Changes in signal molecules and maturation promoting factor levels associate with spontaneous resumption of meiosis in rat oocytes

Prasad, Shilpa; Tiwari, Meenakshi; Tripathi, Anima; Pandey, Ashutosh; Chaube, Shail K.

doi:10.1002/cbin.10444

Cited by 41 publications

(100 citation statements)

References 38 publications

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“…Postovulatory aging mediates abortive SEA and initiation of PBII extrusion, which are characteristic features of SEA (Chebotareva et al, 2011;Prasad et al, 2015b;Chaube, 2013, 2014); this deteriorates egg quality and limits ART outcome (Miao et al, 2009;Prasad et al, 2015a). However, biochemical and molecular changes that drive postovulatory aging-mediated abortive SEA remain poorly understood.…”

Section: Discussionmentioning

confidence: 96%

“…sc-12341), anti-pThr-14/Tyr-15 (sc-12340), cdc2 p34 PSTAIRE antibody (sc-53), anti-cyclin B1 antibody (sc-752), anti-Wee1 antibody (sc-9037), anti-Emi2 antibody (sc-68894), anti-APC/C antibody (sc-896), anti-MAD2 antibody (sc-6329), all purchased from Santa Cruz Biotechnology, Inc. (Santa Cruz, CA, USA). Immunofluorescence analysis was carried out following our previously published protocol (Prasad et al, 2015b). In brief, 12-14 eggs from each group were fixed with 4% buffered formaldehyde.…”

Section: Analyses Of Morphological and Chromosomal Status During Postmentioning

confidence: 99%

“…Thereafter, it was reported in several mammalian species, including mice (Abbott et al, 1998;Lord et al, 2013), rat (Chaube et al, 2007;Chaube, 2013, 2014;Prasad et al, 2015b), hamster ( Juetten and Bavister, 1983), porcine (Ito et al, 2003(Ito et al, , 2004Ruddock et al, 2001), bovine (Sergeev and Norman, 2003), and human eggs (Combelles et al, 2011;Escrich et al, 2011;Lu et al, 2006). Recent studies from our laboratory suggest that postovulatory aging-mediated abortive SEA shows initiation of PBII extrusion that is never completed and further arrest at the metaphase III-(MIII) like stage due to scattering of chromosomes throughout the egg cytoplasm Chaube, 2013, 2014).…”

Section: Introductionmentioning

confidence: 96%

“…Wee1 destabilizes MPF by increasing the Thr-14/Tyr-15 phosphorylated cyclin-dependent kinase 1 (Cdk1) level and decreasing Thr-161 phosphorylated Cdk1 as well as cyclin B1 levels (Kubiak et al, 2008;Oh et al, 2011;Prasad et al, 2015b). However, MPF stabilization requires reduced phosphorylation at Thr-14/Tyr-15 of Cdk1, increased phosphorylation at Thr-161 of Cdk1, and association with cyclin B1 (Kubiak et al, 2008;Prasad et al, 2015a, b).…”

Section: Introductionmentioning

confidence: 96%

“…The aged eggs are unable to handle such an increased cytosolic free Ca 2+ level, and maturation promoting factor (MPF) destabilization is triggered (Prasad et al, 2015b;Chaube, 2013, 2014). Wee1 destabilizes MPF by increasing the Thr-14/Tyr-15 phosphorylated cyclin-dependent kinase 1 (Cdk1) level and decreasing Thr-161 phosphorylated Cdk1 as well as cyclin B1 levels (Kubiak et al, 2008;Oh et al, 2011;Prasad et al, 2015b).…”

Section: Introductionmentioning

confidence: 98%

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Involvement of Cyclin-Dependent Kinase 1 during Postovulatory Aging-Mediated Abortive Spontaneous Egg Activation in Rat Eggs CulturedIn Vitro

Prasad

Koch

Chaube

2016

Cellular Reprogramming

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Freshly ovulated rat eggs do not remain arrested at metaphase II (MII) and undergo exit from MII arrest with initiation of extrusion of the second polar body (PBII), a characteristic feature of abortive spontaneous egg activation (SEA). The biochemical and molecular changes during postovulatory aging-mediated abortive SEA remain poorly understood. We investigated the morphological, cellular, and molecular changes during postovulatory aging-mediated abortive SEA in eggs cultured in vitro. Our results suggest that postovulatory egg aging in vitro induced initiation of PBII extrusion in a time-dependent manner. Postovulatory aging increased Wee1 kinase and Thr-14/Tyr-15 phosphorylated cyclin-dependent kinase 1 (Cdk1) levels, whereas Thr-161 phosphorylated Cdk1 and cyclin B1 levels were significantly decreased in eggs cultured in vitro. The early mitotic inhibitor 2 (Emi2) level was significantly reduced, but anaphase promoting complex/cyclosome (APC/C) and mitotic arrest deficient protein (MAD2) levels were increased initially and then reduced during a later period of in vitro culture. These results suggest that an increased Wee1 kinase level modulated the specific phosphorylation status of Cdk1, increased Cdk1 activity, and decreased the cyclin B1 level. Furthermore, the decreased Emi2 level was associated with an increased level of APC/C and decreased level of cyclin B1, which resulted in maturation promoting factor (MPF) destabilization and finally led to postovulatory aging-mediated abortive SEA in rat eggs cultured in vitro.

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Section: Discussionmentioning

confidence: 96%

Section: Analyses Of Morphological and Chromosomal Status During Postmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 96%

Section: Introductionmentioning

confidence: 98%

See 3 more Smart Citations

Involvement of Cyclin-Dependent Kinase 1 during Postovulatory Aging-Mediated Abortive Spontaneous Egg Activation in Rat Eggs CulturedIn Vitro

Prasad

Koch

Chaube

2016

Cellular Reprogramming

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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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Role of Mitogen Activated Protein Kinase and Maturation Promoting Factor During the Achievement of Meiotic Competency in Mammalian Oocytes

Tiwari

Gupta

Sharma

et al. 2017

J of Cellular Biochemistry

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The oocyte quality remains as one of the major problems associated with poor in vitro fertilization (IVF) rate and assisted reproductive technology (ART) failure worldwide. The oocyte quality is dependent on its meiotic maturation that begins inside the follicular microenvironment and gets completed at the time of ovulation in most of the mammalian species. Follicular oocytes are arrested at diplotene stage of first meiotic prophase. The resumption of meiosis from diplotene arrest, progression through metaphase-I (M-I) and further arrest at metaphase-II (M-II) are important physiological requirements for the achievement of meiotic competency in mammalian oocytes. The achievement of meiotic competency is dependent upon cyclic stabilization/destabilization of maturation promoting factor (MPF). The mitogen-activated protein kinase3/1 (MAPK3/1) modulates stabilization/destabilization of MPF in oocyte by interacting either with signal molecules, transcription and post-transcription factors in cumulus cells or cytostatic factors (CSFs) in oocyte. MPF regulates meiotic cell cycle progression from diplotene arrest to M-II arrest and directly impacts oocyte quality. The MAPK3/1 activity is not reported during spontaneous meiotic resumption but its activity in cumulus cells is required for gonadotropin-induced oocyte meiotic resumption. Although high MAPK3/1 activity is required for the maintenance of M-II arrest in several mammalian species, its cross-talk with MPF remains to be elucidated. Further studies are required to find out the MAPK3/1 activity and its impact on MPF destabilization/stabilization during achievement of meiotic competency, an important period that decides oocyte quality and directly impacts ARTs outcome in several mammalian species including human. J. Cell. Biochem. 119: 123-129, 2018. © 2017 Wiley Periodicals, Inc.

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Changes in signal molecules and maturation promoting factor levels associate with spontaneous resumption of meiosis in rat oocytes

Cited by 41 publications

References 38 publications

Involvement of Cyclin-Dependent Kinase 1 during Postovulatory Aging-Mediated Abortive Spontaneous Egg Activation in Rat Eggs CulturedIn Vitro

Involvement of Cyclin-Dependent Kinase 1 during Postovulatory Aging-Mediated Abortive Spontaneous Egg Activation in Rat Eggs CulturedIn Vitro

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

Role of Mitogen Activated Protein Kinase and Maturation Promoting Factor During the Achievement of Meiotic Competency in Mammalian Oocytes

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