Hormonal therapy for non-obstructive azoospermia: basic and clinical perspectives

Reproductive Medicine and Biology

Volumn 14, Issue 2, 2015, Pages 65-72

  Shiraishi, Koji ^a  

^a YAMAGUCHI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Gonadotropins; Hormonal therapy; Intratesticular testosterone; Non obstructive azoospermia; Testicular sperm extraction

Indexed keywords

ANTIESTROGEN; AROMATASE INHIBITOR; CHORIONIC GONADOTROPIN; CLOMIFENE CITRATE; FOLLITROPIN; GONADOTROPIN; TAMOXIFEN; TESTOSTERONE;

AZOOSPERMIA; DRUG EFFICACY; DRUG INDICATION; HORMONAL THERAPY; HORMONE ACTION; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; MICRODISSECTION TESTICULAR SPERM EXTRACTION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SERTOLI CELL; SPERMATOGENESIS; TESTICULAR SPERM EXTRACTION; TESTOSTERONE BLOOD LEVEL;

EID: 84926309016     PISSN: 14455781     EISSN: 14470578     Source Type: Journal    
DOI: 10.1007/s12522-014-0193-1     Document Type: Review

References (59)

1. Schlegel PN. Nonobstructive azoospermia: a revolutionary surgical approach and results. Semin Reprod Med. 2009;27:165–70.
2. Shiraishi K, Oka S, Matsuyama H. Assessment of quality of life during gonadotrophin treatment for male hypogonadotrophic hypogonadism. Clin Endocrinol (Oxf). 2014;81(2):259–65.
3. McLachlan RI. The endocrine control of spermatogenesis. Baillieres Best Pract Res Clin Endocrinol Metab. 2000;14:345–62.
4. Hussein A, Ozgok Y, Ross L, Rao P, Niederberger C. Optimization of spermatogenesis-regulating hormones in patients with non-obstructive azoospermia and its impact on sperm retrieval: a multicentre study. BJU Int. 2013;111:110–4.
5. Reifsnyder JE, Ramasamy R, Husseini J, Schlegel PN. Role of optimizing testosterone before microdissection testicular sperm extraction in men with non-obstructive azoospermia. J Urol. 2012;188:532–6.
6. Ramasamy R, Ricci JA, Palermo GD, Gosden LV, Rosenwaks Z, Schlegel PN. Successful fertility treatment for Klinefelter’s syndrome. J Urol. 2009;182:1108–13.
7. Shiraishi K, Matsuyama H. Local expression of epidermal growth factor-like factors in human testis and its role in spermatogenesis. J Androl. 2012;33:66–73.
8. Silva FR, Leite LD, Wassermann GF. Rapid signal transduction in Sertoli cells. Eur J Endocrinol. 2002;147:425–33.
9. Takeda H, Chodak G, Mutchnik S, Nakamoto T, Chang C. Immunohistochemical localization of androgen receptors with mono- and polyclonal antibodies to androgen receptor. J Endocrinol. 1990;126(1):17–25.
10. de Ruizeveld Winter JA, Trapman J, Vermey M, Mulder E, Zegers ND, van der Kwast TH. Androgen receptor expression in human tissues: an immunohistochemical study. J Histochem Cytochem. 1991;39:927–36.
11. Iwamura M, Abrahamsson P-A, Benning M, Cockett AT, Sant’Agnese PA. Androgen receptor immunostaining and its tissue distribution in formalin fixed, paraffin-embedded sections after microwave treatment. J Histochem Cytochem. 1994;42:783–8.
12. Van Roijen JH, van Assen S, van der Kwast TH, de Rooij DG, Boersma WJA, Vreeburg JTM, Weber RFA. Androgen receptor immunoexpression in the testes of subfertile men. J Androl. 1995;16:510–6.
13. Kimura N, Mizokami A, Oonuma T, Sasano H, Nagura H. Immunocytochemical localization of androgen receptor with polyclonal antibody in paraffin-embedded human tissues. J Hisiochem Cytochem. 1993;41:671–8.
14. Guillaume E, Pineau C, Evrard B, Dupaix A, Moertz E, Sanchez JC, Hochstrasser DF, et al. Cellular distribution of translationally controlled tumor protein in rat and human testes. Proteomics. 2001;1:880–90.
15. Kato Y, Shiraishi K, Matsuyama H. Expression of testicular androgen receptor in non-obstructive azoospermia and its change after hormonal therapy. Andrology 2014, in press.
16. Singh J, Handelsman DJ. Neonatal administration of FSH increases Sertoli cell numbers and spermatogenesis in gonadotropin-deficient (hpg) mice. J Endocrinol. 1996;151:37–48.
17. McLachlan RI, O`Donnell L, Meacham SJ, Stanton PG, de Krester DM, Pratis K, et al. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Prog Horm Res. 2002;57:149–79.
18. Griswold MD. Perspective on the function of Sertoli cells. In: Griswold MD, editor. Sertoli cell biology. San Diego: Elsevier Science; 2005. p. 15–8.
19. O’Shaughnessy PJ, Verhoeven G, De Gerndt K, Monteiro A, Abel MH. Direct action through the Sertoli cells is essential for androgen stimulation of spermatogenesis. Endocrinology. 2010;151:2343–8.
20. Chang C, Chen YT, Yeh SD, Xu Q, Wang RS, Guillou F, et al. Infertility with defective spermatogenesis and hypotestosteronemia in male mice lacking the androgen receptor in Sertoli cells. Proc Natl Acad Sci USA. 2004;101:6876–81.
21. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, et al. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA. 2004;101:1327–32.
22. Holdcraft RW, Braun RE. Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development. 2004;131:459–67.
23. Hazra R, Corcoran L, Robson M, McTavish KJ, Upton D, Handelsman DJ, Allan CM. Temporal role of Sertoli cell androgen receptor expression in spermatogenic development. Mol Endocrinol. 2013;27:12–24.
24. Jarow JP, Chen H, Rosner TW, Trentacoste S, Zirkin BR. Assessment of the androgen environment within the human testis: minimally invasive method to obtain intratesticular fluid. J Androl. 2001;22:640–5.
25. Coviello AD, Matsumoto AM, Bremner WJ, Herbst KL, Amory JK, Anawalt BD, et al. Low-dose human chorionic gonadotropin maintains intratesticular testosterone in normal men with testosterone-induced gonadotropin suppression. J Clin Endocrinol Metab. 2005;90:595–602.
26. Matthiesson KL, McLachlan RI, O’Donnell L, Frydenberg M, Robertoson DM, Stanton PG, et al. The relative roles of follicle-stimulating hormone and luteinizing hormone in maintaining spermatogonial maturation and spermiation in normal men. J Clin Endocrinol Metab. 2006;91:3962–9.
27. Shinjo E, Shiraishib K, Matsuyama H. The effect of human chorionic gonadotropin-based hormonal therapy on intratesticular testosterone levels and spermatogonial DNA synthesis in men with non-obstructive azoospermia. Andrology. 2013;1:929–35.
28. Sigman M, Vance ML. Medical treatment of idiopathic infertility. Urol Clin North Am. 1987;14:459–69.
29. Chua ME, Escusa KG, Luna S, Tapia LC, Dofitas B, Morales M. Revisiting oestrogen antagonists (clomiphene or tamoxifen) as medical empiric therapy for idiopathic male infertility: a meta-analysis. Andrology. 2013;1:749–57.
30. Raman JD, Schlegel PN. Aromatase inhibitors for male infertility. J Urol. 2002;167:624–9.
31. Pavlovich CP, King P, Goldstein M, Schlegel PN. Evidence of a treatable endocrinopathy in infertile men. J Urol. 2001;165:837–41.
32. Schiff JD, Palermo GD, Veeck LL, Goldstein M, Rosenwaks Z, Schlegel PN. Success of testicular sperm extraction [corrected] and intracytoplasmic sperm injection in men with Klinefelter syndrome. J Clin Endocrinol Metab. 2005;90:6263–7.
33. Cao YX, Zhang ZG. A successful pregnancy outcome using testicular sperm from an infertile male pretreated with hCG. Arch Androl. 2007;53:1–3.
34. Selman HA, Cipollone G, Stuppia L, De Santo M, Sterzik K, El-Danasouri I. Gonadotropin treatment of an azoospermic patient with a Ychromosome microdeletion. Fertil Steril. 2004;82:218–9.
35. Efesoy O, Cayan S, Akbay E. The efficacy of recombinant human follicle stimulating hormone in the treatment of various types of male-factor infertility at a single university hospital. J Androl. 2009;30:679–84.
36. Weiss J, Axelrod L, Whitcomb RW, Harris PE, Crowley WF, Jameson JL. Hypogonadism caused by a single amino acid substitution in the β subunit of luteinizing hormone. N Engl J Med. 1992;326:179–83.
37. Valdes-Socin H, Salvi R, Daly AF, Valdes-Socin H, Salvi R, Daly AF, et al. Hypogonadism in a patient with a mutation in the luteinizing hormone β subunit gene. N Engl J Med. 2004;351:2619–25.
38. Achard C, Courtillot C, Lahuna O, Me´duri G, Soufir JC, et al. Normal spermatogenesis in a man with mutant luteinizing hormone. N Engl J Med. 2009;361:1856–63.
39. Lofrano-Porto A, Barra GB, Giacomini LA, Nascimento PP, Latronico AC, Casulari LA, et al. Luteinizing hormone β mutation and hypogonadism in men and women. N Engl J Med. 2007;357:897–904.
40. Basciani S, Watanabe M, Mariani S, Paseri M, Persichetti A, Fiore D, et al. Hypogonadism in a patient with two novel mutations of the lutteinizing hormone β-subunit gene expressed in a compound heterozygous form. J Clin Endocrinol Metab. 2012;97:3031–8.
41. Shiraishi K, Naito K. Fertile eunuch syndrome with the mutations (Trp8Arg and Ile15Thr) in the beta subunit of luteinizing hormone. Endocr J. 2003;50:733–7.
42. Lamminen T, Jokinen P, Jiang M, et al. Human FSHβsubunit gene is highly conserved. Mol Hum Reprod. 2005;11:601–5.
43. Matthews CH, Borgato S, Beck-Peccoz P, Adams M, Tone Y, Gambino G, et al. Primary amenorrhoea and infertility due to a mutation in the b-subunit of follicle-stimulating hormone. Nat Genet. 1993;5:83–6.
44. Phillip M, Arbelle JE, Segev Y, Parvari R. Male hypogonadism due to a mutation in the gene for the b-subunit of follicle stimulating hormone. N Engl J Med. 1998;338:1729–32.
45. Layman LC, Lee EJ, Peak DB, Namnoum AB, Vu KV, van Lingen BL, et al. Delayed puberty and hypogonadism caused by mutations in the follicle-stimulating hormone b-subunit gene. N Engl J Med. 1997;337:607–11.
46. Lindstedt G, Nystro¨m E, Matthews C, Ernest I, Janson PO, Chatterjee K. Follitropin (FSH) deficiency in an infertile male due to FSHb gene mutation. A syndrome of normal puberty and virilization but underdeveloped testicles with azoospermia, low FSH but high lutropin and normal serum testosterone concentrations. Clin Chem Lab Med. 1998;36:663–5.
47. Themmen AP, Huhtaniemi IT. Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocr Rev. 2000;21:551–83.
48. Foresta C, Bettella A, Spolaore D, Merico M, Rossato M, Ferlin A. Suppression of the high endogenous levels of plasma FSH in infertile men are associated with improved Sertoli cell function as reflected by elevated levels of plasma inhibin B. Hum Reprod. 2004;19:1431–7.
49. Shiraishi K, Ohmi C, Shimabukuro T, Matsuyama H. Human chorionic gonadotrophin treatment prior to microdissection testicular sperm extraction in non-obstructive azoospermia. Hum Reprod. 2012;27:331–9.
50. Steger K, Aleithe I, Behre H, Bergmann M. The proliferation of spermatogonia in normal and pathological human seminiferous epithelium: an immunohistochemical study using monoclonal antibodies against Ki-67 protein and proliferating cell nuclear antigen. Mol Hum Reprod. 1998;4:227–33.
51. Bar-Shira Maymon B, Yogev L, Yavetz H, Lifschitz-Mercer B, Schreiber L, Kleiman S, et al. Spermatogonial proliferation patterns in men with azoospermia of different etiologies. Fertil Steril. 2003;80:1175–80.
52. Salama N, Tsuji M, Tamura M, Kagawa S. Prolifelating cell nuclear antigen in testes of infertile men with varicocele. Scand J Urol Nephrol. 2003;37:48–52.
53. Takagi S, Itoh N, Kimura M, Sasao T, Tsukamoto T. Spermatogonial proliferation and apoptosis in hypospermatogenesis associated with nonobstructive azoospermia. Fertil Steril. 2001;76:901–7.
54. Ruwanpura SM, McLachlan R, Stanton PG, Meacham SJ. Follicle-stimulating hormone affects spermatogonial survival by regulating intrinsic apoptotic pathway in adults rats. Biol Reprod. 2008;78:705–13.
55. Henriksén K, Kangasniemi M, Parvinen M, Kaipa A, Hakovirta H. In vitro, follicle-stimulating hormone prevents apoptosis and stimulates deoxyribonucleic acid synthesis in the rat seminiferous epithelium in a stage-specific fashion. Endocrinology. 1996;137(5):2141–9.
56. Freeman DA, Ascoli M. Desensitization of steroidogenesis in cultured Leydig tumor cells: role of cholesterol. Proc Natl Acad Sci USA. 1982;79:7796–800.
57. Sharpe RM, McKinnell C, Kivlin C, Fisher JS. Proliferation and functional maturation of Sertoli cells, and their relevance to disorders of testis function in adulthood. Reproduction. 2003;125:769–84.
58. Verhoeven G, Willems A, Denolet E, Swinnen JV, De Gendt K. Androgens and spermatogenesis: lessons from transgenic mouse models. Philos Trans R Soc Lond B Biol Sci. 2010;365:1537–56.
59. Hill CM, Anway MD, Zirkin BR, Brown TR. Intratesticular androgen levels, androgen receptor localization, and androgen receptor expression in adult rat Sertoli cells. Biol Reprod. 2004;71:1348–58.