Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation†

Hung, Wei Ting; Navakanitworakul, Raphatphorn; Khan, Tarique; Zhang, Pan; Davis, John S.; McGinnis, Lynda K.; Christenson, Lane K.

doi:10.1093/biolre/iox106

Cited by 75 publications

(70 citation statements)

References 40 publications

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“…The follicular fluid undergoes dynamic changes over late stages of folliculogenesis and its EVs content modify as consequence. As an example, the follicular fluid EVs from different size follicles have distinct concentrations and miRNA content (Navakanitworakul et al, 2016), and it has been described that they can differentially stimulate granulosa cells proliferation in vitro (Hung et al, 2017). Additionally, female age (Diez-Fraile et al, 2014;da Silveira et al, 2015a), and endocrine environment (da Silveira et al, 2015a) are important factors that can alter EVs content.…”

Section: A Novel Communication System In the Antrummentioning

confidence: 99%

“…During the maturation process, the EVs induce cumulus cell expansion and alter expression of genes related to the expansion process, when used as a supplement on cumulus-oocyte complexes (COCs) maturation medium (Hung et al, 2015). In another study, EVs stimulated granulosa cell proliferation by modulating Src, Pi3K/Akt and mitogenactivated protein kinase (MAPK) pathways, and interestingly, the EVs from small follicles were preferentially taken up by granulosa cells (Hung et al, 2017). Further, using EVs as supplements for embryo maturation in culture media, partially altered genes related to metabolism and development as well as miRNA and global DNA methylation and hydroxymethylation of bovine embryos produced in vitro (da Silveira et al, 2017).…”

Section: A Novel Communication System In the Antrummentioning

confidence: 99%

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Intrafollicular barriers and cellular interactions during ovarian follicle development

Andrade¹,

Collado²,

Meirelles³

et al. 2019

Anim Reprod

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Folliclesare composed of different interdependent cell types including oocytes, cumulus, granulosa, and theca cells. Follicular cells and oocytes exchange signaling molecules from the beginning of the development of the primordial follicles until the moment of ovulation. The follicular structure transforms during folliculogenesis; barriers form between the germ and the somatic follicular cells, and between the somatic follicular cells. As such, communication systems need to adapt to maintain the exchange of signaling molecules. Two critical barriers are established at different stages of development: the zona pellucida, separating the oocyte and the cumulus cells limiting the communication through specific connections, and the antrum, separating subpopulations of follicular cells. In both situations, communication is maintained either by the development of specialized connections as transzonal projections or by paracrine signaling and trafficking of extracellular vesicles through the follicular fluid. The bidirectional communication between the oocytes and the follicle cells is vital for driving folliculogenesis and oogenesis. These communication systems are associated with essential functions related to follicular development, oocyte competence, and embryonic quality. Here, we discuss the formation of the zona pellucida and antrum during folliculogenesis, and their importance in follicle and oocyte development. Moreover, this review discusses the current knowledge on the cellular mechanisms such as the movement of molecules via transzonal projections, and the exchange of extracellular vesicles by follicular cells to overcome these barriers to support female gamete development. Finally, we highlight the undiscovered aspects related to intrafollicular communication among the germ and somatic cells, and between the somatic follicular cells and give our perspective on manipulating the above-mentioned cellular communication to improve reproductive technologies.

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Section: A Novel Communication System In the Antrummentioning

confidence: 99%

Section: A Novel Communication System In the Antrummentioning

confidence: 99%

Intrafollicular barriers and cellular interactions during ovarian follicle development

Andrade¹,

Collado²,

Meirelles³

et al. 2019

Anim Reprod

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show abstract

“…Ten sam zespół wykazał na modelu bydlęcym, że egzosomalne miRNA mogą modulować ekspresję genów zaangażowanych w ten proces, który jest kluczowy dla prawidłowej owulacji. Sugeruje to obecność nowego mechanizmu regulującego ekspansję COCs, który może wpływać na utrzymanie płodności przez samice [53].…”

Section: Funkcja Egzosomów W Pęcherzyku Jajnikowymunclassified

Exosomes as a new approach into cell-to-cell communication within the mammalian ovary

Popiołek

Grzesiak

2019

Postepy Biochem

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Pęcherzyk jajnikowy wraz z wypełniającym go płynem pęcherzykowym tworzy optymalne środowisko do wzrostu oraz dojrzewania oocytu. Płyn pęcherzykowy zawiera wiele aktywnych biologicznie cząsteczek, które regulują funkcje oocytu i komórek somatycznych pęcherzyka jajnikowego. Ostatnie doniesienia naukowe dowodzą obecności egzosomów w płynie pęcherzykowym ludzi i zwierząt. Te nanometrowe, kuliste struktury, otoczone dwuwarstwą lipidową niosą aktywny ładunek biologiczny w postaci białek, lipidów, cukrów oraz materiału genetycznego. Dzięki zdolności do biernej migracji w płynach ustrojowych, egzosomy przemieszczają się na znaczne odległości w organizmie i modulują funkcje komórek docelowych. Znaczenie egzosomów w pęcherzyku jajnikowym nie zostało wciąż do końca poznane. Dotychczasowe badania sugerują ich rolę komunikacyjną oraz wpływ na procesy fizjologiczne i patologiczne w jajniku. Badania nad egzosomami płynu pęcherzykowego dają możliwość dokładniejszego poznania procesów, w które są one zaangażowane w pęcherzyku jajnikowym. Ponadto potencjalne kliniczne zastosowanie egzosomów, np. w leczeniu i diagnostyce chorób żeńskiego układu rozrodczego, skłania naukowców do dalszych badań.

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“…They carry a cargo of bioactive molecules such as DNA, RNAs, proteins to be transferred into the extracellular environment to maintain cellular homeostasis (Takahashi et al, ) and/or transfer genetic material to neighbor or distant recipient cells (Saeed‐Zidane et al, ). In addition, its cargo content varies depending on the cell origin (de la Torre Gomez et al, ), physiological status (Hung et al, ; Navakanitworakul et al, ), inflammation (Jolly, Thompson, & Winchester, ) and stress status (Beninson et al, ; Bewicke‐Copley et al, ) of the donor cells. However, the effect and regulation of EVs biogenesis and secretion in bovine embryos during OS condition is not yet fully understood.…”

Section: Introductionmentioning

confidence: 99%

Sexual dimorphic expression and release of transcription factors in bovine embryos exposed to oxidative stress

Taqi

Saeed‐Zidane

Gebremedhn

et al. 2019

Molecular Reproduction Devel

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Sexually dimorphic differences in genome activity, which is orchestrated by transcription factors (TFs), could explain the differential response of male and female embryos to environmental stressors. To proof this hypothesis, the expression of cellular and extracellular TFs was investigated in male and female bovine embryos in vitro cultured either under low (5%) or high (20%) oxygen levels. The intracellular reactive oxygen species (ROS), total cell number, expression of nuclear factor (erythroid‐derived 2) factor 2 (NFE2L2), Krüppel‐like factor 4 (KLF4), notch receptor 1 (NOTCH1), E2F transcription factor 1 (E2F1), and SREBF2 along with extracellular vesicles (EVs) biogenesis genes were assessed at the blastocyst stage and their released EVs. Low blastocyst rate in both sexes due to oxidative stress (OS) was accompanied by increased ROS accumulation and reduced cell number in female embryos. The messenger RNA and protein levels of NFE2L2, as well as KLF4 expression, were higher in male embryos exposed to OS compared with female embryos. However, the expression of NOTCH1 and E2F1 was higher in female embryos cultured in high oxygen level. Male embryos exposed to OS released more EVs enriched with NFE2L2, superoxide dismutase 1, and NOTCH1 accompanied by elevated expression of EVs biogenesis genes. Accordingly, differential expression of TFs and their release into spent media could partially explain the sexual dimorphic response of bovine embryos to environmental stresses.

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Stage-specific follicular extracellular vesicle uptake and regulation of bovine granulosa cell proliferation†

Cited by 75 publications

References 40 publications

Intrafollicular barriers and cellular interactions during ovarian follicle development

Intrafollicular barriers and cellular interactions during ovarian follicle development

Exosomes as a new approach into cell-to-cell communication within the mammalian ovary

Sexual dimorphic expression and release of transcription factors in bovine embryos exposed to oxidative stress

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