Cows are not mice: The role of cyclic AMP, phosphodiesterases, and adenosine monophosphate‐activated protein kinase in the maintenance of meiotic arrest in bovine oocytes

Bilodeau‐Goeseels, Sylvie

doi:10.1002/mrd.21337

Cited by 58 publications

(37 citation statements)

References 99 publications

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“…The inhibition of PKA abolished FID-induced gene expression changes of nine genes evaluated in cumulus cells. This was in concordance with previous reports (5,6). Calcium ionophore, on the other hand, could mimic the FID stimulation for only HK2 and STAR.…”

Section: Discussionsupporting

confidence: 93%

“…Oocyte resumes meiotic division (oocyte maturation) either in response to preovulatory luteinizing hormone (LH) surge or on its removal from its follicular environment (13,18). Additionally, a decline in intracellular cAMP can induce oocyte meiotic resumption, which presages a progressive closure of cumulusoocyte cross talk and transfer of maternal factors to the oocyte (5,7). This suggests a vital role of cAMP in oocyte competence acquisition (1).…”

mentioning

confidence: 99%

“…The downstream pathways through which cAMP modulates meiotic maturation are not fully characterized in bovine (5). Several pathways have been implicated in cAMP signaling that communicate through intricate cross talk.…”

mentioning

confidence: 99%

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Transcriptomic analysis of cyclic AMP response in bovine cumulus cells

Khan

Guillemette

Sirard

et al. 2015

Physiological Genomics

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Khan DR, Guillemette C, Sirard MA, Richard FJ. Transcriptomic analysis of cyclic AMP response in bovine cumulus cells. Physiol Genomics 47: 432-442, 2015. First published June 16, 2015 doi:10.1152/physiolgenomics.00043.2015.-Acquisition of oocyte developmental competence needs to be understood to improve clinical outcomes of assisted reproduction. The stimulation of cumulus cell concentration of cyclic adenosine 3=5=-monophosphate (cAMP) by pharmacological agents during in vitro maturation (IVM) participates in improvement of oocyte quality. However, precise coordination and downstream targets of cAMP signaling in cumulus cells are largely unknown. We have previously demonstrated better embryo development after cAMP stimulation for first 6 h during IVM. Using this model, we investigated cAMP signaling in cumulus cells through in vitro culture of cumulus-oocyte complexes (COCs) in the presence of cAMP raising agents: forskolin, IBMX, and dipyridamole (here called FID treatment). Transcriptomic analysis of cumulus cells indicated that FID-induced differentially expressed transcripts were implicated in cumulus expansion, steroidogenesis, cell metabolism, and oocyte competence. Functional genomic analysis revealed that protein kinase-A (PKA), extracellular signal regulated kinases (ERK1/2), and calcium (Ca 2ϩ ) pathways as key regulators of FID signaling. Inhibition of PKA (H89) in FID-supplemented COCs or substitution of FID with calcium ionophore (A23187) demonstrated that FID activated primarily the PKA pathway which inhibited ERK1/2 phosphorylation and was upstream of calcium signaling. Furthermore, inhibition of ERK1/2 phosphorylation by FID supported a regulation by dual specific phosphatase (DUSP1) via PKA. Our findings imply that cAMP (FID) regulates cell metabolism, steroidogenesis, intracellular signaling and cumulus expansion through PKA which modulates these functions through optimization of ERK1/2 phosphorylation and coordination of calcium signaling. These findings have implications for development of new strategies for improving oocyte in vitro maturation leading to better developmental competence. cumulus cells; cyclic AMP; cell signaling; oocyte maturation; transcriptomics; PKA; ERK1/2 FOLLICULOGENESIS IS CHARACTERIZED by cumulus-oocyte communication, which heralds better oocyte competence. This communication is mediated by gap junctions and affects accumulation of maternal factors within the oocyte that are essential to support early embryonic development (49). Also, through gap junctions, cumulus cells transfer cyclic adenosine 3=5=-monophosphate (cAMP) to the oocyte where one role of cAMP is to maintain arrest at meiotic prophase-I (12, 50). Oocyte resumes meiotic division (oocyte maturation) either in response to preovulatory luteinizing hormone (LH) surge or on its removal from its follicular environment (13,18). Additionally, a decline in intracellular cAMP can induce oocyte meiotic resumption, which presages a progressive closure of cumulusoocyte cross talk and transfer of maternal factors t...

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Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 99%

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Transcriptomic analysis of cyclic AMP response in bovine cumulus cells

Khan

Guillemette

Sirard

et al. 2015

Physiological Genomics

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“…Besides the well-characterized mechanisms of action by which cAMP is known to regulate meiotic resumption (Reviewed in [34,35]) the results of the present work further indicate that cAMP could be also involved in the control of the activity of factors that modulate large-scale chromatin remodeling during the final differentiation of fully grown oocytes, right before the resumption of meiosis. Intra-oocyte cAMP level is maintained by endogenous adenylate cyclases and constitutively active G-protein-coupled receptors [36].…”

Section: Discussionsupporting

confidence: 60%

Role of gap junction-mediated communications in regulating large-scale chromatin configuration remodeling and embryonic developmental competence acquisition in fully grown bovine oocyte

Lodde

Franciosi

Tessaro

et al. 2013

J Assist Reprod Genet

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Purpose This study was aimed to test the hypothesis that gap junction mediated communications (GJC) are required to allow the progressive chromatin configuration remodeling (from GV1 to GV3) process to occur in fully grown oocytes in order to gain the final step of developmental competence acquisition, and that a premature disruption of GJC can alter this process. Methods Bovine cumulus-oocytes complexes collected from medium antral follicles were cultured for 2, 4, 6 and 8 h in the presence of 10 −4 IU/ml of r-hFSH and with 2 mM of the nonselective PDE inhibitor 3-isobutyl-1-methyl-xanthine (IBMX) to prevent meiotic resumption. GJC functionality and chromatin configuration were monitored during the culture period. After meiotic arrest, the developmental capability of oocytes was assessed after IVM and IVF. Results IBMX was effective in significantly sustaining GJC up to 6 h and maintaining meiotic arrest, when compared to control group. Moreover, the percentage of oocytes with less condensed chromatin (GV1) decreased within 4 h of culture, while the proportion of GV2 oocytes gradually increased up to 6 h.Interestingly, a decline in the proportion of GV2 oocytes and an increase in the proportion of GV3 oocytes were observed after 6 h of culture, when the major drop of GJC occurred. On the contrary, when GJC were uncoupled by adding 3 mM of 1-heptanol or through cumulus cells removal, chromatin condensation occurred rapidly throughout the culture period, more promptly in denuded oocytes. Moreover, the maintenance of GJC during meiotic arrest was accompanied by a significant increase of developmental competence compared to the control, as indicated by a higher percentage of hatched blastocysts and blastocyst cell number. Conclusions Altogether, our data indicate that both paracrine and junctional mechanisms are involved in modulating largescale chromatin structure during the final phase of oocyte differentiation.

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“…[7]). The downstream pathways through which cAMP effects meiosis are not fully characterised in larger mammals like cattle [10] or sheep.…”

Section: Introductionmentioning

confidence: 99%