Moderate increase of reactive oxygen species triggers meiotic resumption in rat follicular oocytes

Tiwari, Meenakshi; Chaube, Shail K.

doi:10.1111/jog.12938

Cited by 53 publications

(69 citation statements)

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“…The oocytes are generally arrested at diplotene stage of meiotic cell cycle due to continuous transfer of several signal molecules and inhibitory factors via gap junctions from encircling granulosa cells to the oocyte inside the follicular microenvironment (Mehlmann, ; Pandey et al, ; Tiwari et al, , ). Pituitary gonadotropins surge disrupt gap junctions and thereby cumulus‐oocyte communications resulting interruption in supply of several signal molecules and inhibitory factors to the oocyte leading to meiotic resumption from diplotene arrest (Zhang and Fissore, ; Tiwari and Chaube, ). The physical removal of encircling granulosa cells also disrupt the supply of various signal molecules and inhibitory factors from granulosa cells to the oocyte causing spontaneous meiotic resumption from diplotene arrest under in vitro culture conditions (Pandey et al, ; Hwang and Cheon, ; Pandey and Chaube, , ; Prasad et al, ; Tiwari et al, ).…”

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

“…These signal molecules are generated either by encircling granulosa cells or oocyte itself (Tripathi et al, ; Tiwari et al, ). Different levels of these signal molecules decide whether the meiotic cell cycle has to be maintained at diplotene stage or resumed inside the follicular microenvironment (Hwang and Cheon, ; Prasad et al, ; Tiwari and Chaube, ; Tiwari et al, ). The adenosine 3′,5′‐cyclic monophosphate (cAMP), guanosine 3′,5′‐cyclic monophosphate (cGMP), hydrogen peroxide (H 2 O 2 ), nitric oxide (NO), and calcium (Ca ++ ) are major signal molecules required for modulation of meiotic cell cycle in mammalian oocytes (Pandey et al, ; Tripathi et al, ; Tiwari et al, ).…”

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

“…Diplotene arrest in mammalian oocytes may last for several months to several years depending on the mammalian species (Mehlmann, ; Pandey et al, ; Tripathi et al, ; Tiwari and Chaube, ). These diplotene arrested oocytes, so called as dictyate stage oocyte are morphologically identified by the presence of germinal vesicle (GV) in the cytoplasm and nucleolus within the GV (Mrazek and Fulka Jr, ; Pandey et al, ; Tiwari et al, , ).…”

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

“…An increase of intraoocyte ROS level associates with the decrease of cAMP during meiotic resumption from diplotene arrest (Cheon et al, ; Chaube, ; Pandey and Chaube, ; Nunes et al, ; Tiwari and Chaube, ). Our study suggests that the decrease of intraoocyte cAMP level and increased Ca ++ level induce generation of ROS in rat oocytes cultured in vitro (Prasad et al, ).…”

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

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Calcium Signaling During Meiotic Cell Cycle Regulation and Apoptosis in Mammalian Oocytes

Tiwari

Prasad

Shrivastav

et al. 2016

Journal Cellular Physiology

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Calcium (Ca ) is one of the major signal molecules that regulate various aspects of cell functions including cell cycle progression, arrest, and apoptosis in wide variety of cells. This review summarizes current knowledge on the differential roles of Ca in meiotic cell cycle resumption, arrest, and apoptosis in mammalian oocytes. Release of Ca from internal stores and/or Ca influx from extracellular medium causes moderate increase of intracellular Ca ([Ca ]i) level and reactive oxygen species (ROS). Increase of Ca as well as ROS levels under physiological range trigger maturation promoting factor (MPF) destabilization, thereby meiotic resumption from diplotene as well as metaphase-II (M-II) arrest in oocytes. A sustained increase of [Ca ]i level beyond physiological range induces generation of ROS sufficient enough to cause oxidative stress (OS) in aging oocytes. The increased [Ca ]i triggers Fas ligand-mediated oocyte apoptosis. Further, OS triggers mitochondria-mediated oocyte apoptosis in several mammalian species. Thus, Ca exerts differential roles on oocyte physiology depending upon its intracellular concentration. A moderate increase of [Ca ]i as well as ROS mediate spontaneous resumption of meiosis from diplotene as well as M-II arrest, while their high levels cause meiotic cell cycle arrest and apoptosis by operating both mitochondria- as well as Fas ligand-mediated apoptotic pathways. Indeed, Ca regulates cellular physiology by modulating meiotic cell cycle and apoptosis in mammalian oocytes. J. Cell. Physiol. 232: 976-981, 2017. © 2016 Wiley Periodicals, Inc.

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Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

Section: Role Of Ca++ In Meiotic Resumption From Diplotene Arrestmentioning

confidence: 99%

See 2 more Smart Citations

Calcium Signaling During Meiotic Cell Cycle Regulation and Apoptosis in Mammalian Oocytes

Tiwari

Prasad

Shrivastav

et al. 2016

Journal Cellular Physiology

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“…Recently, oxidative stress was shown to correlate with levels of (sexual) megasporogenesis in a facultative apomictic (asexual) plant, Ranunculus auricomus [72]. In mammals, moderate increases of ROS were shown to trigger meiotic resumption in (rat) follicular oocytes [73].…”

Section: A 'Double Whammy': More Information To Protect Against More mentioning

confidence: 99%

What can we infer about the origin of sex in early eukaryotes?

Speijer

2016

Phil. Trans. R. Soc. B

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One contribution of 15 to a theme issue 'Weird sex: the underappreciated diversity of sexual reproduction'. Current analysis shows that the last eukaryotic common ancestor (LECA) was capable of full meiotic sex. The original eukaryotic life cycle can probably be described as clonal, interrupted by episodic sex triggered by external or internal stressors. The cycle could have started in a highly flexible form, with the interruption of either diploid or haploid clonal growth determined by stress signals only. Eukaryotic sex most likely evolved in response to a high mutation rate, arising from the uptake of the endosymbiont, as this ( proto) mitochondrion generated internal reactive oxygen species. This is consistent with the likely development of full meiotic sex from a diverse set of existing archaeal (the host of the endosymbiont) repair and signalling mechanisms. Meiotic sex could thus have been one of the fruits of symbiogenesis at the basis of eukaryotic origins: a product of the merger by which eukaryotic cells arose. Symbiogenesis also explains the large-scale migration of organellar DNA to the nucleus. I also discuss aspects of uniparental mitochondrial inheritance and mitonuclear interactions in the light of the previous analysis.This article is part of the themed issue 'Weird sex: the underappreciated diversity of sexual reproduction'.

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Role of Cyclic Nucleotide Phosphodiesterases During Meiotic Resumption From Diplotene Arrest in Mammalian Oocytes

et al. 2016

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Cyclic nucleotide phosphodiesterases (PDEs) are group of enzymes that hydrolyze cyclic nucleotides in wide variety of cell types including encircling granulosa cells as well as associated oocytes. One group of PDEs are located in encircling granulosa cells and another group get expressed in the oocyte, while few other PDEs are expressed in both compartments. The PDE1A, PDE4D, PDE5A, PDE8A, and PDE8B are granulosa cell specific PDEs that hydrolyze adenosine 3',5'-cyclic monophosphate (cAMP) as well as guanosine 3',5'-cyclic monophosphate (cGMP) with different affinities. PDE3A, PDE8A as well as PDE9A are expressed in oocyte and specifically responsible for the cyclic nucleotide hydrolysis in the oocyte itself. Few other PDEs such as PDE7B, PDE10A, and PDE11A are either detected in granulosa cells or oocytes. Activation of these PDEs either in encircling granulosa cells or in oocyte directly or indirectly reduces intraoocyte cAMP level. Reduction of intraoocyte cAMP level modulates phosphorylation status of cyclin-dependent kinase 1 (Cdk1) and triggers cyclin B1 degradation that destabilizes maturation promoting factor (MPF) and/or increases Cdk1 activity. The destabilized MPF and/or increased Cdk1 activity leads to resumption of meiosis, which initiates the achievement of meiotic competency in preovulatory follicles of several mammalian species. Use of specific PDEs inhibitors block cyclic nucleotides hydrolysis that results in increase of intraoocyte cyclic nucleotides level, which leads to maintenance of meiotic arrest at diplotene stage in vivo as well as in vitro. Thus, cyclic nucleotide PDEs play important role in the achievement of meiotic competency by reducing intraoocyte cyclic nucleotides level in mammalian oocytes. J. Cell. Biochem. 118: 446-452, 2017. © 2016 Wiley Periodicals, Inc.

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Moderate increase of reactive oxygen species triggers meiotic resumption in rat follicular oocytes

Abstract: Our findings suggest that a moderate increase of ROS in the ovary is beneficial for meiotic resumption from diplotene arrest and extrusion of first polar body in follicular oocytes.

Cited by 53 publications

References 46 publications

Calcium Signaling During Meiotic Cell Cycle Regulation and Apoptosis in Mammalian Oocytes

Calcium Signaling During Meiotic Cell Cycle Regulation and Apoptosis in Mammalian Oocytes

What can we infer about the origin of sex in early eukaryotes?

Role of Cyclic Nucleotide Phosphodiesterases During Meiotic Resumption From Diplotene Arrest in Mammalian Oocytes

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