Could androgen receptor gene CAG tract polymorphism affect spermatogenesis in men with idiopathic infertility?

Journal of Assisted Reproduction and Genetics

Volumn 31, Issue 6, 2014, Pages 689-697

  Giagulli, V A ^a,c,e   Carbone, M D ^b,c   De Pergola, G ^d   Guastamacchia, E ^a   Resta, F ^a   Licchelli, B ^a   Sabba C ^a   Triggiani, V ^a  

^a UNIVERSITY OF BARI   (Italy)

^b Institute of Clinical and Hormonal Research   (Italy)

^c Biomedical Research Association Guglielmo Telesforo   (Italy)

^d Clinical Experimental Oncology Unit   (Italy)

^e ASL Bari   (Italy)

Author keywords

CAG repeat length polymorphism; Idiopathic male infertility; Inhibin B and testosterone; Leydig cell; Sertoli cell; Y chromosome long arm microdeletions

Indexed keywords

ANDROGEN RECEPTOR; FOLLITROPIN; INHIBIN B; LUTEINIZING HORMONE; TESTOSTERONE; TRINUCLEOTIDE;

ADULT; ARTICLE; AZOOSPERMIA; CAG REPEAT; CHROMOSOME DELETION Y; CONTROLLED STUDY; CRYPTORCHISM; DISEASE ASSOCIATION; FOLLITROPIN BLOOD LEVEL; GENETIC POLYMORPHISM; GENOTYPE; HUMAN; IDIOPATHIC DISEASE; LUTEINIZING HORMONE BLOOD LEVEL; MAJOR CLINICAL STUDY; MALE; MULTIPLE PREGNANCY; OBSERVATIONAL STUDY; OLIGOSPERMIA; PHENOTYPE; PRIORITY JOURNAL; SEMEN ANALYSIS; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY; TESTIS SIZE; TESTOSTERONE BLOOD LEVEL; Y CHROMOSOME; CHROMOSOME DELETION; DISORDER OF SEX DEVELOPMENT; GENETICS; MALE INFERTILITY; MIDDLE AGED; PATHOLOGY; SEX CHROMOSOME ABERRATION; TRINUCLEOTIDE REPEAT;

ADULT; CHROMOSOME DELETION; CHROMOSOMES, HUMAN, Y; CRYPTORCHIDISM; HUMANS; INFERTILITY, MALE; MALE; MIDDLE AGED; OLIGOSPERMIA; RECEPTORS, ANDROGEN; SEX CHROMOSOME ABERRATIONS; SEX CHROMOSOME DISORDERS OF SEX DEVELOPMENT; SPERM COUNT; SPERM MOTILITY; SPERMATOGENESIS; TRINUCLEOTIDE REPEATS;

EID: 84904093062     PISSN: 10580468     EISSN: 15737330     Source Type: Journal    
DOI: 10.1007/s10815-014-0221-4     Document Type: Article

References (52)

1. Forti G, Krausz C. Clinical review 100: evaluation and treatment of the infertile couple. J Clin Endocrinol Metab. 1998;83(12):4177-88. (Pubitemid 29100106)
2. De Kretser DM, Baker HW. Infertility in men: recent advances and continuing controversies. J Clin Endocrinol Metab. 1999;84(10): 3443-50. (Pubitemid 30648835)
3. Andersson AM, Petersen JH, Jørgensen N, Jensen TK, Skakkebaek NE. Serum inhibin B and follicle-stimulating hormone levels as tools in the evaluation of infertile men: significance of adequate reference values from proven fertile men. J Clin Endocrinol Metab. 2004;89(6):2873-9. (Pubitemid 38766379)
4. Giagulli VA, Vermeulen A. Leydig cell function in infertile men with idiopathic oligospermic infertility. J Clin Endocrinol Metab. 1988;66(1):62-7. (Pubitemid 18027730)
5. Andersson AM, Jørgensen N, Frydelund-Larsen L, Rajpert-De Meyts E, Skakkebaek NE. Impaired Leydig cell function in infertile men: a study of 357 idiopathic infertile men and 318 proven fertile controls. J Clin Endocrinol Metab. 2004;89(7):3161-7. (Pubitemid 38951879)
6. Andersson AM, Juul A, Petersen JH, Müller J, Groome NP, Skakkebaek NE. Serum inhibin B in healthy pubertal and adolescent boys: relation to age, stage of puberty, and follicle-stimulating hormone, luteinizing hormone, testosterone, and estradiol levels. J Clin Endocrinol Metab. 1997;82(12):3976-81. (Pubitemid 27525498)
7. Giagulli VA, Carbone D. Hormonal control of inhibin B in men. J Endocrinol Investig. 2006;29(8):706-13. (Pubitemid 44756175)
8. Vermeulen A, Kaufman JM, Giagulli VA. Influence of some biological indexes on sex hormone-binding globulin and androgen levels in aging or obese males. J Clin Endocrinol Metab. 1996;81(5):1821-6. (Pubitemid 26152470)
9. Giagulli VA, Kaufman JM, Vermeulen A. Pathogenesis of the decreased androgen levels in obese men. J Clin Endocrinol Metab. 1994;79(4):997-1000. (Pubitemid 24342237)
10. Ukkola O, Gagnon J, Rankinen T, Thompson PA, Hong Y, Leon AS, et al. Age, body mass index, race and other determinants of steroid hormone variability: the HERITAGE Family Study. Eur J Endocrinol. 2001;145(1):1-9. (Pubitemid 32677670)
11. Kaufman JM, Vermeulen A. The decline of androgen levels in elderly men and its clinical and therapeutic implications. Endocr Rev. 2005;26(6):833-76. (Pubitemid 41428540)
12. Andersson AM, Carlsen E, Petersen JH, Skakkebaek NE. Variation in levels of serum inhibin B, testosterone, estradiol, luteinizing hormone, follicle-stimulating hormone, and sex hormone-binding globulin inmonthly samples from healthymen during a 17-month period: possible effects of seasons. J Clin Endocrinol Metab. 2003;88(2):932-7. (Pubitemid 36207844)
13. Marques-Pinto A, Carvalho D. Human infertility: are endocrine disruptors to blame? Endocrinol Connect. 2013;17(2):E15-29.
14. Buchanan G, YangM, Cheong A, Harris JM, Irvine RA, Lambert PF, et al. Structural and functional consequences of glutamine tract variation in the androgen receptor. Hum Mol Genet. 2004;13(16):1677-92. (Pubitemid 39173438)
15. Crabbe P, Bogaert V, De Bacquer D, Goemaere S, Zmierczak H, Kaufman JM. Part of the interindividual variation in serum testosterone levels in healthy men reflects differences in androgen sensitivity and feedback set point: contribution of the androgen receptor polyglutamine tract polymorphism. J Clin Endocrinol Metab. 2007;92(9):3604-10. (Pubitemid 47435345)
16. Huhtaniemi IT, Pye SR, Limer KL, Thomson W, O'Neill TW, Platt H, et al. Increased estrogen rather than decreased androgen action is associated with longer androgen receptor CAG repeats. J Clin Endocrinol Metab. 2009;94(1):277-84.
17. Zitzmann M, Nieschlag E. The CAG repeat polymorphism within the androgen receptor gene and maleness. Int J Androl. 2003;26(2):76-83. (Pubitemid 36408236)
18. Davis-Dao C, Koh CJ, Hardy BE, Chang A, Kim SS, De Filippo R, et al. Shorter androgen receptor CAG repeat lengths associated with cryptorchidism risk among Hispanic white boys. J Clin Endocrinol Metab. 2012;97(3):E393-9.
19. Krausz C. An encore for the repeats: new insights into an old genetic variant. J Clin Endocrinol Metab. 2012;97(3):764-7.
20. World Health Organization. Manual for the standardized investigation and diagnosis of infertile couples. Cambridge: Cambridge University Press; 2000.
21. National Collaborating Centre for Women's and Children's Health. Fertility guideline: assessment and treatment for people with infertility problems (second draft). Available at: http://guidance.nice.org.uk/CG11; (2004).
22. Devroey P, Fauser BC, Diedrich K, Evian Annual Reproduction (EVAR)Workshop Group 2008. Approaches to improve the diagnosis and management of infertility. Hum Reprod Update. 2009;15(4): 391-408.
23. Nenonen HA, Giwercman A, Hallengren E, Giwercman YL. Nonlinear association between androgen receptor CAG repeat length and risk of male subfertility-a meta-analysis. Int J Androl. 2011;34(4): 327-32.
24. Virtanen HE, Bjerknes R, Cortes D, Jørgensen N, Rajpert-De Meyts E, Thorsson AV, et al. Cryptorchidism: classification, prevalence and long-term consequences. Acta Paediatr. 2007;96(5):611-6. (Pubitemid 46653177)
25. Foresta C, Zuccarello D, Garolla A, Ferlin A. Role of hormones, genes, and environment in human cryptorchidism. Endocr Rev. 2008;29(5):560-80.
26. Vogt PH, Edelmann A, Kirsch S, Henegariu O, Hirschmann P, Kiesewetter F, et al. Human Y chromosome azoospermia factors (AZF) mapped to different subregions in Yq11. Hum Mol Genet. 1996;5(7):933-43. (Pubitemid 26232272)
27. Simoni M, Bakker E, EurlingsMC, Matthijs G, Moro E, Müller CR, et al. Laboratory guidelines for molecular diagnosis of Ychromosomal microdeletions. Int J Androl. 1999;22(5):292-9. (Pubitemid 29445884)
28. Simoni M, Bakker E, Krausz C. EAA/EMQN best practice guidelines for molecular diagnosis of y-chromosomalmicrodeletions. State of the art 2004. Int J Androl. 2004;27(4):240-9. (Pubitemid 39062086)
29. Giagulli VA, Carbone MD. Varicocele correction for infertility: which patients to treat? Int J Androl. 2011;34(3):236-41.
30. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Switzerland:WHO; 2010.
31. Nieschlag E, Kamischke A. Empirical therapies for idiopathic male infertility. In: Nieschlag E, Behre HM, Nieschlag S editors. Andrology. Male reproduction heath and dysfunction, 3rd edition. Berlin Heidelberg: Springer-Verlag; 2010. p. 457-467.
32. Jørgensen N, Liu F, Andersson AM, Vierula M, Irvine DS, Auger J, et al. Serum inhibin-b in fertile men is strongly correlated with low but not high sperm counts: a coordinated study of 1,797 European and US men. Fertil Steril. 2010;94(6):2128-34.
33. Singh K, Jaiswal D. Human male infertility: a complex multifactorial phenotype. Reprod Sci. 2011;18(5):418-25.
34. Giwercman A, Giwercman YL. Environmental factors and testicular function. Best Pract Res Clin Endocrinol Metab. 2011;25(2):391-402.
35. O'Flynn O'Brien KL, Varghese AC, Agarwal A. The genetic causes of male factor infertility: a review. Fertil Steril. 2010;93(1):1-12.
36. Weinbauer GF, Niehaus M, Nieschlag E. The role of testosterone in spematogenesis. In: Nieschlag E, Behre HM, Nieschlag S editors. Testosterone action, deficiency, substitution. Cambridge University Press; 2004. p. 173-206.
37. McLachlan RI, O'Bryan MK. State of the art for genetic testing of infertile men. J Clin Endocrinol Metab. 2010;95(3):1013-24.
38. Davis-Dao CA, Tuazon ED, Sokol RZ, Cortessis VK. Male infertility and variation in CAG repeat length in the androgen receptor gene: a meta-analysis. J Clin Endocrinol Metab. 2007;92(11):4319-26. (Pubitemid 350074751)
39. Nenonen H, Björk C, Skjaerpe PA, Giwercman A, Rylander L, Svartberg J, et al. CAG repeat number is not inversely associated with androgen receptor activity in vitro. Mol Hum Reprod. 2010;16(3):153-7.
40. Delli Muti N, Agarwal A, Buldreghini E, Gioia A, Lenzi A, Boscaro M, Balercia G. Have androgen receptor gene CAG and GGC repeat polymorphisms an effect on sperm motility in infertile men? Andrologia. 2013. doi:10.1111/and.12119.
41. Ferlin A, Garolla A, Bettella A, Bartoloni L, Vinanzi C, Roverato A, et al. Androgen receptor gene CAG and GGC repeat lengths in cryptorchidism. Eur J Endocrinol. 2005;152(3):419-25. (Pubitemid 40439495)
42. Canale D, Caglieresi C, Moschini C, Liberati CD, Macchia E, Pinchera A, et al. Androgen receptor polymorphism (CAG repeats) and androgenicity. Clin Endocrinol (Oxf). 2005;63(3):356-61. (Pubitemid 41233456)
43. Blagosklonova O, Joanne C, Roux C, Bittard H, Fellmann F, Bresson JL. Absence of anti-Müllerian hormone (AMH) and M2A immunoreactivities in Sertoli cell-only syndrome and maturation arrest with and without AZF microdeletions. Hum Reprod. 2002;17(8):2062 -5.
44. Bar-Shira Maymon B, Paz G, Elliott DJ, Hammel I, Kleiman SE, Yogev L, et al. Maturation phenotype of Sertoli cells in testicular biopsies of azoospermic men. Hum Reprod. 2000;15(7):1537-42.
45. Rey R, Mebarki F, Forest MG, Mowszowicz I, Cate RL, Morel Y, et al. Anti-müllerian hormone in children with androgen insensitivity. J Clin Endocrinol Metab. 1994;79(4):960-4.
46. Rajpert-De Meyts E, Jørgensen N, Graem N, Müller J, Cate RL, Skakkebaek NE. Expression of anti-Müllerian hormone during normal and pathological gonadal development: association with differentiation of Sertoli and granulosa cells. J Clin Endocrinol Metab. 1999;84(10):3836-44. (Pubitemid 30645250)
47. Sasagawa I, Suzuki Y, Ashida J, Nakada T, Muroya K, Ogata T. CAG repeat length analysis and mutation screening of the androgen receptor gene in Japanese men with idiopathic azoospermia. J Androl. 2001;22(5):804-8. (Pubitemid 32781269)
48. Aschim EL, Nordenskjöld A, Giwercman A, Lundin KB, Ruhayel Y, Haugen TB, et al. Linkage between cryptorchidism, hypospadias, and GGN repeat length in the androgen receptor gene. J Clin Endocrinol Metab. 2004;89(10):5105-9. (Pubitemid 39391456)
49. Silva-RamosM, Oliveira JM, Cabeda JM, Reis A, Soares J, Pimenta A. The CAG repeat within the androgen receptor gene and its relationship to cryptorchidism. Int Braz J Urol. 2006;32(3):330-4.
50. Radpour R, Rezaee M, Tavasoly A, Solati S, Saleki A. Association of long polyglycine tracts (GGN repeats) in exon 1 of the androgen receptor gene with cryptorchidism and penile hypospadias in Iranian patients. J Androl. 2007;28(1):164-9. (Pubitemid 46048090)
51. Rahman F, Christian HC. Non-classical actions of testosterone: an update. Trends Endocrinol Metab. 2007;18(10):371-8. (Pubitemid 350137764)
52. Gatta V, Raicu F, Ferlin A, Antonucci I, Scioletti AP, Garolla A, et al. Testis transcriptome analysis in male infertility: new insight on the pathogenesis of oligo-azoospermia in cases with and without AZFc microdeletion. BMC Genomics. 2010;11:401.