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Department of Pathology (J.A.E., C.Y., P.W., M.M.M.) Department
of Molecular and Human Genetics (J.A.E., M.M.M.), and Department of
Cell Biology (M.M.M.) Baylor College of Medicine Houston, Texas
77030
Department of Applied Biochemistry (K.N.) Tohoku
University Sendai, Miyagi, Japan 981-8555
Growth differentiation factor-9 (GDF-9), a
secreted member of the transforming growth factor-ß superfamily, is
expressed at high levels in the mammalian oocyte beginning at the type
3a primary follicle stage. We have previously demonstrated that
GDF-9-deficient female mice are infertile because of an early block in
folliculogenesis at the type 3b primary follicle stage. To address the
molecular defects that result from the absence of GDF-9, we have
analyzed the expression of several important ovarian marker genes. The
major findings of our studies are as follows: 1) There are no
detectable signals around GDF-9-deficient follicles for several theca
cell layer markers [i.e. 17
-hydroxylase, LH receptor
(LHR), and c-kit, the receptor for kit ligand]. This
demonstrates that in the absence of GDF-9, the follicles are
incompetent to emit a signal that recruits theca cell precursors to
surround the follicle; 2) The primary follicles of GDF-9-deficient mice
demonstrate an up-regulation of kit ligand and inhibin-. This
suggests that these two important secreted growth factors, expressed in
the granulosa cells, may be directly regulated in a paracrine fashion
by GDF-9. Up-regulation of kit ligand, via signaling through
c-kit on the oocyte, may be directly involved in the
increased size of GDF-9-deficient oocytes and the eventual demise of
the oocyte; 3) After loss of the oocyte, the cells of the
GDF-9-deficient follicles remain in a steroidogenic cluster that
histologically resembles small corpora lutea. However, at the molecular
level, these cells are positive for both luteal markers
(e.g. LHR and P-450 side chain cleavage) and nonluteal
markers (e.g. inhibin and P-450 aromatase). This
demonstrates that initially the presence of the oocyte prevents the
expression of luteinized markers, but that the absence of GDF-9 at an
early timepoint alters the differentiation program of the granulosa
cells; and 4) As demonstrated by staining with either proliferating
cell nuclear antigen (PCNA) or Ki-67 and TUNEL
(terminal deoxynucleotidyl transferase-mediated dUTP nick end labeling)
labeling, the granulosa cells of GDF-9-deficient type 3b primary
follicles fail to proliferate but also fail to undergo cell death. This
suggests that granulosa cells of type 3b follicles require GDF-9 for
continued growth and also to become competent to undergo apoptosis,
possibly through a differentiation event. Thus, these studies have
enlightened us as to the paracrine roles of GDF-9 as well as the normal
steps of granulosa cell and theca cell growth and differentiation
within ovarian follicles.
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X. Wu, L. Chen, C. A. Brown, C. Yan, and M. M. Matzuk Interrelationship of Growth Differentiation Factor 9 and Inhibin in Early Folliculogenesis and Ovarian Tumorigenesis in Mice Mol. Endocrinol., June 1, 2004; 18(6): 1509 - 1519. [Abstract] [Full Text] [PDF]
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M Myers, K L Britt, N G M Wreford, F J P Ebling, and J B Kerr Methods for quantifying follicular numbers within the mouse ovary Reproduction, May 1, 2004; 127(5): 569 - 580. [Abstract] [Full Text] [PDF]
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L. Liu, S. Franco, B. Spyropoulos, P. B. Moens, M. A. Blasco, and D. L. Keefe Irregular telomeres impair meiotic synapsis and recombination in mice PNAS, April 27, 2004; 101(17): 6496 - 6501. [Abstract] [Full Text] [PDF]
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W. X. Liao, R. K. Moore, and S. Shimasaki Functional and Molecular Characterization of Naturally Occurring Mutations in the Oocyte-secreted Factors Bone Morphogenetic Protein-15 and Growth and Differentiation Factor-9 J. Biol. Chem., April 23, 2004; 279(17): 17391 - 17396. [Abstract] [Full Text] [PDF]
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K. H. Burns, G. E. Owens, S. C. Ogbonna, J. H. Nilson, and M. M. Matzuk Expression Profiling Analyses of Gonadotropin Responses and Tumor Development in the Absence of Inhibins Endocrinology, October 1, 2003; 144(10): 4492 - 4507. [Abstract] [Full Text] [PDF]
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M. Hsieh, S. M. Mulders, R. R. Friis, A. Dharmarajan, and J. S. Richards Expression and Localization of Secreted Frizzled-Related Protein-4 in the Rodent Ovary: Evidence for Selective Up-Regulation in Luteinized Granulosa Cells Endocrinology, October 1, 2003; 144(10): 4597 - 4606. [Abstract] [Full Text] [PDF]
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Y. Yang, A. Balla, N. Danilovich, and M. R. Sairam Developmental and Molecular Aberrations Associated with Deterioration of Oogenesis During Complete or Partial Follicle-Stimulating Hormone Receptor Deficiency in Mice Biol Reprod, October 1, 2003; 69(4): 1294 - 1302. [Abstract] [Full Text] [PDF]
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K. L. Loveland, M. Bakker, T. Meehan, E. Christy, V. von Schonfeldt, A. Drummond, and D. de Kretser Expression of Bambi Is Widespread in Juvenile and Adult Rat Tissues and Is Regulated in Male Germ Cells Endocrinology, September 1, 2003; 144(9): 4180 - 4186. [Abstract] [Full Text] [PDF]
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X. Wu, P. Wang, C. A. Brown, C. A. Zilinski, and M. M. Matzuk Zygote Arrest 1 (Zar1) Is an Evolutionarily Conserved Gene Expressed in Vertebrate Ovaries Biol Reprod, September 1, 2003; 69(3): 861 - 867. [Abstract] [Full Text] [PDF]
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D. M. Duffy Growth Differentiation Factor-9 Is Expressed by the Primate Follicle Throughout the Periovulatory Interval Biol Reprod, August 1, 2003; 69(2): 725 - 732. [Abstract] [Full Text] [PDF]
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 D. H. Castrillon, L. Miao, R. Kollipara, J. W. Horner, and R. A. DePinho Suppression of Ovarian Follicle Activation in Mice by the Transcription Factor Foxo3a Science, July 11, 2003; 301(5630): 215 - 218. [Abstract] [Full Text] [PDF]
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J. F. Couse, M. M. Yates, V. R. Walker, and K. S. Korach Characterization of the Hypothalamic-Pituitary-Gonadal Axis in Estrogen Receptor (ER) Null Mice Reveals Hypergonadism and Endocrine Sex Reversal in Females Lacking ER{alpha} But Not ER{beta} Mol. Endocrinol., June 1, 2003; 17(6): 1039 - 1053. [Abstract] [Full Text] [PDF]
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C. M. Milner and A. J. Day TSG-6: a multifunctional protein associated with inflammation J. Cell Sci., May 15, 2003; 116(10): 1863 - 1873. [Abstract] [Full Text] [PDF]
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C. R. Harlow, M. Rae, L. Davidson, P. C. Trackman, and S. G. Hillier 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, January 1, 2003; 144(1): 154 - 162. [Abstract] [Full Text] [PDF]
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J.-S. Roh, J. Bondestam, S. Mazerbourg, N. Kaivo-Oja, N. Groome, O. Ritvos, and A. J. W. Hsueh Growth Differentiation Factor-9 Stimulates Inhibin Production and Activates Smad2 in Cultured Rat Granulosa Cells Endocrinology, January 1, 2003; 144(1): 172 - 178. [Abstract] [Full Text] [PDF]
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H. Chang, C. W. Brown, and M. M. Matzuk Genetic Analysis of the Mammalian Transforming Growth Factor-{beta} Superfamily Endocr. Rev., December 1, 2002; 23(6): 787 - 823. [Abstract] [Full Text] [PDF]
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A. Bachelot, P. Monget, P. Imbert-Bollore, K. Coshigano, J. J. Kopchick, P. A. Kelly, and N. Binart Growth Hormone Is Required for Ovarian Follicular Growth Endocrinology, October 1, 2002; 143(10): 4104 - 4112. [Abstract] [Full Text] [PDF]
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C. R. Harlow, L. Davidson, K. H. Burns, C. Yan, M. M. Matzuk, and S. G. Hillier FSH and TGF-{beta} Superfamily Members Regulate Granulosa Cell Connective Tissue Growth Factor Gene Expression in Vitro and in Vivo Endocrinology, September 1, 2002; 143(9): 3316 - 3325. [Abstract] [Full Text] [PDF]
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K. H. Burns, G. E. Owens, J. M. Fernandez, J. H. Nilson, and M. M. Matzuk Characterization of Integrin Expression in the Mouse Ovary Biol Reprod, September 1, 2002; 67(3): 743 - 751. [Abstract] [Full Text] [PDF]
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E. E. Nilsson and M. K. Skinner Growth and Differentiation Factor-9 Stimulates Progression of Early Primary but Not Primordial Rat Ovarian Follicle Development Biol Reprod, September 1, 2002; 67(3): 1018 - 1024. [Abstract] [Full Text] [PDF]
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S. Varani, J. A. Elvin, C. Yan, J. DeMayo, F. J. DeMayo, H. F. Horton, M. C. Byrne, and M. M. Matzuk Knockout of Pentraxin 3, a Downstream Target of Growth Differentiation Factor-9, Causes Female Subfertility Mol. Endocrinol., June 1, 2002; 16(6): 1154 - 1167. [Abstract] [Full Text] [PDF]
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M. Hsieh, M. A. Johnson, N. M. Greenberg, and J. S. Richards Regulated Expression of Wnts and Frizzleds at Specific Stages of Follicular Development in the Rodent Ovary Endocrinology, March 1, 2002; 143(3): 898 - 908. [Abstract] [Full Text] [PDF]
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F. L. Teixeira Filho, E. C. Baracat, T. H. Lee, C. S. Suh, M. Matsui, R. J. Chang, S. Shimasaki, and G. F. Erickson Aberrant Expression of Growth Differentiation Factor-9 in Oocytes of Women with Polycystic Ovary Syndrome J. Clin. Endocrinol. Metab., March 1, 2002; 87(3): 1337 - 1344. [Abstract] [Full Text] [PDF]
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A. L. L. Durlinger, M. J. G. Gruijters, P. Kramer, B. Karels, H. A. Ingraham, M. W. Nachtigal, J. Th. J. Uilenbroek, J. A. Grootegoed, and A. P. N. Themmen Anti-Mullerian Hormone Inhibits Initiation of Primordial Follicle Growth in the Mouse Ovary Endocrinology, March 1, 2002; 143(3): 1076 - 1084. [Abstract] [Full Text] [PDF]
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J. J. Eppig, K. Wigglesworth, and F. L. Pendola The mammalian oocyte orchestrates the rate of ovarian follicular development PNAS, February 20, 2002; (2002) 52658699. [Abstract] [Full Text] [PDF]
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T. El-Hefnawy and A. J. Zeleznik Synergism Between FSH and Activin in the Regulation of Proliferating Cell Nuclear Antigen (PCNA) and Cyclin D2 Expression in Rat Granulosa Cells Endocrinology, October 1, 2001; 142(10): 4357 - 4362. [Abstract] [Full Text] [PDF]
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K. H. Burns, C. Yan, T. R. Kumar, and M. M. Matzuk Analysis of Ovarian Gene Expression in Follicle-Stimulating Hormone {beta} Knockout Mice Endocrinology, July 1, 2001; 142(7): 2742 - 2751. [Abstract] [Full Text] [PDF]
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I. M. Joyce, F. L. Pendola, M. O'Brien, and J. J. Eppig Regulation of Prostaglandin-Endoperoxide Synthase 2 Messenger Ribonucleic Acid Expression in Mouse Granulosa Cells during Ovulation Endocrinology, July 1, 2001; 142(7): 3187 - 3197. [Abstract] [Full Text] [PDF]
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S. E. Yi, P. S. LaPolt, B. S. Yoon, J. Y.-C. Chen, J. K. H. Lu, and K. M. Lyons The type I BMP receptor BmprIB is essential for female reproductive function PNAS, June 12, 2001; (2001) 141002798. [Abstract] [Full Text] [PDF]
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