Hostname: page-component-76fb5796d-2lccl Total loading time: 0 Render date: 2024-04-26T12:59:48.433Z Has data issue: false hasContentIssue false
  • English
  • Français

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
Get access Rights & Permissions [Opens in a new window]

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 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acosta-Martínez, M. (2012). PI3K: an attractive candidate for the central integration of metabolism and reproduction. Front. Endocrinol. 2, 1–16.CrossRefGoogle ScholarPubMed
Andersen, C.B., Roth, R.A. & Conti, M. (1998). Protein kinase B/Akt induces resumption of meiosis in Xenopus oocytes. J. Biol. Chem. 273, 18705–8.Google Scholar
Andersen, C.B., Sakaue, H., Nedachi, T., Kovasina, K.S., Clayberger, C., Conti, M. & Roth, R.A. (2003). Protein kinase B/Akt is essential for the insulin but not progesterone stimulated resumption of meiosis in Xenopus oocyte. Biochem. J. 369, 227–38.Google Scholar
Chaube, S.K. & Haider, S. (1997). Evidence for the stimulation of cyclic AMP phosphodiesterase in catfish (Clarias batrachus) oocytes by 17α,20β-dihydroxy-4-pregnen-3-one. J. Exp. Zool. 277, 166–70.Google Scholar
Chourasia, T.K. & Joy, K.P. (2008). Estrogen-2/4-hydroxylase activity is stimulated during germinal vesicle breakdown induced by hCG, IGF-1, GH and insulin in the catfish Heteropneustes fossilis . Gen. Comp. Endocrinol. 155, 413–21.Google Scholar
Colton, S.A., Pieper, G.M. & Downs, S.M. (2002). Altered meiotic regulation in oocytes from diabetic mice. Biol. Reprod. 67, 220–31.Google Scholar
Conlon, J.M. (2001). Evolution of the insulin molecule: insights into structure-activity and phylogenetic relationships. Peptides 22, 1183–93.Google Scholar
Conti, M., Andersen, C.B., Richard, F., Mehats, C., Chun, S-Y., Horner, K., Jin, C. & Tsafriri, A. (2002). Role of cyclic nucleotide signalling in oocyte maturation. Mol. Cell. Endocrinol. 187, 153–9.Google Scholar
Das, D., Khan, P.P. & Maitra, S. (2013). Participation of PI3-kinase/Akt signalling in insulin stimulation of p34cdc2 activation in zebrafish oocyte: Phosphodiesterase 3 as a potential downstream target. Mol. Cell. Endocrinol. 374, 46–55.CrossRefGoogle ScholarPubMed
Dasgupta, S., Basu, D., Ravi Kumar, L. & Bhattacharya, S. (2001). Insulin alone can lead to a withdrawal of meiotic arrest in the carp oocyte. J. Biosci. 26, 341–7.Google Scholar
Diss, D.A.G. & Greenstein, BD. (1991). Insulin receptors on Xenopus laevis oocytes: effects of injection of ob/ob mouse liver mRNA. J. Cell Sci. 100, 167–71.Google Scholar
El-Etr, M., Schordert-Slatkine, S. & Baulieu, E.E. (1979). Meiotic maturation in Xenopus laevis oocytes is initiated by insulin. Science 205, 1397–9.CrossRefGoogle ScholarPubMed
Giudice, L.C. (1992). Insulin-like growth factors and ovarian follicular development. Endocr. Rev. 13, 641–69.Google Scholar
Gutiérrez, J., Parrizas, M., Carneiro, N., Maestro, J.L., Maestro, M.A. & Planas, J. (1993). Insulin and IGF-I receptors and tyrosine kinase activity in carp ovaries: Changes with reproductive cycle. Fish. Physiol. Biochem. 11, 247–54.Google Scholar
Haider, S. & Baqri, S.S.R. (2000a). Cyclic AMP-mediated control of oocyte maturation in the catfish, Clarias batrachus (Bloch): effects of 17α,20β-dihydroxy-4-pregnen-3-one and phosphodiesterase inhibitors. Indian. J. Exp. Biol. 38, 967–73.Google Scholar
Haider, S. & Baqri, S.S.R. (2000b). β-Adrenoceptor antagonists reinitiate meiotic maturation in Clarias batrachus oocytes. Comp. Biochem. Physiol. Part A 126, 517–25.CrossRefGoogle ScholarPubMed
Haider, S. & Baqri, S.S.R. (2002). Role of cyclic AMP-dependent protein kinase in oocyte maturation of the catfish, Clarias batrachus. J. Exp. Zool. 292, 587–93.CrossRefGoogle ScholarPubMed
Haider, S. & Chaube, S.K. (1995). Changes in total cAMP levels during oocyte maturation in the catfish, Clarias batrachus. Comp. Biochem. Physiol. Part A 112, 379–85.CrossRefGoogle Scholar
Haider, S. & Chaube, S.K. (1996). The in vitro effects of forskolin, IBMX and cyanoketone on meiotic maturation in follicle-enclosed catfish (Clarias batrachus) oocytes. Comp. Biochem. Physiol. Part C 115, 117–23.Google Scholar
Hainaut, P., Kowalski, A., Giorgetti, S., Baron, V. & Van Obberghen, E. (1991). Insulin and insulin-like growth factor-1 (IGF-1) receptors in Xenopus laevis oocyte. Comparison with insulin receptors from liver and muscle. Biochem. J. 273, 673–8.Google Scholar
Han, S.J., Vaccari, S., Nedachi, T., Andersen, C.B., Kovacina, K.S., Roth, R.A. & Conti, M. (2006). Protein kinase B/Akt phosphorylation of PDE3A and its role in mammalian oocyte maturation. EMBO J. 25, 5716–25.CrossRefGoogle ScholarPubMed
Hirai, S, Goascogne, C.L. & Baulieu, E.E. (1983). Induction of germinal vesicle breakdown in Xenopus laevis oocytes: response of denuded oocytes to progesterone and insulin. Dev. Biol. 100, 214–21.CrossRefGoogle ScholarPubMed
Hirai, T., Yamashita, M., Yoshikuni, M., Tokomoto, T., Kajiura, H., Sakai, N. & Nagahama, Y. (1992). Isolation and characterization of goldfish cdk2, a cognate variant of the cell cycle regulator cdc2. Dev. Biol. 152, 113–20.Google Scholar
Ju, J.W., Bandyopadhyay, A., Im, W.B., Chung, J., Kwon, H.B. & Choi, H.S. (2002). Involvement of phosphatidylinositol 3 kinase in the progesterone-induced oocyte maturation in Rana dybowskii . Gen. Comp. Endocrinol. 126, 213–20.CrossRefGoogle ScholarPubMed
Kagawa, H., Kobayashi, M., Hasegawa, Y. & Aida, K. (1994). Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. Gen. Comp. Endocrinol. 95, 293–300.Google Scholar
Khan, P.P. & Maitra, S. (2013). Participation of cAMP-dependent protein kinase and MAP kinase pathways during Anabas testudineus oocyte maturation. Gen. Comp. Endocrinol. 181, 88–97.Google Scholar
King, V.W., Thomas, P. & Sullivan, C.V. (1994). Hormonal regulation of final maturation of striped bass oocytes in vitro . Gen. Comp. Endocrinol. 96, 223–33.CrossRefGoogle ScholarPubMed
Lessman, C.A. (1985). Effect of insulin on meiosis reinitiation induced in vitro by three progestogens in oocytes of the goldfish (Carassius auratus). Dev. Biol. 107, 259–63.Google Scholar
Leung, P.C. & Steele, G.L. (1992) Intracellular signalling in the gonads. Endocr. Rev. 13, 476–98.Google Scholar
Liu, X.J., Sorisky, A. & Pawson, T. (1995). Molecular cloning of an amphibian insulin receptor substrate 1-like cDNA and involvement of phosphatidylinositol 3 kinase in insulin-induced Xenopus oocyte maturation. Mol. Cell. Biol. 15, 3563–70.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.E. & Randall, R.J. (1951). Protein measurement with folin phenol reagent. J. Biol. Chem. 193, 265–75.Google Scholar
Maestro, M.A., Mendez, E., Pairrizas, M. & Gutierrez, J. (1997). Characterization of insulin and insulin-like growth factor-I ovarian receptors during the reproductive cycle of Carp (Cyprinus carpio). Biol. Reprod. 56, 1126–32.CrossRefGoogle ScholarPubMed
Maitra, S., Das, D., Ghosh, P., Hajra, S., Roy, S.S. & Bhattacharya, S. (2014). High cAMP attenuation of insulin-stimulated meiotic G2-M1 transition in zebrafish oocytes: Interaction between the cAMP-dependent protein kinase (PKA) and the MAPK3/1 pathways. Mol. Cell. Endocrinol. 393, 109–19.Google Scholar
Maller, J.L. & Koontz, J.W. (1981). A study of the induction of cell division in amphibian oocytes by insulin. Dev. Biol. 84, 309–16.Google Scholar
Mishra, A. & Joy, K.P. (2006). 2-hydroxyestradiol-17β-induced oocyte maturation: involvement of cAMP–protein kinase A and okadaic acid-sensitive protein phosphatases, and their interplay in oocyte maturation in the catfish Heteropneustes fossilis . J. Exp. Biol. 209, 2567–75.Google Scholar
Mood, K., Bong, Y.S., Lee, H.S., Ishimura, A. & Daar, I.O. (2004). Contribution of JNK, Mek, Mos and PI-3K signalling to GVBD in Xenopus oocytes. Cell. Signal. 16, 631–42.CrossRefGoogle ScholarPubMed
Moore, M.J., Kanter, J.R., Jones, K.C. & Taylor, S.S. (2002). Phosphorylation of the catalytic subunit of protein kinase A. Autophosphorylation versus phosphorylation by phosphoinositide-dependent kinase-1. J. Biol. Chem. 277, 47878–84.Google Scholar
Mukherjee, D., Mukherjee, D., Sen, U., Paul, S. & Bhattacharyya, S.P. (2006). In vitro effects of insulin-like growth factors and insulin on oocyte maturation and maturation-inducing steroid production in ovarian follicles of common carp, Cyprinus carpio. Comp. Biochem. Physiol. Part A 144, 63–77.CrossRefGoogle ScholarPubMed
Nagahama, Y. (1997). 17α,20β-dihydroxy-4-pregnen-3-one, a maturation inducing hormone in fish oocytes: mechanism of synthesis and action. Steroids. 62, 190–6.CrossRefGoogle Scholar
Nagahama, Y. & Yamashita, M. (2008). Regulation of oocyte maturation in fish. Dev. Growth. Differ. 50, S195–219.Google Scholar
Nagahama, Y., Young, G. & Adachi, S. (1985). Effect of actinomycin D and cycloheximide on gonadotropin-induced 17α,20β-dihydroxy-4-pregnen-3-one production by intact follicles and granulosa cells of the amago salmon, Oncorhynchus rhodurus. Dev. Growth. Differ. 27, 213–21.Google Scholar
Nath, P. & Maitra, S. (2001). Role of two plasma vitellogenins from Indian Major Carp (Cirrhinus mrigala) in catfish (Clarias batrachus) vitellogenesis. Gen. Comp. Endocrinol. 124, 30–44.Google Scholar
Negatu, Z., Hsiao, S.M. & Wallace, R.A. (1998). Effects of insulin-like growth factor-I on final oocyte maturation and steroid production in Fundulus heteroclitus . Fish. Physiol. Biochem. 19, 13–21.CrossRefGoogle Scholar
Nelson, S.N. & Van Der Kraak, G. (2010). The role of the insulin-like growth factor (IGF) system in zebrafish (Danio rerio) ovarian development. Gen. Comp. Endocrinol. 168, 103–10.Google Scholar
Pace, M.C. & Thomas, P. (2005). Steroid-induced oocyte maturation in Atlantic Croaker (Micropogonias undulatus) is dependent on activation of the phosphatidylinositol 3-kinase/Akt signal transduction pathway. Biol. Reprod. 73, 988–96.Google Scholar
Patiño, R. & Kagawa, H. (1999). Regulation of gap junctions and oocyte maturational competence by gonadotropin and insulin-like growth factor-I in ovarian follicles of red seabream. Gen. Comp. Endocrinol. 115, 454–62.Google Scholar
Peyton, C. & Thomas, P. (2011). Involvement of epidermal growth factor receptor signalling in estrogen inhibition of oocyte maturation mediated through the G-protein coupled estrogen receptor (GPER) in zebrafish (Danio rerio). Biol. Reprod. 85, 42–50.Google Scholar
Picha, M.E., Shi, B. & Thomas, P. (2012). Dual role of IGF-II in oocyte maturation in southern flounder Paralichthys lethostigma: up-regulation of mPRα and resumption of meiosis. Gen. Comp. Endocrinol. 177, 220–30.Google Scholar
Poretsky, L. & Kalin, M.F. (1987). The gonadotropic function of insulin. Endocr. Rev. 8, 132–41.Google Scholar
Poretsky, L., Cataldo, N.A., Rosenwaks, Z. & Giudice, L.C. (1999). The insulin-related ovarian regulatory system in health and disease. Endocr. Rev. 20, 535–82.Google Scholar
Reinecke, M. (2010). Insulin-like growth factors and fish reproduction. Biol. Reprod. 82, 656–61.Google Scholar
Sadler, K.C. & Ruderman, J.V. (1998). Components of the signalling pathway linking the 1-methyladenine receptor to MPF activation and maturation in starfish oocytes. Dev. Biol. 197, 25–38.Google Scholar
Schmitt, A. & Nebreda, A.R. (2002). Signalling pathways in oocyte maturation. J. Cell. Sci. 115, 2457–9.Google Scholar
Srivastava, R.K. & Van Der Kraak, G. (1994). Insulin as an amplifier of gonadotropin action on steroid production: mechanism and sites of action in Goldfish prematurational full grown ovarian follicles. Gen. Comp. Endocrinol. 95, 60–70.Google Scholar
Trant, J.M. & Thomas, P. (1989). Isolation of a novel maturation inducing steroid produced in vitro by ovaries of Atlantic croaker. Gen. Comp. Endocrinol. 75, 397–404.Google Scholar
Tsafriri, A., Chun, S.Y., Zhang, R., Hsueh, A.J.W. & Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393–402.Google Scholar
Tyler, C.R., Santos, E.M. & Prat, F. (1999). Unscrambling the egg: cellular biochemical molecular and endocrine advances in oogenesis. In Proceedings of the 6th International Symposium on the Reproductive Physiology of Fish (eds Norberg, B., Kjesbu, O.S., Taranger, G.L., Andersson, E. & Stefansson, S.O.), pp. 273–80. Bergen: Institute of Marine Research and University of Bergen.Google Scholar
Van Der Kraak, G. & Wade, M.G. (1994). A comparison of signal transduction pathways mediating gonadotropin actions in vertebrates. In Perspectives in Comparative Endocrinology (eds Davey, K.G., Tobe, S.S. & Peter, R.E.), pp. 59–63. Toronto, Canada: National Research Council of Canada.Google Scholar
Weber, G.M. & Sullivan, C.V. (2000). Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol. Reprod. 63, 1049–57.Google Scholar
Weber, G.M. & Sullivan, C.V. (2001). In vitro hormone induction of final oocyte maturation in striped bass (Morone saxatalis) follicles is inhibited by blockers of phosphatidylinositol 3-kinase activity. Comp. Biochem. Physiol. Part B 129, 467–73.Google Scholar
Weber, G.M. & Sullivan, C.V. (2005). Insulin-like growth factor-I induces oocyte maturational competence but not meiotic resumption in White Bass (Morone chrysops) follicles in vitro: evidence for rapid evolution of insulin-like growth factor action. Biol. Reprod. 72, 1177–86.Google Scholar
Weber, G.M., Moore, A.B. & Sullivan, C.V. (2007). In vitro actions of insulin-like growth factor-I on ovarian follicle maturation in white perch (Morone Americana). Gen. Comp. Endocrinol. 151, 180–7.Google Scholar
Yoshikuni, M. & Nagahama, Y. (1994). Involvement of an inhibitory G-protein in the signal transduction pathway of maturation-inducing hormone (17α,20β-dihydroxy-4-pregnen-3-one) action in rainbow trout (Oncorhynchus mykiss) oocytes. Dev. Biol. 16, 615–22.Google Scholar
Zhu, Y., Rice, C.D., Pang, Y., Pace, M. & Thomas, P. (2003). Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. Proc. Natl. Acad. Sci. USA 100, 2231–6.Google Scholar