Actions of the TGF Superfamily Members in Ovarian Follicle Growth and Development

난포성장 발달에 있어서 TGF-$\beta$ Superfamily의 작용

  • Roh, Jae-Sook (Department of Pharmacological Research, National Institute of Toxicological Research)
  • 노재숙 (국립독성연구원 약리연구부 임상약리팀)
  • Published : 2007.09.30

Abstract

Keywords

References

  1. McGee EA, Hsueh AJ. Initial and cyclic recruitment of ovarian follicles. Endocr Rev 2000; 21: 200-14 https://doi.org/10.1210/er.21.2.200
  2. Knight PG, Glister C. Local roles of TGF-beta superfamily members in the control of ovarian follicle development. Anim Reprod Sci 2003; 78: 165-83 https://doi.org/10.1016/S0378-4320(03)00089-7
  3. Findlay JK, Drummond AE, Dyson ML, Baillie AJ, Robertson DM, Ethier JF. Recruitment and development of the follicle; the roles of the transforming growth factor-beta superfamily. Mol Cell Endocrinol 2002; 191: 35-43 https://doi.org/10.1016/S0303-7207(02)00053-9
  4. Lin SY, Morrison JR, Phillips DJ, de Kretser DM. Regulation of ovarian function by the TGF-beta superfamily and follistatin. Reproduction 2003; 126: 133-48 https://doi.org/10.1530/rep.0.1260133
  5. Pangas SA, Rademaker AW, Fishman DA, Woodruff TK. Localization of the activin signal transduction components in normal human ovarian follicles: implications for autocrine and paracrine signaling in the ovary. J Clin Endocrinol Metab 2002; 87: 2644-57 https://doi.org/10.1210/jc.87.6.2644
  6. Drummond AE, Dyson M, Le MT, Ethier JF, Findlay JK. Ovarian follicle populations of the rat express TGF-beta signalling pathways. Mol Cell Endocrinol 2003; 202: 53-7 https://doi.org/10.1016/S0303-7207(03)00062-5
  7. Drummond AE, Le MT, Ethier JF, Dyson M, Findlay JK. Expression and localization of activin receptors, Smads, and beta glycan to the postnatal rat ovary. Endocrinology 2002; 143: 1423-33 https://doi.org/10.1210/en.143.4.1423
  8. Ami KY, Ohshima K, Watanabe G, Arai K, Uehara K, Taya K. Dynamics of messenger RNAs encoding inhibin/activin subunits and follistatin in the ovary during the rat estrous cycle. Biol Reprod 2002; 66: 1119-26 https://doi.org/10.1095/biolreprod66.4.1119
  9. Sidis Y, Fujiwara T, Leykin L, Isaacson K, Toth T, Schneyer AL. Characterization of inhibin/activin subunit, activin receptor, and follistatin messenger ribonucleic acid in human and mouse oocytes: evidence for activin's paracrine signaling from granulosa cells to oocytes. Biol Reprod 1998; 59: 807-12 https://doi.org/10.1095/biolreprod59.4.807
  10. Piek E, Heldin CH, Ten Dijke P. Specificity, diversity, and regulation in TGF-beta superfamily signaling. Faseb J 1999; 13: 2105-24 https://doi.org/10.1096/fasebj.13.15.2105
  11. Chegini N, Flanders KC. Presence of transforming growth factor-beta and their selective cellular localization in human ovarian tissue of various reproductive stages. Endocrinology 1992; 130: 1707-15 https://doi.org/10.1210/en.130.3.1707
  12. Skinner MK, Keski-Oja J, Osteen KG, Moses HL. Ovarian thecal cells produce transforming growth factor-beta which can regulate granulosa cell growth. Endocrinology 1987; 121: 786-92 https://doi.org/10.1210/endo-121-2-786
  13. Roy SK, Kole AR. Ovarian transforming growth factor-beta (TGF-beta) receptors: in-vitro effects of follicle stimulating hormone, epidermal growth factor and TGF-beta on receptor expression in human preantral follicles. Mol Hum Reprod 1998; 4: 207-14 https://doi.org/10.1093/molehr/4.3.207
  14. Saragueta PE, Lanuza GM, Baranao JL. Autocrine role of transforming growth factor betal on rat granulosa cell proliferation. Biol Reprod 2002; 66: 1862-8 https://doi.org/10.1095/biolreprod66.6.1862
  15. Liu X, Andoh K, Abe Y, Kobayashi J, Yamada K, Mizunuma H, Ibuki Y. A comparative study on transforming growth factor-beta and activin A for preantral follicles from adult, immature, and diethylstilbestrol-primed immature mice. Endocrinology 1999; 140: 2480-5 https://doi.org/10.1210/en.140.6.2480
  16. Attia GR, Dooley CA, Rainey WE, Carr BR. Transforming growth factor beta inhibits steroidogenic acute regulatory (StAR) protein expression in human ovarian thecal cells. Mol Cell Endocrinol 2000; 170: 123-9 https://doi.org/10.1016/S0303-7207(00)00335-X
  17. Inoue K, Nakamura K, Abe K, Hirakawa T, Tsuchiya M, Matsuda H, et al. Effect of transforming growth factor beta on the expression of luteinizing hormone receptor in cultured rat granulosa cells. Biol Reprod 2002; 67: 610-5 https://doi.org/10.1095/biolreprod67.2.610
  18. Drummond AE, Dyson M, Thean E, Groome NP, Robertson DM, Findlay JK. Temporal and hormonal regulation of inhibin protein and subunit mRNA expression by post-natal and immature rat ovaries. J Endocrinol 2000; 166: 339-54 https://doi.org/10.1677/joe.0.1660339
  19. Ethier JF, Findlay JK. Roles of activin and its signal transduction mechanisms in reproductive tissues. Reproduction 2001; 121: 667-75 https://doi.org/10.1530/rep.0.1210667
  20. Findlay JK, Drummond AE, Dyson M, Baillie AJ, Robertson DM, Ethier JF. Production and actions of inhibin and activin during folliculogenesis in the rat. Mol Cell Endocrinol 2001; 180: 139-44 https://doi.org/10.1016/S0303-7207(01)00521-4
  21. Mizunuma H, Liu X, Andoh K, Abe Y, Kobayashi J, Yamada K, et al. Activin from secondary follicles causes small preantral follicles to remain dormant at the resting stage. Endocrinology 1999; 140: 37-42 https://doi.org/10.1210/en.140.1.37
  22. Duleba AJ, Pehlivan T, Carbone R, Spaczynski RZ. Activin stimulates proliferation of rat ovarian thecal-interstitial cells. Biol Reprod 2001; 65: 704-9 https://doi.org/10.1095/biolreprod65.3.704
  23. Hsueh AJ, Dahl KD, Vaughan J, Tucker E, Rivier J, Bardin CW, et al. Heterodimers and homodimers of inhibin subunits have different paracrine action in the modulation of luteinizing hormone-stimulated androgen biosynthesis. Proc Natl Acad Sci U S A 1987; 84: 5082-6 https://doi.org/10.1073/pnas.84.14.5082
  24. Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant activin on androgen synthesis in cultured human thecal cells. J Clin Endocrinol Metab 1991; 72: 1206-11 https://doi.org/10.1210/jcem-72-6-1206
  25. Alak BM, Coskun S, Friedman CI, Kennard EA, Kim MH, Seifer DB. Activin A stimulates meiotic maturation of human oocytes and modulates granulosa cell steroidogenesis in vitro. Fertil Steril 1998; 70; 1126-30 https://doi.org/10.1016/S0015-0282(98)00386-0
  26. Xu J, Oakley J, McGee EA. Stage-specific expression of smad2 and smad3 during folliculogenesis. Biol Reprod 2002; 66: 1571-8 https://doi.org/10.1095/biolreprod66.6.1571
  27. Tomic D, Brodie SG, Deng C, Hickey RJ, Babus JK, Malkas LH, et al. Smad 3 may regulate follicular growth in the mouse ovary. Biol Reprod 2002; 66: 917-23 https://doi.org/10.1095/biolreprod66.4.917
  28. Meunier H, Cajander SB, Roberts VJ, Rivier C, Sawchenko PE, Hsueh AJ, et al. Rapid changes in the expression of inhibin alpha-, beta A, and beta B-subunits in ovarian cell types during the rat estrous cycle. Mol Endocrinol 1998; 2: 1352-63 https://doi.org/10.1210/mend-2-12-1352
  29. Roberts VJ, Barth S, el-Roeiy A, Yen SS. Expression of inhibin/ activin subunits and follistat in messenger ribonucleic acids and proteins in ovarian follicles and the corpus luteum during the human menstrual cycle. J Clin Endocrinol Metab 1993; 77: 1402-10 https://doi.org/10.1210/jc.77.5.1402
  30. Prendergast KA, Burger LL, Aylor KW, Haisenleder DJ, Dalkin AC, Marshall JC. Pituitary Follistatin Gene Expression in Female Rats: Evidence That Inhibin Regulates Transcription. Biol Reprod 2004 Feb; 70(2): 364-70 https://doi.org/10.1095/biolreprod.103.021733
  31. Hillier SG, Yong EL, Illingworth PJ, Baird DT, Schwall RH, Mason AJ. Effect of recombinant inhibin on androgen synthesis in cultured human thecal cells. Mol Cell Endocrinol 1991; 75: R1-6 https://doi.org/10.1016/0303-7207(91)90238-N
  32. Jirnenez-Krassel F, Winn ME, Bums D, Ireland JL, Ireland JJ. Evidence for a negative intrafollicular role for inhibin in regulation of estradiol production by granulosa cells. Endocrinology 2003; 144: 1876-86 https://doi.org/10.1210/en.2002-221077
  33. Vitale AM, Gonzalez OM, Parborell F, Irusta G, Campo S, Tesone M. Inhibin a increases apoptosis in early ovarian antral follicles of diethylstilbestrol-treated rats. Biol Reprod 2002; 67: 989-95
  34. Erickson GF, Shirnasaki S. The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod Biol Endocrinol 2003; 1: 9-29 https://doi.org/10.1186/1477-7827-1-9
  35. Shirnasaki S, Zachow RJ, Li D, Kim H, Iemura S, Ueno N, Sampath K, et al. A functional bone morphogenetic protein system in the ovary. Proc Natl Acad Sci V S A 1999; 96: 7282-7 https://doi.org/10.1073/pnas.96.13.7282
  36. Souza CJ, Campbell BK, McNeilly AS, Baird DT. Effect of bone morphogenetic protein 2 (BMP2) on oestradiol and inhibin A production by sheep granulosa cells, and localization of BMP receptors in the ovary by immunohistochemistry. Reproduction 2002; 123: 363-9 https://doi.org/10.1530/rep.0.1230363
  37. Lee WS, Otsuka F, Moore RK, Shirnasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol Reprod 2001; 65: 994-9 https://doi.org/10.1095/biolreprod65.4.994
  38. Yi SE, LaPolt PS, Yoon BS, Chen JY, Lu JK, Lyons KM. The type I BMP receptor BmprIB is essential for female reproductive function. Proc Natl Acad Sci U S A 2001; 98: 7994-9 https://doi.org/10.1073/pnas.141002798
  39. Chang H, Brown CW, Matzuk MM. Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 2002; 23: 787-823 https://doi.org/10.1210/er.2002-0003
  40. Dooley CA, Attia GR, Rainey WE, Moore DR, Carr BR. Bone morphogenetic protein inhibits ovarian androgen production. J Clin Endocrinol Metab 2000; 85: 3331-7 https://doi.org/10.1210/jc.85.9.3331
  41. Nilsson EE, Skinner MK. Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol Reprod 2003; 69: 1265-72 https://doi.org/10.1095/biolreprod.103.018671
  42. Otsuka F, Moore RK, Shimasaki S. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J Biol Chem 2001; 276: 32889-95 https://doi.org/10.1074/jbc.M103212200
  43. Bondestam J, Kaivo-oja N, Kallio J, Groome N, HydenGranskog C, Fujii M, et al. Engagement of activin and bone morphogenetic protein signaling pathway Smad proteins in the induction of inhibin B production in ovarian granulosa cells. Mol Cell Endocrinol 2002; 195: 79-88 https://doi.org/10.1016/S0303-7207(02)00219-8
  44. Jaatinen R, Bondestam J, Raivio T, Hilden K. Dunkel L, Groome N, et al. Activation of the bone morphogenetic protein signaling pathway induces inhibin beta(B)-subunit mRNA and secreted inhibin B levels in cultured human granulosaluteal cells. J Clin Endocrinol Metab 2002; 87: 1254-61 https://doi.org/10.1210/jc.87.3.1254
  45. Solloway MJ, Dudley AT, Bikoff EK. Lyons KM, Hogan BL, Robertson EJ. Mice lacking Bmp6 function. Dev Genet 1998; 22: 321-39 https://doi.org/10.1002/(SICI)1520-6408(1998)22:4<321::AID-DVG3>3.0.CO;2-8
  46. Baarends WM, Uilenbroek JT, Kramer P, Hoogerbrugge JW, van Leeuwen EC, Themmen AP, et al. Anti-rnullerian hormone and anti-mullerian hormone type II receptor messenger ribonucleic acid expression in rat ovaries during postnatal development, the estrous cycle, and gonadotropin-induced follicle growth. Endocrinology 1995; 136: 4951-62 https://doi.org/10.1210/en.136.11.4951
  47. Durlinger AL, Visser JA, Themmen AP. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002; 124: 601-9 https://doi.org/10.1530/rep.0.1240601
  48. Behringer RR, Finegold MJ, Cate RL. Mullerian-inhibiting substance function during mammalian sexual development. Cell 1994; 79: 415-25 https://doi.org/10.1016/0092-8674(94)90251-8
  49. Durlinger AL, Kramer P, Karels B, de Jong FH, Uilenbroek JT, Grootegoed JA, et al. Control of primordial follicle recruitment by anti-Mullerian hormone in the mouse ovary. Endocrinology 1999; 140: 5789-96 https://doi.org/10.1210/en.140.12.5789
  50. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Ingraham HA, Nachtigal MW, et al. Anti-Mullerian hormone inhibits initiation of primordial follicle growth in the mouse ovary. Endocrinology 2002; 143: 1076-84 https://doi.org/10.1210/en.143.3.1076
  51. Durlinger AL, Gruijters MJ, Kramer P, Karels B, Kumar TR, Matzuk MM, et al. Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 2001; 142: 4891-9 https://doi.org/10.1210/en.142.11.4891
  52. Clarke TR, Hoshiya Y, Yi SE, Liu X, Lyons KM, Donahoe PK. Mullerian inhibiting substance signaling uses a bone morphogenetic protein (BMP)-like pathway mediated by ALK2 and induces SMAD6 expression. Mol Endocrinol 2001; 15: 946-59 https://doi.org/10.1210/me.15.6.946
  53. Vitt UA, Hsueh AJ. Stage-dependent role of growth differentiation factor-9 in ovarian follicle development. Mol Cell Endocrinol 2001; 183: 171-7 https://doi.org/10.1016/S0303-7207(01)00614-1
  54. Otsuka F, Yao Z, Lee T, Yamamoto S, EricksonGF, Shimasaki S. Bone morphogenetic protein-15 . Identification of target cells and biological functions. J Biol Chem 2000; 275: 39523 -8 https://doi.org/10.1074/jbc.M007428200
  55. Duffy DM. Growth differentiation factor-9 is expressed by the primate follicle throughout the periovulatory interval. Biol Reprod 2003; 69: 725-32 https://doi.org/10.1095/biolreprod.103.015891
  56. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996; 383: 531-5 https://doi.org/10.1038/383531a0
  57. Hayashi M, McGee EA, Min G, Klein C, Rose UM, van Duin M, et al. Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles. Endocrinology 1999; 140: 1236-44 https://doi.org/10.1210/en.140.3.1236
  58. Vitt VA, McGee EA, Hayashi M, Hsueh AJ. In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 2000; 141: 3814-20 https://doi.org/10.1210/en.141.10.3814
  59. Hreinsson JG, Scott JE, Rasmussen C, Swahn ML, Hsueh AJ, Hovatta O. Growth differentiation factor-9 promotes the growth, development, and surviUAl of human ovarian follicles in organ culture. J Clin Endocrinol Metab 2002; 87: 316-21 https://doi.org/10.1210/jc.87.1.316
  60. Elvin JA, Clark AT, Wang P, Wolfman NM, Matzuk MM. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 1999; 13: 1035-48 https://doi.org/10.1210/me.13.6.1035
  61. Roh JS, Bondestam J, Mazerbourg S, Kaivo-Oja N, Groome N, Ritvos O, et al. Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 2003; 144: 172-8 https://doi.org/10.1210/en.2002-220618
  62. Kaivo-Oja N, Bondestam J, Kamarainen M, Koskimies J, Vitt U, Cranfield M, et al. Growth differentiation factor-9 induces Smadl activation and inhibin B production in cultured human granulosa-luteal cells. J Clin Endocrinol Metab 2003; 88: 755 -62 https://doi.org/10.1210/jc.2002-021317
  63. Vitt UA, Hayashi M, Klein C, Hsueh AJ. Growth differentiation factor-9 stimulates proliferation but suppresses the folliclestimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 2000; 62: 370-7 https://doi.org/10.1095/biolreprod62.2.370
  64. Mazerbourg S, Hsueh AJ. Growth differentiation factor-9 signaling in the ovary. Mol Cell Endocrinol 2003; 202: 31-6 https://doi.org/10.1016/S0303-7207(03)00058-3
  65. Parrott JA, Skinner MK. Kit ligand actions on ovarian stromal cells: effects on theca cell recruitment and steroid production. Mol Reprod Dev 2000; 55: 55-64 https://doi.org/10.1002/(SICI)1098-2795(200001)55:1<55::AID-MRD8>3.0.CO;2-L
  66. Nilsson EE, Skinner MK. Growth and differentiation factor-9 stimulates progression of early primary but not primordial rat ovarian follicle development. Biol Reprod 2002; 67: 1018-24 https://doi.org/10.1095/biolreprod.101.002527
  67. Solovyeva EV, Hayashi M, Margi K, Barkats C, Klein C, Amsterdam A, et al. Growth differentiation factor-9 stimulates rat theca-interstitial cell androgen biosynthesis. Biol Reprod 2000; 63: 1214-8 https://doi.org/10.1095/biolreprod63.4.1214
  68. Yamamoto N, Christenson LK, McAllister JM, Strauss JF, 3rd. Growth differentiation factor-9 inhibits 3'5'-adenosine monophosphate-stimulated steroidogenesis in human granulosa and theca cells. J Clin Endocrinol Metab 2002; 87: 2849-56 https://doi.org/10.1210/jc.87.6.2849
  69. Otsuka F, Shimasaki S. A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc Natl Acad Sci USA 2002; 99: 8060-5 https://doi.org/10.1073/pnas.122066899
  70. Otsuka F, Yamamoto S, Erickson GF, Shimasaki S. Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J Biol Chem 2001; 276: 11387-92 https://doi.org/10.1074/jbc.M010043200
  71. Galloway SM, McNatty KP, Cambridge LM, Laitinen MP, Juengel JL, Jokiranta TS, et al. Mutations in an oocyte-derived growth factor gene (BMPI5) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 2000; 25: 279-83 https://doi.org/10.1038/77033
  72. Vitt UA, Mazerbourg S, Klein C, Hsueh AJ. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol Reprod 2002; 67: 473-80 https://doi.org/10.1095/biolreprod67.2.473
  73. Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem 2003; 278: 304-10 https://doi.org/10.1074/jbc.M207362200
  74. Ethier JF, Famworth PG, Findlay JK, Ooi GT. Transforming Growth Factor-beta Modulates Inhibin A Bioactivity in the LbetaT2 Gonadotrope Cell Line by Competing for Binding to Betaglycan. Mol Endocrinol 2002; 16: 2754-63 https://doi.org/10.1210/me.2002-0014
  75. Lewis KA, Gray PC, Blount AL, MacConell LA, Wiater E, Bilezikjian LM, et al. Betaglycan binds inhibin and can mediate functional antagonism of activin signalling. Nature 2000; 404: 411-4 https://doi.org/10.1038/35006129
  76. Wiater E, Vale W. Inhibin is an antagonist of bone morphogenetic protein signaling. J Biol Chem 2003; 278: 7934-41 https://doi.org/10.1074/jbc.M209710200
  77. Liu J, Kuulasmaa T, Kosma VM, Butzow R, UAnttinen T, Hyden-Granskog C, et al. Expression of betaglycan, an inhibin coreceptor, in normal human ovaries and ovarian sex cord-stromal tumors and its regulation in cultured human granulosa-luteal cells. J Clin Endocrinol Metab 2003; 88: 5002- https://doi.org/10.1210/jc.2003-030704
  78. Otsuka F, Moore RK, Iemura S, Ueno N, Shimasaki S. Follistatin inhibits the function of the oocyte-derived factor BMP-15. Biochem Biophys Res Commun 2001; 289: 961-6 https://doi.org/10.1006/bbrc.2001.6103
  79. Albertini DF, Combelles CM, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 2001; 121: 647-53 https://doi.org/10.1530/rep.0.1210647
  80. Rodgers RJ, Irving-Rodgers HF, Russell DL. Extracellular matrix of the developing ovarian follicle. Reproduction 2003; 126: 415-24 https://doi.org/10.1530/rep.0.1260415
  81. McIntush EW, Smith ME Matrix metalloproteinases and tissue inhibitors of metalloproteinases in ovarian function. Rev Reprod 1998; 3: 23-30 https://doi.org/10.1530/ror.0.0030023
  82. Harlow CR, Rae M, Davidson L, Trackman PC, Hillier SG. Lysyl oxidase gene expression and enzyme activity in the rat ovary: regulation by follicle-stimulating hormone, androgen, and transforming growth factor-beta superfamily members in vitro. Endocrinology 2003; 144: 154-62 https://doi.org/10.1210/en.2002-220652
  83. Harlow CR, Davidson L, Bums KH, Yan C, Matzuk MM, Hillier SG. FSH and TGF-beta superfamily members regulate granulosa cell connective tissue growth factor gene expression in vitro and in vivo. Endocrinology 2002; 143: 3316-25 https://doi.org/10.1210/en.2001-211389