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Molecular Endocrinology 16 (6): 1154-1167
Copyright © 2002 by The Endocrine Society

Knockout of Pentraxin 3, a Downstream Target of Growth Differentiation Factor-9, Causes Female Subfertility

Simona Varani, Julia A. Elvin, Changning Yan, Janet DeMayo, Francesco J. DeMayo, Heidi F. Horton, Michael C. Byrne and Martin M. Matzuk

Department of Pathology (S.V., J.A.E., C.Y., M.M.M.), Department of Molecular and Cellular Biology (J.D., F.J.D., M.M.M.), Department of Molecular and Human Genetics (M.M.M.), Baylor College of Medicine, Houston, Texas 77030; and Wyeth Research (H.F.H., M.C.B.), Cambridge, Massachusetts 02140

Address all correspondence and requests for reprints to: Martin M. Matzuk, M.D., Ph.D., The Stuart A. Wallace Chair and Professor, Department of Pathology, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77030. E-mail: mmatzuk{at}bcm.tmc.edu.

The ovulatory process is tightly regulated by endocrine as well as paracrine factors. In the periovulatory period, extensive remodeling of the follicle wall occurs to allow the extrusion of the oocyte and accompanying cumulus granulosa cells. Growth differentiation factor-9 (GDF-9) and bone morphogenetic protein-15 (BMP-15) are secreted members of the TGFß superfamily that are expressed beginning in the oocyte of small primary follicles and through ovulation. Besides its critical role as a growth and differentiation factor during early folliculogenesis, GDF-9 also acts as a paracrine factor to regulate several key events in preovulatory follicles. By analyzing GDF-9-regulated expression profiles using gene chip technology, we identified TNF-induced protein 6 (Tnfip6) and pentraxin 3 (Ptx3 or PTX3) as novel factors induced by GDF-9 in granulosa cells of preovulatory follicles. Whereas Tnfip6 is induced in all granulosa cells by the LH surge, Ptx3 expression in the ovary is specifically observed after the LH surge in the cumulus granulosa cells adjacent to the oocyte. PTX3 is a member of the pentraxin family of secreted proteins, induced in several tissues by inflammatory signals. To define PTX3 function during ovulation, we generated knockout mice lacking the Ptx3 gene. Homozygous null (Ptx3-/-) mice develop normally and do not show any gross abnormalities. Whereas Ptx3-/- males are fertile, Ptx3-/- females are subfertile due to defects in the integrity of the cumulus cell-oocyte complex that are reminiscent of Bmp15-/-Gdf9+/- double mutant and BMP type IB receptor mutant mice. These studies demonstrate that PTX3 plays important roles in cumulus cell-oocyte interaction in the periovulatory period as a downstream protein in the GDF-9 signal transduction cascade.




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