Expression of growth-differentiating factor 9 and its type 1 receptor in human ovaries

Reproductive BioMedicine Online

Volumn 21, Issue 1, 2010, Pages 109-117

  Oron, Galia ^a,b   Fisch, Benjamin ^a,b   Ao, Asangla ^c,d   Zhang, Xiao Yun ^c   Farhi, Jacob ^a,b   Haroush, Avi Ben ^a,b   Kesseler Icekson, Gania ^a,b   Abir, Ronit ^a,b  

^a RABIN MEDICAL CENTER   (Israel)

^b TEL AVIV UNIVERSITY   (Israel)

^c ROYAL VICTORIA HOSPITAL   (Canada)

^d MCGILL UNIVERSITY   (Canada)

Author keywords

GDF9; human ovaries; immunohistochemistry; in situ hybridization; reverse transcription polymerase chain reaction; TGF R1

Indexed keywords

GROWTH DIFFERENTIATION FACTOR 9; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1;

ADOLESCENT; ADULT; ARTICLE; CHILD; CONTROLLED STUDY; FEMALE; FEMALE FERTILITY; FETUS; GENETIC TRANSCRIPTION; GESTATIONAL AGE; GRANULOSA CELL; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; NUCLEOTIDE SEQUENCE; OOCYTE; OVARY; OVARY FOLLICLE; PRESCHOOL CHILD; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHOOL CHILD;

ADOLESCENT; ADULT; CHILD; CHILD, PRESCHOOL; FEMALE; FETUS; GRANULOSA CELLS; GROWTH DIFFERENTIATION FACTOR 9; HUMANS; OOCYTES; OVARY; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RNA, MESSENGER;

EID: 78650126137     PISSN: 14726483     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.rbmo.2010.03.011     Document Type: Article

References (39)

1. J. Aaltonen, M.P. Laitinen, K. Vuojolainen, R. Jaatinen, N. Horelli-Kuitunen, and L. Seppa Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis J. Clin. Endocrinol. Metab. 84 1999 2744 2750 (Pubitemid 30642005)
2. R. Abir, A. Ben-Haroush, C. Felz, E. Okon, H. Raanani, and R. Orvieto Selection of patients before and after anticancer treatment for ovarian cryopreservation Hum. Reprod. 23 2008 869 877
3. R. Abir, A. Ben-Haroush, N. Melamed, C. Felz, S. Nitke, and H. Krissi The expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB and II in human ovaries from fetuses and adults Fertil. Steril. 89 2008 1430 1433
4. R. Abir, B. Fisch, X.Y. Zhang, C. Felz, G. Kassler-Icekson, and H. Krissi Keratinocyte growth factor and its receptor in human ovaries from fetuses, girls and women Mol. Hum. Reprod. 15 2009 69 75
5. R. Abir, B. Fisch, S. Jin, M. Barnett, A. Ben Haroush, C. Felz, G. Kessler-Icekson, D. Feldberg, S. Nitke, and A. Ao Presence of NGF and its receptors in ovaries from human fetuses and adults Mol. Hum. Reprod. 11 2005 229 236 (Pubitemid 40662807)
6. R. Abir, S. Nitke, A. Ben-Haroush, and B. Fisch In vitro maturation of human primordial ovarian follicles - clinical significance, progress and methods for growth evaluation Histol. Histopathol. 21 2006 887 898 (Pubitemid 44082731)
7. K.J. Bodensteiner, C.M. Clay, C.L. Moeller, and H.R. Sawyer Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries Biol. Reprod. 60 1999 381 386 (Pubitemid 29063880)
8. S. Cheifetz, H. Hernandez, M. Laiho, P. ten Dijke, K.K. Iwata, and J. Massagué Distinct transforming growth factor-beta (TGF-beta) receptor subsets as determinants of cellular responsiveness to three TGF-beta isoforms J. Biol. Chem. 265 1990 20533 20538 (Pubitemid 120014040)
9. S. Cheifetz, J.A. Weatherbee, M.L. Tsang, J.K. Anderson, J.E. Mole, and R. Lucas The transforming growth factor-beta system, a complex pattern of cross-reactive ligands and receptors Cell 48 1987 409 415
10. J. Dong, D.F. Albertini, K. Nishimori, T.R. Kumar, N. Lu, and M.M. Matzuk Growth differentiation factor-9 is required during early ovarian folliculogenesis Nature 383 1996 531 535 (Pubitemid 26346180)
11. D.C. Eckery, L.J. Whale, S.B. Lawrence, K.A. Wylde, K.P. McNatty, and J.L. Juengel Expression of mRNA encoding growth differentiation factor 9 and bone morphogenetic protein 15 during follicular formation and growth marsupial, the brushtail possum (Trichosurus vulpecula) Mol. Cell. Endocrinol. 192 2002 115 126 (Pubitemid 34667230)
12. E. Feigin, E. Freud, B. Fisch, R. Orvieto, D. Kravarusic, G. Avrahami, and R. Abir Fertility preservation in female adolescents with malignancies M.T. Moorland, Cancer in Female Adolescents 2008 Nova Science Publishers, Inc. Hauppauge, NY, USA 103 138 (Chapter 3)
13. R.G. Gosden Oocyte development throughout life J.G. Grudzinshes, J.L. Yovici, Gametes - The Oocyte 1995 Cambridge University Press Cambridge, UK 119 149
14. A. Gougeon Regulations of ovarian follicular development in primates: facts and hypotheses Endocrinol. Rev. 17 1996 121 154
15. S. Harel, S. Jin, B. Fisch, D. Feldberg, H. Krissi, S. Freimann, S.L. Tan, A. Ao, and R. Abir Tyrosine kinase B receptor and its activated neurotrophins in ovaries from human fetuses and adults Mol. Hum. Reprod. 12 2006 357 365 (Pubitemid 43985606)
16. M. Hayashi, E.A. McGee, G. Min, C. Klein, U.M. Rose, and M. van Duin Recombinant growth differentiation factor-9 (GDF-9) enhances growth and differentiation of cultured early ovarian follicles Endocrinology 140 1999 1236 1244 (Pubitemid 29104226)
17. J.G. Hreinsson, J.E. Scott, C. Rasmussen, M.L. Swahn, J. Hsueh, and O. Hovatta Growth differentiation factor-9 promotes the growth, development, and survival of human ovarian follicles in organ culture J. Clin. Endocrinol. Metab. 87 2002 316 321 (Pubitemid 34084708)
18. R. Jaatinen, M.P. Laitinen, K. Vuojolainen, J. Aaltonen, H. Louhio, and K. Heikinheimo Localization of growth differentiation factor-9 (GDF-9) mRNA and protein in rat ovaries and c DNA cloning of rat GDF-9 and its novel homolog GDF-9B Mol. Cell. Endocrinol. 156 1999 189 193 (Pubitemid 29460758)
19. M. Laitinen, K. Vuojolainen, R. Jaatinen, I. Ketola, J. Aaltonen, and E. Lehtonen A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis Mech. Dev. 78 1998 135 140 (Pubitemid 28566220)
20. G. Liu, F. Shi, U. Blas-Machado, R. Yu, V.L. Davis, and W.G. Foster Dietary galactose inhibits GDF-9 mediated follicular development in the rat ovary Reprod. Toxicol. 21 2006 26 33 (Pubitemid 43050922)
21. S. Margulis, R. Abir, C. Felz, S. Nitke, H. Krissi, and B. Fisch Bone morphogenetic protein 15 expression in human ovaries from fetuses, girls and women Fertil. Steril. 92 2009 1666 1673
22. F.S. Martins, J.J.H. Celestino, M.V.A. Saraiva, M.H.T. Matos, J.B. Bruno, and C. Rocha-Junior Growth and differentiation factor-9 stimulates activation of goat primordial follicles and their progression to secondary follicles Reprod. Fertil. Dev. 20 2008 916 924
23. S. Mazebourg, C. Klein, J. Roh, N. Kaivo-Oja, D.G. Mottershead, and O. Korchynskyi Growth differentiation factor-9 signaling is mediated by the type I receptor, activin receptor-like kinase 5 Mol. Endocrinol. 18 2004 653 665 (Pubitemid 38328209)
24. S.A. McGrath, A.F. Esquela, and S.J. Lee Oocyte-specific expression of growth/differentiation factor-9 Mol. Endocrinol. 9 1995 131 136
25. A.C. McPherron, and S.J. Lee GDF-3 and GDF-9: two new members of the transforming growth factor-β superfamily containing a novel pattern of cysteines J. Biol. Chem. 268 1993 3444 3449 (Pubitemid 23070981)
26. L. Mery, A. Lefevre, M. Benchaib, B. Demirci, B. Salle, and J.-F. Guerin Follicular growth in vitro: detection of growth differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) during in vitro culture of ovine cortical slices Mol. Reprod. Dev. 74 2007 767 774 (Pubitemid 46676840)
27. M. Orisaka, S. Orisaka, J.Y. Jiang, J. Vraig, Y. Wang, and F. Kotsuji Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage Mol. Endocrinol. 20 2006 2456 2468 (Pubitemid 44496414)
28. T. Ota, K.B. Choi, B.C. Gilks, P.C.K. Leung, and N. Auersperg Cell type- and stage-specific changes in HOXA7 protein expression in human ovarian folliculogenesis: possible role of GDF-9 Differentiation 74 2006 1 10
29. H. Pinkas, B. Fisch, G. Rozansky, C. Felz, G. Kessler-Icekson, and H. Krissi Expression of PDGF-A and -B and their receptors in human fetal and adult ovaries Mol. Hum. Reprod. 14 2008 199 206 (Pubitemid 351627289)
30. J.C. Sadeu, and J. Smitz Growth differentiation factor-9 and anti-Mullerian hormone expression in cultured human follicles from frozen-thawed ovarian tissue Reprod. Biomed. Online 17 2008 537 548
31. J.C. Sadeu, T. Adriaenssens, and J. Smitz Expression of growth differentiation factor 9 (GDF-9), bone morphogenetic protein 15 (BMP-15) and anti-mullerian hormone (AMH) in cultured mouse primary follicles Reproduction 136 2008 195 203
32. B. Schilling, and J. Yeh Expression of transforming growth factor (TGF)-β1, TGF-β2, and TGF-β3 and of the type I and II TGF-β receptors during the development of the human fetal ovary Fertil. Steril. 72 1999 147 153 (Pubitemid 29300277)
33. S. Shimasaki, R.J. Zachow, D. Li, H. Kim, S. Iemura, and N. Ueno A functional bone morphogenetic protein system in the ovary Proc. Natl. Acad. Sci. USA 96 1996 7282 7287
34. T. Shimizu, Y. Miyahayashi, M. Yokoo, Y. Hoshino, H. Sasada, and E. Sato Molecular cloning of porcine growth differentiation factor 9 (GDF-9) cDNA and its role in early folliculogenesis: direct ovarian injection of GDF-9 gene fragments promotes early folliculogenesis Reproduction 128 2004 537 543 (Pubitemid 40124284)
35. J.R.V. Silva, R. Van Den Hurk, H.T.A. Van Tol, B.A.J. Roelen, and J.R. Figueiredo Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats Mol. Reprod. Dev. 70 2004 11 19
36. F.L. Teixeira Filho, E.C. Baracat, T.H. Lee, C.S. Suh, M. Matsui, and R.J. Chang Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome J. Clin. Endocrinol. Metab. 87 2002 1337 1344 (Pubitemid 36121106)
37. D. Tomic, S.G. Brodie, C. Deng, R.J. Hickey, J.K. Babus, and L.H. Malkas Smad 3 may regulate follicular growth in the mouse ovary Biol. Reprod. 66 2002 917 923 (Pubitemid 34263110)
38. U.A. Vitt, E.A. McGee, M. Hayashi, and A.J. Hsueh In vivo treatment with GDF-9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats Endocrinology 141 2000 3814 3820
39. U.A. Vitt, M. Hayashi, C. Klein, and A.J. Hsueh Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles Biol. Reprod. 62 2000 370 377 (Pubitemid 30067338)