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Regulation of recombinant human insulin-induced maturational events in Clarias batrachus (L.) oocytes in vitro

Published online by Cambridge University Press:  24 February 2015

Sudip Hajra ,
Debabrata Das ,
Pritha Ghosh ,
Soumojit Pal ,
Poulomi Nath  and
Sudipta Maitra
Sudip Hajra
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan-731235, India
Debabrata Das
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan-731235, India
Pritha Ghosh
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan-731235, India
Soumojit Pal
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan-731235, India
Poulomi Nath
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan-731235, India
Sudipta Maitra*
Affiliation:
Department of Zoology, Visva-Bharati University, Santiniketan 731235, India.
*
All correspondence to: Sudipta Maitra. Department of Zoology, Visva-Bharati University, Santiniketan 731235, India. Tel: +91 9874 405555. Fax: +91 3463 261176. e-mail: smaitra3@gmail.com or sudipta.maitra@visva-bharati.ac.in
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Summary

Regulation of insulin-mediated resumption of meiotic maturation in catfish oocytes was investigated. Insulin stimulation of post-vitellogenic oocytes promotes the synthesis of cyclin B, histone H1 kinase activation and a germinal vesicle breakdown (GVBD) response in a dose-dependent and duration-dependent manner. The PI3K inhibitor wortmannin abrogates recombinant human (rh)-insulin action on histone H1 kinase activation and meiotic G2–M1 transition in denuded and follicle-enclosed oocytes in vitro. While the translational inhibitor cycloheximide attenuates rh-insulin action, priming with transcriptional blocker actinomycin D prevents insulin-stimulated maturational response appreciably, albeit in low amounts. Compared with rh-insulin, human chorionic gonadotrophin (hCG) stimulation of follicle-enclosed oocytes in vitro triggers a sharp increase in 17α,20β-dihydroxy-4-pregnen-3-one (17α,20β-DHP) secreted in the incubation medium at 12 h. Interestingly, the insulin, but not the hCG-induced, maturational response shows less susceptibility to steroidogenesis inhibitors, trilostane or dl-aminoglutethimide. In addition, priming with phosphodiesterase inhibitor, 3-isobutyl-1-methylxanthine (IBMX) or cell-permeable dbcAMP or adenylyl cyclase activator forskolin reverses the action of insulin on meiotic G2–M1 transition. Conversely, the adenylyl cyclase inhibitor, SQ 22536, or PKA inhibitor H89 promotes the resumption of meiosis alone and further potentiates the GVBD response in the presence of rh-insulin. Furthermore, insulin-mediated meiotic maturation involves the down-regulation of endogenous protein kinase A (PKA) activity in a manner sensitive to PI3K activation, suggesting potential involvement of a cross-talk between cAMP/PKA and insulin-mediated signalling cascade in catfish oocytes in vitro. Taken together, these results suggest that rh-insulin regulation of the maturational response in C. batrachus oocytes involves down-regulation of PKA, synthesis of cyclin B, and histone H1 kinase activation and demonstrates reduced sensitivity to steroidogenesis and transcriptional inhibition.

Keywords

cAMP/PKACatfishInsulinOocyteOvarian folliclesPI3K
Type
Research Article
Information
Zygote , Volume 24 , Issue 2 , April 2016 , pp. 181 - 194
Copyright
Copyright © Cambridge University Press 2015 

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