Skip to main content
Top
Published in: Reproductive Biology and Endocrinology 1/2014

Open Access 01-12-2014 | Research

Polymorphisms in estrogen receptors predict the risk of male infertility: a meta-analysis

Authors: Tian-Fu Li, Qiu-Yue Wu, Cui Zhang, Wei-Wei Li, Na Li, Ying-Xia Cui, Xiao-Jun Li, Xin-Yi Xia

Published in: Reproductive Biology and Endocrinology | Issue 1/2014

Login to get access

Abstract

Background

Estrogen receptors play an important role in mediating estrogen action on target tissues, and the estrogen is relevant to male infertility. Single nucleotide polymorphisms (SNPs) in estrogen receptors may be associated with the risk of male infertility. A variety of case control studies have been published evaluating this association. However, the accumulated studies have shown inconsistent conclusions.

Methods

To further determine the potential association between the four common SNPs (rs2234693, rs9340799, rs1256049 and rs4986938) in estrogen receptors gene and male infertility, this meta-analysis was performed according to the 10 published case control studies. The odds ratio (OR) and 95% confidence interval (CI) were used to evaluate the strength of the associations.

Results

It was revealed that the sub-group analysis by the ethnicity, for the rs2234693, a significant association in the comparison of CC vs. TT (OR = 0.61, 95% CI: 0.40-0.93), CT vs. TT (OR = 0.67, 95% CI: 0.49-0.93) and CC + CT vs. TT (OR = 0.66, 95% CI: 0.49-0.89) in the Asian population with male infertility. For rs9340799 polymorphism, increased risks were observed for the comparison of AA vs. GG (OR = 1.75, 95% CI: 1.15-2.68) and AA vs. GA + GG (OR = 1.38, 95% CI: 1.02-1.88). For rs1256049 polymorphism, the comparison of the GA vs. GG (OR = 1.52, 95% CI: 1.00-2.31) and AA + GA vs. GG (OR = 1.74, 95% CI: 1.03-2.94), also increased risks present in Asian and Caucasian population, respectively.

Conclusions

The rs2234693C allele was associated with the decreased risk for male infertility; however, the rs9340799AA genotype and the rs1256049GA genotype were associated with an increased risk for male infertility.
Appendix
Available only for authorised users
Literature
1.
go back to reference De Kretser D, Baker H: Infertility in men: recent advances and continuing controversies. J Clin Endocrinol Metab. 1999, 84: 3443-3450.PubMed De Kretser D, Baker H: Infertility in men: recent advances and continuing controversies. J Clin Endocrinol Metab. 1999, 84: 3443-3450.PubMed
2.
go back to reference Dohle GR, Colpi G, Hargreave T, Papp G, Jungwirth A, Weidner W: EAU guidelines on male infertility. Eur Urol. 2005, 48: 703-711.CrossRefPubMed Dohle GR, Colpi G, Hargreave T, Papp G, Jungwirth A, Weidner W: EAU guidelines on male infertility. Eur Urol. 2005, 48: 703-711.CrossRefPubMed
3.
go back to reference Pieri PC, Pereira DH, Glina S, Hallak J, McElreavey K, Moreira-Filho CA: A cost-effective screening test for detecting AZF microdeletions on the human Y chromosome. Genet Test. 2002, 6: 185-194.CrossRef Pieri PC, Pereira DH, Glina S, Hallak J, McElreavey K, Moreira-Filho CA: A cost-effective screening test for detecting AZF microdeletions on the human Y chromosome. Genet Test. 2002, 6: 185-194.CrossRef
4.
go back to reference Ferlin A, Arredi B, Foresta C: Genetic causes of male infertility. Reprod Toxicol. 2006, 22: 133-141.CrossRefPubMed Ferlin A, Arredi B, Foresta C: Genetic causes of male infertility. Reprod Toxicol. 2006, 22: 133-141.CrossRefPubMed
5.
go back to reference Zalata A, Abdalla H, El-Bayoumy Y, Mostafa T: Oestrogen receptor alpha gene polymorphisms relationship with semen variables in infertile men. Andrologia. 2014, 46: 618-624.CrossRefPubMed Zalata A, Abdalla H, El-Bayoumy Y, Mostafa T: Oestrogen receptor alpha gene polymorphisms relationship with semen variables in infertile men. Andrologia. 2014, 46: 618-624.CrossRefPubMed
6.
go back to reference 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-PubMedCentralCrossRefPubMed 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-PubMedCentralCrossRefPubMed
7.
go back to reference Bianco B, Peluso C, Gava MM, Ghirelli-Filho M, Lipay MVN, Lipay MA, Christofolini DM, Barbosa CP: Polymorphisms of estrogen receptors alpha and beta in idiopathic, infertile Brazilian men: a case–control study. Mol Reprod Dev. 2011, 78: 665-672.CrossRefPubMed Bianco B, Peluso C, Gava MM, Ghirelli-Filho M, Lipay MVN, Lipay MA, Christofolini DM, Barbosa CP: Polymorphisms of estrogen receptors alpha and beta in idiopathic, infertile Brazilian men: a case–control study. Mol Reprod Dev. 2011, 78: 665-672.CrossRefPubMed
8.
go back to reference Zhai J, Lanclos K, Abney T: Estrogen receptor messenger ribonucleic acid changes during Leydig cell development. Biol Reprod. 1996, 55: 782-788.CrossRefPubMed Zhai J, Lanclos K, Abney T: Estrogen receptor messenger ribonucleic acid changes during Leydig cell development. Biol Reprod. 1996, 55: 782-788.CrossRefPubMed
9.
go back to reference Delbès G, Levacher C, Duquenne C, Racine C, Pakarinen P, Habert R: Endogenous estrogens inhibit mouse fetal Leydig cell development via estrogen receptor alpha. Endocrinology. 2005, 146: 2454-2461.CrossRefPubMed Delbès G, Levacher C, Duquenne C, Racine C, Pakarinen P, Habert R: Endogenous estrogens inhibit mouse fetal Leydig cell development via estrogen receptor alpha. Endocrinology. 2005, 146: 2454-2461.CrossRefPubMed
10.
go back to reference Atanassova N, McKinnell C, Walker M, Turner K, Fisher J, Morley M, Millar M, Groome N, Sharpe R: Permanent effects of neonatal estrogen exposure in rats on reproductive hormone levels, sertoli cell number, and the efficiency of spermatogenesis in adulthood. Endocrinology. 1999, 140: 5364-5373.PubMed Atanassova N, McKinnell C, Walker M, Turner K, Fisher J, Morley M, Millar M, Groome N, Sharpe R: Permanent effects of neonatal estrogen exposure in rats on reproductive hormone levels, sertoli cell number, and the efficiency of spermatogenesis in adulthood. Endocrinology. 1999, 140: 5364-5373.PubMed
11.
go back to reference Pentikäinen V, Erkkilä K, Suomalainen L, Parvinen M, Dunkel L: Estradiol acts as a germ cell survival factor in the human testis in vitro. J Clin Endocrinol Metab. 2000, 85: 2057-2067.PubMed Pentikäinen V, Erkkilä K, Suomalainen L, Parvinen M, Dunkel L: Estradiol acts as a germ cell survival factor in the human testis in vitro. J Clin Endocrinol Metab. 2000, 85: 2057-2067.PubMed
12.
go back to reference Gould M, Hurst P, Nicholson H: The effects of oestrogen receptors alpha and beta on testicular cell number and steroidogenesis in mice. Reproduction. 2007, 134: 271-279.CrossRefPubMed Gould M, Hurst P, Nicholson H: The effects of oestrogen receptors alpha and beta on testicular cell number and steroidogenesis in mice. Reproduction. 2007, 134: 271-279.CrossRefPubMed
13.
go back to reference El-Shafei M, Mostafa M, Mostafa T: Oestrogen receptors in the developing rat prostate. Andrologia. 2011, 43: 94-99.CrossRefPubMed El-Shafei M, Mostafa M, Mostafa T: Oestrogen receptors in the developing rat prostate. Andrologia. 2011, 43: 94-99.CrossRefPubMed
14.
go back to reference Filipiak E, Suliborska D, Laszczynska M, Walczak-Jedrzejowska R, Oszukowska E, Marchlewska K, Kula K, Slowikowska-Hilczer J: Estrogen receptor alpha localization in the testes of men with normal spermatogenesis. Folia Histochem Cytobiol. 2012, 50: 340-345.CrossRef Filipiak E, Suliborska D, Laszczynska M, Walczak-Jedrzejowska R, Oszukowska E, Marchlewska K, Kula K, Slowikowska-Hilczer J: Estrogen receptor alpha localization in the testes of men with normal spermatogenesis. Folia Histochem Cytobiol. 2012, 50: 340-345.CrossRef
15.
go back to reference 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: 263-265.CrossRefPubMed 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: 263-265.CrossRefPubMed
16.
go back to reference Ogawa S, Inoue S, Watanabe T, Hiroi H, Orimo A, Hosoi T, Ouchi Y, Muramatsu M: The complete primary structure of human estrogen receptor beta (hERbeta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun. 1998, 243: 122-126.CrossRefPubMed Ogawa S, Inoue S, Watanabe T, Hiroi H, Orimo A, Hosoi T, Ouchi Y, Muramatsu M: The complete primary structure of human estrogen receptor beta (hERbeta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun. 1998, 243: 122-126.CrossRefPubMed
17.
go back to reference Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjöld M, Gustafsson JA: Human estrogen receptor β-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 1997, 82: 4258-4265.PubMed Enmark E, Pelto-Huikko M, Grandien K, Lagercrantz S, Lagercrantz J, Fried G, Nordenskjöld M, Gustafsson JA: Human estrogen receptor β-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 1997, 82: 4258-4265.PubMed
18.
go back to reference Gennari L, Merlotti D, De Paola V, Calabro A, Becherini L, Martini G, Nuti R: Estrogen receptor gene polymorphisms and the genetics of osteoporosis: a HuGE review. Am J Epidemiol. 2005, 161: 307-320.CrossRefPubMed Gennari L, Merlotti D, De Paola V, Calabro A, Becherini L, Martini G, Nuti R: Estrogen receptor gene polymorphisms and the genetics of osteoporosis: a HuGE review. Am J Epidemiol. 2005, 161: 307-320.CrossRefPubMed
19.
go back to reference Meng J, Mu X, Wang Y: Influence of the XbaI polymorphism in the estrogen receptor-α gene on human spermatogenic defects. Genet Mol Res. 2013, 12: 1808-1815.CrossRefPubMed Meng J, Mu X, Wang Y: Influence of the XbaI polymorphism in the estrogen receptor-α gene on human spermatogenic defects. Genet Mol Res. 2013, 12: 1808-1815.CrossRefPubMed
20.
go back to reference Ogata T, Fukami M, Yoshida R, Nagata E, Fujisawa Y, Yoshida A, Yoshimura Y: Haplotype analysis of ESR2 in Japanese patients with spermatogenic failure. J Hum Genet. 2012, 57: 449-452.CrossRefPubMed Ogata T, Fukami M, Yoshida R, Nagata E, Fujisawa Y, Yoshida A, Yoshimura Y: Haplotype analysis of ESR2 in Japanese patients with spermatogenic failure. J Hum Genet. 2012, 57: 449-452.CrossRefPubMed
21.
go back to reference 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: 193-203.CrossRefPubMed 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: 193-203.CrossRefPubMed
22.
go back to reference Lazaros LA, Xita NV, Kaponis AI, Zikopoulos KA, Plachouras NI, Georgiou IA: Estrogen receptor α and β polymorphisms Are associated with semen quality. J Androl. 2010, 31: 291-298.CrossRefPubMed Lazaros LA, Xita NV, Kaponis AI, Zikopoulos KA, Plachouras NI, Georgiou IA: Estrogen receptor α and β polymorphisms Are associated with semen quality. J Androl. 2010, 31: 291-298.CrossRefPubMed
23.
go back to reference Khattri A, Pandey R, Gupta N, Chakravarty B, Deendayal M, Singh L, Thangaraj K: CA repeat and RsaI polymorphisms in ERβ gene are not associated with infertility in Indian men. Int J Androl. 2009, 32: 81-87.CrossRefPubMed Khattri A, Pandey R, Gupta N, Chakravarty B, Deendayal M, Singh L, Thangaraj K: CA repeat and RsaI polymorphisms in ERβ gene are not associated with infertility in Indian men. Int J Androl. 2009, 32: 81-87.CrossRefPubMed
24.
go back to reference Omrani M, Samadzadae S, Farshid B, Jahandidae B, Yazdanpanah K: Is there any association between ER gene polymorphism and infertility in Iranian men?. J Res Med Sci. 2006, 11: 48-52. Omrani M, Samadzadae S, Farshid B, Jahandidae B, Yazdanpanah K: Is there any association between ER gene polymorphism and infertility in Iranian men?. J Res Med Sci. 2006, 11: 48-52.
25.
go back to reference Aschim EL, Giwercman A, Ståhl O, Eberhard J, Cwikiel M, Nordenskjöld A, Haugen TB, Grotmol T, Giwercman YL: The RsaI polymorphism in the estrogen receptor-β gene is associated with male infertility. J Clin Endocrinol Metab. 2005, 90: 5343-5348.CrossRefPubMed Aschim EL, Giwercman A, Ståhl O, Eberhard J, Cwikiel M, Nordenskjöld A, Haugen TB, Grotmol T, Giwercman YL: The RsaI polymorphism in the estrogen receptor-β gene is associated with male infertility. J Clin Endocrinol Metab. 2005, 90: 5343-5348.CrossRefPubMed
26.
go back to reference Kukuvitis A, Georgiou I, Bouba I, Tsirka A, Giannouli C, Yapijakis C, Tarlatzis B, Bontis J, Lolis D, Sofikitis N: Association of oestrogen receptor α polymorphisms and androgen receptor CAG trinucleotide repeats with male infertility: a study in 109 Greek infertile men. Int J Androl. 2002, 25: 149-152.CrossRefPubMed Kukuvitis A, Georgiou I, Bouba I, Tsirka A, Giannouli C, Yapijakis C, Tarlatzis B, Bontis J, Lolis D, Sofikitis N: Association of oestrogen receptor α polymorphisms and androgen receptor CAG trinucleotide repeats with male infertility: a study in 109 Greek infertile men. Int J Androl. 2002, 25: 149-152.CrossRefPubMed
28.
go back to reference Midgette AS, Wong JB, Beshansky JR, Porath A, Fleming C, Pauker SG: Cost-effectiueness of streptokinase for acute myocardial infarction a combined meta-analysis and decision analysis of the effects of infarct location and of likelihood of infarction. Med Decis Making. 1994, 14: 108-117.CrossRefPubMed Midgette AS, Wong JB, Beshansky JR, Porath A, Fleming C, Pauker SG: Cost-effectiueness of streptokinase for acute myocardial infarction a combined meta-analysis and decision analysis of the effects of infarct location and of likelihood of infarction. Med Decis Making. 1994, 14: 108-117.CrossRefPubMed
31.
go back to reference Duval S, Tweedie R: Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000, 56: 455-463.CrossRefPubMed Duval S, Tweedie R: Trim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysis. Biometrics. 2000, 56: 455-463.CrossRefPubMed
35.
go back to reference Couse JF, Korach KS: Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr Rev. 1999, 20: 358-417.CrossRefPubMed Couse JF, Korach KS: Estrogen receptor null mice: what have we learned and where will they lead us?. Endocr Rev. 1999, 20: 358-417.CrossRefPubMed
36.
go back to reference Carreau S, Delalande C, Silandre D, Bourguiba S, Lambard S: Aromatase and estrogen receptors in male reproduction. Mol Cell Endocrinol. 2006, 246: 65-68.CrossRefPubMed Carreau S, Delalande C, Silandre D, Bourguiba S, Lambard S: Aromatase and estrogen receptors in male reproduction. Mol Cell Endocrinol. 2006, 246: 65-68.CrossRefPubMed
37.
go back to reference Watson CE, Gauthier SY, Davies PL: Structure and expression of the highly repetitive histone H1-related sperm chromatin proteins from winter flounder. Eur J Biochem. 1999, 262: 258-267.CrossRefPubMed Watson CE, Gauthier SY, Davies PL: Structure and expression of the highly repetitive histone H1-related sperm chromatin proteins from winter flounder. Eur J Biochem. 1999, 262: 258-267.CrossRefPubMed
38.
go back to reference Hamden K, Silandre D, Delalande C, ElFeki A, Carreau S: Protective effects of estrogens and caloric restriction during aging on various rat testis parameters. Asian J Androl. 2008, 10: 837-845.CrossRefPubMed Hamden K, Silandre D, Delalande C, ElFeki A, Carreau S: Protective effects of estrogens and caloric restriction during aging on various rat testis parameters. Asian J Androl. 2008, 10: 837-845.CrossRefPubMed
39.
go back to reference Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ, Klinge CM: Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol. 2008, 22: 609-622.PubMedCentralCrossRefPubMed Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ, Klinge CM: Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol. 2008, 22: 609-622.PubMedCentralCrossRefPubMed
40.
go back to reference Försti A, Zhao C, Israelsson E, Dahlman-Wright K, Gustafsson J-Å, Hemminki K: Polymorphisms in the estrogen receptor beta gene and risk of breast cancer: no association. Breast Cancer Res Treat. 2003, 79: 409-413.CrossRefPubMed Försti A, Zhao C, Israelsson E, Dahlman-Wright K, Gustafsson J-Å, Hemminki K: Polymorphisms in the estrogen receptor beta gene and risk of breast cancer: no association. Breast Cancer Res Treat. 2003, 79: 409-413.CrossRefPubMed
41.
go back to reference Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M: Molecular cloning and characterization of human estrogen receptor βcx: a potential inhibitor of estrogen action in human. Nucleic Acids Res. 1998, 26: 3505-3512.PubMedCentralCrossRefPubMed Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y, Muramatsu M: Molecular cloning and characterization of human estrogen receptor βcx: a potential inhibitor of estrogen action in human. Nucleic Acids Res. 1998, 26: 3505-3512.PubMedCentralCrossRefPubMed
42.
go back to reference Peng B, Lu B, Leygue E, Murphy L: Putative functional characteristics of human estrogen receptor-beta isoforms. J Mol Endocrinol. 2003, 30: 13-29.CrossRefPubMed Peng B, Lu B, Leygue E, Murphy L: Putative functional characteristics of human estrogen receptor-beta isoforms. J Mol Endocrinol. 2003, 30: 13-29.CrossRefPubMed
43.
go back to reference Shen LX, Basilion JP, Stanton VP: Single-nucleotide polymorphisms can cause different structural folds of mRNA. Proc Natl Acad Sci. 1999, 96: 7871-7876.PubMedCentralCrossRefPubMed Shen LX, Basilion JP, Stanton VP: Single-nucleotide polymorphisms can cause different structural folds of mRNA. Proc Natl Acad Sci. 1999, 96: 7871-7876.PubMedCentralCrossRefPubMed
44.
go back to reference Iida K, Akashi H: A test of translational selection at ‘silent’ sites in the human genome: base composition comparisons in alternatively spliced genes. Gene. 2000, 261: 93-105.CrossRefPubMed Iida K, Akashi H: A test of translational selection at ‘silent’ sites in the human genome: base composition comparisons in alternatively spliced genes. Gene. 2000, 261: 93-105.CrossRefPubMed
45.
go back to reference Kinoshita Y, Chen S: Induction of aromatase (CYP19) expression in breast cancer cells through a nongenomic action of estrogen receptor alpha. Cancer Res. 2003, 63: 3546-3555.PubMed Kinoshita Y, Chen S: Induction of aromatase (CYP19) expression in breast cancer cells through a nongenomic action of estrogen receptor alpha. Cancer Res. 2003, 63: 3546-3555.PubMed
46.
go back to reference Carreau S, Bouraima-Lelong H, Delalande C: Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci. 2012, 57: 31-36.CrossRefPubMed Carreau S, Bouraima-Lelong H, Delalande C: Estrogen, a female hormone involved in spermatogenesis. Adv Med Sci. 2012, 57: 31-36.CrossRefPubMed
47.
go back to reference Robertson KM, O’Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER: Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci. 1999, 96: 7986-7991.PubMedCentralCrossRefPubMed Robertson KM, O’Donnell L, Jones ME, Meachem SJ, Boon WC, Fisher CR, Graves KH, McLachlan RI, Simpson ER: Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc Natl Acad Sci. 1999, 96: 7986-7991.PubMedCentralCrossRefPubMed
48.
go back to reference Westberg L, Baghaei F, Rosmond R, Hellstrand M, Landén M, Jansson M, Holm G, Björntorp P, Eriksson E: Polymorphisms of the androgen receptor gene and the estrogen receptor beta gene are associated with androgen levels in women. J Clin Endocrinol Metab. 2001, 86: 2562-2568.PubMed Westberg L, Baghaei F, Rosmond R, Hellstrand M, Landén M, Jansson M, Holm G, Björntorp P, Eriksson E: Polymorphisms of the androgen receptor gene and the estrogen receptor beta gene are associated with androgen levels in women. J Clin Endocrinol Metab. 2001, 86: 2562-2568.PubMed
49.
go back to reference Ascenzi P, Bocedi A, Marino M: Structure-function relationship of estrogen receptor alpha and beta: impact on human health. Mol Aspects Med. 2006, 27: 299-402.CrossRefPubMed Ascenzi P, Bocedi A, Marino M: Structure-function relationship of estrogen receptor alpha and beta: impact on human health. Mol Aspects Med. 2006, 27: 299-402.CrossRefPubMed
50.
go back to reference Hammond GL: Access of reproductive steroids to target tissues. Obstet Gynecol Clin North Am. 2002, 29: 411-423.CrossRefPubMed Hammond GL: Access of reproductive steroids to target tissues. Obstet Gynecol Clin North Am. 2002, 29: 411-423.CrossRefPubMed
51.
go back to reference Pavlovich CP, King P, Goldstein M, Schlegel PN: Evidence of a treatable endocrinopathy in infertile men. J Urol. 2001, 165: 837-841.CrossRefPubMed Pavlovich CP, King P, Goldstein M, Schlegel PN: Evidence of a treatable endocrinopathy in infertile men. J Urol. 2001, 165: 837-841.CrossRefPubMed
52.
go back to reference Dipple KM, Phelan JK, McCabe ER: Consequences of complexity within biological networks: robustness and health, or vulnerability and disease. Mol Genet Metab. 2001, 74: 45-50.CrossRefPubMed Dipple KM, Phelan JK, McCabe ER: Consequences of complexity within biological networks: robustness and health, or vulnerability and disease. Mol Genet Metab. 2001, 74: 45-50.CrossRefPubMed
Metadata
Title
Polymorphisms in estrogen receptors predict the risk of male infertility: a meta-analysis
Authors
Tian-Fu Li
Qiu-Yue Wu
Cui Zhang
Wei-Wei Li
Na Li
Ying-Xia Cui
Xiao-Jun Li
Xin-Yi Xia
Publication date
01-12-2014
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2014
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-12-79

Other articles of this Issue 1/2014

Reproductive Biology and Endocrinology 1/2014 Go to the issue