Testosterone replacement therapy induces spermatogenesis and partially restores fertility in luteinizing hormone receptor knockout mice

Endocrinology

Volumn 146, Issue 2, 2005, Pages 596-606

  Pakarainen, Tomi ^a   Zhang, Fu Ping ^a,b   Mäkelä, Sari ^a   Poutanen, Matti ^a   Huhtaniemi, Ilpo ^a,c  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; LUTEINIZING HORMONE RECEPTOR; TESTOSTERONE;

ACCESSORY SEX ORGAN; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CRYPTORCHISM; EPIDIDYMIS; FEMALE; FERTILIZATION; GENE EXPRESSION; HISTOLOGY; HORMONE SUBSTITUTION; HYPOGONADISM; INFLAMMATION; KNOCKOUT MOUSE; LEYDIG CELL; MALE; MALE FERTILITY; MATING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PREGNANCY; PREPUBERTY; PRIORITY JOURNAL; PROSTATE; SEXUAL MATURATION; SPERMATID; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON MIGRATION; SUBFERTILITY; TESTIS DESCENT; TESTOSTERONE SYNTHESIS;

ANDROGENS; ANIMALS; BODY WEIGHT; DISEASE MODELS, ANIMAL; EPIDIDYMIS; GENITALIA, MALE; HORMONE REPLACEMENT THERAPY; INFERTILITY, MALE; MALE; MICE; MICE, KNOCKOUT; ORGAN SIZE; RECEPTORS, LH; RNA, MESSENGER; SPERM MOTILITY; SPERMATOGENESIS; TESTOSTERONE;

EID: 12344262662     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2004-0913     Document Type: Article

References (52)

1. Steinberger E 1971 Hormonal control of mammalian spermatogenesis. Physiol Rev 51:1-22
2. Sharpe R 1994 Regulation of spermatogenesis. In: Knobil ENJ, ed. The physiology of reproduction. New York: Raven Press; 1363-1434
3. Smith P 1927 The disabilities caused by hypophysectomy and their repair. J Am Med Assoc 88:158-161
4. Greep RFH, Hisaw F 1936 Effects of two hypophyseal gonadotropic hormones on the reproductive system of the male rat. Anat Rec 65:261-271
5. Cattanach BM, Iddon CA, Charlton HM, Chiappa SA, Fink G 1977 Gonadotrophin-releasing hormone deficiency in a mutant mouse with hypogonadism. Nature 269:338-340
6. Singh J, O'Neill C, Handelsman DJ 1995 Induction of spermatogenesis by androgens in gonadotropin-deficient (hpg) mice. Endocrinology 136:5311-5321
7. Krishnamurthy H, Danilovich N, Morales CR, Sairam MR 2000 Qualitative and quantitative decline in spermatogenesis of the follicle-stimulating hormone receptor knockout (FORKO) mouse. Biol Reprod 62:1146-1159
8. Kumar TR, Wang Y, Lu N, Matzuk MM 1997 Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat Genet 15:201-204
9. Wreford NG, Rajendra Kumar T, Matzuk MM, de Kretser DM 2001 Analysis of the testicular phenotype of the follicle-stimulating hormone β-subunit knockout and the activin type II receptor knockout mice by stereological analysis. Endocrinology 142:2916-2920
10. Zhang FP, Poutanen M, Wilbertz J, Huhtaniemi I 2001 Normal prenatal but arrested postnatal sexual development of luteinizing hormone receptor knock-out (LuRKO) mice. Mol Endocrinol 15:172-183
11. Lei ZM, Mishra S, Zou W, Xu B, Foltz M, Li X, Rao CV 2001 Targeted disruption of luteinizing hormone/human chorionic gonadotropin receptor gene. Mol Endocrinol 15:184-200
12. Zhang FP, Pakarainen T, Zhu F, Poutanen M, Huhtaniemi I 2004 Molecular characterization of postnatal development of testicular steroidogenesis in luteinizing hormone receptor knockout mice. Endocrinology 145:1453-1463
13. Handelsman DJ, Spaliviero JA, Simpson JM, Allan CM, Singh J 1999 Spermatogenesis without gonadotropins: maintenance has a lower testosterone threshold than initiation. Endocrinology 140:3938-3946
14. Zhang FP, Pakarainen T, Poutanen M, Toppari J, Huhtaniemi I 2003 The low gonadotropin-independent constitutive production of testicular testosterone is sufficient to maintain spermatogenesis. Proc Natl Acad Sci USA 100:13692-13697
15. Weiss J, Zimmermann F 1999 Tribromoethanol (Avertin) as an anaesthetic in mice. Lab Anim 33:192-193
16. Haavisto AM, Pettersson K, Bergendahl M, Perheentupa A, Roser JF, Huhtaniemi I 1993 A supersensitive immunofluorometric assay for rat luteinizing hormone. Endocrinology 132:1687-1691
17. van Casteren JI, Schoonen WG, Kloosterboer HJ 2000 Development of time-resolved immunofluorometric assays for rat follicle-stimulating hormone and luteinizing hormone and application on sera of cycling rats. Biol Reprod 62:886-894
18. Huhtaniemi I, Nikula H, Rannikko S 1985 Treatment of prostatic cancer with a gonadotropin-releasing hormone agonist analog: acute and long term effects on endocrine functions of testis tissue. J Clin Endocrinol Metab 61:698-704
19. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
20. Chomczynski P, Sacchi N 1987 Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
21. Penttinen J, Pujianto DA, Sipila P, Huhtaniemi I, Poutanen M 2003 Discovery in silico and characterization in vitro of novel genes exclusively expressed in the mouse epididymis. Mol Endocrinol 17:2138-2151
22. Sipila P, Shariatmadari R, Huhtaniemi IT, Poutanen M 2004 Immortalization of epididymal epithelium in transgenic mice expressing simian virus 40 T antigen: characterization of cell lines and regulation of the polyoma enhancer activator 3. Endocrinology 145:437-446
23. Kolho KL, Huhtaniemi I 1989 Neonatal treatment of male rats with a gonadotropin-releasing hormone antagonist impairs ejaculation and fertility. Physiol Behav 46:373-377
24. Oakberg EF 1956 Duration of spermatogenesis in the mouse and timing of stages of the cycle of the seminiferous epithelium. Am J Anat 99:507-516
25. Spaliviero JA, Jimenez M, Allan CM, Handelsman DJ 2004 Luteinizing hormone receptor-mediated effects on initiation of spermatogenesis in gonadotropin-deficient (hpg) mice are replicated by testosterone. Biol Reprod 70:32-3825
26. Hutson JM 1985 A biphasic model for the hormonal control of testicular descent. Lancet 2:419-2126
27. Adham IM, Emmen JM, Engel W 2000 The role of the testicular factor INSL3 in establishing the gonadal position. Mol Cell Endocrinol 160:11-16
28. Nef S, Parada LF 1999 Cryptorchidism in mice mutant for Insl3. Nat Genet 22:295-928
29. Pakarinen P, Kimura S, El-Gehani F, Pelliniemi LJ, Huhtaniemi I 2002 Pituitary hormones are not required for sexual differentiation of male mice: phenotype of the T/ebp/Nkx2.1 null mutant mice. Endocrinology 143:4477-4482
30. Kendall SK, Samuelson LC, Saunders TL, Wood RI, Camper SA 1995 Targeted disruption of the pituitary glycoprotein hormone α-subunit produces hypogonadal and hypothyroid mice. Genes Dev 9:2007-2019
31. El-Gehani F, Zhang FP, Pakarinen P, Rannikko A, Huhtaniemi I 1998 Gonadotropin-independent regulation of steroidogenesis in the fetal rat testis. Biol Reprod 58:116-123
32. El-Gehani F, Tena-Sempere M, Huhtaniemi I 1998 Vasoactive intestinal peptide is an important endocrine regulatory factor of fetal rat testicular steroidogenesis. Endocrinology 139:1474-1480
33. El-Gehani F, Tena-Sempere M, Ruskoaho H, Huhtaniemi I 2001 Natriuretic peptides stimulate steroidogenesis in the fetal rat testis. Biol Reprod 65:595-600
34. Lei ZM, Zou W, Mishra S, Li X, Rao Ch V 2003 Epididymal phenotype in luteinizing hormone receptor knockout animals and its response to testosterone replacement therapy. Biol Reprod 68:888-895
35. Selye H 1939 The effect of testosterone on the kidney. J Urol 42:637-641
36. Pfeiffer C, Emmel VM, Gardner WU 1940 Renal hypertrophy in mice receiving estrogens and androgens. Yale J Biol Med 12:493-501
37. Malendowicz LK 1979 Sex differences in adrenocortical structure and function. V. The effects of postpubertal gonadectomy and gonadal hormone replacement on nuclear-cytoplasmic ratio, morphology and histochemistry of rat adrenal cortex. Folia Histochem Cytochem 17:195-214
38. McLachlan RI, Wreford NG, O'Donnell L, de Kretser DM, Robertson DM 1996 The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J Endocrinol 148:1-9
39. O'Donnell L, Robertson KM, Jones ME, Simpson ER 2001 Estrogen and spermatogenesis. Endocr Rev 22:289-318
40. Hinton BT, Lan ZJ, Rudolph DB, Labus JC, Lye RJ 1998 Testicular regulation of epididymal gene expression. J Reprod Fertil Suppl 53:47-57
41. Theobald HM, Peterson RE 1997 In utero and lactational exposure to 2,3,7,8-tetrachlorodibenzo-rho-dioxin: effects on development of the male and female reproductive system of the mouse. Toxicol Appl Pharmacol 145:124-135
42. Kotaja N, De Cesare D, Macho B, Monaco L, Brancorsini S, Goossens E, Tournaye H, Gansmuller A, Sassone-Corsi P 2004 Abnormal sperm in mice with targeted deletion of the act (activator of cAMP-responsive element modulator in testis) gene. Proc Natl Acad Sci USA 101:10620-10625
43. Cukierski MA, Sina JL, Prahalada S, Robertson RT 1991 Effects of seminal vesicle and coagulating gland ablation on fertility in rats. Reprod Toxicol 5:347-352
44. Cukierski MA, Sina JL, Prahalada S, Wise LD, Antonello JM, MacDonald JS, Robertson RT 1991 Decreased fertility in male rats administered the 5α-reductase inhibitor, finasteride, is due to deficits in copulatory plug formation. Reprod Toxicol 5:353-362
45. MacLusky NJ, Naftolin F 1981 Sexual differentiation of the central nervous system. Science 211:1294-1302
46. Zhang T, Guo CX, Hu ZY, Liu YX 1997 Localization of plasminogen activator and inhibitor, LH and androgen receptors and inhibin subunits in monkey epididymis. Mol Hum Reprod 3:945-952
47. Gilleran JP, Putz O, DeJong M, DeJong J, Birch L, Pu Y, Huang L, Prins GS 2003 The role of prolactin in the prostatic inflammatory response to neonatal estrogen. Endocrinology 144:2046-2054
48. Bianco JJ, Handelsman DJ, Pedersen JS, Risbridger GP 2002 Direct response of the murine prostate gland and seminal vesicles to estradiol. Endocrinology 143:4922-4933
49. Lane KE, Leav I, Ziar J, Bridges RS, Rand WM, Ho SM 1997 Suppression of testosterone and estradiol-17β-induced dysplasia in the dorsolateral prostate of Noble rats by bromocriptine. Carcinogenesis 18:1505-1510
50. Kawamura K, Kumagai J, Sudo S, Chun SY, Pisarska M, Morita H, Toppari J, Fu P, Wade JD, Bathgate RA, Hsueh AJ 2004 Paracrine regulation of mammalian oocyte maturation and male germ cell survival. Proc Natl Acad Sci USA 101:7323-7328
51. Zimmermann S, Schottler P, Engel W, Adham IM 1997 Mouse Leydig insulin-like (Ley I-L) gene: structure and expression during testis and ovary development. Mol Reprod Dev 47:30-38
52. Zimmermann S, Steding G, Emmen JM, Brinkmann AO, Nayernia K, Holstein AF, Engel W, Adham IM 1999 Targeted disruption of the Insl3 gene causes bilateral cryptorchidism. Mol Endocrinol 13:681-691