Insulin-like growth factors and ovarian physiology

Journal of Obstetrics and Gynaecology Research

Volumn 24, Issue 5, 1998, Pages 305-323

  Yoshimura, Yasunori ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Folliculogenesis; Insulin like growth factor; Insulin like growth factor binding protein; Oocyte maturation; Ovulation

Indexed keywords

ANDROGEN; AROMATASE; GONADOTROPIN; PROGESTERONE; SOMATOMEDIN B; SOMATOMEDIN BINDING PROTEIN; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; SOMATOMEDIN RECEPTOR;

CELL PROLIFERATION; ENZYME ACTIVITY; FEMALE; FEMALE INFERTILITY; HORMONAL REGULATION; HORMONE SYNTHESIS; HUMAN; NONHUMAN; OOCYTE MATURATION; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; OVULATION; REVIEW;

EID: 0031762553     PISSN: 13418076     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1447-0756.1998.tb00103.x     Document Type: Review

References (117)

1. Adashi EY, Resnick CE, D'Ercole AJ, Svoboda ME, Van Wyk JJ. Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocr Rev 1985; 6: 400-420
2. Murphy LJ, Ghahary A. Uterine insulin-like growth factor-1: Regulation of expression and its role in estrogen-induced uterine proliferation. Endocr Rev 1990; 11: 443-453
3. Giudice LC. Insulin-like growth factors and ovarian follicular development. Endocr Rev 1992; 13: 641-669
4. Katz E, Ricciarelli E, Adashi EY. The potential relevance of growth hormone to female reproductive physiology and pathophysiology. Fertil Steril 1993; 59: 8-34
5. Giudice LC. Growth factors and growth modulators in human uterine endometrium: Their potential relevance to reproductive medicine. Fertil Steril 1994; 61: 1-17
6. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: Biological actions. Endocr Rev 1995; 16: 3-34
7. Sara VR, Hall K. Insulin-like growth factors and their binding proteins. Physiol Rev 1990; 70: 591-614
8. Baxter RC, Martin JL. Binding proteins for the insulin-like growth factors: Structure, regulation and function. Prog Growth Factor Res 1989; 1: 49-68
9. Nissley P, Lopaczynski W. Insulin-like growth factor receptors. Growth Factors 1991; 5: 29-43
10. Rosenfeld RG, Lamson G, Pham H, Oh Y, Conover C, De Leon DD, Donovan SM, Ocrant I, Giudice L. Insulin-like growth factor binding proteins. Recent Prog Horm Res 1990; 46: 99-159; discussion 159-163
11. Rechler MM. Insulin-like growth factor binding proteins. Vitam Horm 1993; 47: 1-114
12. Brissenden JE, Ullrich A, Francke U. Human chromosomal mapping of genes for insulin-like growth factors I and II and epidermal growth factor. Nature 1984; 310: 781-784
13. Bell GI, Gerhard DS, Fong NM, Sanchez-Pescador R, Rail LB. Isolation of the human insulin-like growth factor genes: Insulin-like growth factor II and insulin genes are contiguous. Proc Natl Acad Sci USA 1985; 82: 6450-6454
14. de Pagter-Holthuizen P, Jansen M, van Schaik FM, van der Kammen R, Oosterwijk C, Van den Brande JL, Sussenbach JS. The human insulin-like growth factor II gene contains two development-specific promoters. FEBS Lett 1987; 214: 259-264
15. Holthuizen P, van der Lee FM, Ikejiri K, Yamamoto M, Sussenbach JS. Identification and initial characterization of a fourth leader exon and promoter of the human IGF-II gene. Biochem Biophys Acta 1990; 1087: 341-343
16. Rotwein P. Structure, evolution, expression and regulation of insulin-like growth factors I and II. Growth Factors 1991; 5: 3-18
17. Daughaday WH, Rotwein P. Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum, and tissue concentrations. Endocr Rev 1989; 10: 68-91
18. Rotwein P, Pollock KM, Didier DK, Krivi GG. Organization and sequence of the human insulin-like growth factor I gene. Alternative RNA processing produces two insulin-like growth factor I precursor peptides. J Biol Chem 1986; 261: 4828-4832
19. LeRoith D, Roberts CTJr. Insulin-like growth factor I (IGF-I): A molecular basis for endocrine versus local action? Mol Cell Endocrinol 1991; 77: C57-C61
20. Rotwein P, Hall LJ. Evolution of insulin-like growth factor II: Characterization of mouse IGF-II gene and identification of two pseudoexons. DNA Cell Biol 1990; 9: 725-735
21. Steele-Perkins G, Turner J, Edman JC, Hari J, Pierce SB, Stover C, Rutter WJ, Roth RA. Expression and characterization of a functional human insulin-like growth factor I receptor. J Biol Chem 1988; 263: 11486-11492
22. Kato H, Faria TN, Stannard B, Roberts CT Jr., LeRoith D. Role of tyrosine kinase activity in signal transduction by the insulin-like growth factor-I (IGF-I) receptor. Characterization of kinase-deficient IGF-1 receptors and the action of an IGF-I-mimetic antibody (alpha IR-3). J Biol Chem 1993; 268: 2655-2661
23. Frattali AL, Treadway JL, Pessin JE. Transmembrane signaling by the human insulin receptor kinase. Relationship between intramolecular beta subunit trans- and cis-autophosphorylation and substrate kinase activation. J Biol Chem 1992; 267: 19521-19528
24. Frattali AL, Pessin JE. Relationship between alpha subunit ligand occupancy and beta subunit autophosphorylation in insulin/insulin-like growth factor-I hybrid receptors. J Biol Chem 1993; 268: 7393-7400
25. Izumi T, White MF, Kadowaki T, Takaku F, Akanuma Y, Kasuga M. Insulin-like growth factor I rapidly stimulates tyrosine phosphorylation of a Mr 185,000 protein in intact cells. J Biol Chem 1987; 262: 1282-1287
26. Sun XJ, Rothenberg P, Kahn CR, Backer JM, Araki E, Wilden PA, Cahill DA, Goldstein BJ, White MF. Structure of the insulin receptor substrate IRS-1 defines a unique signal transduction protein. Nature 1991; 352: 73-77
27. Chuang LM, Myers MGJr., Seidner GA, Birnbaum MJ, White MF, Kahn CR. Insulin receptor substrate 1 mediates insulin and insulin-like growth factor I-stimulated maturation of Xenopus oocytes. Proc Natl Acad Sci USA 1993; 90: 5172-5175
28. Morgan DO, Edman JC, Standring DN, Fried VA, Smith MC, Roth RA, Rutter WJ. Insulin-like growth factor II receptor as a multifunctional binding protein. Nature 1987; 329: 301-307
29. Braulke T, Causin C, Waheed A, Junghans U, Hasilik A, Maly P, Humbel RE, von Figura K. Mannose 6-phosphate/insulin-like growth factor II receptor: Distinct binding sites for mannose 6-phosphate and insulin-like growth factor II. Biochem Biophys Res Commun 1988; 150: 1287-1293
30. Kiess W, Thomas CL, Sklar MM, Nissley SP. Beta-galactosidase decreases the binding affinity of the insulin-like-growth-factor-II/mannose-6-phosphate receptor for insulin-like-growth-factor II. Eur J Biochem 1990; 190: 71-77
31. Oka Y, Rozek LM, Czech MP. Direct demonstration of rapid insulin-like growth factor II Receptor internalization and recycling in rat adipocytes. Insulin stimulates 1251-insulin-like growth factor II degradation by modulating the IGF-II receptor recycling process. J Biol Chem 1985; 260: 9435-9442
32. Nishimoto I, Murayama Y, Katada T, Ui M, Ogata E. Possible direct linkage of insulin-like growth factor-II receptor with guanine nucleotide-binding proteins. J Biol Chem 1989; 264: 14029-14038
33. Murayama Y, Okamoto T, Ogata E, Asano T, Iiri T, Katada T, Ui M, Grubb JH, Sly WS, Nishimoto I. Distinctive regulation of the functional linkage between the human cation-independent mannose 6-phosphate receptor and GTP-binding proteins by insulin-like growth factor II and mannose 6-phosphate. J Biol Chem 1990; 265: 17456-17462
34. Okamoto T, Nishimoto I. Analysis of stimulation-G protein subunit coupling by using active insulin-like growth factor II receptor peptide. Proc Natl Acad Sci USA 1991; 88: 8020-8023
35. Rogers SA, Hammerman MR. Mannose 6-phosphate potentiates insulin-like growth factor II-stimulated inositol trisphosphate production in proximal tubular basolateral membranes. J Biol Chem 1989; 264: 4273-4276
36. McCusker RH, Clemmons DR. The insulin-like growth factor binding proteins: Structure and biological function. In: Schofield PN, ed. The Insulin-Like Growth Factors: Structure and Biological Functions. Oxford: Oxford Univ Press, 1992; 110-150
37. Bell SC, Patel SR, Jackson JA, Waites GT. Major secretory protein of human decidualized endometrium in pregnancy is an insulin-like growth factor-binding protein. J Endocrinol 1988; 118: 317-328
38. Lamson G, Giudice LC, Rosenfeld RG. Insulin-like growth factor binding proteins: Structural and molecular relationships. Growth Factors 1991; 5: 19-28
39. Bourner MJ, Busby WH Jr, Siegel NR, Krivi GG, McCusker RH, Clemmons DR. Cloning and sequence determination of bovine insulin-like growth factor binding protein-2 (IGFBP-2): Comparison of its structural and functional properties with IGFBP-1. J Cell Biochem 1992; 48: 215-226
40. Ooi GT, Orlowski CC, Brown AL, Becker RE, Unterman TG, Rechler MM. Different tissue distribution and hormonal regulation of messenger RNAs encoding rat insulin-like growth factor-binding proteins-1 and -2. Mol Endocrinol 1990; 4: 321-328
41. Hynes RO. Integrins: Versatility, modulation, and signaling in cell adhesion. Cell 1992; 69: 11-25
42. Wood WI, Cachianes G, Henzel WJ, Winslow GA, Spencer SA, Hellmiss R, Martin JL, Baxter RC. Cloning and expression of the growth hormone-dependent insulin-like growth factor-binding protein. Mol Endocrinol 1988; 2: 1176-1185
43. Albiston AL, Herington AC. Tissue distribution and regulation of insulin-like growth factor (IGF)-binding protein-3 messenger ribonucleic acid (mRNA) in the rat: Comparison with IGF-I mRNA expression. Endocrinology 1992; 130: 497-502
44. Kiefer MC, Masiarz FR, Bauer DM, Zapf J. Identification and molecular cloning of two new 30-kDa insulin-like growth factor binding proteins isolated from adult human serum. J Biol Chem 1991; 266: 9043-9049
45. LaTour D, Mohan S, Linkhart TA, Baylink DJ, Strong DD. Inhibitory insulin-like growth factor-binding protein: Cloning, complete sequence, and physiological regulation. Mol Endocrinol 1990; 4: 1806-1814
46. Shimasaki S, Uchiyama F, Shimonaka M, Ling N. Molecular cloning of the cDNAs encoding a novel insulin-like growth factor-binding protein from rat and human. Mol Endocrinol 1990; 4: 1451-1458
47. Cheung PT, Smith EP, Shimasaki S, Ling N, Chernausek SD. Characterization of an insulin-like growth factor binding protein (IGFBP-4) produced by the B104 rat neuronal cell line: Chemical and biological properties and differential synthesis by sublines. Endocrinology 1991; 129: 1006-1015
48. Nakatani A, Shimasaki S, Erickson GF, Ling N. Tissue-specific expression of four insulin-like growth factor-binding proteins (1, 2, 3, and 4) in the rat ovary. Endocrinology 1991; 129: 1521-1529
49. Shimasaki S, Shimonaka M, Zhang HP, Ling N. Identification of five different insulin-like growth factor binding proteins (IGFBPs) from adult rat serum and molecular cloning of a novel IGFBP-5 in rat and human. J Biol Chem 1991; 266: 10646-10653
50. Kiefer MC, Ioh RS, Bauer DM, Zapf J. Molecular cloning of a new human insulin-like growth factor binding protein. Biochem Biophys Res Commun 1991; 176: 219-225
51. Martin JL, Willetts KE, Baxter RC. Purification and properties of a novel insulin-like growth factor-II binding protein from transformed human fibroblasts. J Biol Chem 1990; 265: 4124-4130
52. Roghani M, Lassarre C, Zapf J, Povoa G, Binoux M. Two insulin-like growth factor (IGF)-binding proteins are responsible for the selective affiniry for IGF-II of cerebrospinal fluid binding proteins. J Clin Endocrinol Metab 1991; 73: 658-666
53. Shimasaki S, Gao L, Shimonaka M, Ling N. Isolation and molecular cloning of insulin-like growth factor-binding protem-6. Mol Endocrinol 1991; 5: 938-948
54. 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
55. Hernandez ER, Roberts CT Jr, LeRoith D, Adashi EY. Rat ovarian insulin-like growth factor I (IGF-I) gene expression is granulosa cell- selective: 5′-untranslated mRNA variant representation and hormonal regulation. Endocrinology 1989; 125: 572-574
56. Hernandez ER, Hurwitz A, Vera A, Pellicer A, Adashi EY, LeRoith D, Roberts CT Jr. Expression of the genes encoding the insulin-like growth factors and their receptors in the human ovary. J Clin Endocrinol Metab 1992; 74: 419-425
57. el-Roeiy A, Chen X, Roberts VJ, LeRoith D, Roberts CTJr, Yen SS. Expression of insulin-like growth factor-I (IGF-I) and IGF-II and the IGF-I, IGF-II, and insulin receptor genes and localization of the gene products in the human ovary. J Clin Endocrinol Metab 1993; 77: 1411-1418
58. Zhou J, Bondy C. Anatomy of the human ovarian insulin-like growth factor system. Biol Reprod 1993; 48: 467-482
59. Adashi EY, Resnick CE, Svoboda ME, van Wyk JJ, Hascall VC, Yanagishita M. Independent and synergistic actions of somatomedin-C in the stimulation of proteoglycan biosynthesis by cultured rat granulosa cells. Endocrinology 1986; 118: 456-458
60. Yoshimura Y, Ando M, Nagamatsu S, Iwashita M, Adachi T, Sueoka K, Miyazaki T, Kuji N, Tanaka M. Effects of insulin-like growth factor-I on follicle growth, oocyte maturation, and ovarian steroidogenesis and plasminogen activator activity in the rabbit. Biol Reprod 1996; 55: 152-160
61. Yoshimura Y, Maruyama K, Shiraki M, Kawakami S, Fukushima M, Nakamura Y. Prolactin inhibits plasminogen activator activity in the preovulatory follicles. Endocrinology 1990; 126: 631-636
62. Kuji N, Miyazaki T, Sueoka K, Tanaka M, Kiyokawa K, Kitaoka Y, Yamauchi J, Hashiba T, Nemoto T, Kobayashi T, Yoshimura Y. Insulin-like growth factor-I induces follicular development by stimulating ovarian production of angiotensin II. Jpn J Fertil Steril 1997; 42: 9-21
63. Magoffin DA, Kurtz KM, Erickson GF. Insulin-like growth factor-I selectively stimulates cholesterol side-chain cleavage expression in ovarian theca-interstitial cells. Mol Endocrinol 1990; 4: 489-496
64. Cara JF, Fan J, Azzarello J, Rosenfield RL. Insulin-like growth factor-I enhances luteinizing hormone binding to rat ovarian theca-interstitial cells. J Clin Invest 1990; 86: 560-565
65. Spicer LJ, Stewart RE, Alvarez P, Francisco CC, Keefer BE. Insulin-like growth factor-binding protein-2 and -3: Their biological effects in bovine thecal cells. Biol Reprod 1997; 56: 1458-1465
66. Magoffin DA, Weitsman SR. Insulin-like growth factor-I stimulates the expression of 3 beta-hydroxysteroid dehydrogenase messenger ribonucleic acid in ovarian theca-interstitial cells. Biol Reprod 1993; 48: 1166-1173
67. Eden JA, Jones J, Carter GD, Alaghband-Zadeh J. A comparison of follicular fluid levels of insulin-like growth factor-1 in normal dominant and cohort follicles, polycystic and multicystic ovaries. Clin Endocrinol 1988; 29: 327-336
68. Rabinovici I, Dandekar P, Angle MJ, Rosenthal S, Martin MC. Insulin-like growth factor-I (IGF-I) levels in follicular fluid from human preovulatory follicles: Correlation with serum IGF-I levels. Fertil Steril 1990; 54: 428-433
69. Hernandez ER, Roberts CTJr, Hurwitz A, LeRoith D, Adashi EY. Rat ovarian insulin-like growth factor II gene expression is theca-interstitial cell-exclusive: Hormonal regulation and receptor distribution. Endocrinology 1990; 127: 3249-3251
70. Owen EJ, Torresani T, West C, Mason BA, Jacobs HS. Serum and follicular fluid insulin like growth factors I and II during growth hormone co-treatment for in-vitro fertilization and embryo transfer. Clin Endocrinol 1991; 35: 327-334
71. Voutilainen R, Franks S, Mason HD, Martikainen H. Expression of insulin-like growth factor (IGF), IGF-binding protein, and IGF receptor messenger ribonucleic acids in normal and polycystic ovaries. J Clin Endocrinol Metob 1996; 81: 1003-1008
72. El-Roeiy A, Chen X, Roberts VJ, Shimasakai S, Ling N, LeRoith D, Roberts CTJr, Yen SS. Expression of the genes encoding the insulin-like growth factors (IGF-I and II), the IGF and insulin receptors, and IGF-binding proteins-1-6 and the localization of their gene products in normal and polycystic ovary syndrome ovaries. J Clin Endocrinol Metab 1994; 78: 1488-1496
73. Barreca A, Artini PG, Del Monte P, Ponzani P, Pasquini P, Cariola G, Volpe A, Genazzani AR, Giordano G, Minuto F. In vivo and in vitro effect of growth hormone on estradiol secretion by human granulosa cells. J Clin Endocrinol Metab 1993; 77: 61-67
74. Mason HD, Willis DS, Holly JM, Franks S. Insulin preincubation enhances insulin-like growth factor-II (IGF-II) action on steroidogenesis in human granulosa cells. J Clin Endocrinol Metab 1994; 78: 1265-1267
75. Di Blasio AM, Vigano P, Ferrari A. Insulin-like growth factor-II stimulates human granulosaluteal cell proliferation in vitro. Fertil Steril 1994; 61: 483-487
76. Thierry van Dessel HJ, Chandrasekher Y, Yap OW, Lee PD, Hintz RL, Faessen GH, Braat DD, Fauser BC, Giudice LC. Serum and follicular fluid levels of insulin-like growth factor I (IGF-I), IGF-II, and IGF-binding protein-1 and -3 during the normal menstrual cycle. J Clin Endocrinol Metab 1996; 81: 1224-1231
77. Ricciarelli E, Hernandez ER, Hurwitz A, Kokia E, Rosenfeld RG, Schwander J, Adashi EY. The ovarian expression of the antigonadotropic insulin-like growth factor binding protein-2 is theca-interstitial cell-selective: Evidence for hormonal regulation. Endocrinology 1991; 129: 2266-2268
78. Ricciarelli E, Hernandez ER, Tedeschi C, Botero LF, Kokia E, Rohan RM, Rosenfeld RG, Albiston AL, Herington AC, Adashi EY. Rat ovarian insulin-like growth factor binding protein-3: A growth hormone-dependent theca-interstitial cell-derived antigonadotropin. Endocrinology 1992; 130: 3092-3094
79. Samaras SE, Hagen DR, Shimasaki S, Ling N, Hammond JM. Expression of insulin-like growth factor-binding protein-2 and -3 messenger ribonucleic acid in the porcine ovary: Localization and physiological changes. Endocrinology 1992; 130: 2739-2744
80. Giudice LC, Milki AA, Milkowski DA, el Danasouri I. Human granulosa contain messenger ribonucleic acids encoding insulin-like growth factor-binding proteins (IGFBPs) and secrete IGFBPs in culture. Fertil Steril 1991; 56: 475-480
81. Cataldo NA, Woodruff TK, Giudice LC. Regulation of insulin-like growth factor binding protein production by human luteinizing granulosa cells cultured in denned medium. J Clin Endocrinol Metab 1993; 76: 207-215
82. Mason HD, Margara R, Winston RM, Seppala M, Koistinen R, Franks S. Insulin-like growth factor-I (IGF-I) inhibits production of IGF-binding protein-1 while stimulating estradiol secretion in granulosa cells from normal and polycystic human ovaries. J Clin Endocrinol Metab 1993; 76: 1275-1279
83. Bicsak TA, Shimonaka M, Malkowski M, Ling N. Insulin-like growth factor-binding protein (IGF-BP) inhibition of granulosa cell function: Effect on cyclic adenosine 3′,5′-monophosphate, deoxyribonucleic acid synthesis, and comparison with the effect of an IGF-I antibody. Endocrinology 1990; 126: 2184-2189
84. Shimasaki S, Shimonaka M, Ui M, Inoue S, Shibata F, Ling N. Structural characterization of a follicle-stimulating hormone action inhibitor in porcine ovarian follicular fluid. Its identification as the insulin-like growth factor-binding protein. J Biol Chem 1990; 265: 2198-2202
85. Bicsak TA, Ling N, DePaolo LV. Ovarian intrabursal administration of insulin-like growth factor-binding protein inhibits follicle rupture in gonadotropin-treated immature female rats. Biol Reprod 1991; 44: 599-603
86. Yoshimura Y, Nagamatsu S, Ando M, Iwashita M, Oda T, Katsumata Y, Shiokawa S, Nakamura Y. Insulin-like growth factor binding protein-3 inhibits gonadotropin-induced ovulation, oocyte maturation, and steroidogenesis in rabbit ovary. Endocrinology 1996; 137: 438-446
87. Yoshimura Y, Aoki N, Sueoka K, Miyazaki T, Kuji N, Tanaka M, Kobayashi T. Interactions between insulin-like growth factor-I (IGF-I) and the renin-angiotensin system in follicular growth and ovulation. J Clin Invest 1996; 98: 308-316
88. Mason HD, Willis D, Holly JM, Cwyfan-Hughes SC, Seppala M, Franks S. Inhibitory effects of insulin-like growth factor-binding proteins on steroidogenesis by human granulosa cells in culture. Mol Cell Endocrinol 1992; 89: R1-4
89. Yoshimura Y, Iwashita M, Karube M, Oda T, Akiba M, Shiokawa S, Ando M, Yoshinaga A, Nakamura Y. Growth hormone stimulates follicular development by stimulating ovarian production of insulin-like growth factor-I. Endocrinology 1994; 135: 887-894
90. Yoshimura Y, Nakamura Y, Koyama N, Iwashita M, Adachi T, Takeda Y. Effects of growth hormone on follicle growth, oocyte maturation, and ovarian steroidogenesis. Fertil Steril 1993; 59: 917-923
91. Yoshimura Y, Karube M, Oda T, Koyama N, Shiokawa S, Akiba M, Yoshinaga A, Nakamura Y. Locally produced angiotensin 11 induces ovulation by stimulating prostaglandin production in in vitro perfused rabbit ovaries. Endocrinology 1993; 133: 1609-1616
92. Binoux M, Lalou C, Lassarre C, Segovia B. Regulation of IGF bioavailability by IGFBP proteases. In: Gluckman PD, Rosenfeld RG, eds. The Insulin-like Growth Factors and Their Regulatory Proteins. Proceedings of the third international symposium on IGFs. New York: Elsevier, 1994; 217-226
93. Baxter RC. Circulating binding proteins for the insulin-like growth factors. Trends Endocrinol Metab 1993; 4: 91-96
94. Liu XJ, Malkowski M, Guo Y, Erickson GF, Shimasaki S, Ling N. Development of specific antibodies to rat insulin-like growth factor-binding proteins (IGFBP-2 to -6): Analysis of IGFBP production by rat granulosa cells. Endocrinology 1993; 132: 1176-1183
95. Fielder PJ, Pham H, Adashi EY, Rosenfeld RG. Insulin-like growth factors (IGFs) block FSH-induced proteolysis of IGF-binding protein-5 (BP-5) in cultured rat granulosa cells. Endocrinology 1993; 133: 415-418
96. Grimes RW, Hammond JM. Proteolytic degradation of insulin-like growth factor (IGF)-binding protein-3 by porcine ovarian granulosa cells in culture: Regulation by IGF-I. Endocrinology 1994; 134: 337-343
97. Adashi EY, Resnick CE, Rosenfeld RG. Insulin-like growth factor-I (IGF-I) and IGF-II hormonal action in cultured rat granulosa cells: Mediation via type I but not type II IGF receptors. Endocrinology 1990; 126: 216-222
98. Hernandez ER, Hurwitz A, Botero L, Ricciarelli E, Werner H, Roberts CT Jr, LeRoith D, Adashi EY. Insulin-like growth factor receptor gene expression in the rat ovary: Divergent regulation of distinct receptor species. Mol Endocrinol 1991; 5: 1799-1805
99. Teissier MP, Monget P, Monniaux D, Durand P. Changes in insulin-like growth factor-II/mannose-6-phosphate receptor during growth and atresia of ovine ovarian follicles. Biol Reprod 1994; 50: 111-119
100. Zhou J, Chin E, Bondy C. Cellular pattern of insulin-like growth factor-I (IGF-I) and IGF-I receptor gene expression in the developing and mature ovarian follicle. Endocrinology 1991; 129: 3281-3288
101. Spicer LJ, Alpizar E, Vernon RK. Insulin-like growth factor-I receptors in ovarian granulosa cells: Effect of follicle size and hormones. Mol Cell Endocrinol 1994; 102: 69-76
102. Perks CM, Denning-Kendall PA, Gilmour RS, Wathes DC. Localization of messenger ribonucleic acids for insulin-like growth factor I (IGF-I), IGF-II, and the type 1 IGF receptor in the ovine ovary throughout the estrous cycle. Endocrinology 1995; 136: 5266-5273
103. Dor J, Ben-Shlomo I, Lunenfeld B, Pariente C, Levran D, Karasik A, Seppala M, Mashiach S. Insulin-like growth factor-I (IGF-I) may not be essential for ovarian follicular development: Evidence from IGF-I deficiency. J Clin Endocrinol Metab 1992; 74: 539-542
104. Tornell J, Billig H, Hillensjo T. Regulation of oocyte maturation by changes in ovarian levels of cyclic nucleotides. Hum Reprod 1991; 6: 411-422
105. Yoshimura Y, Nakamura Y, Ando M, Jinno M, Oda T, Karube M, Koyama N, Nanno T. Stimulatory role of cyclic adenosine monophosphate as a mediator of meiotic resumption in rabbit oocytes. Endocrinology 1992; 131: 351-356
106. Sadler SE, Maller JL. In vivo regulation of cyclic AMP phosphodiesterase in Xenopus oocytes. Stimulation by insulin and insulin-like growth factor-I. J Biol Chem 1987; 262: 10644-10650
107. Feng P, Catt KJ, Knecht M. Transforming growth factor-beta stimulates meiotic maturation of the rat oocyte. Endocrinology 1988; 122: 181-186
108. Gomez E, Tarin JJ, Pellicer A. Oocyte maturation in humans: The role of gonadotropins and growth factors. Fertil Steril 1993; 60: 40-46
109. Taghon MS, Sadler SE. Insulin-like growth factor 1 receptor-mediated endocytosis in Xenopus laevis oocytes. A role for receptor tyrosine kinase activity. Developmental Biology 1994; 163: 66-74
110. Zhu L, Ohan N, Agazie Y, Cummings C, Farah S, Liu XJ. Molecular cloning and characterization of Xenopus insulin-like growth factor-I receptor: Its role in mediating insulin-induced Xenopus oocyte maturation and expression during embryogenesis. Endocrinology 1998; 139: 949-954
111. Apa R, Lanzone A, Miceli F, Mastrandrea M, Caruso A, Mancuso S, Canipari R. Growth hormone induces in vitro maturation of follicle- and cumulus-enclosed rat oocytes. Mol Cell Endocrinol 1994; 106: 207-212
112. Oliver JE, Aitman TJ, Powell JF, Wilson CA, Clayton RN. Insulin-like growth factor I gene expression in the rat ovary is confined to the granulosa cells of developing follicles. Endocrinology 1989; 124: 2671-2679
113. Hainaut P, Kowalski A, Giorgetti S, Baron V, Van Obberghen E. Insulin and insulin-like-growth-factor-I (IGF-I) receptors in Xenopus laevis oocytes. Comparison with insulin receptors from liver and muscle. Biochem J 1991; 273: 673-678
114. Yoshimura Y, Hosoi Y, Iritani A, Nakamura Y, Atlas SJ, Wallach EE. Developmental potential of rabbit oocyte matured in vitro: The possible contribution of prolactin. Biol Reprod 1989; 41: 26-33
115. 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
116. Jones JI, D'Ercole AJ, Camacho-Hubner C, Clemmons DR. Phosphorylation of insulin-like growth factor (IGF)-binding protein 1 in cell culture and in vivo: Effects on affinity for IGF-I. Proc Natl Acad Sci USA 1991; 88: 7481-7485
117. Chun SY, Billig H, Tilly JL, Furuta I, Tsafriri A, Hsueh AJ. Gonadotropin suppression of apoptosis in cultured preovulatory follicles: Mediatory role of endogenous insulin-like growth factor I. Endocrinology 1994; 135: 1845-1853