Cumulus oophorus as a sperm sequestering device, in vivo

Bedford, J. M.; Kim, H. H.

doi:10.1002/jez.1402650314

Cited by 67 publications

(47 citation statements)

References 40 publications

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“…HA oligosaccharides with 8 or more monosaccharide units were potent acceptors in the HC transfer reaction (Fig. 1B, lanes [5][6][7][8]. In these reactions, the size of the I␣I-reactive bands at the HC level increased with the size of the HA oligosaccharide, indicating that the HCs were actually transferred onto the oligosaccharides.…”

Section: Tnfip6-mediated Hcs Transfer From I␣i and P␣i To Hamentioning

confidence: 88%

“…This matrix is involved in the expulsion of the COC from the follicle (2), enhances the pickup and transport of the COC by the oviduct (3,4), and influences sperm penetration and oocyte fertilization (5)(6)(7). The cellular events of matrix formation, which include the synthesis and organization of hyaluronan (HA) around the cumulus cells, have been studied extensively in mouse COCs both in vivo and in vitro (8).…”

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confidence: 99%

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Specificity of the Tumor Necrosis Factor-induced Protein 6-mediated Heavy Chain Transfer from Inter-α-trypsin Inhibitor to Hyaluronan

Mukhopadhyay

Asari

Rugg

et al. 2004

Journal of Biological Chemistry

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The formation of the hyaluronan-rich cumulus extracellular matrix is crucial for female fertility and accompanied by a transesterification reaction in which the heavy chains (HCs) of inter-␣-trypsin inhibitor (I␣I)-related proteins are covalently transferred to hyaluronan. Tumor necrosis factor-induced protein-6 (TNFIP6) is essential for this transfer reaction. Female mice deficient in TNFIP6 are infertile due to the lack of a correctly formed cumulus matrix. In this report, we characterize the specificity of TNFIP6-mediated HC transfer from I␣I to hyaluronan. Hyaluronan oligosaccharides with eight or more monosaccharide units are potent acceptors in the HC transfer, with longer oligosaccharides being somewhat more efficient. Epimerization of the N-acetylglucosamine residues to N-acetyl-galactosamines (i.e. in chondroitin) still allows the HC transfer although at a significantly lower efficiency. Sulfation of the N-acetylgalactosamines in dermatan-4-sulfate or chondroitin-6-sulfate prevents the HC transfer. Hyaluronan oligosaccharides disperse cumulus cells from expanding cumulus cell-oocyte complexes with the same size specificity as their HC acceptor specificity. This process is accompanied by the loss of hyaluronan-linked HCs from the cumulus matrix and the appearance of oligosaccharidelinked HCs in the culture medium. Chondroitin interferes with the expansion of cumulus cell-oocyte complexes only when added with exogenous TNFIP6 before endogenous hyaluronan synthesis starts, supporting that chondroitin is a weaker HC acceptor than hyaluronan. Our data indicate that TNFIP6-mediated HC transfer to hyaluronan is a prerequisite for the correct cumulus matrix assembly and hyaluronan oligosaccharides and chondroitin interfere with this assembly by capturing the HCs of the I␣I-related proteins.In response to the luteinizing hormone (LH) 1 surge, the cumulus cell-oocyte complex (COC) in the preovulatory follicle undergoes immense changes, which results in the formation of an expanded extracellular matrix (1). This matrix is involved in the expulsion of the COC from the follicle (2), enhances the pickup and transport of the COC by the oviduct (3, 4), and influences sperm penetration and oocyte fertilization (5-7). The cellular events of matrix formation, which include the synthesis and organization of hyaluronan (HA) around the cumulus cells, have been studied extensively in mouse COCs both in vivo and in vitro (8). After the LH surge, COCs quickly upregulate the expression of hyaluronan synthase 2, the enzyme required to produce hyaluronan (9). Although the mediators that induce hyaluronan synthesis in the COCs in vivo have yet to be determined, prostaglandin E 2 , follicular stimulating hormone and epidermal growth factor are potent initiators of hyaluronan production in vitro (10 -13). Hyaluronan synthesis is also under the control of the oocyte (14, 15), and growth differentiation factor-9 and bone morphogenic protein 15 are the most likely oocyte-derived growth factors involved in this regulation (16,17).Several...

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Section: Tnfip6-mediated Hcs Transfer From I␣i and P␣i To Hamentioning

confidence: 88%

mentioning

confidence: 99%

Specificity of the Tumor Necrosis Factor-induced Protein 6-mediated Heavy Chain Transfer from Inter-α-trypsin Inhibitor to Hyaluronan

Mukhopadhyay

Asari

Rugg

et al. 2004

Journal of Biological Chemistry

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“…Sperm are required to move through the extracellular matrix of the cumulus oophorus to achieve successful fertilization. It has been suggested that the cumulus oophorus attracts sperm via chemotaxis [54] and directs the few sperm that reach the ampulla to the immediate vicinity of the oocyte [55]. Thus, the cumulus oophorus has an important role in controlling the number of sperm that interact with the Zp.…”

Section: Discussionmentioning

confidence: 99%

Sperm competition risk generates phenotypic plasticity in ovum fertilizability

Firman

Simmons

2013

Proc. R. Soc. B.

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Theory predicts that sperm competition will generate sexual conflict that favours increased ovum defences against polyspermy. A recent study on house mice has shown that ovum resistance to fertilization coevolves in response to increased sperm fertilizing capacity. However, the capacity for the female gamete to adjust its fertilizability as a strategic response to sperm competition risk has never, to our knowledge, been studied. We sourced house mice (Mus domesticus) from natural populations that differ in the level of sperm competition and sperm fertilizing capacity, and manipulated the social experience of females during their sexual development to simulate conditions of either a future 'risk' or 'no risk' of sperm competition. Consistent with coevolutionary predictions, we found lower fertilization rates in ova produced by females from a high sperm competition population compared with ova from a low sperm competition population, indicating that these populations are divergent in the fertilizability of their ova. More importantly, females exposed to a 'risk' of sperm competition produced ova that had greater resistance to fertilization than ova produced by females reared in an environment with 'no risk'. Consequently, we show that variation in sperm competition risk during development generates phenotypic plasticity in ova fertilizability, which allows females to prepare for prevailing conditions during their reproductive life.

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“…Furthermore, it is suggested that chemoattractants originate both from mature oocytes and the surrounding cumulus cells [29[. Involvement of oocytes and their cumulus investments to divert spermatozoa towards the ova has been considered previously [30][31][32], but putative molecular mechanisms are still speculative [33]. In the pig, there is no experimental evidence of association of oocytes and sperm release.…”

Section: Discussionmentioning

confidence: 99%

Experimental Evidence for the Influence of Cumulus-Oocyte-Complexes on Sperm Release from the Porcine Oviductal Sperm Reservoir

Brüssow

Torner

Rátky³

et al. 2006

Journal of Reproduction and Development

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Abstract. In the pig, a temporal relationship is suggested between sperm release from the sperm reservoir (SR) and ovulation, but the mechanism(s) is still under discussion. In two experiments, the influence of transferred ova on the release of SR-spermatozoa at ovulation and the effect of supplementation with non-sulfated glycosaminglycan hyaluronan (HA) on embryo development and the number of accessory spermatozoa, respectively, were examined. PMSG/hCG primed ovectomized gilts that had previously received endoscopic low-dose insemination into the cranial uterine horn were used as an experimental model. After salpingectomy, tubal segments (ampulla, cranial, and caudal isthmus) were flushed and sperm numbers or respective accessory spermatozoa were counted. In Experiment 1, the distribution of the sperm population was altered in the presence of cumulus-oocyte-complexes (COCs). A higher proportion of spermatozoa was found after transfer of COCs into one oviduct in the ampulla and cranial isthmus segments compared with the controls (17.5 vs. 4.9%, p<0.05). In Experiment 2, the quality of the transferred ova and treatment influenced the presence of accessory spermatozoa. Transfer of COCs together with HA increased (p<0.05) the number of accessory spermatozoa compared with the other treatment groups and was similar to those in the "undisturbed" controls. No modifications were obtained regarding mean blastomere numbers (2.6 ± 0.2 to 3.1 ± 0.2). In summary, this study was demonstrated that cumulus-oocyte-complexes may be involved in triggering sperm release from the pig oviductal SR and that HA might be related to sperm release.

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Cumulus oophorus as a sperm sequestering device, in vivo

Cited by 67 publications

References 40 publications

Specificity of the Tumor Necrosis Factor-induced Protein 6-mediated Heavy Chain Transfer from Inter-α-trypsin Inhibitor to Hyaluronan

Specificity of the Tumor Necrosis Factor-induced Protein 6-mediated Heavy Chain Transfer from Inter-α-trypsin Inhibitor to Hyaluronan

Sperm competition risk generates phenotypic plasticity in ovum fertilizability

Experimental Evidence for the Influence of Cumulus-Oocyte-Complexes on Sperm Release from the Porcine Oviductal Sperm Reservoir

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