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Abstract
In the mammalian ovary, the hyaluronan (HA)-rich cumulus extracellular matrix (ECM) organized during the gonadotropin-induced process of oocyte maturation is essential for ovulation of the oocyte-cumulus complex (OCC) and fertilization. Versican is an HA-binding proteoglycan that regulates cell function and ECM assembly. Versican cleavage and function remain to be determined in ovarian follicle. We investigated versican expression in porcine ovarian follicles by real-time (RT)-PCR and western blotting. The aims of the present work were to determine whether 1) versican was produced and cleaved by porcine OCCs during gonadotropin stimulation; 2) these processes were autonomous or required the participation of mural granulosa cells (MGCs); and 3) versican cleavage was involved in the formation or degradation of expanded cumulus ECM. We demonstrate two cleavage products of G1 domain of versican (V1) accumulated in the HA-rich cumulus ECM. One of them, a G1-DPEAAE N-terminal fragment (VG1) of ~70 kDa, was generated from V1 during organization of HA in in vivo and in vitro expanded porcine OCCs. Second, the V1-cleaved DPEAAE-positive form of ~65 kDa was the only species detected in MGCs. No versican cleavage products were detected in OCCs cultured without follicular fluid. In summary, porcine OCCs are autonomous in producing and cleaving V1; the cleaved fragment of ~70 kDa VG1 is specific for formation of the expanded cumulus HA-rich ECM.
Highlights
IntroductionGrowth and development of the ovarian follicles requires a coordinated series of events controlled by circulating gonadotropins (follicle-stimulating hormone, FSH, and luteinizing hormone, LH) and locally produced growth factors leading to somatic cell proliferation, oocyte development, and steroidogenesis [1]
In mammals, growth and development of the ovarian follicles requires a coordinated series of events controlled by circulating gonadotropins and locally produced growth factors leading to somatic cell proliferation, oocyte development, and steroidogenesis [1]
In order to detect both core protein fragments (~220 and ~70 kDa for V0 and Versican 1 (V1), respectively), the oocyte-cumulus complex (OCC) expanded in vivo were isolated from naturally cycling gilts and treated with chondroitinase ABC (ChABC)
Summary
Growth and development of the ovarian follicles requires a coordinated series of events controlled by circulating gonadotropins (follicle-stimulating hormone, FSH, and luteinizing hormone, LH) and locally produced growth factors leading to somatic cell proliferation, oocyte development, and steroidogenesis [1]. The cumulus matrix newly organized in oocyte-cumulus complex (OCC) is essential for successful ovulation and fertilization [2,3] This expanded cumulus extracellular matrix (ECM) is formed by interaction of high molecular weight hyaluronan (HA) and at least three proteins: the serum-derived inter-alpha-trypsin inhibitor (IαI), and two factors produced by cumulus cells, tumor necrosis factor-alpha-induced protein 6 (TNFAIP6) and pentraxin 3 (PTX3) [4,5,6]. Deletion of these corresponding genes in mice produces female infertility due to disorganization of the oocyte-cumulus ECM [3]. It has been proposed that complexes of HC (of IαI)-HA play a central role in matrix organization because they serve as docking sites for the attachment of other proteins to support matrix stabilization [24]
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