Regulation of germ cell development by intercellular signaling in the mammalian ovarian follicle.
TLDR
Oocyte differentiation depends on continuous signaling interactions with the somatic cells of the follicle and may be regulated by extracellular vesicles newly identified in follicular fluid and at TZP tips, which could mediate intercellular transfer of macromolecules.Abstract:
Prior to ovulation, the mammalian oocyte undergoes a process of differentiation within the ovarian follicle that confers on it the ability to give rise to an embryo. Differentiation comprises two phases-growth, during which the oocyte increases more than 100-fold in volume as it accumulates macromolecules and organelles that will sustain early embryogenesis; and meiotic maturation, during which the oocyte executes the first meiotic division and prepares for the second division. Entry of an oocyte into the growth phase appears to be triggered when the adjacent granulosa cells produce specific growth factors. As the oocyte grows, it elaborates a thick extracellular coat termed the zona pellucida. Nonetheless, cytoplasmic extensions of the adjacent granulosa cells, termed transzonal projections (TZPs), enable them to maintain contact-dependent communication with the oocyte. Through gap junctions located where the TZP tips meet the oocyte membrane, they provide the oocyte with products that sustain its metabolic activity and signals that regulate its differentiation. Conversely, the oocyte secretes diffusible growth factors that regulate proliferation and differentiation of the granulosa cells. Gap junction-permeable products of the granulosa cells prevent precocious initiation of meiotic maturation, and the gap junctions also enable oocyte maturation to begin in response to hormonal signals received by the granulosa cells. Development of the oocyte or the somatic compartment may also be regulated by extracellular vesicles newly identified in follicular fluid and at TZP tips, which could mediate intercellular transfer of macromolecules. Oocyte differentiation thus depends on continuous signaling interactions with the somatic cells of the follicle. WIREs Dev Biol 2018, 7:e294. doi: 10.1002/wdev.294 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Cellular Differentiation Signaling Pathways > Cell Fate Signaling Early Embryonic Development > Gametogenesis.read more
Citations
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Disruption of gap junctional communication within the ovarian follicle induces oocyte maturation
TL;DR: Because experimentally induced breakdown of communication within the ovarian follicle is associated with a drop in intraoocyte cAMP concentrations and results in resumption of meiosis, this could be the physiological mechanism employed by LH to stimulate oocyte maturation.
Journal ArticleDOI
Oocyte stage-specific effects of MTOR determine granulosa cell fate and oocyte quality in mice
Jing Guo,Teng Zhang,Yueshuai Guo,Tao Sun,Hui Li,Xiaoyun Zhang,Hong Yin,Guangyi Cao,Yaoxue Yin,Hao Wang,Lanying Shi,Xuejiang Guo,Jiahao Sha,John J. Eppig,You-Qiang Su +14 more
TL;DR: It is shown that conditional knockout (cKO) of Mtor in either primordial or growing oocytes caused infertility but differentially affected oocyte quality, granulosa cell fate, and follicular development.
Journal Article
Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary
Patricia Da Silva-Buttkus,Gayani Jayasooriya,Jocelyn M. Mora,Margaret A. Mobberley,Timothy A. Ryder,Marianne Baithun,Jaroslav Stark,Stephen Franks,Kate Hardy +8 more
TL;DR: It is proposed that the basement membrane and/or theca cells that surround the follicle provide an important confinement for rapidly dividing columnar cells so that they attain maximum packing density, which restricts lateral mitosis and promotes inwardly oriented cell divisions and subsequent multilayering.
Journal ArticleDOI
Molecular regulation of follicle-stimulating hormone synthesis, secretion and action.
Nandana Das,T. Rajendra Kumar +1 more
TL;DR: Several key players that regulate FSH synthesis, sorting, secretion and action in gonads and extragonadal tissues have been identified in a physiological setting and it is anticipated that several exciting new discoveries uncovering all aspects of FSH biology will soon be forthcoming.
Journal ArticleDOI
Mammalian Oocytes Locally Remodel Follicular Architecture to Provide the Foundation for Germline-Soma Communication
TL;DR: It is shown that TZP number and germline-soma communication are strikingly reduced in reproductively aged females, and an inability of somatic follicle cells to respond appropriately to oocyte-derived cues may contribute to human infertility.
References
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Journal ArticleDOI
Driving folliculogenesis by the oocyte-somatic cell dialog: Lessons from genetic models
TL;DR: Various models of transgenic mice and sheep carrying natural loss-of-function mutations associated with sterility have established that the oocyte-derived factors, bone morphogenetic protein (BMP) 15 and growth differentiation factor 9 orchestrate follicle development, support cumulus metabolism and maturation and participate in oocyte meiosis arrest.
Journal ArticleDOI
Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes.
Jeremy R. Egbert,Leia C. Shuhaibar,Aaron B. Edmund,Dusty Van Helden,Jerid W. Robinson,Tracy F. Uliasz,Valentina Baena,Andreas Geerts,Frank Wunder,Lincoln R. Potter,Laurinda A. Jaffe +10 more
TL;DR: Using rat follicles, it is shown that within 10 min, LH signaling causes dephosphorylation and inactivation of NPR2 through a process that requires the activity of phosphoprotein phosphatase (PPP)-family members.
Book ChapterDOI
The control of meiotic maturation in mammalian oocytes.
TL;DR: This work examines how CDK1 is suppressed during meiotic arrest and raised for oocyte maturation, and focuses on signaling: intercellular signaling between the oocytes and the somatic cells of the follicle, and spatial signaling involving the anaphase-promoting complex (APC) within the oocyte.
Journal Article
Effect of cell shape and packing density on granulosa cell proliferation and formation of multiple layers during early follicle development in the ovary
Patricia Da Silva-Buttkus,Gayani Jayasooriya,Jocelyn M. Mora,Margaret A. Mobberley,Timothy A. Ryder,Marianne Baithun,Jaroslav Stark,Stephen Franks,Kate Hardy +8 more
TL;DR: It is proposed that the basement membrane and/or theca cells that surround the follicle provide an important confinement for rapidly dividing columnar cells so that they attain maximum packing density, which restricts lateral mitosis and promotes inwardly oriented cell divisions and subsequent multilayering.
Journal ArticleDOI
DNA methylation establishment during oocyte growth: mechanisms and significance.
TL;DR: These findings lead to a new perspective that transcription events dictate the placing and timing of methylation in specific genes and suggest a mechanism by which methylation could be coordinated by the events and factors regulating oocyte growth.
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