Association of polymorphisms in estrogen receptors (ESR1 and ESR2) with male infertility: a meta-analysis and systematic review

详细信息    查看全文

• 作者：Yu-Zheng Ge (1)
  Lu-Wei Xu (1)
  Rui-Peng Jia (1)
  Zheng Xu (1)
  Wen-Cheng Li (1)
  Ran Wu (1)
  Sheng Liao (1)
  Fei Gao (1)
  Si-Jia Tan (1)
  Qun Song (1)
  Hui Xin (1)
  
• 关键词：Estrogen receptor ; Polymorphism ; Male infertility ; Meta ; analysis
• 刊名：Journal of Assisted Reproduction and Genetics
• 出版年：2014
• 出版时间：May 2014
• 年：2014
• 卷：31
• 期：5
• 页码：601-611
• 全文大小：
• 参考文献：1. Maduro MR, Lamb DJ. Understanding new genetics of male infertility. J Urol. 2002;168(5):2197-05. doi:10.1097/07.ju.0000023290.61978.b2 . CrossRef
  2. Boivin J, Bunting L, Collins JA, Nygren KG. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum Reprod. 2007;22(6):1506-2. doi:10.1093/humrep/dem046 . CrossRef
  3. Pasqualotto FF, Pasqualotto EB, Sobreiro BP, Hallak J, Medeiros F, Lucon AM. Clinical diagnosis in men undergoing infertility investigation in a university hospital. Urol Int. 2006;76(2):122-. doi:10.1159/000090873 . CrossRef
  4. Kovac JR, Pastuszak AW, Lamb DJ. The use of genomics, proteomics, and metabolomics in identifying biomarkers of male infertility. Fertil Steril. 2013;99(4):998-007. doi:10.1016/j.fertnstert.2013.01.111 . CrossRef
  5. Giwercman A. Estrogens and phytoestrogens in male infertility. Curr Opin Urol. 2011;21(6):519-6. doi:10.1097/MOU.0b013e32834b7e7c . CrossRef
  6. Carreau S, Lambard S, Delalande C, Denis-Galeraud I, Bilinska B, Bourguiba S. Aromatase expression and role of estrogens in male gonad: a review. Reprod Biol Endocrinol. 2003;1:35. CrossRef
  7. Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS, et al. A role for oestrogens in the male reproductive system. Nature. 1997;390(6659):509-2. doi:10.1038/37352 . CrossRef
  8. Hess RA. Estrogen in the adult male reproductive tract: a review. Reprod Biol Endocrinol. 2003;1:52. doi:10.1186/1477-7827-1-52 . CrossRef
  9. Atanassova N, McKinnell C, Turner KJ, Walker M, Fisher JS, Morley M, et al. Comparative effects of neonatal exposure of male rats to potent and weak (environmental) estrogens on spermatogenesis at puberty and the relationship to adult testis size and fertility: evidence for stimulatory effects of low estrogen levels. Endocrinology. 2000;141(10):3898-07.
  10. Hawkins MB, Thornton JW, Crews D, Skipper JK, Dotte A, Thomas P. Identification of a third distinct estrogen receptor and reclassification of estrogen receptors in teleosts. Proc Natl Acad Sci U S A. 2000;97(20):10751-. CrossRef
  11. Luconi M, Forti G, Baldi E. Genomic and nongenomic effects of estrogens: molecular mechanisms of action and clinical implications for male reproduction. J Steroid Biochem Mol Biol. 2002;80(4-):369-1. CrossRef
  12. Menasce LP, White GR, Harrison CJ, Boyle JM. Localization of the estrogen receptor locus (ESR) to chromosome 6q25.1 by FISH and a simple post-FISH banding technique. Genomics. 1993;17(1):263-. doi:10.1006/geno.1993.1320 . CrossRef
  13. Ponglikitmongkol M, Green S, Chambon P. Genomic organization of the human oestrogen receptor gene. EMBO J. 1988;7(11):3385-.
  14. Ogawa S, Inoue S, Watanabe T, Hiroi H, Orimo A, Hosoi T, et al. The complete primary structure of human estrogen receptor beta (hER beta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun. 1998;243(1):122-. doi:10.1006/bbrc.1997.7893 . CrossRef
  15. Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 1997;82(12):4258-5.
  16. O’Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev. 2001;22(3):289-18.
  17. Shearman AM, Cupples LA, Demissie S, Peter I, Schmid CH, Karas RH, et al. Association between estrogen receptor alpha gene variation and cardiovascular disease. JAMA. 2003;290(17):2263-0. doi:10.1001/jama.290.17.2263 . CrossRef
  18. Rosenkranz K, Hinney A, Ziegler A, Hermann H, Fichter M, Mayer H, et al. Systematic mutation screening of the estrogen receptor beta gene in probands of different weight extremes: identification of several genetic variants. J Clin Endocrinol Metab. 1998;83(12):4524-. CrossRef
  19. Kukuvitis A, Georgiou I, Bouba I, Tsirka A, Giannouli CH, Yapijakis C, et al. Association of oestrogen receptor alpha polymorphisms and androgen receptor CAG trinucleotide repeats with male infertility: a study in 109 Greek infertile men. Int J Androl. 2002;25(3):149-2. CrossRef
  20. Suzuki Y, Sasagawa I, Itoh K, Ashida J, Muroya K, Ogata T. Estrogen receptor alpha gene polymorphism is associated with idiopathic azoospermia. Fertil Steril. 2002;78(6):1341-. CrossRef
  21. Aschim EL, Giwercman A, Stahl O, Eberhard J, Cwikiel M, Nordenskjold A, et al. The RsaI polymorphism in the estrogen receptor-beta gene is associated with male infertility. J Clin Endocrinol Metab. 2005;90(9):5343-. doi:10.1210/jc.2005-0263 . CrossRef
  22. Galan JJ, Buch B, Cruz N, Segura A, Moron FJ, Bassas L, et al. Multilocus analyses of estrogen-related genes reveal involvement of the ESR1 gene in male infertility and the polygenic nature of the pathology. Fertil Steril. 2005;84(4):910-. doi:10.1016/j.fertnstert.2005.03.070 . CrossRef
  23. Omrani MD, Samadzadae S, Farshid B, Jahandidae B, Yazdanpanah K. Is there any association between ER(beta) gene polymorphism and infertility in Iranian men? J Res Med Sci. 2006;11(1):48-2.
  24. Galan JJ, Guarducci E, Nuti F, Gonzalez A, Ruiz M, Ruiz A, et al. Molecular analysis of estrogen receptor alpha gene AGATA haplotype and SNP12 in European populations: potential protective effect for cryptorchidism and lack of association with male infertility. Hum Reprod. 2007;22(2):444-. doi:10.1093/humrep/del391 .
  25. Khattri A, Pandey RK, Gupta NJ, Chakravarty B, Deendayal M, Singh L, et al. CA repeat and RsaI polymorphisms in ERbeta gene are not associated with infertility in Indian men. Int J Androl. 2009;32(1):81-. doi:10.1111/j.1365-2605.2007.00821.x . CrossRef
  26. Khattri A, Pandey RK, Gupta NJ, Chakravarty B, Deenadayal M, Singh L, et al. Estrogen receptor beta gene mutations in Indian infertile men. Mol Hum Reprod. 2009;15(8):513-0. doi:10.1093/molehr/gap044 . CrossRef
  27. Su MT, Chen CH, Kuo PH, Hsu CC, Lee IW, Pan HA, et al. Polymorphisms of estrogen-related genes jointly confer susceptibility to human spermatogenic defect. Fertil Steril. 2010;93(1):141-. doi:10.1016/j.fertnstert.2008.09.030 . CrossRef
  28. Lazaros LA, Xita NV, Kaponis AI, Zikopoulos KA, Plachouras NI, Georgiou IA. Estrogen receptor alpha and beta polymorphisms are associated with semen quality. J Androl. 2010;31(3):291-. doi:10.2164/jandrol.109.007542 . CrossRef
  29. Safarinejad MR, Shafiei N, Safarinejad S. Association of polymorphisms in the estrogen receptors alpha, and beta (ESR1, ESR2) with the occurrence of male infertility and semen parameters. J Steroid Biochem Mol Biol. 2010;122(4):193-03. doi:10.1016/j.jsbmb.2010.06.011 . CrossRef
  30. Romerius P, Giwercman A, Moell C, Relander T, Cavallin-Stahl E, Wiebe T, et al. Estrogen receptor alpha single nucleotide polymorphism modifies the risk of azoospermia in childhood cancer survivors. Pharmacogenet Genomics. 2011;21(5):263-. doi:10.1097/FPC.0b013e328343a132 . CrossRef
  31. Bianco B, Peluso C, Gava MM, Ghirelli-Filho M, Lipay MV, Lipay MA, et al. Polymorphisms of estrogen receptors alpha and beta in idiopathic, infertile Brazilian men: a case–control study. Mol Reprod Dev. 2011;78(9):665-2. doi:10.1002/mrd.21365 . CrossRef
  32. Ogata T, Fukami M, Yoshida R, Nagata E, Fujisawa Y, Yoshida A, et al. Haplotype analysis of ESR2 in Japanese patients with spermatogenic failure. J Hum Genet. 2012;57(7):449-2. doi:10.1038/jhg.2012.53 . CrossRef
  33. Meng J, Mu X, Wang YM. Influence of the XbaI polymorphism in the estrogen receptor-alpha gene on human spermatogenic defects. Genet Mol Res. 2013;12(2):1808-5. doi:10.4238/2013.June.11.1 . CrossRef
  34. Zalata A, Abdalla HA, El-Bayoumy Y, Mostafa T. Oestrogen receptor alpha gene polymorphisms relationship with semen variables in infertile men. Andrologia. 2013. doi:10.1111/and.12123 .
  35. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097 . CrossRef
  36. Ge YZ, Wu R, Jia RP, Liu H, Yu P, Zhao Y, et al. Association between interferon gamma +874T>a polymorphism and acute renal allograft rejection: evidence from published studies. Mol Biol Rep. 2013;40(10):6043-1. doi:10.1007/s11033-013-2714-0 . CrossRef
  37. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557-0. doi:10.1136/bmj.327.7414.557 . CrossRef
  38. Mantel N, Haenszel W. Statistical aspects of the analysis of data from retrospective studies of disease. J Natl Cancer Inst. 1959;22(4):719-8.
  39. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177-8. CrossRef
  40. Thakkinstian A, McElduff P, D’Este C, Duffy D, Attia J. A method for meta-analysis of molecular association studies. Stat Med. 2005;24(9):1291-06. doi:10.1002/sim.2010 . CrossRef
  41. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994;50(4):1088-01. CrossRef
  42. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629-4. CrossRef
  43. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A. 1998;95(26):15677-2. CrossRef
  44. Sinkevicius KW, Laine M, Lotan TL, Woloszyn K, Richburg JH, Greene GL. Estrogen-dependent and -independent estrogen receptor-alpha signaling separately regulate male fertility. Endocrinology. 2009;150(6):2898-05. doi:10.1210/en.2008-1016 . CrossRef
  45. Wang Y, Cui M, Zheng L. Genetic polymorphisms in the estrogen receptor-alpha gene and the risk of endometrial cancer: a meta-analysis. Acta Obstet Gynecol Scand. 2012;91(8):911-. doi:10.1111/j.1600-0412.2012.01393.x . CrossRef
  46. Sikka SC, Wang R. Endocrine disruptors and estrogenic effects on male reproductive axis. Asian J Androl. 2008;10(1):134-5. doi:10.1111/j.1745-7262.2008.00370.x . CrossRef
  
• 作者单位：Yu-Zheng Ge (1)
  Lu-Wei Xu (1)
  Rui-Peng Jia (1)
  Zheng Xu (1)
  Wen-Cheng Li (1)
  Ran Wu (1)
  Sheng Liao (1)
  Fei Gao (1)
  Si-Jia Tan (1)
  Qun Song (1)
  Hui Xin (1)
  
  1. Department of Urology, Nanjing First Hospital, Nanjing Medical University, 68 Changle Road, Nanjing, 210006, China
  
• ISSN：1573-7330

文摘

Purpose Estrogens play an important role in male reproduction via interacting with estrogen receptors (ERs), whose expression can be regulated by the polymorphisms in different regions of ESR1 and ESR2 genes. However, results from published studies on the association between four well-characterized polymorphisms (PvuII, XbaI, RsaI, and AluI) in the gene of ERs (ESR1 and ESR2) and male infertility risk are inconclusive. Methods To investigate the strength of relationship of PvuII and XbaI in ESR1 and RsaI and AluI in ESR2 with male infertility, we conducted a meta-analysis of 12 eligible studies with odds ratio (OR) and its corresponding 95?% confidence intervals (95?% CI). Results Overall, ESR1 PvuII and ESR2 RsaI polymorphisms were significantly associated with male infertility risk. The subgroup analyses by ethnicities demonstrated that in Asians, ESR1 PvuII, XbaI and ESR2 RsaI polymorphisms were significantly associated with a decreased infertility risk, while in Caucasians both ESR1 PvuII and ESR2 RsaI polymorphisms increased the susceptibility to male infertility. As for ESR2 AluI polymorphism, no significant association was detected in either overall analysis or subgroup analyses by ethnicities/genotyping methods. Conclusions This meta-analysis suggested that polymorphisms in the genes of ERs (ESR1 and ESR2) may have differential roles in the predisposition to male infertility according to the different ethnic backgrounds. Further well-designed and unbiased studies with larger sample size and diverse ethnic backgrounds should be conducted to verify our findings