Top

Published in:

01-11-2015 | Original Article

AURKA Phe31Ile polymorphism interacted with use of alcohol, betel quid, and cigarettes at multiplicative risk of oral cancer occurrence

Authors: Chi-Pin Lee, Shang-Lun Chiang, Chien-Hung Lee, Yi-Shan Tsai, Zhi-Hong Wang, Chun-Hung Hua, Yuan-Chien Chen, Eing-Mei Tsai, Ying-Chin Ko

Published in: Clinical Oral Investigations | Issue 8/2015

Abstract

Objectives

The expression levels of two DNA repair genes (CHAF1A and CHAF1B) and a chromosome segregation gene (AURKA) were susceptible to arecoline exposure, a major alkaloid of areca nut. We hypothesize that genetic variants of these genes might also be implicated in the risk of oral cancer and could be modified by substance use of betel quid or alcohol and cigarettes.

Material and methods

A case–control study, which included 507 patients with oral cancer and 717 matched controls, was performed in order to evaluate the cancer susceptibility by the tagging single-nucleotide polymorphisms (tagSNPs) in AURKA, CHAF1A, and CHAF1B using a genotyping assay and gene–environment interaction analysis.

Results

The Phe31Ile polymorphism (rs2273535, T91A) of AURKA was significantly associated with an increased risk of oral cancer (odds ratio (OR) = 2.1, 95 % confidence interval (CI) 1.2–3.5). The gene dosage of the 91A allele also showed a significant trend in risk of oral cancer (P = 0.008). Furthermore, we found the AURKA 91AA homozygote was modifiable by substance use of alcohol, betel quid, and cigarettes (ABC), leading to increased risk of oral cancer in an additive or a multiplicative model (combined effect indexes = 1.2–4.0 and 1.5–2.2, respectively). However, no association was observed between the genetic variants of CHAF1A or CHAF1B and oral cancer risk in the study.

Conclusion

These findings reveal the functional Phe31Ile polymorphism tagSNP of AURKA may be a strong susceptibility gene in ABC-related oral cancer occurrence.

Clinical relevance

The results of this betel-related oral cancer study provide the evidence of environment–gene interaction for early prediction and molecular diagnosis.

Gupta PC, Warnakulasuriya S (2002) Global epidemiology of areca nut usage. Addict Biol 7:77–83CrossRefPubMed

International Agency for Research on Cancer (IARC) (2004) Monographs on the evaluation of carcinogenic risks to humans volume 85. Betel-quid and areca-nut chewing and some areca-nut derived nitrosamines. Lyon: IARC

Ko YC, Huang YL, Lee CH, Chen MJ, Lin LM, Tsai CC (1995) Betel quid chewing, cigarette smoking and alcohol consumption related to oral cancer in Taiwan. J Oral Pathol Med 24:450–453CrossRefPubMed

Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Bouvard V et al (2007) Carcinogenicity of alcoholic beverages. Lancet Oncol 8:292–293CrossRefPubMed

Chyou PH, Nomura AM, Stemmermann GN (1995) Diet, alcohol, smoking and cancer of the upper aerodigestive tract: a prospective study among Hawaii Japanese men. Int J Cancer 60:616–621CrossRefPubMed

Lee CH, Lee KW, Fang FM, Wu DC, Tsai SM, Chen PH et al (2012) The neoplastic impact of tobacco-free betel-quid on the histological type and the anatomical site of aerodigestive tract cancers. Int J Cancer 131:E733–E743CrossRefPubMed

Lee CH, Lee KW, Fang FM, Wu DC, Shieh TY, Huang HL et al (2011) The use of tobacco-free betel-quid in conjunction with alcohol/tobacco impacts early-onset age and carcinoma distribution for upper aerodigestive tract cancer. J Oral Pathol Med 40:684–692CrossRefPubMed

Maser RS, DePinho RA (2002) Connecting chromosomes, crisis, and cancer. Science 297:565–569CrossRefPubMed

Storchova Z, Pellman D (2004) From polyploidy to aneuploidy, genome instability and cancer. Nature Rev Mol Cell Biol 5:45–54CrossRef

10.

International Agency for Research on Cancer (IARC) (1988) Monographs on the evaluation of carcinogenic risks to humans volume 44. Alcohol Drinking. Lyon: IARC

11.

Chiang SL, Jiang SS, Wang YJ, Chiang HC, Chen PH, Tu HP et al (2007) Characterization of arecoline-induced effects on cytotoxicity in normal human gingival fibroblasts by global gene expression profiling. Toxicol Sci 100:66–74CrossRefPubMed

12.

Kaufman PD, Kobayashi R, Kessler N, Stillman B (1995) The p150 and p60 subunits of chromatin assembly factor I: a molecular link between newly synthesized histones and DNA replication. Cell 81:1105–1114CrossRefPubMed

13.

Verreault A, Kaufman PD, Kobayashi R, Stillman B (1996) Nucleosome assembly by a complex of CAF-1 and acetylated histones H3/H4. Cell 87:95–104CrossRefPubMed

14.

Benhamou S, Tuimala J, Bouchardy C, Dayer P, Sarasin A, Hirvonen A (2004) DNA repair gene XRCC2 and XRCC3 polymorphisms and susceptibility to cancers of the upper aerodigestive tract. Int J Cancer 112:901–904CrossRefPubMed

15.

Elahi A, Zheng Z, Park J, Eyring K, McCaffrey T, Lazarus P (2010) The human OGG1 DNA repair enzyme and its association with orolaryngeal cancer risk. Carcinogenesis 23:1229–1234CrossRef

16.

Wang YC, Tsai YS, Huang JL, Lee KW, Kuo CC, Wang CS (2010) Arecoline arrests cells at prometaphase by deregulating mitotic spindle assembly and spindle assembly checkpoint: implication for carcinogenesis. Oral Oncol 46:255–262CrossRefPubMed

17.

Bischoff JR, Plowman GD (1999) The Aurora/Ipl1p kinase family: regulators of chromosome segregation and cytokinesis. Trends Cell Biol 9:454–459CrossRefPubMed

18.

Giet R, Petretti C, Prigent C (2005) Aurora kinases, aneuploidy and cancer, a coincidence or a real link? Trends Cell Biol 15:241–250CrossRefPubMed

19.

Wang X, Zhou YX, Qiao W, Tominaga Y, Ouchi M, Ouchi T et al (2006) Overexpression of aurora kinase A in mouse mammary epithelium induces genetic instability preceding mammary tumor formation. Oncogene 25:7148–7158CrossRefPubMed

20.

Zhou H, Kuang J, Zhong L, Kuo WL, Gray JW, Sahin A et al (1998) Tumour amplified kinase STK15/BTAK induces centrosome amplification, aneuploidy and transformation. Nat Genet 20:189–193CrossRefPubMed

21.

Kao SY, Chen YP, Tu HF, Liu CJ, Yu AH, Wu CH et al (2010) Nuclear STK15 expression is associated with aggressive behaviour of oral carcinoma cells in vivo and in vitro. J Pathol 222:99–109PubMed

22.

Reiter R, Gais P, Jutting U, Steuer-Vogt MK, Pickhard A, Bink K et al (2006) Aurora kinase A messenger RNA overexpression is correlated with tumor progression and shortened survival in head and neck squamous cell carcinoma. Clin Cancer Res 12:5136–5141CrossRefPubMed

23.

Ewart-Toland A, Briassouli P, de Koning JP, Mao JH, Yuan J, Chan F et al (2003) Identification of Stk6/STK15 as a candidate low-penetrance tumor-susceptibility gene in mouse and human. Nat Genet 34:403–412CrossRefPubMed

24.

Miao X, Sun T, Wang Y, Zhang X, Tan W, Lin D (2004) Functional STK15 Phe31Ile polymorphism is associated with the occurrence and advanced disease status of esophageal squamous cell carcinoma. Cancer Res 64:2680–2683CrossRefPubMed

25.

Cox DG, Hankinson SE, Hunter DJ (2006) Polymorphisms of the AURKA (STK15/Aurora kinase) gene and breast cancer risk (United States). Cancer Causes Control 17:81–83CrossRefPubMed

26.

Sun T, Miao X, Wang J, Tan W, Zhou Y, Yu C et al (2004) Functional Phe31Ile polymorphism in Aurora A and risk of breast carcinoma. Carcinogenesis 25:2225–2230CrossRefPubMed

27.

Dicioccio RA, Song H, Waterfall C, Kimura MT, Nagase H, McGuire V et al (2004) STK15 polymorphisms and association with risk of invasive ovarian cancer. Cancer Epidemiol Biomarkers Prev 13:1589–1594PubMed

28.

Hienonen T, Salovaara R, Mecklin JP, Jarvinen H, Karhu A, Aaltonen LA (2006) Preferential amplification of AURKA 91A (Ile31) in familial colorectal cancers. Int J Cancer 118:505–508CrossRefPubMed

29.

Lo YL, Yu JC, Chen ST, Yang HC, Fann CS, Mau YC et al (2005) Breast cancer risk associated with genotypic polymorphism of the mitosis-regulating gene Aurora-A/STK15/BTAK. Int J Cancer 115:276–283CrossRefPubMed

30.

Feik E, Baierl A, Madersbacher S, Schatzl G, Maj-Hes A, Berges R et al (2009) Common genetic polymorphisms of AURKA and prostate cancer risk. Cancer Causes Control 20:147–152CrossRefPubMed

31.

Chiang SL, Lee CP, Chang JG, Lee CH, Yeh KT, Tsai YS et al (2013) Joint effects of differentiation factor 15 and substance use of alcohol, betel quid and cigarette on risk of head and neck cancer. Head Neck Oncol 5:23

32.

Shields PG, Harris CC (1991) Molecular epidemiology and the genetics of environmental cancer. JAMA 266:681–687CrossRefPubMed

33.

Chen PH, Lee KW, Chen CH, Shieh TY, Ho PS, Wang SJ et al (2011) CYP26B1 is a novel candidate gene for betel quid-related oral squamous cell carcinoma. Oral Oncol 47:594–600CrossRefPubMed

34.

Chiang SL, Chen PH, Lee CH, Ko AM, Lee KW, Lin YC et al (2008) Up-regulation of inflammatory signalings by areca nut extract and role of cyclooxygenase-2-1195G > A polymorphism reveal risk of oral cancer. Cancer Res 68:8489–8498CrossRefPubMed

35.

Tsai YS, Lin CS, Chiang SL, Lee CH, Lee KW, Ko YC (2011) Areca nut induces miR-23a and inhibits repair of DNA double-strand breaks by targeting FANCG. Toxicol Sci 123:480–490CrossRefPubMed

36.

Lee CH, Ko AM, Yen CF, Chu KS, Gao YJ, Warnakulasuriya S et al (2012) Betel-quid dependence and oral potentially malignant disorders in six Asian countries. Br J Psychiatry 201:383–391CrossRefPubMed

37.

Ewart-Toland A, Dai Q, Gao YT, Nagase H, Dunlop MG, Farrington SM et al (2005) Aurora-A/STK15 T + 91A is a general low penetrance cancer susceptibility gene: a meta-analysis of multiple cancer types. Carcinogenesis 26:1368–1373CrossRefPubMed

38.

Lee CH, Ko AM, Warnakulasuriya S, Yin BL, Sunarjo ZRB et al (2011) Intercountry prevalences and practices of betel-quid use in south, southeast and eastern Asia regions and associated oral preneoplastic disorders: an international collaborative study by Asian betel-quid consortium of south and east Asia. Int J Cancer 129:1741–1751CrossRefPubMed

Title: AURKA Phe31Ile polymorphism interacted with use of alcohol, betel quid, and cigarettes at multiplicative risk of oral cancer occurrence
Authors: Chi-Pin Lee
Shang-Lun Chiang
Chien-Hung Lee
Yi-Shan Tsai
Zhi-Hong Wang
Chun-Hung Hua
Yuan-Chien Chen
Eing-Mei Tsai
Ying-Chin Ko
Publication date: 01-11-2015
Publisher: Springer Berlin Heidelberg
Published in: Clinical Oral Investigations / Issue 8/2015
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI: https://doi.org/10.1007/s00784-015-1432-5

Keynote webinar | Spotlight on medication adherence

Springer Medicine

AURKA Phe31Ile polymorphism interacted with use of alcohol, betel quid, and cigarettes at multiplicative risk of oral cancer occurrence

Abstract

Objectives

Material and methods

Results

Conclusion

Clinical relevance

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Objectives

Material and methods

Results

Conclusion

Clinical relevance

Please log in to get access to this content

Other articles of this Issue 8/2015

Evaluation of salivary mucins in children with deciduous and mixed dentition: comparative analysis between high and low caries-risk groups

Niobium pentoxide as radiopacifying agent of calcium silicate-based material: evaluation of physicochemical and biological properties

Association of caries increment in preschool children with nutritional and preventive variables

Risk factors for technical and biological complications with zirconia single crowns

Quantitative skeletal maturation estimation using cone-beam computed tomography-generated cervical vertebral images: a pilot study in 5- to 18-year-old Japanese children

Nonsurgical treatment of peri-implantitis using an air-abrasive device or mechanical debridement and local application of chlorhexidine. Twelve-month follow-up of a prospective, randomized, controlled clinical study