Hospital, Guwahati, Assam, India
K Sharma

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S K Sahu
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Sahu, S., Chakrabarti, S., Roy, S. et al. Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis. Oncogenesis 5, e225 (2016). https://doi.org/10.1038/oncsis.2016.31

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Received: 24 December 2015
Revised: 24 December 2015
Accepted: 26 January 2016
Published: 09 May 2016
Issue Date: May 2016
DOI: https://doi.org/10.1038/oncsis.2016.31
Springer Nature Limited

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Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis

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Nasopharyngeal carcinoma: current views on the tumor microenvironment's impact on drug resistance and clinical outcomes

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Association of p53 codon72 Arg>Pro polymorphism with susceptibility to nasopharyngeal carcinoma: evidence from a case–control study and meta-analysis

Abstract

Similar content being viewed by others

The association between gene polymorphisms and risk of nasopharyngeal carcinoma

Association of regenerating gene 1A single-nucleotide polymorphisms and nasopharyngeal carcinoma susceptibility in southern Chinese population

Association between polymorphisms in genes related to DNA base-excision repair with risk and prognosis of oropharyngeal squamous cell carcinoma

Introduction

References

Acknowledgements

Author information

Authors and Affiliations

Corresponding author

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Competing interests

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Nasopharyngeal carcinoma: current views on the tumor microenvironment's impact on drug resistance and clinical outcomes

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