The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function

Seminars in Reproductive Medicine

Volumn 27, Issue 1, 2009, Pages 43-51

  Kwintkiewicz, Jakub ^a   Giudice, Linda C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Endocrine disruptors; Insulin like growth factors (igfs); Signaling pathways; Steroidogenesis

Indexed keywords

ANDROGEN; ENDOCRINE DISRUPTOR; FOLLITROPIN; GONADOTROPIN; PROTEINASE; SOMATOMEDIN; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 6;

BIOAVAILABILITY; CELL DIFFERENTIATION; CELL EXPANSION; CUMULUS CELL; ENDOCRINE FUNCTION; GRANULOSA CELL; HORMONE ACTION; HUMAN; NONHUMAN; OOCYTE MATURATION; OVARY DEVELOPMENT; OVARY FOLLICLE DEVELOPMENT; OVARY FUNCTION; OVARY POLYCYSTIC DISEASE; REPRODUCTION; REVIEW; SIGNAL TRANSDUCTION; STEROIDOGENESIS; THECA CELL;

ANIMALS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL POLLUTANTS; FEMALE; GONADOTROPINS; HUMANS; MICE; MODELS, ANIMAL; MODELS, BIOLOGICAL; OVARIAN FOLLICLE; SIGNAL TRANSDUCTION; SOMATOMEDINS;

EID: 61449225762     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0028-1108009     Document Type: Review

References (91)

1. McNatty KP, Reader K, Smith P, Heath DA, Juenguel JL. Control of ovarian follicular development to the gonadotrophin-dependent phase:a 2006 perspective. Soc Reprod Fertil Suppl 2007;64:55-68
2. Dupont J, Dunn SE, Barrett JC, LeRoith D. Microarray analysis and identification of novel molecules involved in insulin-like growth factor-1 receptor signaling and gene expression. Recent Prog Horm Res 2003;58:325-342
3. Hernandez ER. Regulation of the genes for insulin-like growth factor (IGF) I and II and their receptors by steroids and gonadotropins in the ovary. J Steroid Biochem Mol Biol 1995;53:219-221
4. Samani AA, Yakar S, LeRoith D, Brodt P. The role of the IGF system in cancer growth and metastasis:overview and recent insights. Endocr Rev 2007;28(1):20-47
5. Rose PP, Bogyo M, Moses AV, Fruh K. Insulin-like growth factor II receptor-mediated intracellular retention of cathepsin B is essential for transformation of endothelial cells by Kaposi's sarcoma-associated herpesvirus. J Virol 2007;81(15):8050-8062
6. Boldt HB, Conover CA. Pregnancy-associated plasma protein-A (PAPP-A):a local regulator of IGF bioavailability through cleavage of IGFBPs. Growth Horm IGF Res 2007;17(1):10-18
7. Clemmons DR. Role of insulin-like growth factor binding proteins in controlling IGF actions. Mol Cell Endocrinol 1998;140(1-2):19-24
8. Giudice LC. Insulin-like growth factor family in Graafian follicle development and function. J Soc Gynecol Investig 2001;8(1, Suppl):S26-S29
9. Balasubramanian K, Lavoie HA, Garmey JC, Stocco DM, Veldhuis JD. Regulation of porcine granulosa cell steroidogenic acute regulatory protein (StAR) by insulin-like growth factor I:synergism with follicle-stimulating hormone or protein kinase A agonist. Endocrinology 1997;138(1):433-439
10. Davoren JB, Hsueh AJ. Insulin enhances FSH-stimulated steroidogenesis by cultured rat granulosa cells. Mol Cell Endocrinol 1984;35(2-3):97-105
11. Urban RJ, Garmey JC, Shupnik MA, Veldhuis JD. Insulinlike growth factor type I increases concentrations of messenger ribonucleic acid encoding cytochrome P450 cholesterol side- chain cleavage enzyme in primary cultures of porcine granulosa cells. Endocrinology 1990;127(5):2481-2488
12. Veldhuis JD, Kolp LA, Toaff ME, Strauss JF III, Demers LM. Mechanisms subserving the trophic actions of insulin on ovarian cells. In vitro studies using swine granulosa cells. J Clin Invest 1983;72(3):1046-1057
13. Veldhuis JD, Rodgers RJ. Mechanisms subserving the steroidogenic synergism between follicle-stimulating hormone and insulin-like growth factor I (somatomedin C). Alterations in cellular sterol metabolism in swine granulosa cells. J Biol Chem 1987;262(16):7658-7664
14. Pellegrini S, Fuzzi B, Pratesi S, et al. In-vivo studies on ovarian insulin-like growth factor I concentrations in human preovulatory follicles and human ovarian circulation. Hum Reprod 1995;10(6):1341-1345
15. Bondy CA, Chin E, Zhou J. Significant species differences in local IGF-I and -II gene expression. Adv Exp Med Biol 1993;343:73-77
16. Vendola K, Zhou J, Wang J, Bondy CA. Androgens promote insulin-like growth factor-I and insulin-like growth factor-I receptor gene expression in the primate ovary. Hum Reprod 1999;14(9):2328-2332
17. Vendola K, Zhou J, Wang J, et al. Androgens promote oocyte insulin-like growth factor I expression and initiation of follicle development in the primate ovary. Biol Reprod 1999;61(2):353-357
18. Baker J, Hardy MP, Zhou J, et al. Effects ofan Igf1 gene null mutation on mouse reproduction. Mol Endocrinol 1996;10(7):903-918
19. Liu JL, Yakar S, LeRoith D. Conditional knockout of mouse insulin-like growth factor-1 gene using the Cre/loxP system. Proc Soc Exp Biol Med 2000;223(4):344-351
20. Kadakia R, Arraztoa JA, Bondy C, Zhou J. Granulosa cell proliferation is impaired in the Igf1 null ovary. Growth Horm IGF Res 2001;11(4):220-224
21. Zhou J, Bievre M, Bondy CA. Reduced GLUT1 expression in Igf1 -/- null oocytes and follicles. Growth Horm IGF Res 2000;10(3):111-117
22. Dierich A, Sairam MR, Monaco L, et al. Impairing follicle-stimulating hormone (FSH) signaling in vivo:targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. Proc Natl Acad Sci USA 1998;95(23):13612-13617
23. Abel MH, Wootton AN, Wilkins V, et al. The effect of a null mutation in the follicle-stimulating hormone receptor gene on mouse reproduction. Endocrinology 2000;141(5):1795-1803
24. Sasaki N, Rees-Jones RW, Zick Y, Nissley SP, Rechler MM. Characterization of insulin-like growth factor I-stimulated tyrosine kinase activity associated with the beta-subunit of type I insulin-like growth factor receptors of rat liver cells. J Biol Chem 1985;260(17):9793-9804
25. Ludwig T, Eggenschwiler J, Fisher P, et al. Mouse mutants lacking the type 2 IGF receptor (IGF2R) are rescued from perinatal lethality in Igf2 and Igf1r null backgrounds. Dev Biol 1996;177(2):517-535
26. Khamsi F, Roberge S, Yavas Y, et al. Recent discoveries in physiology of insulin-like growth factor-1 and its interaction with gonadotropins in folliculogenesis. Endocrine 2001;16(3):151-165
27. Sekar N, Garmey JC, Veldhuis JD. Mechanisms underlying the steroidogenic synergy of insulin and luteinizing hormone in porcine granulosa cells:joint amplification of pivotal sterol-regulatory genes encoding the low-density lipoprotein (LDL) receptor, steroidogenic acute regulatory (StAR) protein and cytochrome P450 side-chain cleavage (P450scc) enzyme. Mol Cell Endocrinol 2000;159(1-2):25-35
28. Eimerl S, Orly J. Regulation of steroidogenic genes by insulin-like growth factor-1 and follicle-stimulating hormone:differential responses of cytochrome P450 side-chain cleavage, steroidogenic acute regulatory protein, and 3beta-hydroxysteroid dehydrogenase/isomerase in rat granulosa cells. Biol Reprod 2002;67(3):900-910
29. Costrici N, Lunenfeld B, Pariente C, et al. Induction of aromatase in human granulosa cells by both follicle stimulating hormone and insulin-like growth factor-I involves tyrosine phosphorylation. Gynecol Endocrinol 1994;8(3):183-189
30. Erickson GF, Garzo VG, Magoffin DA. Insulin-like growth factor-I regulates aromatase activity in human granulosa and granulosa luteal cells. J Clin Endocrinol Metab 1989;69(4):716-724
31. Erickson GF, Magoffin DA, Cragun JR, Chang RJ. The effects of insulin and insulin-like growth factors-I and -II on estradiol production by granulosa cells of polycystic ovaries. J Clin Endocrinol Metab 1990;70(4):894-902
32. Kanzaki M, Hattori MA, Horiuchi R, Kojima I. Co-ordinate actions of FSH and insulin-like growth factor-I on LH receptor expression in rat granulosa cells. J Endocrinol 1994;141(2):301-308
33. Safi M, Onagbesan OM, Bruggeman V, et al. Regulation of inhibin alpha- and beta(A)-subunit messenger ribonucleic acid levels by gonadotropins and IGF-I in cultured chicken granulosa cells. Gen Comp Endocrinol 2003;131(2):159-167
34. Schoenfelder M, Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol Reprod 2003;69(1):269-277
35. Chen L, Mao SJ, Larsen WJ. Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-alpha-trypsin inhibitor family. J Biol Chem 1992;267(17):12380-12386
36. Yoshioka S, Ochsner S, Russell DL, et al. Expression of tumor necrosis factor-stimulated gene-6 in the rat ovary in response to an ovulatory dose of gonadotropin. Endocrinology 2000;141(11):4114-4119
37. Salustri A, Garlanda C, Hirsch E, et al. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 2004;131(7):1577-1586
38. KobayashiH,SunGW,HirashimaY,TeraoT.Identi- fication of link protein during follicle development and cumulus cell cultures in rats. Endocrinology 1999;140(8):3835-3842
39. Minegishi T, Hirakawa T, Kishi H, et al. A role of insulinlike growth factor I for follicle-stimulating hormone receptor expression in rat granulosa cells. Biol Reprod 2000;62(2):325-333
40. Sun GW, Kobayashi H, Suzuki M, Kanayama N, Terao T. Follicle-stimulating hormone and insulin-like growth factor I synergistically induce up-regulation of cartilage link protein (Crtl1) via activation of phosphatidylinositol-dependent kinase/Akt in rat granulosa cells. Endocrinology 2003;144(3):793-801
41. Wasielak M, Bogacki M. Apoptosis inhibition by insulin-like growth factor (IGF)-I during in vitro maturation of bovine oocytes. J Reprod Dev 2007;53(2):419-426
42. Demeestere I, Gervy C, Centner J, et al. Effect of insulinlike growth factor-I during preantral follicular culture on steroidogenesis, in vitro oocyte maturation, and embryo development in mice. Biol Reprod 2004;70(6):1664-1669
43. Quirk SM, Cowan RG, Harman RM, Hu CL, Porter DA. Ovarian follicular growth and atresia:the relationship between cell proliferation and survival. J Anim Sci 2004;82(Suppl):E40-E52
44. Xin X, Hou YT, Li L, et al. IGF-I increases IGFBP-5 and collagen alphal(I) mRNAs by the MAPK pathway in rat intestinal smooth muscle cells. Am J Physiol Gastrointest Liver Physiol 2004;286(5):G777-G783
45. Hunzicker-Dunn M, Maizels ET. FSH signaling pathways in immature granulosa cells that regulate target gene expression:branching out from protein kinase A. Cell Signal 2006;18(9):1351-1359
46. Salvador LM, Park Y, Cottom J, et al. Follicle-stimulating hormone stimulates protein kinase A-mediated histone H3 phosphorylation and acetylation leading to select gene activation in ovarian granulosa cells. J Biol Chem 2001;276(43):40146-40155
47. Weck J, Mayo KE. Switching of NR5A proteins associated with the inhibin alpha-subunit gene promoter after activation of the gene in granulosa cells. Mol Endocrinol 2006;20(5):1090-1103
48. Falender AE, Lanz R, Malenfant D, Belanger L, Richards JS. Differential expression of steroidogenic factor-1 and FTF/LRH-1 in the rodent ovary. Endocrinology 2003;144(8):3598-3610
49. Kwintkiewicz J, Cai Z, Stocco C. Follicle-stimulating hormone-induced activation of Gata4 contributes in the up-regulation ofCyp19 expression in rat granulosa cells. Mol Endocrinol 2007;21(4):933-947
50. Gillio-Meina C, Hui YY, LaVoie HA. Expression of CCAAT/enhancer binding proteins alpha and beta in the porcine ovary and regulation in primary cultures of granulosa cells. Biol Reprod 2005;72(5):1194-1204
51. Yazawa T, Mizutani T, Yamada K, et al. Involvement of cyclic adenosine 5′-monophosphate response element-binding protein, steroidogenic factor 1, and Dax-1 in the regulation of gonadotropin-inducible ovarian transcription factor 1 gene expression by follicle-stimulating hormone in ovarian granulosa cells. Endocrinology 2003;144(5):1920-1930
52. Sekar N, Veldhuis JD. Involvement of Spl and SREBP-la in transcriptional activation of the LDL receptor gene by insulin and LH in cultured porcine granulosa-luteal cells. Am J Physiol Endocrinol Metab 2004;287(1):E128-E135
53. LaVoie HA, Garmey JC, Veldhuis JD. Mechanisms of insulin-like growth factor I augmentation of follicle-stimulating hormone-induced porcine steroidogenic acute regulatory protein gene promoter activity in granulosa cells. Endocrinology 1999;140(1):146-153
54. Manna PR, Chandrala SP, King SR, et al. Molecular mechanisms of insulin-like growth factor-I mediated regulation of the steroidogenic acute regulatory protein in mouse Leydig cells. Mol Endocrinol 2006;20(2):362-378
55. Manna PR, Wang XJ, Stocco DM. Involvement of multiple transcription factors in the regulation of steroidogenic acute regulatory protein gene expression. Steroids 2003;68(14):1125-1134
56. Stocco DM, Clark BJ, Reinhart AJ, et al. Elements involved in the regulation of the StAR gene. Mol Cell Endocrinol 2001;177(1-2):55-59
57. Urban RJ, Shupnik MA, Bodenburg YH. Insulin-like growth factor-I increases expression of the porcine P-450 cholesterol side chain cleavage gene through a GC-rich domain. J Biol Chem 1994;269(41):25761-25769
58. Stocco C, Kwintkiewicz J, Cai Z. Identification of regulatory elements in the Cyp19 proximal promoter in rat luteal cells. J Mol Endocrinol 2007;39(4):211-221
59. Monte D, DeWitte F, Hum DW. Regulation of the human P450scc gene by steroidogenic factor 1 is mediated by CBP/p300. J Biol Chem 1998;273(8):4585- 4591
60. Liu Z, Simpson ER. Steroidogenic factor 1 (SF-1) and SP1 are required for regulation of bovine CYP11A gene expression in bovine luteal cells and adrenal Y1 cells. Mol Endocrinol 1997;11(2):127-137
61. Ahlgren R, Suske G, Waterman MR, Lund J. Role of Spl in cAMP-dependent transcriptional regulation of the bovine CYP11A gene. J Biol Chem 1999;274(27):19422-19428
62. Ahlgren R, Simpson ER, Waterman MR, Lund J. Characterization of the promoter/regulatory region of the bovine CYP11A (P-450scc) gene. Basal and cAMP-dependent expression. J Biol Chem 1990;265(6):3313-3319
63. Basile A, Sica A, d'Aniello E, et al. Characterization of the promoter for the human long pentraxin PTX3. Role of NF- kappaB in tumor necrosis factor-alpha and interleukin-1beta regulation. J Biol Chem 1997;272(13):8172- 8178
64. Yamada Y, Itano N, Zako M, et al. The gene structure and promoter sequence of mouse hyaluronan synthase 1. Biochem J 1998;330(Pt 3):1223-1227
65. Cataldo NA, Giudice LC. Insulin-like growth factor binding protein profiles in human ovarian follicular fluid correlate with follicular functional status. J Clin Endocrinol Metab 1992;74(4):821-829
66. Giudice LC. Growth factor action on ovarian function in polycystic ovary syndrome. Endocrinol Metab Clin North Am 1999;28(2):325-339 vi
67. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins:biological actions. Endocr Rev 1995;16(1):3-34
68. Qin QP, Christiansen M, Oxvig C, et al. Double- monoclonal immunofluorometric assays for pregnancy-associated plasma protein A/proeosinophil major basic protein (PAPP-A/proMBP) complex in first-trimester maternal serum screening for Down syndrome. Clin Chem 1997;43(12):2323-2332
69. Sinosich MJ, Porter R, Sloss P, Bonifacio MD, Saunders DM. Pregnancy-associated plasma protein A in human ovarian follicular fluid. J Clin Endocrinol Metab 1984;58(3):500-504
70. Sinosich MJ, Seppala M, Saunders DM, Grudzinskas JG. Pregnancy-associated plasma protein-A and placental protein 5 in human seminal plasma. Ann N Y Acad Sci 1985;442:287-292
71. Tsakok FH, Koh S, Chua SE, et al. Prognostic significance of the new placental proteins in trophoblastic disease. Br J Obstet Gynaecol 1983;90(5):483-486
72. Qin X, Byun D, Lau KH, Baylink DJ, Mohan S. Evidence that the interaction between insulin-like growth factor (IGF)-II and IGF binding protein (IGFBP)-4 is essential for the action of the IGF-II-dependent IGFBP-4 protease. Arch Biochem Biophys 2000;379(2):209-216
73. Conover CA, Faessen GF, Ilg KE, et al. Pregnancy-associated plasma protein-a is the insulin-like growth factor binding protein-4 protease secreted by human ovarian granulosa cells and is a marker of dominant follicle selection and the corpus luteum. Endocrinology 2001;142(5):2155
74. Overgaard MT, Nyegaard M, Su YQ, et al. Lack of functional PAPP-A compromises female fertility. Paper presented at:The Endocrine Society annual meeting;June 24-27, 2006;Boston, MA
75. Overgaard MT, Glerup S, Boldt HB, et al. Inhibition of proteolysis by the proform of eosinophil major basic protein (proMBP) requires covalent binding to its target proteinase. FEBS Lett 2004;560(1-3):147-152
76. Glerup S, Boldt HB, Overgaard MT, et al. Proteinase inhibition by proform of eosinophil major basic protein (pro- MBP) is a multistep process of intra- and intermolecular disulfide rearrangements. J Biol Chem 2005;280(11):9823-9832
77. Glerup S, Kloverpris S, Laursen LS, et al. Cell surface detachment of pregnancy-associated plasma protein-A requires the formation of intermolecular proteinase-inhibitor disulfide bonds and glycosaminoglycan covalently bound to the inhibitor. J Biol Chem 2007;282(3):1769-1778
78. Poretsky L, Cataldo NA, Rosenwaks Z, Giudice LC. The insulin-related ovarian regulatory system in health and disease. Endocr Rev 1999;20(4):535-582
79. Rhoton-Vlasak A, Gleich GJ, Bischof P, Chegini N. Localization and cellular distribution of pregnancy-associated plasma protein-a and major basic protein in human ovary and corpora lutea throughout the menstrual cycle. Fertil Steril 2003;79(5):1149-1153
80. Sabuncu T, Vural H, Harma M, Harma M. Oxidative stress in polycystic ovary syndrome and its contribution to the risk of cardiovascular disease. Clin Biochem 2001;34(5):407-413
81. Adler V, Yin Z, Tew KD, Ronai Z. Role of redox potential and reactive oxygen species in stress signaling. Oncogene 1999;18(45):6104-6111
82. el-Roeiy A, Chen X, Roberts VJ, et al. 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(6):1488-1496
83. Magoffin DA, San Roman GA, Muderspach LI. Insulin-like growth factor binding proteins in a natural pre-ovulatory follicle from a woman with polycystic ovary syndrome. Hum Reprod 1995;10(9):2248-2252
84. Peng X, Maruo T, Samoto T, Mochizuki M. Comparison of immunocytologic localization of insulin-like growth factor binding protein-4 in normal and polycystic ovary syndrome human ovaries. Endocr J 1996;43(3):269-278
85. Pocar P, Brevini TA, Fischer B, Gandolfi F. The impact of endocrine disruptors on oocyte competence. Reproduction 2003;125(3):313-325
86. Propper CR. The study ofendocrine-disrupting compounds:past approaches and new directions. Integr Comp Biol 2005;45(1):194-200
87. Minegishi T, Hirakawa T, Abe K, Kishi H, Miyamoto K. Effect of IGF-1 and 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on the expression of LH receptors during cell differentiation in cultured granulosa cells. Mol Cell Endocrinol 2003;202(1-2):123-131
88. Holloway AC, Petrik JJ, Younglai EV. Influence of dichlorodiphenylchloroethylene on vascular endothelial growth factor and insulin-like growth factor in human and rat ovarian cells. Reprod Toxicol 2007;24(3-4):359-364
89. Mlynarcikova A, Kolena J, Fickova M, Scsukova S. Alterations in steroid hormone production by porcine ovarian granulosa cells caused by bisphenol A and bisphenol A dimethacrylate. Mol Cell Endocrinol 2005;244(1-2):57-62
90. Kwintkiewicz J, Giudice LC. Endocrine disruptor bisphenol A induces expression of peroxisome proliferator-activated receptor which contributes to down-regulation of FSH stimulated aromatase expression and estradiol production in human granulosa KGN cells. Paper presented at:The Society for the Study of Reproduction annual meeting;May 27-30, 2008;Kona, HI
91. Kwintkiewicz J, Giudice LC. Endocrine disruptor bisphenol A (BPA) reduces FSH stimulated cyp19 expression and downstream estradiol production in human granulosa KGN cells. Paper presented at:The Society for Gynecologic Investigation annual meeting;March 23-29, 2008;San Diego, CA