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Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1.
Reproduction 2016; 151(1):59-72R

Abstract

Binding of 17β-estradiol (E2) to novel G-protein coupled receptor, Gper1, promotes intra-oocyte adenylyl cyclase activity and transactivates epidermal growth factor receptor to ensure prophase-I arrest. Although involvement of either membrane progestin receptor (mPR) or Igf system has been implicated in regulation of meiosis resumption, possibility of concurrent activation and potential synergism between 17α,20β-dihydroxy-4-pregnen-3-one (DHP)- and Igf-mediated signalling cascades in alleviating E2 inhibition of oocyte maturation (OM) has not been investigated. Here using zebrafish (Danio rerio) defolliculated oocytes, we examined the effect of DHP and Igf1, either alone or in combination, in presence or absence of E2, on OM in vitro. While priming of denuded oocytes with E2 blocked spontaneous maturation, co-treatment with DHP (3 nM) and Igf1 (10 nM), but not alone, reversed E2 inhibition and promoted a robust increase in germinal vesicle breakdown (GVBD). Although stimulation with either Igf1 or DHP promoted Akt phosphorylation, pharmacological inhibition of PI3K/Akt signalling prevented Igf1-induced GVBD but delayed DHP action till 4-5 h of incubation. Moreover, high intra-oocyte cAMP attenuates both DHP and Igf1-mediated OM and co-stimulation with DHP and Igf1 could effectively reverse E2 action on PKA phosphorylation. Interestingly, data from in vivo studies reveal that heightened expression of igf1, igf3 transcripts in intact follicles corresponded well with elevated phosphorylation of Igf1r and Akt, mPRa immunoreactivity, PKA inhibition and accelerated GVBD response just prior to ovulation. This indicates potential synergism between maturational steroid and Igf1 which might have physiological relevance in overcoming E2 inhibition of meiosis resumption in zebrafish oocytes.

Authors+Show Affiliations

Department of ZoologyVisva-Bharati University, Santiniketan 731235, India.Department of ZoologyVisva-Bharati University, Santiniketan 731235, India.Department of ZoologyVisva-Bharati University, Santiniketan 731235, India smaitra3@gmail.com sudipta.maitra@visva-bharati.ac.in.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

26500283

Citation

Das, Debabrata, et al. "Releasing Prophase Arrest in Zebrafish Oocyte: Synergism Between Maturational Steroid and Igf1." Reproduction (Cambridge, England), vol. 151, no. 1, 2016, pp. 59-72.
Das D, Pal S, Maitra S. Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1. Reproduction. 2016;151(1):59-72.
Das, D., Pal, S., & Maitra, S. (2016). Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1. Reproduction (Cambridge, England), 151(1), pp. 59-72. doi:10.1530/REP-15-0389.
Das D, Pal S, Maitra S. Releasing Prophase Arrest in Zebrafish Oocyte: Synergism Between Maturational Steroid and Igf1. Reproduction. 2016;151(1):59-72. PubMed PMID: 26500283.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1. AU - Das,Debabrata, AU - Pal,Soumojit, AU - Maitra,Sudipta, Y1 - 2015/10/23/ PY - 2015/04/23/received PY - 2015/10/22/accepted PY - 2015/10/27/entrez PY - 2015/10/27/pubmed PY - 2016/8/25/medline SP - 59 EP - 72 JF - Reproduction (Cambridge, England) JO - Reproduction VL - 151 IS - 1 N2 - Binding of 17β-estradiol (E2) to novel G-protein coupled receptor, Gper1, promotes intra-oocyte adenylyl cyclase activity and transactivates epidermal growth factor receptor to ensure prophase-I arrest. Although involvement of either membrane progestin receptor (mPR) or Igf system has been implicated in regulation of meiosis resumption, possibility of concurrent activation and potential synergism between 17α,20β-dihydroxy-4-pregnen-3-one (DHP)- and Igf-mediated signalling cascades in alleviating E2 inhibition of oocyte maturation (OM) has not been investigated. Here using zebrafish (Danio rerio) defolliculated oocytes, we examined the effect of DHP and Igf1, either alone or in combination, in presence or absence of E2, on OM in vitro. While priming of denuded oocytes with E2 blocked spontaneous maturation, co-treatment with DHP (3 nM) and Igf1 (10 nM), but not alone, reversed E2 inhibition and promoted a robust increase in germinal vesicle breakdown (GVBD). Although stimulation with either Igf1 or DHP promoted Akt phosphorylation, pharmacological inhibition of PI3K/Akt signalling prevented Igf1-induced GVBD but delayed DHP action till 4-5 h of incubation. Moreover, high intra-oocyte cAMP attenuates both DHP and Igf1-mediated OM and co-stimulation with DHP and Igf1 could effectively reverse E2 action on PKA phosphorylation. Interestingly, data from in vivo studies reveal that heightened expression of igf1, igf3 transcripts in intact follicles corresponded well with elevated phosphorylation of Igf1r and Akt, mPRa immunoreactivity, PKA inhibition and accelerated GVBD response just prior to ovulation. This indicates potential synergism between maturational steroid and Igf1 which might have physiological relevance in overcoming E2 inhibition of meiosis resumption in zebrafish oocytes. SN - 1741-7899 UR - https://www.unboundmedicine.com/medline/citation/26500283/Releasing_prophase_arrest_in_zebrafish_oocyte:_synergism_between_maturational_steroid_and_Igf1_ L2 - https://rep.bioscientifica.com/doi/10.1530/REP-15-0389 DB - PRIME DP - Unbound Medicine ER -