DOI QR코드

DOI QR Code

Association Analysis of Single Nucleotide Polymorphisms in miR-146a and miR-196a2 on the Prevalence of Cancer in Elderly Japanese: A Case-Control Study

  • Parlayan, Cuneyd (Department of Molecular Epidemiology, Medical Research Institute) ;
  • Ikeda, Shinobu (Department of Molecular Epidemiology, Medical Research Institute) ;
  • Sato, Noriko (Department of Molecular Epidemiology, Medical Research Institute) ;
  • Sawabe, Motoji (Department of Molecular Pathology, Graduate School of Health Care Sciences, Tokyo Medical and Dental University) ;
  • Muramatsu, Masaaki (Department of Molecular Epidemiology, Medical Research Institute) ;
  • Arai, Tomio (Department of Pathology, Tokyo Metropolitan Geriatric Hospital)
  • Published : 2014.03.01

Abstract

Background: Single nucleotide polymorphisms (SNPs) affecting microRNA (miR) sequences may influence carcinogenesis. Our current study primarily aimed to confirm previously conducted association studies between rs2910164 found on miR-146a, and rs11614913 located on miR-196a2 polymorphisms and cancer phenotypes in the Japanese elderly population. rs2910164 (G/C) and rs11614913 (T/C) polymorphisms were determined by genotyping on the samples collected from 1,351 consecutive autopsy cases registered in the Japanese SNPs for geriatric research (JG-SNP) data base. Cancer samples were systematically reviewed, pathologically verified and assessed with respect to miR-146a and miR-196a2 genotypic variation. The current study covered 726 males and 625 females with a mean age of $80.3{\pm}8.9$ years. The study included 524 subjects without cancer and 827 subjects with at least one type of cancer, such as gastric (n=160), lung (n=148), colorectal (n=116) or others. Males with cancers (n=467) were more numerous than females (n=360). Both rs11614913 (CT: TT adjusted odds ratio (OR) 95% confidence interval (95%CI)=0.98 (0.75-1.28), p=0.873, CC: TT adjusted OR (95%CI)=1.06 (0.76-1.47), p=0.737, CT+CC: TT, adjusted OR (95%CI)=0.99 (0.77-1.29), p=0.990), and rs2910164 (CG: CC adjusted OR (95%CI)=1.12 (0.87-1.44), p=0.383, GG: CC adjusted OR (95%CI)=1.03 (0.71-1.48), p=0.887, CG+GG: CC adjusted OR (95%CI)=1.10 (0.87-1.39), p=0.446) polymorphisms did not show significant association with overall cancer in all subjects. However, "CC" genotype in rs11614913 polymorphism was significantly associated with increased gastric cancer (n=160) in all subjects (CC: CT+TT, adjusted OR (95%CI)=1.50 (1.02-2.22), p=0.040). We found that rs11614913 and rs2910164 do not pose general cancer risk, but rs11614913 may influence gastric cancer in Japanese elderly population. Confirmation of our study results requires further investigations with larger subject populations.

Keywords

References

  1. Ambros V (2004). The functions of animal microRNAs. Nature, 431, 350-5. https://doi.org/10.1038/nature02871
  2. Bartel DP (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-97. https://doi.org/10.1016/S0092-8674(04)00045-5
  3. Brennecke J, Hipfner DR, Stark A, et al (2003). bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell, 113, 25-36. https://doi.org/10.1016/S0092-8674(03)00231-9
  4. Calvo R, West J, Franklin W, et al (2000). Altered HOX and WNT7A expression in human lung cancer. Proc Natl Acad Sci USA, 97, 12776-81. https://doi.org/10.1073/pnas.97.23.12776
  5. Christensen BC, Avissar-Whiting M, Ouellet LG, et al (2010). Mature miRNA sequence polymorphism in MIR196A2 is associated with risk and prognosis of head and neck cancer. Clin Cancer Res, 16, 3713-20. https://doi.org/10.1158/1078-0432.CCR-10-0657
  6. Chu H, Wang M, Shi D, et al (2011). Hsa-miR-196a2 Rs11614913 Polymorphism Contributes to cancer susceptibility: evidence from 15 case-control Studies. PLoS ONE, 6, 18108. https://doi.org/10.1371/journal.pone.0018108
  7. Du W, Ma XL, Zhao C, et al (2014). Associations of single nucleotide polymorphisms in miR-146a, miR-196a, miR-149 and miR-499 with colorectal cancer susceptibility. Asian Pac J Cancer Prev, 15, 1047-55. https://doi.org/10.7314/APJCP.2014.15.2.1047
  8. Duan S, Mi S, Zhang W, Dolan ME (2009). Comprehensive analysis of the impact of SNPs and CNVs on human microRNAs and their regulatory genes. RNA Biol, 6, 412-25. https://doi.org/10.4161/rna.6.4.8830
  9. Esquela-Kerscher A, Slack FJ (2006). Oncomirs -microRNAs with a role in cancer. Nature Rev Cancer, 6, 259-69. https://doi.org/10.1038/nrc1840
  10. Feng W, Ma YL, Zhang P, et al (2012). A genetic variant in microRNA-196a2 is associated with increased cancer risk: a meta-analysis. Mol Biol Rep, 39, 269-75. https://doi.org/10.1007/s11033-011-0735-0
  11. George PG, Gangwar R, Mandal RK, et al (2011). Genetic variation in microRNA genes and prostate cancer risk in North Indian population. Mol Biol Rep, 38, 1609-15. https://doi.org/10.1007/s11033-010-0270-4
  12. Guo H, Wang K, Xiong G, et al (2010). A functional variant in microRNA-146a is associated with risk of esophageal squamous cell carcinoma in Chinese Han. Fam Cancer, 9, 599-603. https://doi.org/10.1007/s10689-010-9370-5
  13. Hamada JI, Omatsu T, Okada F et al (2001). Overexpression of Homeobox gene HOXD3 induces coordinate expression of metastasis-related genes in human lung cancer. Int J Cancer, 93, 516-25. https://doi.org/10.1002/ijc.1357
  14. Hanahan D, Weinberg RA (2000). The hallmarks of cancer. Cell, 100, 57-70. https://doi.org/10.1016/S0092-8674(00)81683-9
  15. Hao YX, Wang JP, Zhao LF (2013). Associations between three common microRNA polymorphisms and hepatocellular carcinoma risk in Chinese. Asian Pac J Cancer Prev, 14, 6601-4. https://doi.org/10.7314/APJCP.2013.14.11.6601
  16. He B, Pan Y, Cho WC, et al (2012). The association between four genetics variants in microRNAs (rs11614913, rs2910164, rs376444, rs2292832) and cancer risk: evidence from published studies. PLoS ONE, 7, 49032. https://doi.org/10.1371/journal.pone.0049032
  17. Hezova R, Kovarikova A, Bienertova-Vasku J, et al (2012). Evaluation of SNPs in miR-196-a2, miR-27a and miR-146a as risk factors of colorectal cancer. World J Gastroenterol, 18, 2827-31. https://doi.org/10.3748/wjg.v18.i22.2827
  18. Hoffman AE, Zheng T, Yi C, et al (2009). microRNA miR-196a-2 and breast cancer: a genetic and epigenetic association study and functional analysis. Cancer Res, 69, 5970-7. https://doi.org/10.1158/0008-5472.CAN-09-0236
  19. Hong YS, Kang HJ, Kwak JY, et al (2011). Association between microrna196a2 rs11614913 genotypes and the risk of nonsmall cell lung cancer in Korean population. J Prev Med Public Health, 44, 125-30. https://doi.org/10.3961/jpmph.2011.44.3.125
  20. Hu Z, Chen J, Tian T, et al (2006). Genetic variants of miRNA sequences and non-small cell lung cancer survival. J Clin Invest, 118, 2600-8.
  21. Kent OA, Mendell JT (2006). A small piece in the cancer puzzle: microRNAs as tumor suppressors and oncogenes. Oncogene, 25, 6188-96. https://doi.org/10.1038/sj.onc.1209913
  22. Kogo R, Mimori K, Tanaka F, Komune S, Mori M (2011). Clinical significance of miR-146a in gastric cancer cases. Clin Cancer Res, 17, 4277-84. https://doi.org/10.1158/1078-0432.CCR-10-2866
  23. Kumar MS, Lu J, Mercer KL, et al (2007). Impaired microRNA processing enhances cellular transformation and tumorigenesis. Nat Genet, 39, 673-7. https://doi.org/10.1038/ng2003
  24. Kupcinskas J, Wex T, Link A, et al (2014). Gene polymorphisms of microRNAs in Helicobacter pylori-induced high risk atrophic gastritis and gastric cancer. PLoS ONE, 9, 87467. https://doi.org/10.1371/journal.pone.0087467
  25. Lehmann U, Hasemeier B, Christgen M, et al (2008). Epigenetic inactivation of microRNA gene hsa-mir-9-1 in human breast cancer. J Pathol, 214, 17-24. https://doi.org/10.1002/path.2251
  26. Li L, Sheng Y, Lv L, et al (2013). The association between two microrna variants (mir-499, mir-149) and gastrointestinal cancer risk: a meta-analysis. PLoS ONE, 8, 81967. https://doi.org/10.1371/journal.pone.0081967
  27. Li XD, Li ZG, Song XX, et al (2010). A variant in microRNA-196a2 is associated with susceptibility to hepatocellular carcinoma in Chinese patients with cirrhosis. Pathology, 42, 669-73. https://doi.org/10.3109/00313025.2010.522175
  28. Li YJ, Zhang YZ, Mao YY, et al (2014). A genetic variant in mir-146a modifies digestive system cancer risk: a meta-analysis. Asian Pac J Cancer Prev, 15, 145-50. https://doi.org/10.7314/APJCP.2014.15.1.145
  29. Linhares JJ, Azevedo M Jr, Siufi AA, et al (2012). Evaluation of single nucleotide poly morphisms in microRNAs (hsa-miR-196a2 rs11614913 C/T) from Brazilian women with breast cancer. BMC Med Genet, 13, 119. https://doi.org/10.1186/1471-2350-13-119
  30. Long XJ, Lin S, Sun YN, Zheng ZF (2012). Diabetes mellitus and prostate cancer risk in Asian countries: a meta-analysis. Asian Pac J Cancer Prev, 13, 4097-100. https://doi.org/10.7314/APJCP.2012.13.8.4097
  31. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, et al (2005). MicroRNA expression profiles classify human cancers. Nature, 435, 834-8. https://doi.org/10.1038/nature03702
  32. Lu K, Song XL, Han SL, Wang CH, Zhong N, Qi LF (2014). Potential study perspectives on mechanisms and correlations between adiposity and malignancy. Asian Pac J Cancer Prev, 15, 1057-6 0. https://doi.org/10.7314/APJCP.2014.15.2.1057
  33. Lu L, Katsaros D, de la Longrais IA, Sochirca O, Yu H (2007). Hypermethylation of let-7a-3 in epithelial ovarian cancer is associated with low insulin-like growth factor-II expression and favorable prognosis. Cancer Res, 67, 10117-22. https://doi.org/10.1158/0008-5472.CAN-07-2544
  34. Ma XP, Zhang T, Peng B, et al (2013). Association between microRNA Polymorphisms and Cancer Risk Based on the Findings of 66 Case- Control Studies. PLoS ONE, 8, 79584. https://doi.org/10.1371/journal.pone.0079584
  35. McGrowder DA, Jackson LA, Crawford TV (2012). Prostate cancer and metabolic syndrome: is there a link? Asian Pac J Cancer Prev, 13, 1-13. https://doi.org/10.7314/APJCP.2012.13.1.001
  36. Miller GJ, Miller HL, van Bokhoven A, et al (2003). Aberrant HOXC expression accompanies the malignant phenotype in human prostate. Cancer Res, 63, 5879-88.
  37. Oda K, Tanaka N, Arai T, et al (2007). Polymorphisms in proand anti-inflammatory cytokine genes and susceptibility to atherosclerosis a pathological study of 1503 consecutive autopsy cases. Hum Mol Genet, 16, 592-9.
  38. Okubo M, Tahara T, Shibata T, et al (2010). Association between common genetic variants in Pre-microRNAs and gastric cancer risk in Japanese population. Helicobacter, 15, 524-31. https://doi.org/10.1111/j.1523-5378.2010.00806.x
  39. Okubo M, Tahara T, Shibata T, et al (2010). Association between common genetic variants in pre-microRNAs and the clinicopathological characteristics and survival of gastric cancer patients. Exp Ther Med, 1, 1035-40.
  40. Peng S, Kuang Z, Sheng C, et al (2010). Association of microRNA-196a-2 gene polymorphism with gastric cancer risk in a Chinese population. Dig Dis Sci, 55, 2288-93. https://doi.org/10.1007/s10620-009-1007-x
  41. Permuth-Wey J, Thompson RC, Nabors B, et al (2011). A functional polymorphism in the pre-miR-146a gene is associated with risk and prognosis in adult glioma. J Neurooncol, 105, 639-46. https://doi.org/10.1007/s11060-011-0634-1
  42. Pillai RS, Bhattacharyya SN, Artus CG, et al (2005). Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science, 309, 1573-6. https://doi.org/10.1126/science.1115079
  43. Qi P, Dou TH, Geng L, et al (2010). Association of a variant in MIR 196A2 with susceptibility to hepatocellular carcinoma in male Chinese patients with chronic hepatitis B virus infection. Hum Immunol, 71, 621-6. https://doi.org/10.1016/j.humimm.2010.02.017
  44. Raisch J, Darfeuille-Michaud A, Nguyen HTT (2013). Role of microRNAs in the immune system, inflammation and cancer. World J Gastroenterol, 19, 2985-96. https://doi.org/10.3748/wjg.v19.i20.2985
  45. Ryan BM, Robles AI, Harris CC (2010). Genetic variation in microRNA networks: the implication for cancer research. Nat Rev Cancer, 10, 389-402. https://doi.org/10.1038/nrc2867
  46. Saunders MA, Liang H, Li WH (2007). Human polymorphism at microRNAs and microRNA target sites. Proc Natl Acad Sci USA, 104, 3300-5. https://doi.org/10.1073/pnas.0611347104
  47. Sawabe, M, Arai T, Kasahara I, et al (2004). Developments of geriatric autopsy database and Internet-based database of Japanese single nucleotide polymorphisms for geriatric research (JG-SNP). Mech Ageing Dev, 125, 547-52. https://doi.org/10.1016/j.mad.2004.06.005
  48. Shen J, Ambrosome CB, DiCioccio RA, et al (2008). A functional polymorphism in the miR-146a gene and age of familial breast/ovarian cancer diagnosis. Carcinogenesis, 29, 1963-6. https://doi.org/10.1093/carcin/bgn172
  49. Sherr CJ (2004). Principles of tumor suppression. Cell, 116, 235-46. https://doi.org/10.1016/S0092-8674(03)01075-4
  50. Srivastava K, Srivastava A (2012). Comprehensive review of genetic association studies and meta-analyses on miRNA polymorphisms and cancer risk. PLoS ONE, 7, 50966. https://doi.org/10.1371/journal.pone.0050966
  51. Sun G, Yan J, Noltner K, Feng J, et al (2009). SNPs in human miRNA genes affect biogenesis and function. RNA, 15, 1640-51. https://doi.org/10.1261/rna.1560209
  52. Taganov KD, Boldin MP, Chang KJ, Baltimore D (2006). NF-$\kappa{B}$-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc Natl Acad Sci USA, 103, 12481-6. https://doi.org/10.1073/pnas.0605298103
  53. Takei K, Ikeda S, Arai T, et al (2008). Lympotoxin-alpha polymorphisms and presence of cancer in 1,536 consecutive autopsy cases. BMC Cancer, 8, 235. https://doi.org/10.1186/1471-2407-8-235
  54. Tian T, Shu Y, Chen J, et al (2009). A functional genetic variant in microRNA-196a2 is associated with increased susceptibility of lung cancer in Chinese. Cancer Epidemiol Biomarkers Prev, 18, 1183-7. https://doi.org/10.1158/1055-9965.EPI-08-0814
  55. Tian T, Xu Y, Dai J, et al (2010). Functional polymorphisms in two pre-microRNAs and cancer risk: a meta-analysis. Int J Mol Epidemiol Genet, 1, 358-66.
  56. Wang J, Bi J, Liu X, et al (2012). Has-miR-146a polymorphism (rs2910164) and cancer risk: meta-analysis of 19 casecontrol studies. Mol Bio Rep, 39, 4571-9. https://doi.org/10.1007/s11033-011-1247-7
  57. Wang Z, Cao Y, Jiang C, et al (2012). Lack of association of two common polymorphisms rs2910164 and rs11614913 with susceptibility to hepatocellular carcinoma: a meta-analysis. PLoS ONE, 7, 40039. https://doi.org/10.1371/journal.pone.0040039
  58. Wienholds E, Kloosterman WP, Miska E, et al (2005). MicroRNA expression in zebrafish embryonic development. Science, 309, 310-1. https://doi.org/10.1126/science.1114519
  59. Woo HY, Park H, Kwon MJ, Chang Y, Ryu S (2012). Association of prostate specific antigen concentration with lifestyle characteristics in Korean men. Asian Pac J Cancer Prev, 13, 5695-9. https://doi.org/10.7314/APJCP.2012.13.11.5695
  60. Wu D, Wang F, Dai WQ, et al (2013). The miR-146a rs2910164 G > C polymorphism and susceptibility to digestive cancer in Chinese. Asian Pac J Cancer Prev, 14, 399-403. https://doi.org/10.7314/APJCP.2013.14.1.399
  61. Xu B, Feng NH, Li PC, et al (2010). A functional polymorphism in Pre-miR-146a gene is associated with prostate cancer risk and mature miR-146a expression in vivo. Prostate, 70, 467-72.
  62. Xu T, Zhu Y, Wei QK, et al (2008). A functional polymorphism in the miR-146a gene is associated with the risk for hepatocellular carcinoma. Carcinogenesis, 29, 2126-31. https://doi.org/10.1093/carcin/bgn195
  63. Xu W, Xu J, Liu S, et al (2011). Effects of common polymorphisms rs11614913 in miR-196a2 and rs2910164 in miR-146a on cancer susceptibility: a meta-analysis. PLoS ONE, 6, 20471. https://doi.org/10.1371/journal.pone.0020471
  64. Xu Y, Gu L, Pan Y, et al (2013). Different effects of three polymorphisms in MicroRNAs on cancer risk in Asian population: evidence from published literatures. PLoS ONE, 8, 65123. https://doi.org/10.1371/journal.pone.0065123
  65. Ye Y, Wang KK, Gu J, et al (2008). Genetic variations in microRNA-related genes are novel susceptibility loci for esophageal cancer risk. Cancer Prev Res, 1, 460-9. https://doi.org/10.1158/1940-6207.CAPR-08-0135
  66. Yekta S, Shih IH, Bartel DP (2004). MicroRNA- directed cleavage of HOXB8 mRNA. Science, 304, 594-6. https://doi.org/10.1126/science.1097434
  67. Yuan Z, Zeng X, Yang D, et al (2013). Effects of common polymorphism rs11614913 in hsa-mir-196a2 on lung cancer risk. PLoS ONE, 8, e61047. https://doi.org/10.1371/journal.pone.0061047
  68. Zeng Y, Sun QM, Liu NN, et al (2010). Correlation between pre-miR-146a C/G polymorphism and gastric cancer risk in Chinese population. World J Gastroenterol, 16, 3578-83. https://doi.org/10.3748/wjg.v16.i28.3578
  69. Zhang H, Su YL, Yu H, Qian BY (2012). Meta-Analysis of the Association between Mir-196a-2 Polymorphism and Cancer Susceptibility. Cancer Biol Med, 9, 63-72.
  70. Zhang J, Wang R, Ma YY, et al (2013). Association between single nucleotide polymorphisms in miRNA196a-2 and miRNA146a and susceptibility to hepatocellular carcinoma in a Chinese population. Asian Pac J Cancer Prev, 14, 6427-31. https://doi.org/10.7314/APJCP.2013.14.11.6427
  71. Zhou J, Ruixue Lv R, Song X, et al (2011). Association between two genetic variants in miRNA and primary liver cancer risk in the Chinese population. DNA Cell Biol, 31, 524-30.

Cited by

  1. Association between a Polymorphism in miR-34b/c and Susceptibility to Cancer - a Meta-analysis vol.15, pp.17, 2014, https://doi.org/10.7314/APJCP.2014.15.17.7251
  2. Effects of four single nucleotide polymorphisms in microRNA-coding genes on lung cancer risk vol.35, pp.11, 2014, https://doi.org/10.1007/s13277-014-2371-5
  3. Effects of Two Common Polymorphisms rs2910164 in miR-146a and rs11614913 in miR-196a2 on Gastric Cancer Susceptibility vol.2015, pp.1687-630X, 2015, https://doi.org/10.1155/2015/764163
  4. Genetic polymorphism of miR-146a is associated with gastric cancer risk: a meta-analysis vol.26, pp.2, 2015, https://doi.org/10.1111/ecc.12355
  5. MicroRNA gene polymorphisms and the risk of colorectal cancer vol.13, pp.5, 2017, https://doi.org/10.3892/ol.2017.5885
  6. C/G polymorphism increased the risk of head and neck cancer, but overall cancer risk: an analysis of 89 studies vol.38, pp.1, 2018, https://doi.org/10.1042/BSR20171342
  7. Comprehensive Review of Genetic Association Studies and Meta-Analysis on polymorphisms in microRNAs and Urological Neoplasms Risk vol.8, pp.1, 2018, https://doi.org/10.1038/s41598-018-21749-4