Hormonal regulation of spermatogenesis: Mutant mice challenging old paradigms

European Journal of Endocrinology

Volumn 179, Issue 3, 2018, Pages R143-R150

  Huhtaniemi, Ilpo ^a,b  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FLUTAMIDE; FOLLITROPIN; FOLLITROPIN RECEPTOR; GESTAGEN; GONADOTROPIN; LUTEINIZING HORMONE; LUTEINIZING HORMONE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; MUELLERIAN INHIBITING FACTOR; TESTOSTERONE; FOLLITROPIN BETA SUBUNIT;

ACROMEGALY; ANDROGEN SYNTHESIS; AZOOSPERMIA; CELL MATURATION; CONTRACEPTION; GENE OVEREXPRESSION; GONADOTROPIN RELEASE; HISTOLOGY; HORMONAL REGULATION; HUMAN; HYPOPHYSECTOMY; HYPOPHYSIS PORTAL SYSTEM; KNOCKOUT MOUSE; LEYDIG CELL; MALE; MALE FERTILITY; NEGATIVE FEEDBACK; NONHUMAN; OLIGOSPERMIA; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; REVIEW; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOON COUNT; SPERMATOZOON MATURATION; STEROIDOGENESIS; TESTIS SIZE; TESTOSTERONE BLOOD LEVEL; TESTOSTERONE SYNTHESIS; TRANSGENIC MOUSE; ANIMAL; CHEMISTRY; DEFICIENCY; DRUG EFFECT; GENETIC CROSS; GENETICS; METABOLISM; MOUSE; MUTATION; PHYSIOLOGY; TESTIS;

ANIMALS; CROSSES, GENETIC; FOLLICLE STIMULATING HORMONE; FOLLICLE STIMULATING HORMONE, BETA SUBUNIT; HUMANS; LUTEINIZING HORMONE; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MUTATION; RECEPTORS, FSH; RECEPTORS, LH; SERTOLI CELLS; SPERMATOGENESIS; TESTIS; TESTOSTERONE;

EID: 85051691483     PISSN: 08044643     EISSN: 1479683X     Source Type: Journal    
DOI: 10.1530/EJE-18-0396     Document Type: Review

References (37)

1. McLachlan RI, O'Donnell L, Meachem SJ, Stanton PG, de Kretser DM, Pratis K & Robertson DM. Identification of specific sites of hormonal regulation in spermatogenesis in rats, monkeys, and man. Recent Progress in Hormone Research 2002 57 149-179. (https://doi.org/10.1210/rp.57.1.149).
2. Anderson RA & Baird DT. Male contraception. Endocrine Reviews 2002 23 735-762. (https://doi.org/10.1210/er.2002-0002).
3. Smith LB & Walker WH. Hormonal signaling in the testis. In Knobil and Neill's Physiology of Reproduction, vol 1, pp 637-675. Eds TM Plant & AJ Zeleznik. Waltham: Academic Press, 2015. (https://doi.org/10.1016/B978-0-12-397475-3.00016-8).
4. Turner TT, Jones CE, Howards SS, Ewing LL, Zegeye B & Gunsalus GL. On the androgen microenvironment of maturing spermatozoa. Endocrinology 1984 115 1925-1932. (https://doi.org/10.1210/endo-115-5-1925).
5. Huhtaniemi I, Nikula H & Rannikko S. Treatment of prostatic cancer with a gonadotropin-releasing hormone agonist analog: Acute and long term effects on endocrine functions of testis tissue. Journal of Clinical Endocrinology and Metabolism 1985 61 698-704. (https://doi.org/10.1210/jcem-61-4-698).
6. Singh J, O'Neill C & Handelsman DJ. Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology 1995 136 5311-5321. (https://doi.org/10.1210/endo.136.12.7588276).
7. Roberts KP & Zirkin BR. Androgen regulation of spermatogenesis in the rat. Annals of the New York Academy of Sciences 1991 637 90-106. (https://doi.org/10.1111/j.1749-6632.1991.tb27303.x).
8. Huhtaniemi I. A hormonal contraceptive for men: how close are we? Progress in Brain Research 2010 181 273-288. (https://doi.org/10.1016/S0079-6123(08)81015-1).
9. Tapanainen JS, Aittomäki K, Min J, Vaskivuo T & Huhtaniemi IT. Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nature Genetics 1997 15 205-206. (https://doi.org/10.1038/ng0297-205).
10. Steinberger E. Hormonal control of mammalian spermatogenesis. Physiological Reviews 1991 51 1-22. (https://doi.org/10.1152/physrev.1971.51.1.1).
11. Kumar TR, Wang Y, Lu N & Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not for male fertility. Nature Genetics 1997 15 201-204. (https://doi.org/10.1038/ng0297-201).
12. Dierich A, Sairam MR, Monaco L, Fimia FM, Gansmuller A, Le Meur M & Sassone-Corsi P. Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogeneseis and hormonal imbalance. PNAS 1998 95 13612-13617. (https://doi.org/10.1073/pnas.95.23.13612).
13. Abel MH, Wootton AN, Wilkins V, Huhtaniemi I, Knight PG & Charlton HM. The effect of a null mutation in the FSH receptor gene on mouse reproduction. Endocrinology 2000 141 1795-1803. (https://doi.org/10.1210/endo.141.5.7456).
14. Zheng J, Mao J, Cui M, Liu Z, Wang X, Xiong S, Nie M & Wu X. Novel FSHβ mutation in a male patient with isolated FSH deficiency and infertility. European Journal of Medical Genetics 2017 60 335-339. (https://doi.org/10.1016/j.ejmg.2017.04.004).
15. Zhang FP, Poutanen M, Wilbertz J & Huhtaniemi I. Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knockout (LuRKO) mice. Molecular Endocrinology 2001 15 172-183. (https://doi.org/10.1210/mend.15.1.0582).
16. Peltoketo H, Strauss L, Karjalainen R, Zhang M, Stamp GW, Segaloff DL, Poutanen M & Huhtaniemi IT. Female mice expressing constitutively active mutants of FSH receptor present with a phenotype of premature follicle depletion and estrogen excess. Endocrinology 2010 151 1872-1883. (https://doi.org/10.1210/en.2009-0966).
17. El-Hefnawy T, Luconi M, Baldi E, Slotte JP, Manna PR & Huhtaniemi I. Progesterone action in a murine Leydig tumor cell line (mLTC-1) possibly through a non-classical receptor type. Endocrinology 2000 141 247-255. (https://doi.org/10.1210/endo.141.1.7253).
18. El-Gehani F, Zhang F-P, Pakarinen P, Rannikko A & Huhtaniemi I. Gonadotropin-independent regulation of steroidogenesis in the rat fetal testis. Biology of Reproduction 1998 58 116-123. (https://doi.org/10.1095/biolreprod58.1.116).
19. Pakarinen P, Kimura S, El-Gehani F, Pelliniemi LJ & Huhtaniemi I. Pituitary hormones are not required for sexual differentiation of male mice: phenotype of the T/ebp/Nkx2.1 null mutant mice. Endocrinology 2002 143 4477-4482. (https://doi.org/10.1210/en.2002-220052).
20. Zhang FP, Pakarainen T, Poutanen M, Toppari J & Huhtaniemi I. The low gonadotropin independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. PNAS 2003 100 13692-13697. (https://doi.org/10.1073/pnas.2232815100).
21. Oduwole OO, Vydra N, Wood NEM, Samanta L, Owen L, Keevil B, Donaldson M, Naresh K & Huhtaniemi IT. The overlapping dose-responses of spermatogenic and extragonadal testosterone actions jeopardise the principle of hormonal male contraception. FASEB Journal 2014 28 2566-2576. (https://doi.org/10.1096/fj.13-249219).
22. Norio R. The Finnish disease heritage III: the individual diseases. Human Genetics 2003 112 470-526.
23. Aittomäki K, Dieguez Lucena JL, Pakarinen P, Sistonen P, Tapanainen J, Gromoll J, Kaskikari R, Sankila E-M, Lehväslaiho H, Reyes Engel A et al. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995 82 959-968. (https://doi.org/10.1016/0092-8674(95)90275-9).
24. Rannikko A, Pakarinen P, Manna PR, Beau I, Misrahi M & Aittomäki K. Functional characterization of the human FSH receptor with an inactivating Ala189Val mutation. Molecular Human Reproduction 2002 8 311-317. (https://doi.org/10.1093/molehr/8.4.311).
25. Gromoll J, Simoni M & Nieschlag E. An activating mutation of the follicle-stimulating hormone receptor autonomously sustains spermatogenesis in a hypophysectomized man. Journal of Clinical Endocrinology and Metabolism 1996 81 1367-1370. (https://doi.org/10.1210/jcem.81.4.8636335).
26. Casas-González P, Scaglia HE, Pérez-Solís MA, Durand G, Scaglia J, Zariñán T, Dias JA, Reiter E & Ulloa-Aguirre A. Normal testicular function without detectable follicle-stimulating hormone. A novel mutation in the follicle-stimulating hormone receptor gene leading to apparent constitutive activity and impaired agonist-induced desensitization and internalization. Molecular and Cellular Endocrinology 2012 364 71-82. (https://doi.org/10.1016/j.mce.2012.08.011).
27. Oduwole OO, Peltoketo H, Poliandri A, Vengadabady L, Chrusciel M, Doroszko M, Samanta L, Owen L, Keevil B, Rahman NA et al. Constitutively active follicle-stimulating hormone receptor enables androgen-independent spermatogenesis. Journal of Clinical Investigation 2018 128 1787-1792. (https://doi.org/10.1172/JCI96794).
28. De Gendt K, Swinnen JV, Saunders PTK, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lécureuil C et al. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. PNAS 2004 1012 1327-1332. (https://doi.org/10.1073/pnas.0308114100).
29. Welsh M, Saunders PTK, Atanassova N, Sharpe RM & Smith LB. Androgen action via testicular peritubular myoid cells is essential for male fertility. FASEB Journal 2014 23 4218-4230. (https://doi.org/10.1096/fj.09-138347).
30. Plant TM & Marshall GR. The functional significance of FSH in spermatogenesis and the control of its secretion in male primates. Endocrine Reviews 2001 22 764-786. (https://doi.org/10.1210/edrv.22.6.0446).
31. Walker WH & Cheng J. FSH and testosterone signaling in Sertoli cells. Reproduction 2005 130 15-28. (https://doi.org/10.1530/rep.1.00358).
32. Toocheck C, Clister T, Shupe J, Crum C, Ravindranathan P, Lee TK, Ahn JM, Raj GV, Sukhwani M, Orwig KE et al. Mouse spermatogenesis requires classical and nonclassical testosterone signaling. Biology of Reproduction 2016 94 11. (https://doi.org/10.1095/biolreprod.115.132068).
33. Gorczynska E & Handelsman DJ. Androgens rapidly increase the cytosolic calcium concentration in Sertoli cells. Endocrinology 1995 136 2052-2059. (https://doi.org/10.1210/endo.136.5.7720654).
34. Lyng FM, Jones GR & Rommerts FF. Rapid androgen actions on calcium signaling in rat Sertoli cells and two human prostatic cell lines: similar biphasic responses between 1 picomolar and 100 nanomolar concentrations. Biology of Reproduction 2000 63 736-747. (https://doi.org/10.1095/biolreprod63.3.736).
35. Attia AM, Abou-Setta AM & Al-Inany HG. Gonadotrophins for idiopathic male factor subfertility. Cochrane Database Systematic Reviews 2013 23 005071. (https://doi.org/10.1002/14651858.CD005071.pub4).
36. Paradisi R, Busacchi P, Seracchioli R, Porcu E & Venturoli S. Effects of high doses of recombinant human folliclestimulating hormone in the treatment of male factor infertility: results of a pilot study. Fertility and Sterility 2006 86 728-731. (https://doi.org/10.1016/j.fertnstert.2006.02.087).
37. Ding YM, Zhang X-J, Li J-P, Chen S-S, Zhang R-T, Tan W-L & Shi X-J. Treatment of idiopathic oligozoospermia with recombinant human follicle stimulating hormone: A prospective, randomized, double-blind, placebo-controlled clinical study in Chinese population. Clinical Endocrinology 2015 83 866-871. (https://doi.org/10.1111/cen.12770).