Testicular phenotype in luteinizing hormone receptor knockout animals and the effect of testosterone replacement therapy

Biology of Reproduction

Volumn 71, Issue 5, 2004, Pages 1605-1613

  Lei, Z M ^a   Mishra, S ^a   Ponnuru, P ^a   Li, X ^a   Yang, Z W ^b   Rao, Ch V ^a  

^a UNIVERSITY OF LOUISVILLE   (United States)

^b AFFILIATED HOSPITAL OF NORTH SICHUAN MEDICAL COLLEGE   (China)

Author keywords

Androgen; Leydig cells; LH receptor; Luteinizing hormone; Spermatogenesis; Testis; Testosterone

Indexed keywords

FOLLITROPIN; LUTEINIZING HORMONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL COUNT; CONTROLLED STUDY; HISTOPATHOLOGY; HORMONAL REGULATION; HORMONE SUBSTITUTION; KNOCKOUT MOUSE; MACROPHAGE; MALE; MOUSE; NONHUMAN; ORCHIDOPEXY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINIFEROUS TUBULE EPITHELIUM; SERTOLI CELL; SIGNAL TRANSDUCTION; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM;

11-BETA-HYDROXYSTEROID DEHYDROGENASES; 3-HYDROXYSTEROID DEHYDROGENASES; ANDROGENS; ANIMALS; APOPTOSIS; BODY TEMPERATURE; CELL SHAPE; FEMALE; FOLLICLE STIMULATING HORMONE; LUTEINIZING HORMONE; MALE; MICE; MICE, KNOCKOUT; PHENOTYPE; RECEPTORS, LH; SEMINIFEROUS TUBULES; SPERM COUNT; SPERMATIDS; SPERMATOCYTES; SPERMATOGENESIS; TESTIS; TESTOSTERONE;

ANIMALIA;

EID: 6344282787     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.104.031161     Document Type: Article

References (49)

1. de Krege DM, Kerr JB. The cytology of the testis. In: Neil EKJ (ed.), The Physiology of Reproduction. New York: Raven Press; 1994: 1177-1290.
2. Mendis-Handagama SM, Ariyaratne HB. Differentiation of the adult Leydig cell population in the postnatal testis. Biol Reprod 2001; 65:660-671.
3. Mendis-Handagama SM. Luteinizing hormone on Leydig cell structure and function. Histol Histopathol 1997; 12:869-882.
4. Lui WY, Mruk D, Lee WM, Cheng CY. Sertoli cell tight junction dynamics: their regulation during spermatogenesis. Biol Reprod 2003; 68:1087-1097.
5. Griswold MD. Interactions between germ cells and Sertoli cells in the testis. Biol Reprod 1995; 52:211-216.
6. Sharpe R. Regulation of spermatogenesis. In: Neill EKJ (ed.), The Physiology of Reproduction, 2nd ed. New York: Raven Press; 1994: 1363-1463.
7. Sharpe RM, McKinell C. Interactions between androgens, Sertoli cells and germ cells in the control of spermatogenesis. In: Habenicht GVU (ed.), Molecular and Cellular Endocrinology of the Testis. Berlin: Springer; 1994:143-151.
8. Steinberger E. Hormonal control of mammalian spermatogenesis. Physiol Rev 1971; 51:1-22.
9. Spaliviero JA, Jimenez M, Allan CM, Handelsman DJ. Luteinizing hormone receptor-mediated effects on initiation of spermatogenesis in gonadotropin-deficient (hpg) mice are replicated by testosterone. Biol Reprod 2004; 70:32-38.
10. Simpson E, Rubin G, Clyne C, Robertson K, O'Donnell L, Davis S, Jones M. Local estrogen biosynthesis in males and females. Endocr Relat Cancer 1999; 6:131-137.
11. Carreau S, Bourguiba S, Lambard S, Galeraud-Denis I, Genissel C, Bilinska B, Benahmed M, Levallet J. Aromatase expression in male germ cells. J Steroid Biochem Mol Biol 2001; 79:203-208.
12. O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001; 22:289-318.
13. Williams K, McKinnell C, Saunders PT, Walker M, Fisher JS, Turner KJ, Atanassova N, Sharpe M. Neonatal exposure to potent and environmental oestrogens and abnormalities of the male reproductive system in the rat: evidence for importance of the androgen-oestrogen balance and assessment of the relevance to man. Hum Reprod Update 2001; 7:236-247.
14. Hess RA, Bunick D, Bahr J. Oestrogen, its receptors and function in the male reproductive tract-a review. Mol Cell Endocrinol 2001; 178:29-38.
15. Sharpe RM. The Oestrogen hypothesis'-where do we stand now? Int J Androl 2003; 26:2-15.
16. Carreau S, Bourguiba S, Lambard S, Galeraud-Denis I, Genissel C, Levallet J. Reproductive system: aromatase and estrogens. Mol Cell Endocrinol 2002; 193:137-143.
17. Gill-Sharma MK, Dsouza S, Padwal V, Balasinor N, Aleem M, Parte P, Juneja HS. Antifertility effects of estradiol in adult male rats. J Endocrinol Invest 2001; 24:598-607.
18. Toyama Y, Hosoi I, Ichikawa S, Maruoka M, Yashiro E, Ito H, Yuasa S. Beta-estradiol 3-benzoate affects spermatogenesis in the adult mouse. Mol Cell Endocrinol 2001; 178:161-168.
19. Nie R, Zhou Q, Jassim E, Saunders PT, Hess RA. Differential Expression of estrogen receptors alpha and beta in the reproductive tracts of adult male dogs and cats. Biol Reprod 2002; 66:1161-1168.
20. Zhou Q, Nie R, Prins GS, Saunders PT, Katzenellenbogen BS, Hess RA. Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J Androl 2002; 23:870-881.
21. Saunders PT, Fisher JS, Sharpe RM, Millar MR. Expression of oestrogen receptor beta (ER beta) occurs in multiple cell types, including some germ cells, in the rat testis. J Endocrinol 1998; 156:R13-17.
22. Hess RA, Bunick D, Lee KH, Bahr J, Taylor JA, Korach KS, Lubahn DB. A role for oestrogens in the male reproductive system. Nature 1997; 390:509-512.
23. Zhai J, Lanclos KD, Abney TO. Estrogen receptor messenger ribonucleic acid changes during Leydig cell development. Biol Reprod 1996; 55:782-788.
24. Kumar TR, Wang Y, Lu N, Matzuk MM. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 1997; 15:201-204.
25. Sairam MR, Krishnamurthy H. The role of follicle-stimulating hormone in spermatogenesis: lessons from knockout animal models. Arch Med Res 2001; 32:601-608.
26. Lei ZM, Mishra S, Zou W, Xu B, Foltz M, Li X, Rao CV. Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol Endocrinol 2001; 15:184-200.
27. Lei ZM, Zou W, Mishra S, Li X, Rao Ch V. Epididymal phenotype in luteinizing hormone receptor knockout animals and its response to testosterone replacement therapy. Biol Reprod 2003; 68:888-895.
28. Zini A, Abitbol J, Girardi SK, Schulsinger D, Goldstein M, Schlegel PN. Germ cell apoptosis and endothelial nitric oxide synthase (eNOS) expression following ischemia-reperfusion injury to testis. Arch Androl 1998; 41:57-65.
29. Zini A, Abitbol J, Schulsinger D, Goldstein M, Schlegel PN. Restoration of spermatogenesis after scrotal replacement of experimentally cryptorchid rat testis: assessment of germ cell apoptosis and eNOS expression. Urology 1999; 53:223-227.
30. Allan CM, Garcia A, Spaliviero J, Zhang FP, Jimenez M, Huhtaniemi I, Handelsman DJ. Complete Sertoli cell proliferation induced by follicle-stimulating hormone (FSH) independently of luteinizing hormone activity: evidence from genetic models of isolated FSH action. Endocrinology 2004; 145:1587-1593.
31. Gao HB, Tong MH, Hu YQ, Guo QS, Ge R, Hardy MP. Glucocorticoid induces apoptosis in rat Leydig cells. Endocrinology 2002; 143:130-138.
32. Haider SG, Passia D, Rommert FF. Histochemical demonstration of 11 beta-hydroxysteroid dehydrogenase as a marker for Leydig cell maturation in rat. Acta Histochem Suppl 1990; 38:203-207.
33. Rao CV, Lei ZM. Consequences of targeted inactivation of LH receptors. Mol Cell Endocrinol 2002; 187:57-67.
34. Huhtaniemi I, Toppari J. Endocrine, paracrine and autocrine regulation of testicular steroidogenesis. Adv Exp Med Biol 1995; 377:33-54.
35. Weinbauer GF, Nieschlag E. Endocrine control of germ cell proliferation in the primate testis. What do we really know? Adv Exp Med Biol 1997; 424:51-58.
36. 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 Prog Horm Res 2002; 57:149-179.
37. Toledo SP. Inactivating mutations of the LH receptor gene: more than two different phenotypes. Eur J Endocrinol 1999; 140:186.
38. Toledo SP, Brunner HG, Kraaij R, Post M, Dahia PL, Hayashida CY, Kremer HTAP. An inactivating mutation of the luteinizing hormone receptor causes amenorrhea in a 46,XX female. J Clin Endocrinol Metab 1996; 81:3850-3854.
39. Toledo SP, Marino F, Toledo SF. Inactivating mutations in the LH receptor-as rare as "a hen with teeth" or as frequent as polycystic ovary syndrome? Fertil Steril 2000; 73:655.
40. Martens JW, Verhoef-Post M, Abelin N, Ezabella M, Toledo SP, Brunner HG, Themmen AP. A homozygous mutation in the luteinizing hormone receptor causes partial Leydig cell hypoplasia: correlation between receptor activity and phenotype. Mol Endocrinol 1998; 12:775-784.
41. Eblen A, Bao S, Lei ZM, Nakajima ST, Rao CV. The presence of functional luteinizing hormone/chorionic gonadotropin receptors in human sperm. J Clin Endocrinol Metab 2001; 86:2643-2648.
42. Hedger MP. Macrophages and the immune responsiveness of the testis. J Reprod Immunol 2002; 57:19-34.
43. Miller SC, Bowman BM. Tissue, cellular, and subcellular distribution of 241Pu in the rat testis. Radiat Res 1983; 94:416-426.
44. Zhang FP, Pakarainen T, Zhu F, Poutanen M, Huhtaniemi I. Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 2004; 145:1453-1463.
45. Lo KC, Lei ZM, Rao Ch V, Lamb DJ. De novo testosterone production in luteinizing hormone receptor knockout mice after transplantation of Leydig stem cells. Endocrinology 2004 (May 3, Epub ahead of print).
46. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lecureuil C, Heyns W, Carmeliet P, Guillou F, Sharpe RM, Verhoeven G. A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci U S A 2004; 101:1327-1332.
47. Holdcraft RW, Braun RE. Androgen receptor function is required in Sertoli cells for the terminal differentiation of haploid spermatids. Development 2004; 131:459-467.
48. Yeh S, Tsai MY, Xu Q, Mu XM, Lardy H, Huang KE, Lin H, Yeh SD, Altuwaijri S, Zhou X, Xing L, Boyce BF, Hung MC, Zhang S, Gan L, Chang C. Generation and characterization of androgen receptor knockout (ARKO) mice: an in vivo model for the study of androgen functions in selective tissues. Proc Natl Acad Sci U S A 2002; 99:13498-13503.
49. McKinnell C, Atanassova N, Williams K, Fisher JS, Walker M, Turner KJ, Saunders TK, Sharpe RM. Suppression of androgen action and the induction of gross abnormalities of the reproductive tract in male rats treated neonatally with diethylstilbestrol. J Androl 2001; 22:323-338.