Meta-analysis of Hsa-mir-499 polymorphism (rs3746444) for cancer risk: evidence from 31 case-control studies

BMC Medical Genetics

Dao Wen Wang²  Yan Wang²  Sandip Chaugai²  Shenglan Yang¹  Chen Chen² 

[1] Department of Internal Medicine, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China;Department of Internal Medicine and the Institute of Hypertension, Tongji Hospital, Tongji Medical College of Huazhong University of Science and Technology, 1095# Jiefang Ave, Wuhan 430030, People’s Republic of China

关键词: Meta-analysis;    rs3746444;    Asian;    Cancer risk;    miRNA polymorphism;   

Others  :  1090175
DOI  :  10.1186/s12881-014-0126-1

 received in 2013-10-09, accepted in 2014-11-11,  发布年份 2014

【 摘 要 】

Background

MicroRNAs (miRNAs) are a family of endogenous, small and non-coding RNAs that regulate gene expression negatively at the post-transcriptional level by suppressing translation or degrading target mRNAs, and are involved in diverse biological and pathological processes. Single nucleotide polymorphisms (SNPs) which are located in the miRNA-coding genes may participate in the process of development and diseases by altering the expression of mature miRNA. Recent studies investigating the association between hsa-mir-499 polymorphism (rs3746444) and cancer risk have yielded conflicting results.

Methods

In this meta-analysis, we conducted a search of case–control studies on the associations of SNP rs3746444 with susceptibility to cancer in electronic databases. A total of 31 studies involving 12799 cases and 14507 controls were retrieved and the strength of the association was estimated by pooled odds ratios (ORs) and 95% confidence intervals (CIs). Hardy-Weinberg equilibrium (HWE) was assessed by the goodness-of-fit chi-square test in controls. Subgroup analyses were done by racial descent and cancer type. Publication bias of literatures was evaluated by visual inspection of funnel plots and the linear regression asymmetry test by Egger et al. Sensitivity analysis was conducted by excluding one study at a time to examine the influence of individual data set on the pooled ORs.

Results

Overall, significant association between rs3746444 polymorphism and susceptibility to cancer was identified in TC versus TT and TC/CC versus TT (dominant) models. In the stratified analyses, increased risks were found in Asians, but not in Caucasians in all comparison models tested. Moreover, significant association with an increased risk was found in Chinese population. Also, much higher significant association with increased cancer risks were found in Iranian population. In different cancer types, a decreased risk was found in esophageal cancer.

Conclusion

Our meta-analysis suggested that hsa-mir-499 rs3746444 T > C polymorphism is associated with the risk of cancer in Asians, mainly in Iranian and Chinese population. However, rs3746444 T > C polymorphism is negatively associated with the risk of esophageal cancer.

【 授权许可】

   
2014 Chen et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

【 参考文献 】

• [1]Lee RC, Feinbaum RL, Ambros V: The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 1993, 75(5):843-854.
• [2]Wightman B, Ha I, Ruvkun G: Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 1993, 75(5):855-862.
• [3]Mendell JT, Olson EN: MicroRNAs in stress signaling and human disease. Cell 2012, 148(6):1172-1187.
• [4]Heinrich EM, Dimmeler S: MicroRNAs and stem cells: control of pluripotency, reprogramming, and lineage commitment. Circ Res 2012, 110(7):1014-1022.
• [5]Boettger T, Braun T: A new level of complexity: the role of microRNAs in cardiovascular development. Circ Res 2012, 110(7):1000-1013.
• [6]Cheng W, Liu T, Wan X, Gao Y, Wang H: MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. FEBS J 2012, 279(11):2047-2059.
• [7]Rottiers V, Naar AM: MicroRNAs in metabolism and metabolic disorders. Nat Rev Mol Cell Biol 2012, 13(4):239-250.
• [8]Grueter CE, van Rooij E, Johnson BA, DeLeon SM, Sutherland LB, Qi X, Gautron L, Elmquist JK, Bassel-Duby R, Olson EN: A cardiac microRNA governs systemic energy homeostasis by regulation of MED13. Cell 2012, 149(3):671-683.
• [9]Akbari Moqadam F, Pieters R, den Boer ML: The hunting of targets: challenge in miRNA research. Leukemia 2013, 27(1):16-23.
• [10]Vira D, Basak SK, Veena MS, Wang MB, Batra RK, Srivatsan ES: Cancer stem cells, microRNAs, and therapeutic strategies including natural products. Cancer Metastasis Rev 2012, 31(3–4):733-751.
• [11]Ebert MS, Sharp PA: Roles for microRNAs in conferring robustness to biological processes. Cell 2012, 149(3):515-524.
• [12]Pritchard CC, Cheng HH, Tewari M: MicroRNA profiling: approaches and considerations. Nat Rev Genet 2012, 13(5):358-369.
• [13]Kim YK, Kim VN: Processing of intronic microRNAs. EMBO J 2007, 26(3):775-783.
• [14]Meister G, Tuschl T: Mechanisms of gene silencing by double-stranded RNA. Nature 2004, 431(7006):343-349.
• [15]Yang JS, Lai EC: Alternative miRNA biogenesis pathways and the interpretation of core miRNA pathway mutants. Mol Cell 2011, 43(6):892-903.
• [16]Cheloufi S, Dos Santos CO, Chong MM, Hannon GJ: A dicer-independent miRNA biogenesis pathway that requires Ago catalysis. Nature 2010, 465(7298):584-589.
• [17]Cai Y, Yu X, Hu S, Yu J: A brief review on the mechanisms of miRNA regulation. Genomics Proteomics Bioinformatics 2009, 7(4):147-154.
• [18]Mishra PJ, Banerjee D, Bertino JR: MiRSNPs or MiR-polymorphisms, new players in microRNA mediated regulation of the cell: Introducing microRNA pharmacogenomics. Cell Cycle 2008, 7(7):853-858.
• [19]Wu C, Gong Y, Sun A, Zhang Y, Zhang C, Zhang W, Zhao G, Zou Y, Ge J: The human MTHFR rs4846049 polymorphism increases coronary heart disease risk through modifying miRNA binding. Nutr Metab Cardiovasc Dis 2013, 23(7):693-698.
• [20]Wang K, Li J, Guo H, Xu X, Xiong G, Guan X, Liu B, Chen X, Yang K, Bai Y: MiR-196a binding-site SNP regulates RAP1A expression contributing to esophageal squamous cell carcinoma risk and metastasis. Carcinogenesis 2012, 33(11):2147-2154.
• [21]Luo J, Cai Q, Wang W, Huang H, Zeng H, He W, Deng W, Yu H, Chan E, Ng CF, Huang J, Lin T: A microRNA-7 binding site polymorphism in HOXB5 leads to differential gene expression in bladder cancer. PLoS One 2012, 7(6):e40127.
• [22]Liu Y, Zhang Y, Wen J, Liu L, Zhai X, Liu J, Pan S, Chen J, Shen H, Hu Z: A genetic variant in the promoter region of miR-106b-25 cluster and risk of HBV infection and hepatocellular carcinoma. PLoS One 2012, 7(2):e32230.
• [23]Wu Y, Xiao Y, Ding X, Zhuo Y, Ren P, Zhou C, Zhou J: A miR-200b/200c/429-binding site polymorphism in the 3′ untranslated region of the AP-2alpha gene is associated with cisplatin resistance. PLoS One 2011, 6(12):e29043.
• [24]Hu Z, Liang J, Wang Z, Tian T, Zhou X, Chen J, Miao R, Wang Y, Wang X, Shen H: Common genetic variants in pre-microRNAs were associated with increased risk of breast cancer in Chinese women. Hum Mutat 2009, 30(1):79-84.
• [25]Catucci I, Yang R, Verderio P, Pizzamiglio S, Heesen L, Hemminki K, Sutter C, Wappenschmidt B, Dick M, Arnold N, Bugert P, Niederacher D, Meindl A, Schmutzler RK, Bartram CC, Ficarazzi F, Tizzoni L, Zaffaroni D, Manoukian S, Barile M, Pierotti MA, Radice P, Burwinkel B, Peterlongo P: Evaluation of SNPs in miR-146a, miR196a2 and miR-499 as low-penetrance alleles in German and Italian familial breast cancer cases. Hum Mutat 2010, 31(1):E1052-E1057.
• [26]Omrani M, Hashemi M, Eskandari-Nasab E, Hasani SS, Mashhadi MA, Arbabi F, Taheri M: hsa-mir-499 rs3746444 gene polymorphism is associated with susceptibility to breast cancer in an Iranian population. Biomark Med 2014, 8(2):259-267.
• [27]Tian T, Shu Y, Chen J, Hu Z, Xu L, Jin G, Liang J, Liu P, Zhou X, Miao R, Ma H, Chen Y, Shen H: A functional genetic variant in microRNA-196a2 is associated with increased susceptibility of lung cancer in Chinese. Cancer Epidemiol Biomarkers Prev 2009, 18(4):1183-1187.
• [28]Xu J, Hu Z, Xu Z, Gu H, Yi L, Cao H, Chen J, Tian T, Liang J, Lin Y, Qiu W, Ma H, Shen H, Chen Y: Functional variant in microRNA-196a2 contributes to the susceptibility of congenital heart disease in a Chinese population. Hum Mutat 2009, 30(8):1231-1236.
• [29]Zhou B, Rao L, Peng Y, Wang Y, Chen Y, Song Y, Zhang L: Common genetic polymorphisms in pre-microRNAs were associated with increased risk of dilated cardiomyopathy. Clin Chim Acta 2010, 411(17–18):1287-1290.
• [30]Srivastava K, Srivastava A, Mittal B: Common genetic variants in pre-microRNAs and risk of gallbladder cancer in North Indian population. J Hum Genet 2010, 55(8):495-499.
• [31]Liu Z, Li G, Wei S, Niu J, El-Naggar AK, Sturgis EM, Wei Q: Genetic variants in selected pre-microRNA genes and the risk of squamous cell carcinoma of the head and neck. Cancer 2010, 116(20):4753-4760.
• [32]Li LJ, Gao LB, Lv ML, Dong W, Su XW, Liang WB, Zhang L: Association between SNPs in pre-miRNA and risk of chronic obstructive pulmonary disease. Clin Biochem 2011, 44(10–11):813-816.
• [33]Zhou J, Lv R, Song X, Li D, Hu X, Ying B, Wei Y, Wang L: Association between two genetic variants in miRNA and primary liver cancer risk in the Chinese population. DNA Cell Biol 2012, 31(4):524-530.
• [34]Yang B, Chen J, Li Y, Zhang J, Li D, Huang Z, Cai B, Li L, Shi Y, Ying B, Wang L: Association of polymorphisms in pre-miRNA with inflammatory biomarkers in rheumatoid arthritis in the Chinese Han population. Hum Immunol 2012, 73(1):101-106.
• [35]Zhi H, Wang L, Ma G, Ye X, Yu X, Zhu Y, Zhang Y, Zhang J, Wang B: Polymorphisms of miRNAs genes are associated with the risk and prognosis of coronary artery disease. Clin Res Cardiol 2012, 101(4):289-296.
• [36]Min KT, Kim JW, Jeon YJ, Jang MJ, Chong SY, Oh D, Kim NK: Association of the miR-146aC > G, 149C > T, 196a2C > T, and 499A > G polymorphisms with colorectal cancer in the Korean population. Mol Carcinog 2012, 51(Suppl 1):E65-E73.
• [37]Chen QH, Wang QB, Zhang B: Ethnicity modifies the association between functional microRNA polymorphisms and breast cancer risk: a HuGE meta-analysis. Tumour Biol 2014, 35(1):529-543.
• [38]Ma XP, Zhang T, Peng B, Yu L, Jiang de K: Association between microRNA polymorphisms and cancer risk based on the findings of 66 case–control studies. PLoS One 2013, 8(11):e79584.
• [39]Wang PY, Gao ZH, Jiang ZH, Li XX, Jiang BF, Xie SY: The associations of single nucleotide polymorphisms in miR-146a, miR-196a and miR-499 with breast cancer susceptibility. PLoS One 2013, 8(9):e70656.
• [40]Wang L, Qian S, Zhi H, Zhang Y, Wang B, Lu Z: The association between hsa-miR-499 T > C polymorphism and cancer risk: A meta-analysis. Gene 2012, 508(1):9-14.
• [41]Du W, Ma XL, Zhao C, Liu T, Du YL, Kong WQ, Wei BL, Yu JY, Li YY, Huang JW, Li ZK, Liu L: Associations of single nucleotide polymorphisms in miR-146a, miR-196a, miR-149 and miR-499 with colorectal cancer susceptibility. Asian Pac J Cancer Prev 2014, 15(2):1047-1055.
• [42]Wang Y, Yang B, Ren X: Hsa-miR-499 polymorphism (rs3746444) and cancer risk: a meta-analysis of 17 case–control studies. Gene 2012, 509(2):267-272.
• [43]Wang F, Sun G, Zou Y, Li Y, Hao L, Pan F: Association of microRNA-499 rs3746444 polymorphism with cancer risk: evidence from 7188 cases and 8548 controls. PLoS One 2012, 7(9):e45042.
• [44]Chen P, Zhang J, Zhou F: miR-499 rs3746444 polymorphism is associated with cancer development among Asians and related to breast cancer susceptibility. Mol Biol Rep 2012, 39(12):10433-10438.
• [45]He B, Pan Y, Cho WC, Xu Y, Gu L, Nie Z, Chen L, Song G, Gao T, Li R, Wang S: The association between four genetic variants in MicroRNAs (rs11614913, rs2910164, rs3746444, rs2292832) and cancer risk: evidence from published studies. PLoS One 2012, 7(11):e49032.
• [46]Wang Z, Cao Y, Jiang C, Yang G, Wu J, Ding Y: Lack of association of two common polymorphisms rs2910164 and rs11614913 with susceptibility to hepatocellular carcinoma: a meta-analysis. PLoS One 2012, 7(6):e40039.
• [47]Egger M, Davey Smith G, Schneider M, Minder C: Bias in meta-analysis detected by a simple, graphical test. BMJ 1997, 315(7109):629-634.
• [48]Xiang Y, Fan S, Cao J, Huang S, Zhang LP: Association of the microRNA-499 variants with susceptibility to hepatocellular carcinoma in a Chinese population. Mol Biol Rep 2012, 39(6):7019-7023.
• [49]Akkiz H, Bayram S, Bekar A, Akgollu E, Uskudar O: 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 2011, 12(11):3107-3112.
• [50]Kim WH, Min KT, Jeon YJ, Kwon CI, Ko KH, Park PW, Hong SP, Rim KS, Kwon SW, Hwang SG, Kim NK: Association study of microRNA polymorphisms with hepatocellular carcinoma in Korean population. Gene 2012, 504(1):92-97.
• [51]Zou HZ, Zhao YQ: Positive association between miR-499A > G and hepatocellular carcinoma risk in a Chinese population. Asian Pac J Cancer Prev 2013, 14(3):1769-1772.
• [52]Shan YF, Huang YH, Chen ZK, Huang KT, Zhou MT, Shi HQ, Song QT, Yu ZP, Deng AM, Zhang QY: miR-499A > G rs3746444 and miR-146aG > C expression and hepatocellular carcinoma risk in the Chinese population. Genet Mol Res 2013, 12(4):5365-5371.
• [53]Ma Y, Wang R, Zhang J, Li W, Gao C, Liu J, Wang J: Identification of miR-423 and miR-499 polymorphisms on affecting the risk of hepatocellular carcinoma in a large-scale population. Genet Test Mol Biomarkers 2014, 18(7):516-524.
• [54]Chu YH, Hsieh MJ, Chiou HL, Liou YS, Yang CC, Yang SF, Kuo WH: MicroRNA gene polymorphisms and environmental factors increase patient susceptibility to hepatocellular carcinoma. PLoS One 2014, 9(2):e89930.
• [55]Alshatwi AA, Shafi G, Hasan TN, Syed NA, Al-Hazzani AA, Alsaif MA, Alsaif AA: Differential expression profile and genetic variants of microRNAs sequences in breast cancer patients. PLoS One 2012, 7(2):e30049.
• [56]Ahn DH, Rah H, Choi YK, Jeon YJ, Min KT, Kwack K, Hong SP, Hwang SG, Kim NK: Association of the miR-146aC > G, miR-149 T > C, miR-196a2T > C, and miR-499A > G polymorphisms with gastric cancer risk and survival in the Korean population. Mol Carcinog 2013, 52(Suppl 1):E39-E51.
• [57]Okubo M, Tahara T, Shibata T, Yamashita H, Nakamura M, Yoshioka D, Yonemura J, Ishizuka T, Arisawa T, Hirata I: Association between common genetic variants in pre-microRNAs and gastric cancer risk in Japanese population. Helicobacter 2010, 15(6):524-531.
• [58]Wu XJ, Mi YY, Yang H, Hu AK, Li C, Li XD, Zhang QG: Association of the hsa-mir-499 (rs3746444) polymorphisms with gastric cancer risk in the Chinese population. Onkologie 2013, 36(10):573-576.
• [59]Pu JY, Dong W, Zhang L, Liang WB, Yang Y, Lv ML: No association between single nucleotide polymorphisms in pre-mirnas and the risk of gastric cancer in Chinese population. Iranian J Basic Med Sci 2014, 17(2):128-133.
• [60]Lv M, Dong W, Li L, Zhang L, Su X, Wang L, Gao L, Zhang L: Association between genetic variants in pre-miRNA and colorectal cancer risk in a Chinese population. J Cancer Res Clin Oncol 2013, 139(8):1405-1410.
• [61]Hu X, Li L, Shang M, Zhou J, Song X, Lu X, Wang J, Ying B, Wang L: Association between microRNA genetic variants and susceptibility to colorectal cancer in Chinese population. Tumour Biol 2014, 35(3):2151-2156.
• [62]Vinci S, Gelmini S, Pratesi N, Conti S, Malentacchi F, Simi L, Pazzagli M, Orlando C: Genetic variants in miR-146a, miR-149, miR-196a2, miR-499 and their influence on relative expression in lung cancers. Clin Chem Lab Med 2011, 49(12):2073-2080.
• [63]Umar M, Upadhyay R, Prakash G, Kumar S, Ghoshal UC, Mittal B: Evaluation of common genetic variants in pre-microRNA in susceptibility and prognosis of esophageal cancer. Mol Carcinog 2013, 52(Suppl 1):E10-E18.
• [64]Wei J, Zheng L, Liu S, Yin J, Wang L, Wang X, Shi Y, Shao A, Tang W, Ding G, Liu C, Chen S, Gu H: MiR-196a2 rs11614913 T > C polymorphism and risk of esophageal cancer in a Chinese population. Hum Immunol 2013, 74(9):1199-1205.
• [65]Zhou B, Wang K, Wang Y, Xi M, Zhang Z, Song Y, Zhang L: Common genetic polymorphisms in pre-microRNAs and risk of cervical squamous cell carcinoma. Mol Carcinog 2011, 50(7):499-505.
• [66]Mittal RD, Gangwar R, George GP, Mittal T, Kapoor R: Investigative role of pre-microRNAs in bladder cancer patients: a case–control study in North India. DNA Cell Biol 2011, 30(6):401-406.
• [67]George GP, Gangwar R, Mandal RK, Sankhwar SN, Mittal RD: Genetic variation in microRNA genes and prostate cancer risk in North Indian population. Mol Biol Rep 2011, 38(3):1609-1615.
• [68]Hasani SS, Hashemi M, Eskandari-Nasab E, Naderi M, Omrani M, Sheybani-Nasab M: A functional polymorphism in the miR-146a gene is associated with the risk of childhood acute lymphoblastic leukemia: a preliminary report. Tumour Biol 2014, 35(1):219-225.
• [69]Du M, Lu D, Wang Q, Chu H, Tong N, Pan X, Qin C, Yin C, Wang M, Zhang Z: Genetic variations in microRNAs and the risk and survival of renal cell cancer. Carcinogenesis 2014, 35(7):1629-1635.
• [70]Hou YY, Lee JH, Chen HC, Yang CM, Huang SJ, Liou HH, Chi CC, Tsai KW, Ger LP: The association between miR-499a polymorphism and oral squamous cell carcinoma progression. Oral Dis. 2014 Apr 2. doi:10.1111/odi.12241. [Epub ahead of print]
• [71]Salzman DW, Weidhaas JB: SNPing cancer in the bud: MicroRNA and microRNA-target site polymorphisms as diagnostic and prognostic biomarkers in cancer. Pharmacol Ther 2013, 137(1):55-63.
• [72]Saunders MA, Liang H, Li WH: Human polymorphism at microRNAs and microRNA target sites. Proc Natl Acad Sci U S A 2007, 104(9):3300-3305.
• [73]Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM: Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005, 433(7027):769-773.
• [74]Fan C, Chen C, Wu D: The association between common genetic variant of microRNA-499 and cancer susceptibility: a meta-analysis. Mol Biol Rep 2013, 40(4):3389-3394.
• [75]Yin Z, Yan L, Cui Z, Li X, Ren Y, Zhou B: Effects of common polymorphisms rs2910164 in miR-146a and rs3746444 in miR-499 on cancer susceptibility: a meta-analysis. Mol Biol Rep 2013, 40(4):3003-3013.
• [76]Hu M, Zhao L, Hu S, Yang J: The association between two common polymorphisms in MicroRNAs and hepatocellular carcinoma risk in Asian population. PLoS One 2013, 8(2):e57012.
• [77]Qiu MT, Hu JW, Ding XX, Yang X, Zhang Z, Yin R, Xu L: Hsa-miR-499 rs3746444 polymorphism contributes to cancer risk: a meta-analysis of 12 studies. PLoS One 2012, 7(12):e50887.
• [78]Schaid DJ, Jacobsen SJ: Biased tests of association: comparisons of allele frequencies when departing from Hardy-Weinberg proportions. Am J Epidemiol 1999, 149(8):706-711.
• [79]Attia J, Thakkinstian A, D’Este C: Meta-analyses of molecular association studies: methodologic lessons for genetic epidemiology. J Clin Epidemiol 2003, 56(4):297-303.