The consequences of altered somatotropic system on reproduction

Biology of Reproduction

Volumn 71, Issue 1, 2004, Pages 17-27

  Chandrashekar, Varadaraj ^a   Zaczek, Denise ^a   Bartke, Andrzej ^a  

^a SOUTHERN ILLINOIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Growth hormone; Neuroendocrinology; Ovary; Pituitary hormones; Testis

Indexed keywords

GONADORELIN; GONADOTROPIN; GROWTH HORMONE; PHEROMONE; PROLACTIN; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; CORPUS LUTEUM FUNCTION; DELAYED PUBERTY; DWARFISM; ENDOCRINE FUNCTION; ENDOCRINE SYSTEM; FERTILITY; GENE; GONAD FUNCTION; GONADOTROPIN RELEASE; GROWTH HORMONE DEFICIENCY; GROWTH HORMONE RECEPTOR GENE; GROWTH HORMONE RESISTANCE; HORMONE RESISTANCE; HYPOPHYSIS; HYPOPHYSIS FUNCTION; HYPOTHALAMUS; KNOCKOUT MOUSE; LARON SYNDROME; LEYDIG CELL; MOUSE; NEUROENDOCRINE SYSTEM; NONHUMAN; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; OVULATION; PREGNANCY; PRIORITY JOURNAL; PUBERTY; REPRODUCTION; SEXUAL MATURATION; SHORT SURVEY; SIGNAL TRANSDUCTION; SOMATOMEDIN C GENE; SOMATOTROPIC SYSTEM; SPERMATOGENESIS;

ANIMALS; GROWTH HORMONE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; REPRODUCTION;

ANIMALIA;

EID: 3142758618     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.103.027060     Document Type: Short Survey

References (147)

1. Bartke A, Chandrashekar V, Bailey B, Zaczek D, Turyn D. Consequences of growth hormone (GH) overexpression and GH resistance. Neuropeptides 2002; 36:201-208.
2. Zhou J, Xu BC, Maheshwari HG, He L, Reed M, Lozykowski M, Okada S, Wagner TE, Cataldo LA, Coschigano K, Kopchick JJ. A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci 1997; 94:13215-13220.
3. Baker J, Hardy MP, Zhou J, Bondy C, Lupu F, Bellve AR, Efstratiadis A. Effects of an Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996; 10:903-918.
4. Nakae J, Kido Y, Accili D. Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev 2001; 22:818-835.
5. Ramaley JA, Phares CK. Delay of puberty onset in females due to suppression of growth hormone. Endocrinology 1980; 106:1989-1993.
6. Advis JP, White SS, Ojeda SR. Activation of growth hormone short loop negative feedback delays puberty in the female rat. Endocrinology 1981; 108:1343-1352.
7. Arsenijevic Y, Wehrenberg WB, Conz A, Eshkol A, Sizonenko PC, Aubert ML. Growth hormone (GH) deprivation induced by passive immunization against rat GH-releasing factor delays sexual maturation in the male rat. Endocrinology 1989; 124:3050-3059.
8. Keene DE, Suescun MO, Bostwick MG, Chandrashekar V, Bartke A, Kopchick JJ. Puberty is delayed in male growth hormone receptor gene-disrupted mice. J Androl 2002; 23:661-668.
9. Chandrashekar V, Bartke A, Coschigano KT, Kopchick JJ. Pituitary and testicular function in growth hormone receptor gene knockout mice. Endocrinology 1999; 140:1082-1088.
10. Chandrashekar V, Bartke A, Awoniyi CA, Tsai-Morris CH, Dufau ML, Russell LD, Kopchick JJ. Testicular endocrine function in growth hormone receptor gene disrupted mice. Endocrinology 2001; 142:3443-3450.
11. Laron Z. The essential role of IGF-I: lessons from the long-term study and treatment of children and adults with Laron syndrome. J Clin Endocrinol Metab 1999; 84:4397-4404.
12. Laron Z. Growth hormone insensitivity (Laron syndrome). Rev Endocr Metab Disord 2002; 3:347-355.
13. Colao A, De Rosa M, Pivonello R, Balestrieri A, Cappabianca P, Di Sarno A, Rochira V, Carani C, Lombardi G. Short-term suppression of GH and IGF-I levels improves gonadal function and sperm parameters in men with acromegaly. J Clin Endocrinol Metab 2002; 87:4193-4197.
14. Melmed S, Ho K, Klibanski A, Reichlin S, Thorner M. Clinical review 75: recent advances in pathogenesis, diagnosis, and management of acromegaly. J Clin Endocrinol Metab 1995; 80:3395-3402.
15. Bartke A, Chandrashekar V, Turyn D, Steger RW, Debeljuk L, Winters TA, Mattison JA, Danilovich NA, Croson W, Wernsing DR, Kopchick JJ. Effects of growth hormone overexpression and growth hormone resistance on neuroendocrine and reproductive functions in transgenic and knock-out mice. Proc Soc Exp Biol Med 1999; 222: 113-123.
16. Bartke A. Effects of growth hormone on male reproductive functions. J Androl 2000; 21:181-188.
17. Hull KL, Harvey S. GH as a co-gonadotropin: the relevance of correlative changes in GH secretion and reproductive state. J Endocrinol 2002; 172:1-19.
18. Chandrashekar V, Bartke A. The role of insulin-like growth factor-I in neuroendocrine function and the subsequent effects on sexual maturation: inferences from animal models. Reprod Biol 2003; 3:7-28.
19. Chandrashekar V, Bartke A, Wagner TE. Endogenous human growth hormone (GH) modulates the effect of gonadotropin-releasing hormone on pituitary function and the gonadotropin response to the negative feedback effect of testosterone in adult male transgenic mice bearing human GH gene. Endocrinology 1988; 123:2717-2722.
20. Chandrashekar V, Bartke A, Wagner TE. Neuroendocrine function in adult female transgenic mice expressing the human growth hormone gene. Endocrinology 1992; 130:1802-1808.
21. Bartke A, Cecim M, Tang K, Steger RW, Chandrashekar V, Turyn D. Neuroendocrine and reproductive consequences of overexpression of growth hormone in transgenic mice. Proc Soc Exp Biol Med 1994; 206:345-359.
22. Chandrashekar V, Coschigano KT, Bartke A, Kopchick JJ. Neuroendocrine and reproductive functions in transgenic mice with altered growth hormone secretion and in growth hormone receptor gene disrupted mice. In: Castro MG (ed.), Transgenic Models in Endocrinology. Boston: Kluwer Academic Press; 2001:105-121.
23. Chandrashekar V, Bartke A. The role of growth hormone in the control of gonadotropin secretion in adult male rats. Endocrinology 1998; 139:1067-1074.
24. Juul A, Andersson AM, Pedersen SA, Jorgensen JO, Christiansen JS, Groome NP, Skakkebaek NE. Effects of growth hormone replacement therapy on IGF-related parameters and on the pituitary-gonadal axis in GH-deficient males. A double-blind, placebo-controlled crossover study. Horm Res 1998; 6:269-278.
25. Lackey BR, Gray SL, Henricks DM. The insulin-like growth factor (IGF) system and gonadotropin regulation: actions and interactions. Cytokine Growth Factor Rev 1999; 10:201-217.
26. Hiney JK, Ojeda SR, Dees WL. Insulin-like growth factor I: a possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology 1991; 54:420-423.
27. Hiney JK, Srivastava V, Nyberg CL, Ojeda SR, Dees WL. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 1996; 137:3717-3728.
28. Bartlett JM, Charlton HM, Robinson IC, Nieschlag E. Pubertal development and testicular function in the male growth hormone-deficient rat. J Endocrinol 1990; 126:193-201.
29. Woods MC, Simpson MS. Pituitary control of the testis of the hypophysectomized rat. Endocrinology 1961; 69:91-125.
30. Swerdloff RS, Odell WD. Modulating influences of FSH, GH, and prolactin on LH-stimulated testosterone secretion. In: Troen P, Nankin HR (eds.), The Testis in Normal and Infertile Men. New York: Raven Press; 1977:395-401.
31. Zipf WB, Payne AH, Kelch RP. Prolactin, growth hormone, and luteinizing hormone in the maintenance of testicular luteinizing hormone receptors. Endocrinology 1978; 103:595-600.
32. Hull KL, Harvey S. Growth hormone: roles in female reproduction. J Endocrinol 2001; 168:1-23.
33. Danilovich N, Wernsing D, Coschigano KT, Kopchick JJ, Bartke A. Deficits in female reproductive function in GH-R-KO mice; role of IGF-I. Endocrinology 1999; 140:2637-2640.
34. Mazerbourg S, Bondy CA, Zhou J, Monget P. The insulin-like growth factor system: a key determinant role in the growth and selection of ovarian follicles? A comparative species study. Reprod Domest Anim 2003; 38:247-258.
35. Jia XC, Kalmijn J, Hsueh AJ. Growth hormone enhances follicle-stimulating hormone-induced differentiation of cultured rat granulosa cells. Endocrinology 1986; 118:1401-1409.
36. Vickers MH, Casey PJ, Champion ZJ, Gravance CG, Breier BH. IGF-I treatment increases motility and improves morphology of immature spermatozoa in the GH-deficient dwarf (dw/dw) rat. Growth Horm IGF Res 1999; 9:236-240.
37. Ovesen P, Jorgensen JO, Kjaer T, Ho KK, Orskov H, Christiansen JS. Impaired growth hormone secretion and increased growth hormone-binding protein levels in subfertile males. Fertil Steril 1996; 65:165-169.
38. Becker AJ, Uckert S, Stief CG, Scheller F, Knapp WH, Hartmann U, Brabant G, Jonas U. Serum levels of human growth hormone during different penile conditions in the cavernous and systemic blood of healthy men and patients with erectile dysfunction. Urology 2002; 59:609-614.
39. Ra S, Aoki H, Fujioka T, Sato F, Kubo T, Yasuda N. In vitro contraction of the canine corpus cavernosum penis by direct perfusion with prolactin or growth hormone. J Urol 1996; 156:522-525.
40. Bartke A. Delayed aging in Ames dwarf mice. Relationships to endocrine function and body size. Results Probl Cell Differ 2000; 29: 181-202.
41. Bauman DE, Vernon RG. Effects of exogenous bovine somatotropin on lactation. Annu Rev Nutr 1993; 13:437-461.
42. Kleinberg DL. Role of IGF-I in normal mammary development. Breast Cancer Res Treat 1998; 47:201-208.
43. Homburg R, West C, Torresani T, Jacobs HS. Cotreatment with human growth hormone and gonadotropins for induction of ovulation: a controlled clinical trial. Fertil Steril 1990; 53:254-260.
44. Shoham Z, Conway GS, Ostergaard H, Lahlou N, Bouchard P, Jacobs HS. Cotreatment with growth hormone for induction of spermatogenesis in patients with hypogonadotropic hypogonadism. Fertil Steril 1992; 57:1044-1051.
45. Delemarre-van de Waal HA, van Coeverden SC, Rotteveel J. Hormonal determinants of pubertal growth. J Pediatr Endocrinol Metab 2001; 14(suppl 6):1521-1526.
46. Clark PA, Rogol AD. Growth hormones and sex steroid interactions at puberty. Endocrinol Metab Clin North Am 1996; 25:665-681.
47. Schneider HJ, Pagotto U, Stalla GK. Central effects of the somatotropic system. Eur J Endocrinol 2003; 149:377-392.
48. Codner E, Cassorla F. Growth hormone and reproductive function. Mol Cell Endocrinol 2002; 186:133-136.
49. Tres LL, Smith EP, Van Wyk JJ, Kierszenbaum AL. Immunoreactive sites and accumulation of somatomedin-C in rat Sertoli-spermatogenic cell co-cultures. Exp Cell Res 1986; 162:33-50.
50. Vannelli BG, Barni T, Orlando C, Natali A, Serio M, Balboni GC. Insulin-like growth factor-I (IGF-I) and IGF-I receptor in human testis: an immunohistochemical study. Fertil Steril 1988; 49:666-669.
51. Chuzel F, Clark AM, Avallet O, Saez JM. Transcriptional regulation of the lutropin/human choriogonadotropin receptor and three enzymes of steroidogenesis by growth factors in cultured pig Leydig cells. Eur J Biochem 1996; 239:8-16.
52. Laron Z, Sarel R. Penis and testicular size in patients with growth hormone insufficiency. Acta Endocrinol (Copenh) 1970; 63:625-633.
53. Bondanelli M, Ambrosio MR, Margutti A, Franceschetti P, Zatelli MC, Degli Uberti EC. Activation of the somatotropic axis by testosterone in adult men: evidence for a role of hypothalamic growth hormone-releasing hormone. Neuroendocrinology 2003; 77:380-387.
54. Kanzaki M, Morris PL. Growth hormone regulates steroidogenic acute regulatory protein expression and steroidogenesis in Leydig cell progenitors. Endocrinology 1999; 140:1681-1686.
55. Toogood AA, Shalet SM. Ageing and growth hormone status. Baillieres Clin Endocrinol Metab 1998; 12:281-296.
56. Hoffman AR, Lieberman SA, Butterfield G, Thompson J, Hintz RL, Ceda GP, Marcus R. Functional consequences of the somatopause and its treatment. Endocrine 1997; 7:73-76.
57. Bartke A. Is growth hormone deficiency a beneficial adaptation to aging? Evidence from experimental animals. Trends Endocrinol Metab 2003; 14:340-344.
58. Bartke A. Can growth hormone (GH) accelerate aging? Evidence from GH-transgenic mice. Neuroendocrinology 2003; 78:210-216.
59. Holzenberger M, DuPont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003; 421:182-187.
60. Monget P, Fabre S, Mulsant P, Lecerf F, Elsen JM, Mazerbourg S, Pisselet C, Monniaux D. Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domest Anim Endocrinol 2002; 23:139-154.
61. Adashi EY. The IGF family and folliculogenesis. J Reprod Immunol 1998; 39:13-19.
62. Giudice LC. Insulin-like growth factor family in Graafian follicle development and function. J Soc Gynecol Invest 2001; 8(suppl proceedings):S26-29.
63. Ge Z, Miller E, Nicholson W, Hedgpeth V, Gadsby J. Insulin-like growth factor (IGF)-I and IGF binding proteins-2, -3, -4, -5 in porcine corpora lutea during the estrous cycle; evidence for inhibitory actions of IGFBP-3. Domest Anim Endocrinol 2003; 25:183-197.
64. Erickson GF, Shimasaki S. The physiology of folliculogenesis: the role of novel growth factors. Fertil Steril 2001; 76:943-949.
65. Bienvenu G, Seurin D, Grellier P, Froment P, Baudrimont M, Monget P, Le Bouc Y, Babajko S. IGFBP-6 transgenic mice: postnatal growth, brain development and reproduction abnormalities. Endocrinology 2004; 145:2412-2420.
66. Froment P, Seurin D, Hembert S, Levine JE, Pisselet C, Monniaux D, Binoux M, Monget P. Reproductive abnormalities in human IGF binding protein-1 transgenic female mice. Endocrinology 2002; 143: 1801-1808.
67. Sharara FI, Nieman LK. Identification and cellular localization of growth hormone receptor gene expression in the human ovary. J Clin Endocrinol Metab 1994; 79:670-672.
68. Lobie PE, Breipohl W, Aragon JG, Waters MJ. Cellular localization of the growth hormone receptor/binding protein in the male and female reproductive systems. Endocrinology 1990; 126:2214-2221.
69. Tiong TS, Herington AC. Tissue distribution, characterization, and regulation of messenger ribonucleic acid for growth hormone receptor and serum binding protein in the rat. Endocrinology 1991; 129: 1628-1634.
70. Ilkbahar YN, Wu K, Thordarson G, Talamantes F. Expression and distribution of messenger ribonucleic acids for growth hormone (GH) receptor and GH-binding protein in mice during pregnancy. Endocrinology 1995; 136:386-392.
71. Yuan W, Lucy MC. Messenger ribonucleic acid expression for growth hormone receptor, luteinizing hormone receptor, and steroidogenic enzymes during the estrous cycle and pregnancy in porcine and bovine corpora lutea. Domest Anim Endocrinol 1996; 13:431-444.
72. Sakaguchi K, Tanaka M, Ohkubo T, Yoshizato H, Hanai Y, Fujikawa T, Kaneko H, Nakashima K. Tissue-specific regulation of growth hormone receptor and growth hormone binding protein gene expression during pregnancy and lactation in the rat. Endocr J 1998; 45(suppl):S105-107.
73. Schams D, Berisha B, Kosmann M, Einspanier R, Amselgruber WM. Possible role of growth hormone, IGFs, and IGF-binding proteins in the regulation of ovarian function in large farm animals. Domest Anim Endocrinol 1999; 17:279-285.
74. Zhao J, Taverne MA, van der Weijden GC, Bevers MM, van den Hurk R. Immunohistochemical localisation of growth hormone (GH), GH receptor (GHR), insulin-like growth factor I (IGF-I) and type I IGF-I receptor, and gene expression of GH and GHR in rat preantral follicles. Zygote 2002; 10:85-94.
75. Sirotkin AV, Makarevich AV. Growth hormone can regulate functions of porcine ovarian granulosa cells through the cAMP/protein kinase A system. Anim Reprod Sci 2002; 70:111-126.
76. Bachelot A, Monget P, Imbert-Bollore P, Coshigano K, Kopchick JJ, Kelly PA, Binart N. Growth hormone is required for ovarian follicular growth. Endocrinology 2002; 143:4104-4112.
77. Zaczek D, Hammond J, Suen L, Wandji S, Service D, Bartke A, Chandrashekar V, Coschigano KT, Kopchick JJ. Impact of growth hormone resistance on female reproductive function: new insights from growth hormone receptor knockout mice. Biol Reprod 2002; 67:1115-1124.
78. Xiao E, Xia-Zhang L, Ferin M. Stress and the menstrual cycle: short- and long-term response to a five-day endotoxin challenge during the luteal phase in the rhesus monkey. J Clin Endocrinol Metab 1999; 84:623-629.
79. Roosendaal MM, Swarts HJ, Wiegant VM, Mattheij JA. Effect of restraint stress on the preovulatory luteinizing hormone profile and ovulation in the rat. Eur J Endocrinol 1995; 133:347-353.
80. Magiakou MA, Mastorakos G, Webster E, Chrousos GP. The hypothalamic-pituitary-adrenal axis and the female reproductive system. Ann N Y Acad Sci 1997; 816:842-856.
81. Hauck SJ, Hunter WS, Danilovich N, Kopchick JJ, Bartke A. Reduced levels of thyroid hormones, insulin, and glucose, and lower body core temperature in the growth hormone receptor/binding protein knockout mouse. Exp Biol Med 2001; 226:552-558.
82. Laron Z, Sarel R, Pertzelan A. Puberty in Laron type dwarfism. Eur J Pediatr 1980; 134:79-83.
83. Chandrashekar V, Bostwick MG, Panici JA, Bartke A, Kopchick JJ. Neuroendocrine function in adult female growth hormone receptor gene disrupted mice. In: Program of the 84th Endocrine Society annual meeting; 2002; San Francisco, CA. Abstract P1-166.
84. Aberg ND, Carlsson B, Rosengren L, Oscarsson J, Isaksson OGP, Ronnback L, Eriksson PS. Growth hormone increases connexin-43 expression in the cerebral cortex and hypothalamus. Endocrinology 2000; 131:3879-3886.
85. Fernandez-Galez MC, Morschl E, Chowen JA, Torres-Aleman I, Naftolin F, Garcia-Segura LM. Role of astroglia and insulin-like growth factor-I in gonadal hormone-dependent synaptic plasticity. Brain Res Bul 1997; 44:525-531.
86. Wernsing D, Zaczek D, Kopchick J, Bartke A. Fetal and placental development, length of gestation, and pregnancy outcome in growth hormone receptor-deficient mice. Biol Reprod 1999; 60(suppl 1):108.
87. Davoren JB, Hsueh AJ. Growth hormone increases ovarian levels of immunoreactive somatomedin C/insulin-like growth factor-I in vivo. Endocrinology 1986; 118:888-890.
88. Hsu CJ, Hammond JM. Gonadotropins and estradiol stimulate immunoreactive insulin-like growth factor-I production by porcine granulosa cells in vitro. Endocrinology 1987; 120:198-207.
89. Mondschein JS, Hammond JM. Growth factors regulate immunoreactive insulin-like growth-I production by cultured porcine granulosa cells. Endocrinology 1988; 123:463-468.
90. Gallego MI, Binart N, Robinson GW, Okagaki R, Coschigano KT, Perry J, Kopchick JJ, Oka T, Kelly PA, Henninghausen L. Prolactin, growth hormone, and epidermal growth factor activate Stat5 in different compartments of mammary tissues and exert different and overlapping developmental effects. Dev Biol 2001; 229:163-175.
91. Hansson HA, Billig H, Isgaard J. Insulin-like growth factor I in the developing and mature rat testis: immunohistochemical aspects. Biol Reprod 1989; 40:1321-1328.
92. Lin T, Wang DL, Calkins JH, Guo H, Chi R, Housley PR. Regulation of insulin-like growth factor-I messenger ribonucleic acid expression in Leydig cells. Mol Cell Endocrinol 1990; 73:147-152.
93. Naville D, Chatelain PG, Avallet O, Saez JM. Control of production of insulin-like growth factor I by pig Leydig and Sertoli cells cultured alone or together. Cell-cell interactions. Mol Cell Endocrinol 1990; 70:217-224.
94. Bernier M, Chatelain P, Mather JP, Saez JM. Regulation of gonadotropin receptors, gonadotropin responsiveness, and cell multiplication by somatomedin-C and insulin in cultured pig Leydig cells. J Cell Physiol 1986; 129:257-263.
95. Perrard-Sapori MH, Chatelain PG, Jaillard C, Saez JM. Characterization and regulation of somatomedin-C/insulin-like growth factor I (Sm-C/IGF-I) receptors on cultured pig Leydig cells. Effects of Sm-C/IGF-I on luteotropin receptors and steroidogenesis. Eur J Biochem 1987; 165:209-214.
96. Lin T, Haskell J, Vinson N, Terracio L. Characterization of insulin and insulin-like growth factor I receptors of purified Leydig cells and their role in steroidogenesis in primary culture: a comparative study. Endocrinology 1986; 119:1641-1647.
97. Kasson BG, Hsueh AJ. Insulin-like growth factor-I augments gonadotropin-stimulated androgen biosynthesis by cultured rat testicular cells. Mol Cell Endocrinol 1987; 52:27-34.
98. Gelber SJ, Hardy MP, Mendis-Handagama SM, Casella SJ. Effects of insulin-like growth factor-I on androgen production by highly purified pubertal and adult rat Leydig cells. J Androl 1992; 13:125-130.
99. Cailleau J, Vermeire S, Verhoeven G. Independent control of the production of insulin-like growth factor I and its binding protein by cultured testicular cells. Mol Cell Endocrinol 1990; 69:79-89.
100. Kulin HE, Samojlik E, Santen R, Santner S. The effect of growth hormone on the Leydig cell response to chorionic gonadotrophin in boys with hypopituitarism. Clin Endocrinol 1981; 15:463-472.
101. Chatelain PG, Sanchez P, Saez JM. Growth hormone and insulin-like growth factor I treatment increase testicular luteinizing hormone receptors and steroidogenic responsiveness of growth hormone deficient dwarf mice. Endocrinology 199; 128:1857-1862.
102. Chandrashekar V, Bartke A. Induction of endogenous insulin-like growth factor-I secretion alters the hypothalamic-pituitary-testicular function in growth hormone-deficient adult dwarf mice. Biol Reprod 1993; 48:544-551.
103. Wang GM, O'Shaughnessy PJ, Chubb C, Robaire B, Hardy MP. Effects of insulin-like growth factor I on steroidogenic enzyme expression levels in mouse Leydig cells. Endocrinology 2003; 144: 5058-5064.
104. Verhoeven G, Cailleau J. Influence of coculture with Sertoli cells on steroidogenesis in immature rat Leydig cells. Mol Cell Endocrinol 1990; 71:239-251.
105. Hull KL, Harvey S. Growth hormone: a reproductive endocrine-paracrine regulator? Rev Reprod 2000; 5:175-182.
106. Childs GV. Growth hormone cells as co-gonadotropes: partners in the regulation of the reproductive system. Trends Endocrinol Metab 2000; 11:168-175.
107. Wilson ME. The impact of the GH-IGF-I axis on gonadotropin secretion: inferences from animal models. J Pediatr Endocrinol Metab 2001; 14:115-140.
108. Chandrashekar V, Bartke A, Wagner TE. Interactions of human growth hormone and prolactin on pituitary and Leydig cell function in adult transgenic mice expressing the human growth hormone gene. Biol Reprod 1991; 44:135-140.
109. Bex F, Bartke A, Goldman BD, Dalterio S. Prolactin, growth hormone, luteinizing hormone receptors, and seasonal changes in testicular activity in the golden hamster. Endocrinology 1978; 103:2069-2080.
110. Childs GV, Unabia G, Rougeau D. Cells that express luteinizing hormone (LH) and follicle-stimulating hormone (FSH) beta-subunit messenger ribonucleic acids during the estrous cycle: the major contributors contain LH beta, FSH beta, and/or growth hormone. Endocrinology 1994; 134:990-997.
111. Childs GV, Unabia G, Miller BT. Cytochemical detection of gonadotropin-releasing hormone-binding sites on rat pituitary cells with luteinizing hormone, follicle-stimulating hormone, and growth hormone antigens during diestrous up-regulation. Endocrinology 1994; 134:1943-1951.
112. Harvey S, Baumbach WR, Sadeghi H, Sanders EJ. Ultrastructural colocalization of growth hormone binding protein and pituitary hormones in adenohypophyseal cells of the rat. Endocrinology 1993; 133:1125-1130.
113. Childs GV, Unabia G, Wu P. Differential expression of growth hormone messenger ribonucleic acid by somatotropes and gonadotropes in male and cycling female rats. Endocrinology 2000; 141:1560-1570.
114. Childs GV, Unabia G, Miller BT, Collins TJ. Differential expression of gonadotropin and prolactin antigens by GHRH target cells from male and female rats. J Endocrinol 1999; 162:177-187.
115. Henricks DM, Kouba AJ, Lackey BR, Boone WR, Gray SL. Identification of insulin-like growth factor I in bovine seminal plasma and its receptor on spermatozoa: influence on sperm motility. Biol Reprod 1998; 59:330-337.
116. Laron Z, Klinger B. Effect of insulin-like growth factor-I treatment on serum androgens and testicular and penile size in males with Laron syndrome (primary growth hormone resistance). Eur J Endocrinol 1998; 138:176-180.
117. Smith EP, Dickson BA, Chernausek SD. Insulin-like growth factor binding protein-3 secretion from cultured rat Sertoli cells: dual regulation by follicle stimulating hormone and insulin-like growth factor-I. Endocrinology 1990; 127:2744-2751.
118. Rappaport MS, Smith EP. Insulin-like growth factor (IGF) binding protein 3 in the rat testis: follicle-stimulating hormone dependence of mRNA expression and inhibition of IGF-I action on cultured Sertoli cells. Biol Reprod 1995; 52:419-425.
119. Lin T, Wang D, Nagpal ML, Shimasaki S, Ling N. Expression and regulation of insulin-like growth factor-binding protein-1, -2, -3, and -4 messenger ribonucleic acids in purified rat Leydig cells and their biological effects. Endocrinology 1993; 132:1898-1904.
120. Zhou J, Bondy C. Anatomy of the insulin-like growth factor system in the human testis. Fertil Steril 1993; 60:897-904.
121. Schneider MR, Lahm H, Wu M, Hoeflich A, Wolf E. Transgenic mouse models for studying the functions of insulin-like growth factor-binding proteins. FASEB J 2000; 14:629-640.
122. Wood TL, Rogler LE, Czick ME, Schuller AG, Pintar JE. Selective alterations in organ sizes in mice with a targeted disruption of the insulin-like growth factor binding protein-2 gene. Mol Endocrinol 2000; 14:1472-1482.
123. Bradshaw SL, Schuller AGP, Grewal A, Pintar JE. Analysis of reproductive capability in IGFBP-6 deficient mice. In: Program of the 81st Endocrine Society annual meeting; 1999; San Diego, CA. Abstract P2-594.
124. Froment P, Staub C, Hembert S, Pisselet C, Magistrini M, Delaleu B, Seurin D, Levine JE, Johnson L, Binoux M, Monget P. Reproductive abnormalities in hIGFBP-1 transgenic male mice. Endocrinology 2004; 145:2080-2091.
125. Mani Maran RR, Sivakumar R, Ravisankar B, Valli G, Ravichandran K, Arunakaran J, Aruldhas MM. Growth hormone directly stimulates testosterone and oestradiol secretion by rat Leydig cells in vitro and modulates the effects of LH and T3. Endocr J 2000; 47:111-118.
126. Koike S, Noumura T. Immunohistochemical localization of insulin-like growth factor-II in the perinatal rat gonad. Growth Regul 1995; 5:185-189.
127. Tsuruta JK, Eddy EM, O'Brien DA. Insulin-like growth factor-II/cation- independent mannose 6-phosphate receptor mediates paracrine interactions during spermatogonial development. Biol Reprod 2000; 63:1006-1013.
128. Murphy LJ, Bell GI, Friesen HG. Tissue distribution of insulin-like growth factor I and II messenger ribonucleic acid in the adult rat. Endocrinology 1987; 120:1279-1282.
129. DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 1990; 345:78-80.
130. Korenbrot CC, Huhtaniemi IT, Weiner RI. Preputial separation as an external sign of pubertal development in the male rat. Biol Reprod 1977; 17:298-303.
131. Spiteri-Grech J, Bartlett JM, Nieschlag E. Regulation of testicular insulin-like growth factor-I in pubertal growth hormone-deficient male rats. J Endocrinol 1991; 131:279-285.
132. Chandrashekar V, Panici JA, Bostwick MG, Bartke A, Kopchick JJ. Effect of insulin-like growth factor-I on testicular endocrine function in growth hormone receptor gene knockout mice. Biol Reprod 2002; 66(suppl 1):145(abstract 117).
133. Coschigano KT, Holland AN, Riders ME, List EO, Flyvbjerg A, Kopchick JJ. Deletion, but not antagonism, of the mouse growth hormone receptor results in severely decreased body weights, insulin, and insulin-like growth factor I levels and increased life span. Endocrinology 2003; 144:3799-3810.
134. Gay E, Seurin D, Babajko S, Doublier S, Cazillis M, Binoux M. Liver-specific expression of human insulin-like growth factor binding protein-1 in transgenic mice: repercussions on reproduction, ante- and perinatal mortality and postnatal growth. Endocrinology 1997; 138:2937-2947.
135. Chubb C, Nolan C. Animal models of male infertility: mice bearing single-gene mutations that induce infertility. Endocrinology 1985; 117:338-346.
136. Chubb C. Sexual behavior and fertility of little mice. Biol Reprod 1987; 37:564-569.
137. Donahue LR, Beamer WG. Growth hormone deficiency in 'little' mice results in aberrant body composition, reduced insulin-like growth factor-I and insulin-like growth factor-binding protein-3 (IGFBP-3), but does not affect IGFBP-2, -1 or -4. J Endocrinol 1993; 136:91-104.
138. Eicher EM, Beamer WG. Inherited ateliotic dwarfism in mice. Characteristics of the mutation, little, on chromosome 6. J Hered 1976; 67:87-91.
139. Hammer RE, Palmiter RD, Brinster RL. Partial correction of murine hereditary growth disorder by germ-line incorporation of a new gene. Nature 1984; 311:65-67.
140. Carmignac DF, Bennett PA, Robinson IC. Effects of growth hormone secretagogues on prolactin release in anesthetized dwarf (dw/dw) rats. Endocrinology 1998; 139:3590-3596.
141. Charlton HM, Clark RG, Robinson IC, Goff AE, Cox BS, Bugnon C, Bloch BA. Growth hormone-deficient dwarfism in the rat: a new mutation. J Endocrinol 1988; 119:51-58.
142. Umezu M, Kawada K, Miwa A, Ishii S, Masaki J. Pituitary and plasma levels of growth hormone (GH), follicle stimulating hormone (FSH) and luteinizing hormone (LH) in hereditary dwarf rats (rdw/rdw). Jikken Dobutsu 1991; 40:511-515.
143. Umezu M, Fujimura T, Sugawara S, Kagabu S. Pituitary and serum levels of prolactin (PRL), thyroid stimulating hormone (TSH) and serum thyroxine (T4) in hereditary dwarf rats (rdw/rdw). Jikken Dobutsu 1993; 42:211-216.
144. Ono M, Harigai T, Furudate S. Pituitary-specific transcription factor Pit-1 in the rdw rat with growth hormone- and prolactin-deficient dwarfism. J Endocrinol 1994; 143:479-487.
145. Jiang JY, Umezu M, Sato E. Improvement of follicular development rather than gonadotrophin secretion by thyroxine treatment in infertile immature hypothyroid rdw rats. J Reprod Fertil 2001; 119:193-199.
146. Matsushima M, Kuroda K, Shirai M, Ando K, Sugisaki T, Noguchi T. Spermatogenesis in Snell dwarf, little and congenitally hypothyroid mice. Int J Androl 1986; 9:132-140.
147. Chandrashekar V, Bartke A. Influence of hypothalamus and ovary on pituitary function in transgenic mice expressing the bovine growth hormone gene and in growth hormone-deficient Ames dwarf mice. Biol Reprod 1996; 54:1002-1008.