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Submitted on January 22, 2007
Accepted on June 21, 2007
Department of Applied Animal Science, Graduate School of Biosphere Science, Hiroshima University, 1-4-4 Kagamiyama, Higashi-Hiroshima, 739-8528, Japan; Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030; Department of Internal Medicine, University of Texas Medical Branch, Galveston, TX, 77555; Department of Neurosciences, University of New Mexico Health Sciences Center, Albuquerque, NM, 87131
* To whom correspondence should be addressed. E-mail: mashimad{at}hiroshima-u.ac.jp.
During ovulation, granulosa cells and cumulus cells synthesize and secrete a wide variety of factors including members of the Interleukin (IL) cytokine family via the process of exocytosis. Exocytosis is controlled by the SNARE complex consisting of proteins residing in the vesicle membrane and the plasma membrane. One of the SNARE proteins, SNAP25, is expressed abundantly in neuronal cells and is also induced transiently in the rat ovary in response to LH. Therefore, we sought to determine the molecular mechanisms controlling ovarian expression of the Snap25 gene, and the role of SNAP25 in exocytosis of secreted factors, such as ILs from cumulus cells and granulosa cells. In preovulatory (PO) follicles of eCG-primed mice, expression of Snap25 mRNA was neglible but was induced markedly 8hr post-hCG stimulation. In Pgr null mice Snap25 mRNA and protein levels were significantly lower at 8 hr post-hCG compared to wild type mice. To analyze the molecular mechanisms by which PGR regulates this gene, a 1517 bp murine Snap25 promoter-luciferase reporter construct was generated and transfected into granulosa cell cultures. Three SP1/SP3 sites but not consensus AP1 or CRE sites were essential for basal and Forskolin/PMA-induced promoter activity in granulosa cells. The induction was significantly suppressed by PGR antagonist, RU486. Treatment of cumulus oocyte complexes (COCs) or granulosa ceslls with FSH/Amphiregulin, LH or Forskolin/PMA induced elevated expression of Snap25 mRNA and increased the secretion of 8 cytokine and chemokine factors. Transfection of granulosa cells with Snap25 siRNA significantly reduced the levels of both SNAP25 protein and the secretion of cytokines. From these results, we conclude that progesterone-PGR-mediated SNAP25 expression in COCs and granulosa cells regulates cytokine and chemokine secretion via an exocytosis system.
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