Abstract
During follicle development, oocytes secrete factors that influence the development of granulosa and cumulus cells (CCs). In response to oocyte and somatic cell signals, CCs produce extracellular matrix (ECM) molecules resulting in cumulus expansion, which is essential for ovulation, fertilisation, and is predictive of oocyte quality. The cumulus ECM is largely made up of hyaluronan (HA), TNF-stimulated gene-6 (TSG-6, also known as TNFAIP6), pentraxin-3 (PTX3), and the heavy chains (HCs) of serum-derived inter-α-inhibitor proteins. In contrast to other in vivo models where modified expansion impairs fertility, the cumulus mass of C1galt1 Mutants, which have oocyte-specific deletion of core 1-derived O-glycans, is modified without impairing fertility. In this report, we used C1galt1 Mutant (C1galt1 FF:ZP3Cre) and Control (C1galt1 FF) mice to investigate how cumulus expansion is affected by oocyte-specific deletion of core 1-derived O-glycans without adversely affecting oocyte quality. Mutant cumulus–oocyte complexes (COCs) are smaller than Controls, with fewer CCs. Interestingly, the CCs in Mutant mice are functionally normal as each cell produced normal levels of the ECM molecules HA, TSG-6, and PTX3. However, HC levels were elevated in Mutant COCs. These data reveal that oocyte glycoproteins carrying core 1-derived O-glycans have a regulatory role in COC development. In addition, our study of Controls indicates that a functional COC can form provided all essential components are present above a minimum threshold level, and thus some variation in ECM composition does not adversely affect oocyte development, ovulation or fertilisation. These data have important implications for IVF and the use of cumulus expansion as a criterion for oocyte assessment.
Highlights
The process of follicle development begins with the activation of a quiescent primordial follicle and culminates with the ovulation of a single fertilisable egg
Antral fluid is deposited between the granulosa cells which facilitates the physical separation and differentiation of the granulosa cell population into mural granulosa cells and cumulus cells (CCs) that are associated with the oocyte
Cumulus expansion in the preovulatory follicles of mice requires paracrine signals from the oocyte, which act on CCs to promote the formation of a HA-rich extracellular matrix (ECM)
Summary
The process of follicle development begins with the activation of a quiescent primordial follicle and culminates with the ovulation of a single fertilisable egg. Antral fluid is deposited between the granulosa cells which facilitates the physical separation and differentiation of the granulosa cell population into mural granulosa cells (mGCs; which line the wall of the follicle) and cumulus cells (CCs) that are associated with the oocyte. An extracellular matrix (ECM) is assembled between the CCs leading to expansion of the cumulus mass that surrounds the oocyte. The expanded cumulus mass is believed to facilitate efficient capture of an ovulated egg by the oviductal fimbriae and transport into the oviduct (Chen et al 1993, Tanghe et al 2002). ECM deposition and cumulus expansion are important for ovulation, fertilisation and implantation
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