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Associations of Single Nucleotide Polymorphisms in miR-146a, miR-196a, miR-149 and miR-499 with Colorectal Cancer Susceptibility

  • Du, Wei (Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Ma, Xue-Lei (Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Zhao, Chong (Department of Radiation Oncology, the 7th Hospital of Chengdu) ;
  • Liu, Tao (Ya'an People Hospital) ;
  • Du, Yu-Liang (Xinjin People Hospital) ;
  • Kong, Wei-Qi (West China School of Medicine, Sichuan University) ;
  • Wei, Ben-Ling (The Secend Affiliated Hospital of Xuzhou Medical College) ;
  • Yu, Jia-Yun (Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Li, Yan-Yan (Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University) ;
  • Huang, Jing-Wen (West China Hospital, Sichuan University) ;
  • Li, Zi-Kang (Ya'an People Hospital) ;
  • Liu, Lei (Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University)
  • Published : 2014.01.30

Abstract

Background: MicroRNAs (miRNAs) are an abundant class of endogenous small non-coding RNAs of 20-25 nucleotides in length that function as negative gene regulators. MiRNAs play roles in most biological processes, as well as diverse human diseases including cancer. Recently, many studies investigated the association between SNPs in miR-146a rs2910164, miR-196a2 rs11614913, miR-149 rs229283, miR-499 rs3746444 and colorectal cancer (CRC), which results have been inconclusive. Methodology/Principal Findings: PubMed, EMBASE, CNKI databases were searched with the last search updated on November 5, 2013. For miR-196a2 rs11614913, a significantly decreased risk of CRC development was observed under three genetic models (dominant model: OR = 0.848, 95%CI: 0.735-0.979, P = 0.025; recessive model: OR = 0.838, 95%CI: 0.721-0.974, P = 0.021; homozygous model: OR = 0.754, 95%CI: 0.627-0.907, P = 0.003). In the subgroup analyses, miR-$196a2^*T$ variant was associated with a significantly decreased susceptibility of CRC (allele model: OR = 0.839, 95%CI: 0.749-0.940, P = 0.000; dominant model: OR = 0.770, 95%CI: 0.653-0.980, P = 0.002; recessive model: OR = 0.802, 95%CI: 0.685-0.939, P = 0.006; homozygous model: OR = 0.695, 95%CI: 0.570-0.847, P = 0.000). As for miR-149 rs2292832, the two genetic models (recessive model: OR = 1.199, 95% CI 1.028-1.398, P = 0.021; heterozygous model: OR = 1.226, 95% CI 1.039-1.447, P = 0.013) demonstrated increased susceptibility to CRC. On subgroup analysis, significantly increased susceptibility of CRC was found in the genetic models (recessive model: OR = 1.180, 95% CI 1.008-1.382, P = 0.040; heterozygous model: OR = 1.202, 95% CI 1.013-1.425, P = 0.013) in the Asian group. Conclusions: These findings supported that the miR-196a2 rs11614913 and miR-149 rs2292832 polymorphisms may contribute to susceptibility to CRC.

Keywords

References

  1. Akkiz H, Bayram S, Bekar A, et al (2011). Genetic variation in the microRNA-499 gene and hepatocellular carcinoma risk in a Turkish population: lack of any association in a case-control study. Asian Pac J Cancer Prev, 12, 3107-12.
  2. Alshatwi AA, Shafi G, Hasan TN, et al (2012). Differential expression profile and genetic variants of microRNAs sequences in breast cancer patients. PLoS One, 7, e30049. https://doi.org/10.1371/journal.pone.0030049
  3. Bartel DP (2009). MicroRNAs: target recognition and regulatory functions. Cell, 136, 215-33. https://doi.org/10.1016/j.cell.2009.01.002
  4. Begg CB, Mazumdar M (1994). Operating characteristics of a rank correlation test for publication bias. Biometrics, 50, 1088-101. https://doi.org/10.2307/2533446
  5. Bhaumik D, Scott GK, Schokrpur S, et al (2008). Expression of microRNA-146 suppresses NF-kappaB activity with reduction of metastatic potential in breast cancer cells. Oncogene, 27, 5643-7. https://doi.org/10.1038/onc.2008.171
  6. Brodersen P, Voinnet O (2009). Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Bio, 10, 141-8. https://doi.org/10.1038/nrm2619
  7. Calin GA, Croce CM (2006). MicroRNA signatures in human cancers. Nature Reviews Cancer, 6, 857-66. https://doi.org/10.1038/nrc1997
  8. Catucci I, Yang R, Verderio P, et al (2010). Evaluation of SNPs in miR-146a, miR196a2 and miR-499 as low-penetrance alleles in German and Italian familial breast cancer cases. Hum Mutat, 31, E1052-7. https://doi.org/10.1002/humu.21141
  9. Chae YS, Kim JG, Lee SJ, et al (2013). A miR-146a polymorphism (rs2910164) predicts risk of and survival from colorectal cancer. Anticancer Res, 33, 3233-9.
  10. Chen H, Sun LY, Chen LL, et al (2012a). A variant in microRNA-196a2 is not associated with susceptibility to and progression of colorectal cancer in Chinese. Intern Med J, 42, e115-9. https://doi.org/10.1111/j.1445-5994.2011.02434.x
  11. Chen K, Song F, Calin GA, et al (2008). Polymorphisms in microRNA targets: a gold mine for molecular epidemiology. Carcinogenesis, 29, 1306-11. https://doi.org/10.1093/carcin/bgn116
  12. Chen P, Zhang J, Zhou F (2012b). miR-499 rs3746444 polymorphism is associated with cancer development among Asians and related to breast cancer susceptibility. Mol Biol Rep, 39, 10433-8. https://doi.org/10.1007/s11033-012-1922-3
  13. Cheng T, Wang L, Li Y, et al (2013). Differential microRNA expression in renal cell carcinoma. Oncol Lett, 6, 769-76.
  14. Cochran WG (1954). The combination of estimates from different experiments. Biometrics, 10, 101-29. https://doi.org/10.2307/3001666
  15. Croce CM (2009). Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet, 10, 704-14. https://doi.org/10.1038/nrg2634
  16. DerSimonian R, Laird N (1986). Meta-analysis in clinical trials. Control Clin Trials, 7, 177-88. https://doi.org/10.1016/0197-2456(86)90046-2
  17. Ding SL, Wang JX, Jiao JQ, et al (2013). A pre-microRNA-149 (miR-149) genetic variation affects miR-149 maturation and its ability to regulate the Puma protein in apoptosis. J Biol Chem, 288, 26865-77. https://doi.org/10.1074/jbc.M112.440453
  18. Dominguez G (2013). Deciphering the epigenetic network in colorectal cancer. J Pathol, 229, 1-3.
  19. Egger M, Smith GD, Schneider M, Minder C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ, 315, 629-34. https://doi.org/10.1136/bmj.315.7109.629
  20. Fabian MR, Sonenberg N, Filipowicz W (2010). Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem, 79, 351-79. https://doi.org/10.1146/annurev-biochem-060308-103103
  21. Ferlay J, Shin HR, Bray F, et al (2010). Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer, 127, 2893-917. https://doi.org/10.1002/ijc.25516
  22. Garcia A I, Cox DG, Barjhoux L, et al (2011). The rs2910164:G>C SNP in the MIR146A gene is not associated with breast cancer risk in BRCA1 and BRCA2 mutation carriers. Hum Mutat, 32, 1004-7. https://doi.org/10.1002/humu.21539
  23. Garzon R, Calin GA, Croce CM (2009). MicroRNAs in cancer. Annu Rev Med, 60, 167-79. https://doi.org/10.1146/annurev.med.59.053006.104707
  24. 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
  25. Higgins J, Thompson SG (2002). Quantifying heterogeneity in a meta-analysis. Stat Med, 21, 1539-58. https://doi.org/10.1002/sim.1186
  26. 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
  27. Hong MJ, Choi YY, Jang JA, et al (2013). Association between genetic variants in pre-microRNAs and survival of earlystage NSCLC. J Thorac Oncol, 8, 703-10. https://doi.org/10.1097/JTO.0b013e318288dc0a
  28. Hu X, Li L, Shang M, et al (2013). Association between microRNA genetic variants and susceptibility to colorectal cancer in Chinese population. Tumour Biol.
  29. Hu Z, Liang J, Wang Z, et al (2009). Common genetic variants in pre-microRNAs were associated with increased risk of breast cancer in Chinese women. Hum Mutat, 30, 79-84. https://doi.org/10.1002/humu.20837
  30. Hurst DR, Edmonds MD, Scott GK, et al (2009). Breast cancer metastasis suppressor 1 up-regulates miR-146, which suppresses breast cancer metastasis. Cancer Res, 69, 1279-83. https://doi.org/10.1158/0008-5472.CAN-08-3559
  31. Jazdzewski K, Murray EL, Franssila K, et al (2008). Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma. Proc Natl Acad Sci U S A, 105, 7269-74. https://doi.org/10.1073/pnas.0802682105
  32. Krol J, Loedige I, Filipowicz W (2010). The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet, 11, 597-610.
  33. Landi D, Gemignani F, Barale R, Landi S (2008). A catalog of polymorphisms falling in microRNA-binding regions of cancer genes. Dna Cell Biol, 27, 35-43. https://doi.org/10.1089/dna.2007.0650
  34. Leung AK, Sharp PA (2010). MicroRNA functions in stress responses. Mol Cell, 40, 205-15. https://doi.org/10.1016/j.molcel.2010.09.027
  35. Levin B, Lieberman DA, McFarland B, et al (2008). Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA: a cancer journal for clinicians, 58, 130-60. https://doi.org/10.3322/CA.2007.0018
  36. Li Y, Vandenboom T G, 2nd, Wang Z, et al (2010). miR-146a suppresses invasion of pancreatic cancer cells. Gastroenterology, 134, 1570-95.
  37. Lin RJ, Lin YC, Yu AL (2010). miR-149* induces apoptosis by inhibiting Akt1 and E2F1 in human cancer cells. Mol Carcinog, 49, 719-27.
  38. Lv M, Dong W, Li L, et al (2013). Association between genetic variants in pre-miRNA and colorectal cancer risk in a Chinese population. J Cancer Res Clin Oncol, 139, 1405-10. https://doi.org/10.1007/s00432-013-1456-7
  39. Ma L, Zhu L, Gu D, et al (2013). A genetic variant in miR-146a modifies colorectal cancer susceptibility in a Chinese population. Arch Toxicol, 87, 825-33. https://doi.org/10.1007/s00204-012-1004-2
  40. Mantel N, Haenszel W (2004). Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst, 22, 719-48.
  41. Marino M, Cirello V, Gnarini V, et al (2013). Are pre-miR-146a and PTTG1 associated with papillary thyroid cancer? Endocr Connect, 2, 178-85. https://doi.org/10.1530/EC-13-0066
  42. Meili L, Wei D, Yonggang W, et al (2013). Association between genetic variants in pre-miRNA and colorectal cancer risk in a Chinese Population. J Cancer Res Clin Oncol, 139, 1405-10. https://doi.org/10.1007/s00432-013-1456-7
  43. Min KT, Kim JW, Jeon YJ, et al (2012). Association of the miR-146aC>G, 149C>T, 196a2C>T, and 499A>G polymorphisms with colorectal cancer in the Korean population. Mol Carcinog, 51, E65-73. https://doi.org/10.1002/mc.21849
  44. Mishra PJ, Bertino JR (2009). MicroRNA polymorphisms: the future of pharmacogenomics, molecular epidemiology and individualized medicine. Pharmacogenomics, 10, 399-416. https://doi.org/10.2217/14622416.10.3.399
  45. Mueller DW, Bosserhoff AK (2011). MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression. Int J Cancer, 129, 1064-74. https://doi.org/10.1002/ijc.25768
  46. Niinuma T, Suzuki H, Nojima M, et al (2012). Upregulation of miR-196a and HOTAIR drive malignant character in gastrointestinal stromal tumors. Cancer Res, 72, 1126-36. https://doi.org/10.1158/0008-5472.CAN-11-1803
  47. 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
  48. Schimanski CC, Frerichs K, Rahman F, et al (2009). High miR-196a levels promote the oncogenic phenotype of colorectal cancer cells. World J Gastroenterol, 15, 2089. https://doi.org/10.3748/wjg.15.2089
  49. Shi KQ, Lin Z, Li DW, et al (2013). Meta-analysis of the association between a polymorphism in microRNA-196a2 and susceptibility to colorectal cancer. Onkologie, 36, 560-5. https://doi.org/10.1159/000355158
  50. Siegel R, Naishadham D, Jemal A (2013). Cancer statistics, 2013. CA Cancer J Clin, 63, 11-30. https://doi.org/10.3322/caac.21166
  51. 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
  52. Tu HF, Liu CJ, Chang CL, et al (2012). The association between genetic polymorphism and the processing efficiency of miR-149 affects the prognosis of patients with head and neck squamous cell carcinoma. PLoS One, 7, e51606. https://doi.org/10.1371/journal.pone.0051606
  53. Vinci S, Gelmini S, Mancini I, et al (2013). Genetic and epigenetic factors in regulation of microRNA in colorectal cancers. Methods, 59, 138-46. https://doi.org/10.1016/j.ymeth.2012.09.002
  54. Visone R, Croce CM (2009). MiRNAs and cancer. Am J Pathol, 174, 1131-8. https://doi.org/10.2353/ajpath.2009.080794
  55. Wang F, Sun GP, Zou YF, et al (2013). Quantitative assessment of the association between miR-196a2 rs11614913 polymorphism and gastrointestinal cancer risk. Mol Biol Rep, 40, 109-16. https://doi.org/10.1007/s11033-012-2039-4
  56. Wang P, Xie S, Cui A, et al (2012). miR-196a2 polymorphisms and susceptibility to cancer: A meta-analysis involving 24, 697 subjects. Exp Ther Med, 3, 324-30.
  57. Wei WJ, Wang YL, Li DS, et al (2013). Association between the rs2910164 polymorphism in pre-Mir-146a sequence and thyroid carcinogenesis. PLoS One, 8, e56638. https://doi.org/10.1371/journal.pone.0056638
  58. Xiao C, Rajewsky K (2009). MicroRNA control in the immune system: basic principles. Cell, 136, 26-36. https://doi.org/10.1016/j.cell.2008.12.027
  59. Xu Y, Gu L, Pan Y, et al (2013b). Different effects of three polymorphisms in MicroRNAs on cancer risk in Asian population: evidence from published literatures. PLoS One, 8, e65123. https://doi.org/10.1371/journal.pone.0065123
  60. Xu Y, Li L, Xiang X, et al (2013a). Three common functional polymorphisms in microRNA encoding genes in the susceptibility to hepatocellular carcinoma: a systematic review and meta-analysis. Gene, 527, 584-93. https://doi.org/10.1016/j.gene.2013.05.085
  61. 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
  62. Zhan JF, Chen LH, Chen ZX, et al (2011). A functional variant in microRNA-196a2 is associated with susceptibility of colorectal cancer in a Chinese population. Arch Med Res, 42, 144-8. https://doi.org/10.1016/j.arcmed.2011.04.001
  63. Zhang MW, Jin MJ, Yu YX, et al (2012). Associations of lifestyle-related factors, hsa-miR-149 and hsa-miR-605 gene polymorphisms with gastrointestinal cancer risk. Mol Carcinog, 51, E21-31. https://doi.org/10.1002/mc.20863
  64. Zhou F, Zhu H, Luo D, et al (2012). A functional polymorphism in Pre-miR-146a is associated with susceptibility to gastric cancer in a Chinese population. Dna Cell Biol, 31, 1290-5. https://doi.org/10.1089/dna.2011.1596
  65. Zhu L, Chu H, Gu D, et al (2012). A functional polymorphism in miRNA-196a2 is associated with colorectal cancer risk in a Chinese population. Dna Cell Biol, 31, 350-4. https://doi.org/10.1089/dna.2011.1348

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