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Association of gastrointestinal gland cancer susceptibility loci with esophageal carcinoma among the Chinese Han population: a case–control study

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Tumor Biology

Abstract

Esophageal carcinoma (EC) is a common malignancy worldwide. Previous studies indicated that gastrointestinal gland cancer and EC share some susceptibility loci. Our aim was to identify new single nucleotide polymorphisms (SNPs) associated with EC by investigating whether known gastrointestinal cancers susceptibility loci are found in EC patients. A Chinese Han population case–control study was conducted to assess SNP associations with EC risk. Twenty-six SNPs were selected from gastrointestinal cancer susceptibility loci, and 360 EC patients and 310 controls were genotyped for these SNPs using Sequenom MassARRAY technology. The association of SNP frequencies with EC was analyzed by chi-square tests, and genetic model analysis. After Hardy–Weinberg equilibrium (HWE) p value screening, we excluded two SNPs. Based on chi-square tests, the minor alleles of rs13294589 (p = 0.046) and rs4924935 (p = 0.046) were correlated with reduced EC risk and rs4269383 (p = 0.010) and rs10953615 (p = 0.036) were correlated with increased EC risk. In the genetic model analyses, we found that the minor alleles “T” of rs401681, “A” of rs10088262, and “C” of rs4924935 may reduce the risk of EC. rs401681 has previously been reported to be associated with EC. To the best of our knowledge, we are the first to report an association of the other five SNPs with EC. Our findings provide evidence for the genetic variants associated with susceptibility to EC in the Chinese Han population, which might be used as potential molecular markers for detecting susceptibility to EC in Chinese Han people.

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References

  1. Xu X, Guan X, Tao H, Yang K, Bai Y. An association study on genetic polymorphisms of Rab37 gene with the risk of esophageal squamous cell carcinoma in a Chinese Han population. Int J Med Sci. 2013;10(3):235–42. doi:10.7150/ijms.5524.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Bray F, Ren JS, Masuyer E, Ferlay J. Global estimates of cancer prevalence for 27 sites in the adult population in 2008. Int J Cancer J Int Du Cancer. 2013;132(5):1133–45. doi:10.1002/ijc.27711.

    Article  CAS  Google Scholar 

  3. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer J int Du Cancer. 2015;136(5):E359–86. doi:10.1002/ijc.29210.

    Article  CAS  Google Scholar 

  4. Chen W, Zheng R, Zhang S, Zeng H, Fan Y, Qiao Y et al. Esophageal cancer incidence and mortality in China, 2010. Thoracic Cancer. 2014.

  5. Ferlay J, Shin HR, Bray F, Forman D, Mathers C, Parkin DM. Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer. 2010;127(12):2893–917. doi:10.1002/ijc.25516.

    Article  CAS  PubMed  Google Scholar 

  6. Schottenfeld D, Fraumeni Jr JF. Cancer epidemiology and prevention. Eastbourne, UK; WB Saunders Co; 1982.

  7. Lagergren J, Bergström R, Lindgren A, Nyren O. The role of tobacco, snuff and alcohol use in the aetiology of cancer of the oesophagus and gastric cardia. Int J Cancer. 2000;85(3):340–6.

    Article  CAS  PubMed  Google Scholar 

  8. Wu M, Zhao J-K, Zhang Z-F, Han R-Q, Yang J, Zhou J-Y, et al. Smoking and alcohol drinking increased the risk of esophageal cancer among Chinese men but not women in a high-risk population. Cancer Causes Control. 2011;22(4):649–57.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Gao Y, Hu N, Han XY, Ding T, Giffen C, Goldstein AM, et al. Risk factors for esophageal and gastric cancers in Shanxi Province, China: a case–control study. Cancer Epidemiol. 2011;35(6):e91–e9.

    Article  PubMed  PubMed Central  Google Scholar 

  10. LaFramboise T, Weir BA, Zhao X, Beroukhim R, Li C, Harrington D, et al. Allele-specific amplification in cancer revealed by SNP array analysis. PLoS Comput Biol. 2005;1(6):e65. doi:10.1371/journal.pcbi.0010065.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Lerand SJ, Ireland M, Blum RW. Individual and environmental impacts on sexual health of Caribbean youth. The Scientific World Journal. 2006;6:707–17. doi:10.1100/tsw.2006.150.

    Article  PubMed  Google Scholar 

  12. Wu C, Hu Z, He Z, Jia W, Wang F, Zhou Y, et al. Genome-wide association study identifies three new susceptibility loci for esophageal squamous-cell carcinoma in Chinese populations. Nat Genet. 2011;43(7):679–84. doi:10.1038/ng.849.

    Article  CAS  PubMed  Google Scholar 

  13. Ek WE, Levine DM, D’Amato M, Pedersen NL, Magnusson PK, Bresso F, et al. Germline genetic contributions to risk for esophageal adenocarcinoma, Barrett’s esophagus, and gastroesophageal reflux. J Natl Cancer Inst. 2013;105(22):1711–8. doi:10.1093/jnci/djt303.

    Article  PubMed  PubMed Central  Google Scholar 

  14. Li S, Qian J, Yang Y, Zhao W, Dai J, Bei JX, et al. GWAS identifies novel susceptibility loci on 6p21.32 and 21q21.3 for hepatocellular carcinoma in chronic hepatitis B virus carriers. PLoS Genet. 2012;8(7):e1002791. doi:10.1371/journal.pgen.1002791.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Low SK, Kuchiba A, Zembutsu H, Saito A, Takahashi A, Kubo M, et al. Genome-wide association study of pancreatic cancer in Japanese population. PLoS One. 2010;5(7):e11824. doi:10.1371/journal.pone.0011824.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Wu L, Goldstein AM, Yu K, Yang XR, Rabe KG, Arslan AA, et al. Variants associated with susceptibility to pancreatic cancer and melanoma do not reciprocally affect risk. Cancer Epidemiol Biomarkers Prev. 2014;23(6):1121–4. doi:10.1158/1055-9965.EPI-13-0627.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Campa D, Rizzato C, Bauer AS, Werner J, Capurso G, Costello E, et al. Lack of replication of seven pancreatic cancer susceptibility loci identified in two Asian populations. Cancer Epidemiol Biomarkers Prev. 2013;22(2):320–3. doi:10.1158/1055-9965.EPI-12-1182.

    Article  CAS  PubMed  Google Scholar 

  18. Wu C, Miao X, Huang L, Che X, Jiang G, Yu D, et al. Genome-wide association study identifies five loci associated with susceptibility to pancreatic cancer in Chinese populations. Nat Genet. 2012;44(1):62–6. doi:10.1038/ng.1020.

    Article  CAS  Google Scholar 

  19. Wu C, Kraft P, Stolzenberg-Solomon R, Steplowski E, Brotzman M, Xu M, et al. Genome-wide association study of survival in patients with pancreatic adenocarcinoma. Gut. 2014;63(1):152–60. doi:10.1136/gutjnl-2012-303477.

    Article  CAS  PubMed  Google Scholar 

  20. Petersen GM, Amundadottir L, Fuchs CS, Kraft P, Stolzenberg-Solomon RZ, Jacobs KB, et al. A genome-wide association study identifies pancreatic cancer susceptibility loci on chromosomes 13q22.1, 1q32.1 and 5p15.33. Nat Genet. 2010;42(3):224–8. doi:10.1038/ng.522.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Cha PC, Zembutsu H, Takahashi A, Kubo M, Kamatani N, Nakamura Y. A genome-wide association study identifies SNP in DCC is associated with gallbladder cancer in the Japanese population. J Hum Genet. 2012;57(4):235–7. doi:10.1038/jhg.2012.9.

    Article  CAS  PubMed  Google Scholar 

  22. Yang Q, Guo CY, Cupples LA, Levy D, Wilson PW, Fox CS. Genome-wide search for genes affecting serum uric acid levels: the Framingham Heart Study. Metabolism. 2005;54(11):1435–41. doi:10.1016/j.metabol.2005.05.007.

    Article  CAS  PubMed  Google Scholar 

  23. Gabriel S, Ziaugra L, Tabbaa D. SNP genotyping using the Sequenom MassARRAY iPLEX platform. Curr Protocols Human Genet. 2009:2.12. 1-2. 6.

  24. Thomas RK, Baker AC, DeBiasi RM, Winckler W, LaFramboise T, Lin WM, et al. High-throughput oncogene mutation profiling in human cancer. Nat Genet. 2007;39(3):347–51.

    Article  CAS  PubMed  Google Scholar 

  25. Simon E. Chi2 test for two by two percentage comparison table. Gynecol Obstetrique Fertilite. 2009;37(1):95–6. doi:10.1016/j.gyobfe.2008.11.005.

    Article  CAS  Google Scholar 

  26. Sole X, Guino E, Valls J, Iniesta R, Moreno V. SNPStats: a web tool for the analysis of association studies. Bioinformatics. 2006;22(15):1928–9. doi:10.1093/bioinformatics/btl268.

    Article  CAS  PubMed  Google Scholar 

  27. Bland JM, Altman DG. Statistics notes. The odds ratio. BMJ. 2000;320(7247):1468.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21(2):263–5. doi:10.1093/bioinformatics/bth457.

    Article  CAS  PubMed  Google Scholar 

  29. Shi YY, He L. SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res. 2005;15(2):97–8. doi:10.1038/sj.cr.7290272.

    Article  CAS  PubMed  Google Scholar 

  30. Yin J, Wang L, Zheng L, Wang X, Shi Y, Shao A, et al. TERT-CLPTM1L Rs401681 C>T polymorphism was associated with a decreased risk of esophageal cancer in a Chinese population. PLoS One. 2014;9(7):e100667. doi:10.1371/journal.pone.0100667.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zhao DP, Yang CL, Zhou X, Ding JA, Jiang GN. Association between CLPTM1L polymorphisms (rs402710 and rs401681) and lung cancer susceptibility: evidence from 27 case-control studies. Mol Genet Genomics: MGG. 2014;289(5):1001–12. doi:10.1007/s00438-014-0868-7.

    Article  CAS  PubMed  Google Scholar 

  32. James MA, Wen W, Wang Y, Byers LA, Heymach JV, Coombes KR, et al. Functional characterization of CLPTM1L as a lung cancer risk candidate gene in the 5p15.33 locus. PLoS One. 2012;7(6):e36116. doi:10.1371/journal.pone.0036116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Zhang Y, Sun Y, Chen T, Hu H, Xie W, Qiao Z, et al. Genetic variations rs11892031 and rs401681 are associated with bladder cancer risk in a Chinese population. Int J Mol Sci. 2014;15(11):19330–41. doi:10.3390/ijms151119330.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu C, Wang Y, Huang H, Wang C, Zhang H, Kong Y, et al. Association between CLPTM1L-TERT rs401681 polymorphism and pancreatic cancer risk among Chinese Han population. Tumour Biol. 2014;35(6):5453–7. doi:10.1007/s13277-014-1711-9.

    Article  CAS  PubMed  Google Scholar 

  35. Yamamoto-Ibusuki M, Yamamoto Y, Fujiwara S, Sueta A, Yamamoto S, Hayashi M, et al. C6ORF97-ESR1 breast cancer susceptibility locus: influence on progression and survival in breast cancer patients. Eur J Human Genet: EJHG. 2014. doi:10.1038/ejhg.2014.219.

    PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work is supported by the National 863 High-Technology Research and Development Program (No. 2012AA02A519). We are grateful to the patients and control subjects for their participation in this study. We also thank the clinicians and hospital staff who contributed to the sample and data collection for this study. For sample collection, we thank the First Affiliated Hospital of Xi’an Jiaotong University and Tangdu Hospital for their assistance. We would also like to thank the BioScience Writers for their assistance in the preparation of this manuscript.

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Correspondence to Tianbo Jin or Yong Zhang.

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Junqi Wang and Baoping Zhang are joint first authors.

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Wang, J., Zhang, B., Yang, Z. et al. Association of gastrointestinal gland cancer susceptibility loci with esophageal carcinoma among the Chinese Han population: a case–control study. Tumor Biol. 37, 1627–1633 (2016). https://doi.org/10.1007/s13277-015-3945-6

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  • DOI: https://doi.org/10.1007/s13277-015-3945-6

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