Role of anti-Müllerian hormone and bone morphogenetic proteins in the regulation of FSH sensitivity

Molecular and Cellular Endocrinology

Volumn 382, Issue 1, 2014, Pages 460-465

  Visser, Jenny A ^a   Themmen, Axel P N ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

AMH; BMP; Folliculogenesis; FSH; Ovary

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FOLLITROPIN; GROWTH FACTOR; LUTEINIZING HORMONE; MUELLERIAN INHIBITING FACTOR;

CORPUS LUTEUM; GRANULOSA CELL; HORMONAL REGULATION; HUMAN; HYPOPHYSIS; HYPOTHALAMUS; MICROENVIRONMENT; NONHUMAN; OOCYTE; OVARY; OVARY FOLLICLE; OVULATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; THECA CELL;

AMH; BMP; FOLLICULOGENESIS; FSH; OVARY;

ANIMALS; ANTI-MULLERIAN HORMONE; BONE MORPHOGENETIC PROTEINS; FEMALE; FOLLICLE STIMULATING HORMONE; HUMANS; MODELS, BIOLOGICAL; OVARY;

EID: 84888304947     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2013.08.012     Document Type: Review

References (79)

1. Aittomaki K., Lucena J.L., Pakarinen P., Sistonen P., Tapanainen J., Gromoll J., Kaskikari R., Sankila E.M., Lehvaslaiho H., Engel A.R., Nieschlag E., Huhtaniemi I., de la Chapelle A. Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 1995, 82:959-968.
2. Baarends W.M., van Helmond M.J., Post M., van der Schoot P.J., Hoogerbrugge J.W., de Winter J.P., Uilenbroek J.T., Karels B., Wilming L.G., Meijers J.H., et al. A novel member of the transmembrane serine/threonine kinase receptor family is specifically expressed in the gonads and in mesenchymal cells adjacent to the mullerian duct. Development 1994, 120:189-197.
3. Baarends W.M., Uilenbroek J.T., Kramer P., Hoogerbrugge J.W., van Leeuwen E.C., Themmen A.P., Grootegoed J.A. Anti-mullerian 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, 136:4951-4962.
4. Behre H.M., Greb R.R., Mempel A., Sonntag B., Kiesel L., Kaltwasser P., Seliger E., Ropke F., Gromoll J., Nieschlag E., Simoni M. Significance of a common single nucleotide polymorphism in exon 10 of the follicle-stimulating hormone (FSH) receptor gene for the ovarian response to FSH: a pharmacogenetic approach to controlled ovarian hyperstimulation. Pharmacogenet. Genom. 2005, 15:451-456.
5. Bodensteiner K.J., Clay C.M., Moeller C.L., Sawyer H.R. Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 1999, 60:381-386.
6. Brown J.B. Pituitary control of ovarian function-concepts derived from gonadotrophin therapy. Aust. N Z J. Obstet. Gynaecol. 1978, 18:46-54.
7. Campbell B.K., Souza C.J., Skinner A.J., Webb R., Baird D.T. Enhanced response of granulosa and theca cells from sheep carriers of the FecB mutation in vitro to gonadotropins and bone morphogenic protein-2, -4, and -6. Endocrinology 2006, 147:1608-1620.
8. Campbell B.K., Clinton M., Webb R. The role of anti-Mullerian hormone (AMH) during follicle development in a monovulatory species (sheep). Endocrinology 2012, 153:4533-4543.
9. Dierich A., Sairam M.R., Monaco L., Fimia G.M., Gansmuller A., LeMeur M., Sassone-Corsi P. 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, 95:13612-13617.
10. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., Matzuk M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996, 383:531-535.
11. Dragovic R.A., Ritter L.J., Schulz S.J., Amato F., Armstrong D.T., Gilchrist R.B. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 2005, 146:2798-2806.
12. Dube J.L., Wang P., Elvin J., Lyons K.M., Celeste A.J., Matzuk M.M. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 1998, 12:1809-1817.
13. Durlinger A.L., Gruijters M.J., Kramer P., Karels B., Kumar T.R., Matzuk M.M., Rose U.M., de Jong F.H., Uilenbroek J.T., Grootegoed J.A., Themmen A.P. Anti-Mullerian hormone attenuates the effects of FSH on follicle development in the mouse ovary. Endocrinology 2001, 142:4891-4899.
14. Durlinger A.L., Visser J.A., Themmen A.P. Regulation of ovarian function: the role of anti-Mullerian hormone. Reproduction 2002, 124:601-609.
15. Elvin J.A., Clark A.T., Wang P., Wolfman N.M., Matzuk M.M. Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol. Endocrinol. 1999, 13:1035-1048.
16. Elvin J.A., Yan C., Wang P., Nishimori K., Matzuk M.M. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 1999, 13:1018-1034.
17. Elvin J.A., Yan C., Matzuk M.M. Oocyte-expressed TGF-beta superfamily members in female fertility. Mol. Cell Endocrinol. 2000, 159:1-5.
18. Erickson G.F., Shimasaki 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.
19. Fatehi A.N., van den Hurk R., Colenbrander B., Daemen A.J., van Tol H.T., Monteiro R.M., Roelen B.A., Bevers M.M. Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 2005, 63:872-889.
20. Fenwick M.A., Mansour Y.T., Franks S., Hardy K. Identification and regulation of bone morphogenetic protein antagonists associated with preantral follicle development in the ovary. Endocrinology 2011, 152:3515-3526.
21. Galloway S.M., McNatty K.P., Cambridge L.M., Laitinen M.P., Juengel J.L., Jokiranta T.S., McLaren R.J., Luiro K., Dodds K.G., Montgomery G.W., Beattie A.E., Davis G.H., Ritvos O. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 2000, 25:279-283.
22. Gilchrist R.B., Lane M., Thompson J.G. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Human Reprod. Update. 2008, 14:159-177.
23. Glister C., Satchell L., Knight P.G. Changes in expression of bone morphogenetic proteins (BMPs), their receptors and inhibin co-receptor betaglycan during bovine antral follicle development: inhibin can antagonize the suppressive effect of BMPs on thecal androgen production. Reproduction 2010, 140:699-712.
24. Grondahl M.L., Nielsen M.E., Dal Canto M.B., Fadini R., Rasmussen I.A., Westergaard L.G., Kristensen S.G., Yding Andersen C. Anti-Mullerian hormone remains highly expressed in human cumulus cells during the final stages of folliculogenesis. Reprod. Biomed. Online 2011, 22:389-398.
25. Grossman M.P., Nakajima S.T., Fallat M.E., Siow Y. Mullerian-inhibiting substance inhibits cytochrome P450 aromatase activity in human granulosa lutein cell culture. Fertil. Steril. 2008, 89:1364-1370.
26. Hanrahan J.P., Gregan S.M., Mulsant P., Mullen M., Davis G.H., Powell R., Galloway S.M. Mutations in the genes for oocyte-derived growth factors GDF9 and BMP15 are associated with both increased ovulation rate and sterility in Cambridge and Belclare sheep (Ovis aries). Biol. Reprod. 2004, 70:900-909.
27. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 2005, 118:5257-5268.
28. Ingraham H.A., Hirokawa Y., Roberts L.M., Mellon S.H., McGee E., Nachtigal M.W., Visser J.A. Autocrine and paracrine Mullerian inhibiting substance hormone signaling in reproduction. Recent Prog. Horm. Res. 2000, 55:53-67. discussion 67-58.
29. Jaatinen R., Laitinen M.P., Vuojolainen K., Aaltonen J., Louhio H., Heikinheimo K., Lehtonen E., Ritvos O. Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and cDNA cloning of rat GDF-9 and its novel homolog GDF-9B. Mol. Cell Endocrinol. 1999, 156:189-193.
30. Jeppesen, J.V., Anderson, R.A., Kelsey, T.W., Christiansen, S.L., Kristensen, S.G., Jayaprakasan, K., Raine-Fenning, N., Campbell, B.K., Yding Andersen, C., 2013. Which follicles make the most anti-Mullerian hormone in humans? Evidence for an abrupt decline in AMH production at the time of follicle selection. Mol. Hum. Reprod. April 23 [Epub ahead of print].
31. Kaipia A., Hsueh A.J. Regulation of ovarian follicle atresia. Annu. Rev. Physiol. 1997, 59:349-363.
32. Khalaf M., Morera J., Bourret A., Reznik Y., Denoual C., Herlicoviez M., Mittre H., Benhaim A. BMP system expression in GCs from polycystic ovary syndrome women and the in vitro effects of BMP4, BMP6, and BMP7 on GC steroidogenesis. Eur. J. Endocrinol. 2013, 168:437-444.
33. Kumar T.R., Wang Y., Lu N., Matzuk M.M. Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nat. Genet. 1997, 15:201-204.
34. Laitinen M., Vuojolainen K., Jaatinen R., Ketola I., Aaltonen J., Lehtonen E., Heikinheimo M., Ritvos O. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech. Dev. 1998, 78:135-140.
35. Lee W.S., Otsuka F., Moore R.K., Shimasaki S. Effect of bone morphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol. Reprod. 2001, 65:994-999.
36. Lee W.S., Yoon S.J., Yoon T.K., Cha K.Y., Lee S.H., Shimasaki S., Lee S., Lee K.A. Effects of bone morphogenetic protein-7 (BMP-7) on primordial follicular growth in the mouse ovary. Mol. Reprod. Dev. 2004, 69:159-163.
37. Lin H.Y., Wang X.F., Ng-Eaton E., Weinberg R.A., Lodish H.F. Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase. Cell 1992, 68:775-785.
38. Macklon N.S., Fauser B.C. Follicle development during the normal menstrual cycle. Maturitas 1998, 30:181-188.
39. Massague J. TGF-beta signal transduction. Annu. Rev. Biochem. 1998, 67:753-791.
40. Massague J., Wotton D. Transcriptional control by the TGF-beta/Smad signaling system. EMBO J. 2000, 19:1745-1754.
41. Matzuk M.M., Burns K.H., Viveiros M.M., Eppig J.J. Intercellular communication in the mammalian ovary: oocytes carry the conversation. Science 2002, 296:2178-2180.
42. McGee E.A., Hsueh A.J. Initial and cyclic recruitment of ovarian follicles. Endocr. Rev. 2000, 21:200-214.
43. McGrath S.A., Esquela A.F., Lee S.J. Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 1995, 9:131-136.
44. McNatty K.P., Juengel J.L., Reader K.L., Lun S., Myllymaa S., Lawrence S.B., Western A., Meerasahib M.F., Mottershead D.G., Groome N.P., Ritvos O., Laitinen M.P. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 2005, 129:473-480.
45. McNatty K.P., Smith P., Moore L.G., Reader K., Lun S., Hanrahan J.P., Groome N.P., Laitinen M., Ritvos O., Juengel J.L. Oocyte-expressed genes affecting ovulation rate. Mol. Cell Endocrinol. 2005, 234:57-66.
46. Miyazono K., Kamiya Y., Morikawa M. Bone morphogenetic protein receptors and signal transduction. J. Biochem. 2010, 147:35-51.
47. Miyoshi T., Otsuka F., Inagaki K., Otani H., Takeda M., Suzuki J., Goto J., Ogura T., Makino H. Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly regulated kinase signaling and oocyte actions in follicle-stimulating hormone-induced estrogen production. Endocrinology 2007, 148:337-345.
48. Moore R.K., Otsuka F., Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J. Biol. Chem. 2003, 278:304-310.
49. Moustakas A., Heldin C.H. Non-Smad TGF-beta signals. J. Cell Sci. 2005, 118:3573-3584.
50. Mueller T.D., Nickel J. Promiscuity and specificity in BMP receptor activation. FEBS Lett. 2012, 586:1846-1859.
51. Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem. 2000, 275:39523-39528.
52. Otsuka F., Moore R.K., Shimasaki S. Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J. Biol. Chem. 2001, 276:32889-32895.
53. Otsuka F., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15 inhibits follicle-stimulating hormone (FSH) action by suppressing FSH receptor expression. J. Biol. Chem. 2001, 276:11387-11392.
54. Pangas S.A., Rademaker A.W., Fishman D.A., Woodruff T.K. 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, 87:2644-2657.
55. Pellatt L., Rice S., Dilaver N., Heshri A., Galea R., Brincat M., Brown K., Simpson E.R., Mason H.D. Anti-Mullerian hormone reduces follicle sensitivity to follicle-stimulating hormone in human granulosa cells. Fertil. Steril. 2011, 96(1246-1251):e1241.
56. Perez Mayorga M., Gromoll J., Behre H.M., Gassner C., Nieschlag E., Simoni M. Ovarian response to follicle-stimulating hormone (FSH) stimulation depends on the FSH receptor genotype. J. Clin. Endocrinol. Metab. 2000, 85:3365-3369.
57. Pierre A., Pisselet C., Dupont J., Bontoux M., Monget P. Bone morphogenetic protein 5 expression in the rat ovary: biological effects on granulosa cell proliferation and steroidogenesis. Biol. Reprod. 2005, 73:1102-1108.
58. Richards J.S., Russell D.L., Ochsner S., Hsieh M., Doyle K.H., Falender A.E., Lo Y.K., Sharma S.C. Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog. Horm. Res. 2002, 57:195-220.
59. Rider C.C., Mulloy B. Bone morphogenetic protein and growth differentiation factor cytokine families and their protein antagonists. Biochem. J. 2010, 429:1-12.
60. Roh J.S., Bondestam J., Mazerbourg S., Kaivo-Oja N., Groome N., Ritvos O., Hsueh A.J. Growth differentiation factor-9 stimulates inhibin production and activates Smad2 in cultured rat granulosa cells. Endocrinology 2003, 144:172-178.
61. Salmon N.A., Handyside A.H., Joyce I.M. Oocyte regulation of anti-Mullerian hormone expression in granulosa cells during ovarian follicle development in mice. Dev. Biol. 2004, 266:201-208.
62. Schipper I., de Jong F.H., Fauser B.C. Lack of correlation between maximum early follicular phase serum follicle stimulating hormone concentrations and menstrual cycle characteristics in women under the age of 35 years. Hum. Reprod. 1998, 13:1442-1448.
63. Schipper I., Hop W.C., Fauser B.C. The follicle-stimulating hormone (FSH) threshold/window concept examined by different interventions with exogenous FSH during the follicular phase of the normal menstrual cycle: duration, rather than magnitude, of FSH increase affects follicle development. J. Clin. Endocrinol. Metab. 1998, 83:1292-1298.
64. Shi J., Yoshino O., Osuga Y., Koga K., Hirota Y., Nose E., Nishii O., Yano T., Taketani Y. Bone morphogenetic protein-2 (BMP-2) increases gene expression of FSH receptor and aromatase and decreases gene expression of LH receptor and StAR in human granulosa cells. Am. J. Reprod. Immunol. 2011, 65:421-427.
65. Shimasaki S., Zachow R.J., Li D., Kim H., Iemura S., Ueno N., Sampath K., Chang R.J., Erickson G.F. A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. USA 1999, 96:7282-7287.
66. Shimasaki S., Moore R.K., Otsuka F., Erickson G.F. The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 2004, 25:72-101.
67. Silva J.R., van den Hurk R., van Tol H.T., Roelen B.A., Figueiredo J.R. Gene expression and protein localisation for activin-A, follistatin and activin receptors in goat ovaries. J. Endocrinol. 2004, 183:405-415.
68. Solloway M.J., Dudley A.T., Bikoff E.K., Lyons K.M., Hogan B.L., Robertson E.J. Mice lacking Bmp6 function. Develop. Genet. 1998, 22:321-339.
69. Spicer L.J., Aad P.Y., Allen D., Mazerbourg S., Hsueh A.J. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. J. Endocrinol. 2006, 189:329-339.
70. Su Y.Q., Sugiura K., Eppig J.J. Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin. Reprod. Med. 2009, 27:32-42.
71. van der Meer M., Hompes P.G., Scheele F., Schoute E., Veersema S., Schoemaker J. Follicle stimulating hormone (FSH) dynamics of low dose step-up ovulation induction with FSH in patients with polycystic ovary syndrome. Hum. Reprod. 1994, 9:1612-1617.
72. Van Houten E.L., Themmen A.P., Visser J.A. Anti-Müllerian hormone (AMH): regulator and marker of ovarian function. Ann. Endocrinol. (Paris) 2010, 71:191-197.
73. Visser J.A. AMH signaling: from receptor to target gene. Mol. Cell Endocrinol. 2003, 211:65-73.
74. Visser J.A., Durlinger A.L., Peters I.J., van den Heuvel E.R., Rose U.M., Kramer P., de Jong F.H., Themmen A.P. Increased oocyte degeneration and follicular atresia during the estrous cycle in anti-Mullerian hormone null mice. Endocrinology 2007, 148:2301-2308.
75. von Schalburg K.R., McCarthy S.P., Rise M.L., Hutson J.C., Davidson W.S., Koop B.F. Expression of morphogenic genes in mature ovarian and testicular tissues: potential stem-cell niche markers and patterning factors. Mol. Reprod. Dev. 2006, 73:142-152.
76. Weenen C., Laven J.S., Von Bergh A.R., Cranfield M., Groome N.P., Visser J.A., Kramer P., Fauser B.C., Themmen A.P. Anti-Mullerian hormone expression pattern in the human ovary: potential implications for initial and cyclic follicle recruitment. Mol. Hum. Reprod. 2004, 10:77-83.
77. Wilson T., Wu X.Y., Juengel J.L., Ross I.K., Lumsden J.M., Lord E.A., Dodds K.G., Walling G.A., McEwan J.C., O'Connell A.R., McNatty K.P., Montgomery G.W. Highly prolific Booroola sheep have a mutation in the intracellular kinase domain of bone morphogenetic protein IB receptor (ALK-6) that is expressed in both oocytes and granulosa cells. Biol. Reprod. 2001, 64:1225-1235.
78. Yan C., Wang P., DeMayo J., DeMayo F.J., Elvin J.A., Carino C., Prasad S.V., Skinner S.S., Dunbar B.S., Dube J.L., Celeste A.J., Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15:854-866.
79. Yi J.Y., Shin I., Arteaga C.L. Type I transforming growth factor beta receptor binds to and activates phosphatidylinositol 3-kinase. J. Biol. Chem. 2005, 280:10870-10876.