Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins

Hussein, T. S.; Froiland, D. A.; Amato, F.; Thompson, Jeremy G.; Gilchrist, Robert B.

doi:10.1242/jcs.02644

Cited by 315 publications

(262 citation statements)

References 48 publications

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“…This may be due to timing of tissue analysis, the in vitro bias, and species differences. Interestingly, the expression of some proliferative genes was reported to be induced by the oocyte (Hussein et al 2005), and we can assume that it may compensate/counteract the early apoptosis signs. This survival behavior was also reinforced by the activation of cell morphology and cellular assembly functions.…”

Section: Cellular and Molecular Function Analysismentioning

confidence: 93%

Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence

Assidi¹,

Dieleman²,

Sirard³

2010

Reproduction

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Cumulus cells (CCs) are essential for oocytes to reach full development competency and become fertilized. Many major functional properties of CCs are triggered by gonadotropins and governed by the oocyte. Consequently, cumulus may reflect oocyte quality and is often used for oocyte selection. The most visible function of CCs is their ability for rapid extracellular matrix expansion after the LH surge. Although unexplained, LH induces the final maturation and improves oocyte quality. To study the LH signaling and gene expression cascade patterns close to the germinal vesicle breakdown, bovine CCs collected at 2 h before and 6 h after the LH surge were hybridized to a custom-made microarray to better understand the LH genomic action and find differentially expressed genes associated with the LH-induced oocyte final maturation. Functional genomic analysis of the 141 overexpressed and 161 underexpressed clones was performed according to their molecular functions, gene networks, and cell compartments. Following real-time PCR validation of our gene lists, some interesting pathways associated with the LH genomic action on CCs and their possible roles in oocyte final maturation, ovulation, and fertilization are discussed. A list of early potential markers of oocyte competency in vivo and in vitro is thereafter suggested. These early biomarkers are a preamble to understand the LH molecular pathways that trigger the final oocyte competence acquisition process in bovine.

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Section: Cellular and Molecular Function Analysismentioning

confidence: 93%

Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence

Assidi¹,

Dieleman²,

Sirard³

2010

Reproduction

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“…Recent studies have proven that oocytes may regulate the functions of cumulus itself instead of being controlled by cumulus (Gilchrist et al, 2008). Hussein et al(2005) demonstrated that soluble paracrine signals from the oocyte may contribute to the levels of apoptosis in cumulus cells rather than gap junctions, because destroying the gap junctions between cumulus cells and oocytes has effects on apoptosis in all cumulus cell layers instead of the closest layer to the oocyte. Growth-differentiation factor 9 (GDF9) and bone morphogenetic protein 15 (BMP15) are two key oocyte-secreted factors (OSFs), which are expressed in the ooplasm and function in cumulus cells.…”

Section: Interaction Between Ooplasmic Mitochondria and Cumulus Cellsmentioning

confidence: 99%

Mitochondrial functions on oocytes and preimplantation embryos

Wang

Zou

et al. 2009

J. Zhejiang Univ. Sci. B

134

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Oocyte quality has long been considered as a main limiting factor for in vitro fertilization (IVF). In the past decade, extensive observations demonstrated that the mitochondrion plays a vital role in the oocyte cytoplasm, for it can provide adenosine triphosphate (ATP) for fertilization and preimplantation embryo development and also act as stores of intracellular calcium and proapoptotic factors. During the oocyte maturation, mitochondria are characterized by distinct changes of their distribution pattern from being homogeneous to heterogeneous, which is correlated with the cumulus apoptosis. Oocyte quality decreases with the increasing maternal age. Recent studies have shown that low quality oocytes have some age-related dysfunctions, which include the decrease in mitochondrial membrane potential, increase of mitochondrial DNA (mtDNA) damages, chromosomal aneuploidies, the incidence of apoptosis, and changes in mitochondrial gene expression. All these dysfunctions may cause a high level of developmental retardation and arrest of preimplantation embryos. It has been suggested that these mitochondrial changes may arise from excessive reactive oxygen species (ROS) that is closely associated with the oxidative energy production or calcium overload, which may trigger permeability transition pore opening and subsequent apoptosis. Therefore, mitochondria can be seen as signs for oocyte quality evaluation, and it is possible that the oocyte quality can be improved by enhancing the physical function of mitochondria. Here we reviewed recent advances in mitochondrial functions on oocytes.

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“…Oocytes define the cumulus cell phenotype by promoting glycolysis (Sugiura et al 2005), cholesterol synthesis (Su et al 2008), proliferation (Vanderhyden et al 1992, Gilchrist et al 2006, survival (Hussein et al 2005) and gene expression , while suppressing luteinization (Pincus & Enzmann 1935, Nekola & Nalbandov 1971 and opposing FSH-stimulated gene expression . The effects of oocytes on cumulus cells are mediated, in part, by factors such as GDF9 and BMP15, which activate the SMAD1/5/9 (Sugiura et al 2007) and SMAD2/3 signaling pathways.…”

Section: Introductionmentioning

confidence: 99%

Oocyte–cumulus cell interactions regulate free intracellular zinc in mouse oocytes

Lisle¹,

Anthony²,

Randall³

et al. 2013

Reproduction

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Zinc increases in the oocyte during maturation and is required for progression and completion of meiosis. The objective of this study was to determine whether cumulus cells regulate the levels of free intracellular zinc in the oocyte during maturation. In the cumulus-oocyte complex (COC) the relative level of free intracellular zinc was almost fourfold higher in cumulus cells compared with the resident germinal vesicle-stage oocyte. Removal of cumulus cells caused a fourfold increase in intracellular zinc in the oocyte by 1 h after cumulus cell removal, but subsequent coculture of denuded oocytes with COC decreased free intracellular zinc in the oocyte by 65%. Thus, cumulus cells suppress free intracellular zinc in the oocyte. The mRNA transcripts for the zinc transporter proteins Slc39a6, Slc39a8, Slc39a9, Slc39a10, Slc39a12, Slc30a2, Slc30a4, Slc30a5 and Slc30a8 mRNAs were higher in oocytes, while Slc39a1, Slc39a7, Slc39a13, Slc39a14, Slc30a6, Slc30a7 and Slc30a9 mRNAs were higher in cumulus cells. Thus a complex zinc transport network is present in the COC. Pretreatment with epidermal growth factor for 4 h abolished the ability of COCs to restrict free intracellular zinc in denuded oocytes. Coculture of denuded metaphase II oocytes with COC lowers free intracellular zinc in mature oocytes. Oocytes matured in vivo or oocytes from older mice had lower levels of free intracellular zinc than oocytes matured in vitro or from younger mice. Thus, a precise mechanism for regulating oocyte zinc homeostasis has been uncovered in the COC that is disrupted with increasing age or by removal of cumulus cells.

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Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins

Cited by 315 publications

References 48 publications

Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence

Cumulus cell gene expression following the LH surge in bovine preovulatory follicles: potential early markers of oocyte competence

Mitochondrial functions on oocytes and preimplantation embryos

Oocyte–cumulus cell interactions regulate free intracellular zinc in mouse oocytes

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