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Role of cyclic AMP in the maturation of Ciona intestinalis oocytes

Published online by Cambridge University Press:  02 September 2010

Francesco Silvestre ,
Alessandra Gallo ,
Annunziata Cuomo ,
Tiziana Covino  and
Elisabetta Tosti
Francesco Silvestre
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy
Alessandra Gallo
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy
Annunziata Cuomo
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy
Tiziana Covino
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy
Elisabetta Tosti*
Affiliation:
Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy.
*
All correspondence to: Elisabetta Tosti, Animal Physiology and Evolution Laboratory, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121–Naples, Italy. Tel: +39 081 5833288. Fax: +39 081 7641355. e-mail: tosti@szn.it
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Summary

Immature oocytes are arrested at prophase I of the meiotic process and maturation onset is indicated by oocyte nuclear disassembly (germinal vesicle breakdown or GVBD). Signaling pathways that elevate intracellular cyclic AMP (cAMP) may either prevent or induce oocyte maturation depending on the species. In some marine invertebrates and, in particular, in ascidian oocytes, cAMP triggers GVBD rather than blocking it. In this paper, we tested different cAMP elevators in fully grown oocytes at the germinal vesicle stage (GV) of the ascidian Ciona intestinalis. We demonstrated that through the activation of adenylate cyclase or the inhibition and phosphodiesterases the oocyte remained at the GV stage. This effect was reversible as the GV-arrested oocytes, rinsed and incubated in sea water, are able to undergo spontaneous maturation and extrusion of follicle cells. In addition, oocytes acquire the ability to be fertilized and start early development. However, morphology of follicle cells, embryos and larvae from in vitro matured oocytes showed different morphology from those derived from in vivo mature oocytes. The role and the transduction mechanism of cAMP in the regulation of oocyte maturation were discussed. Finally, we indicated a variation of biological mechanisms present in the ascidian species; moreover, we sustain evidence proving that tunicates share some biological mechanisms with vertebrates. This information provided new hints on the importance of ascidians in the evolution of chordates.

Keywords

AscidianscAMPCiona intestinalisGVBDOocyte maturation
Type
Research Article
Information
Zygote , Volume 19 , Issue 4 , November 2011 , pp. 365 - 371
Copyright
Copyright © Cambridge University Press 2010

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References

Aoyama, M., Kawada, T., Fujie, M., Hotta, K., Sakai, T., Sekiguchi, T., Oka, K., Satoh, N. & Satake, H. (2008). A novel biological role of tachykinins as an up-regulator of oocyte growth: identification of an evolutionary origin of tachykininergic functions in the ovary of the ascidian, Ciona intestinalis. Endocrinology 149, 4346–56.CrossRefGoogle ScholarPubMed
Chen, J. & Downs, S.M. (2008). AMP-activated protein kinase is involved in hormone-induced mouse oocyte meiotic maturation in vitro. Dev. Biol. 313, 47–57.CrossRefGoogle ScholarPubMed
Chen, J., Chi, M.M., Moley, K.H. & Downs, S.M. (2009). cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138, 759–70.CrossRefGoogle ScholarPubMed
Conti, M., Andersen, C.B., Richard, F.J., Shitsukawa, K. & Tsafriri, A. (1998). Role of cyclic nucleotide phosphodiesterases in resumption of meiosis. Mol. Cell. Endocrinol. 145, 9–14.CrossRefGoogle ScholarPubMed
Cuomo, A., Silvestre, F., De Santis, R. & Tosti, E. (2006). Ca2+ and Na+ current patterns during oocyte maturation, fertilization and early developmental stages of Ciona intestinalis. Mol. Reprod. Dev. 73, 501–11.CrossRefGoogle ScholarPubMed
Dale, B. & Elder, K. (1997). In vitro fertilization. Cambridge: Cambridge University Press.Google Scholar
Deguchi, R. & Osanai, K. (1994). Repetitive intracellular Ca2+ increases at fertilization and the role of Ca2+ in meiosis reinitiation from the first metaphase in oocytes of marine bivalve. Dev. Biol. 163, 162–74.CrossRefGoogle Scholar
Deguchi, R. & Morisawa, M. (2003). External Ca2+ is predominantly used for cytoplasmic and nuclear Ca2+ increases in fertilized oocytes of the marine bivalve Mactra chinensis. J. Cell. Sci. 116, 367–76.CrossRefGoogle ScholarPubMed
Dekel, N., Galiani, D. & Sherlizy, I. (1988). Dissociation between inhibitory and the stimulatory action of cAMP on maturation of rat oocytes. Mol. Cell. Endocrinol. 56, 115–21.CrossRefGoogle ScholarPubMed
Delsuc, F., Brinkmann, H., Chrout, D. & Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965–8.CrossRefGoogle Scholar
Downs, S.M. & Chen, J. (2006). Induction of meiotic maturation in mouse oocytes by adenosine analogs. Mol. Reprod. Dev. 73, 1159–68.CrossRefGoogle ScholarPubMed
Downs, S.M., Daniel, S.A., Bornslaeger, E.A., Hoppe, P.C. & Eppig, J.J. (1989). Maintenance of meiotic arrest in mouse oocytes by purines: modulation of cAMP levels and cAMP phosphodiesterase activity. Gamete Res. 23, 323–34.CrossRefGoogle ScholarPubMed
Dubè, F. (1992). Thapsigargin induces meiotic maturation in surf clam oocytes. Bioch. Biophys. Res. Comm. 189, 79–84.CrossRefGoogle ScholarPubMed
Ducibella, T.A., Anderson, D.F., Alberini, F., Aalberg, J. & Rangarajan, S. (1988). Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during maturation. Dev. Biol. 130, 184–97.CrossRefGoogle Scholar
Edwards, R.G. (1965). Maturation in vitro of mouse, sheep, cow, pig, rhesus monkey and human ovarian oocytes. Nature 208, 349–51.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1989). The participation of cyclic adenosine monophosphate (cAMP) in the regulation of meiotic maturation of oocytes in the laboratory mouse. J. Reprod. Fertil. Suppl. 38, 3–8.Google ScholarPubMed
Eppig, J.J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. Bioessays, 13, 569–74.CrossRefGoogle ScholarPubMed
Eppig, J.J., Freter, R.R., Ward-Bailey, P.F. & Schultz, R.M. (1983). Inhibition of oocyte maturation in the mouse: participation of cAMP, steroid hormones, and a putative maturation-inhibitory factor. Dev. Biol. 100, 39–49.CrossRefGoogle Scholar
Foote, W.D. & Thibault, C. (1969). Recherches expérimentales sur la maturation in vitro des ovocytes de truie et de veau. Ann. Biol. Anim. Bioch. Biophys. 9, 329–49.CrossRefGoogle Scholar
Freeman, G. & Ridgway, E.B. (1988). The role of cAMP in oocyte maturation and the role of the germinal vesicle contents in mediating maturation and subsequent developmental events in hydrozoans. Roux. Arch. Dev. Biol. 197, 197–211.CrossRefGoogle ScholarPubMed
Gilchrist, R. & Thompson, J.G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6–15.CrossRefGoogle ScholarPubMed
Guerrier, P., Leclerc-David, C. & Moreau, M. (1993). Evidence for the involvement of internal calcium stores during serotonin-induced meiosis reinitiation in oocytes of the bivalve mollusc Ruditapes philippinarum. Dev. Biol. 159, 474–84.CrossRefGoogle ScholarPubMed
Homa, S.T. (1995). Calcium and meiotic maturation of the mammalian oocyte. Mol. Repr. Dev. 40, 122–34.CrossRefGoogle ScholarPubMed
Kanatani, H. (1983). Nature and action of the mediators inducing maturation of the starfish oocyte. Ciba Found Symp. 98, 159–70.Google ScholarPubMed
Kren, R., Ogushi, S. & Miyano, T. (2004). Effect of caffeine on meiotic maturation of porcine oocytes. Zygote 12, 31–8.CrossRefGoogle ScholarPubMed
Lambert, C. (2008). Signaling pathways in ascidian oocyte maturation: the role of cyclic AMP and follicle cells in germinal vesicle breakdown. Dev. Growth Differ. 50, 181–8.CrossRefGoogle ScholarPubMed
Masui, Y. (1996). A quest for cytoplasmic factors that control the cell cycle. Prog. Cell Cycle Res. 2, 1–13.Google ScholarPubMed
Mattioli, M. & Barboni, B. (2000). Signal transduction mechanism for LH in the cumulus–oocyte complex. Mol. Cell. Endocrinol. 161, 19–23.CrossRefGoogle ScholarPubMed
Mehlmann, L.M. (2005). Stops and starts in mammalian oocytes: recent advances in understanding the regulation of meiotic arrest and oocyte maturation. Reproduction 130, 791–9.CrossRefGoogle ScholarPubMed
Mehlmann, L.M., Saeki, Y., Tanaka, S., Brennan, T.J., Evsikov, A.V., Pendola, F.L., Knowles, B.B., Eppig, J.J. & Jaffe, L.A. (2004). The Gs-linked receptor GPR3 maintains meiotic arrest in mammalian oocytes. Science 306, 1947–50.CrossRefGoogle ScholarPubMed
Mita, M. (2000). 1-Methyiladenine: a starfish oocyte maturation-inducing substance. Zygote 8, S9–11.CrossRefGoogle ScholarPubMed
Monroy, A. (1985). Processes controlling sperm–egg fusion. Eur. J. Biochem. 152, 51–56.CrossRefGoogle ScholarPubMed
Moor, R.M., Osborne, J.C., Cran, D.G. & Walters, D.E. (1981). Selective effect of gonadotropins on cell coupling, nuclear maturation, and protein synthesis in mammalian oocytes. J. Embr. Exp. Morph. 61, 347–65.Google ScholarPubMed
Nogueira, D., Albano, C., Adriaenssens, T., Cortvrindt, R., Bourgain, C., Devroey, P. & Smitz, J. (2003). Human oocytes reversibly arrested in prophase I by phosphodiesterase type 3 inhibitor in vitro. Biol. Reprod. 69, 1042–52.CrossRefGoogle ScholarPubMed
O'Donnel, J., Hill, J. & Gross, D.J. (2004). Epidermal growth factor activates cytosolic Ca++ elevations and subsequent membrane permeabilization in mouse cumulus–oocyte complexes. Reproduction 127, 207–20.CrossRefGoogle Scholar
Ozawa, M., Nagai, T., Somfai, T., Nakai, M., Maedomari, N., Fahrudin, M., Karja, N.W.K., Kaneko, H., Noguchi, J., Ohnuma, K., Yoshimi, N., Miyazaki, H. & Kikuchi, K. (2008). Comparison between effects of 3-isobutyl-1-methylxanthine and FSH on gap junctional communication, LH-receptor expression, and meiotic maturation of cumulus–oocyte complexes in pigs. Mol. Reprod. Dev. 75, 857–66.CrossRefGoogle ScholarPubMed
Park, J.Y., Su, Y.Q., Ariga, M., Law, E., Jin, S.L. & Conti, M. (2004). EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303, 682–4.CrossRefGoogle ScholarPubMed
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and in vitro. Dev. Biol. 108, 191–202.CrossRefGoogle ScholarPubMed
Richard, F.J. (2007). Regulation of meiotic maturation. J. Animal. Sci. 85, E4–6.CrossRefGoogle ScholarPubMed
Sakairi, K. & Shirai, H. (1991). Possible MS production by follicle cells in spontaneous oocyte maturation of the ascidian. Halocynthia roretzi. Dev. Growth. Differ. 33, 155–62.CrossRefGoogle Scholar
Sánchez-Toranzo, G., Oterino, J., Zelarayàn, L., Bonilla, F. & Bühler, M.I. (2007). Spontaneous and LH-induced maturation in Bufo arenarum oocytes: importance of gap junctions. Zygote 15, 65–80.CrossRefGoogle Scholar
SAS. (1988). User's guide/STAT (Release 6.03 edition). Cary, NC: Statistical Analysis System Institute.Google Scholar
Schorderet-Slatkine, S. (1972). Action of progesterone and related steroids on oocyte maturation in Xenopus laevis. An in vitro study. Cell. Differ. 1, 179–89.CrossRefGoogle ScholarPubMed
Silvestre, F., Cuomo, A. & Tosti, E. (2009). Ion current activity and molecules modulating maturation and growth stages of ascidian (Ciona intestinalis) oocytes. Mol. Reprod. Dev. 76, 1084–93.CrossRefGoogle ScholarPubMed
Stricker, S.A. & Smythe, T.L. (2006). Differing mechanisms of cAMP versus seawater-induced oocyte maturation in marine nemertean worms. I. The roles of serine/threonine kinases and phosphatases. Mol. Reprod. Dev. 73, 1578–90.CrossRefGoogle Scholar
Stricker, S.A., Swiderek, L. & Nguyen, T. (2010) Stimulators of AMP-activated kinase (AMPK) inhibit seawater—but not cAMP-induced oocyte maturation in a marine worm: implications for interactions between cAMP and AMPK signaling. Mol. Reprod. Dev. 77, 497–510.CrossRefGoogle ScholarPubMed
Sun, Q.Y., Miao, Y.L. & Schatten, H. (2009) Towards a new understanding on the regulation of mammalian oocyte meiosis resumption. Cell Cycle 8, 2741–7.CrossRefGoogle ScholarPubMed
Takeda, N., Kyozuka, K. & Deguchi, R. (2006). Increase in intracellular cAMP is a prerequisite signal for initiation of physiological oocyte meiotic maturation in the hydrozoan Cytaeis uchidae. Dev. Biol. 298, 248–58.CrossRefGoogle ScholarPubMed
Thomas, R., Armstrong, D. & Gilchrist, R. (2004). Bovine cumulus cell–oocyte gap junctions communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3′,5′-monophosphate levels. Biol. Reprod. 70, 548–56.CrossRefGoogle Scholar
Tosti, E. (2006). Calcium ion currents mediating oocyte maturation events. Reprod. Biol. Endocrinol. 4, 26.CrossRefGoogle ScholarPubMed
Tripathi, A., Kumar, K.V. & Chaube, S.K. (2010). Meiotic cell cycle arrest in mammalian oocytes. J. Cell Physiol. 223, 592–600.CrossRefGoogle ScholarPubMed
Tsafriri, A. (1979). Mammalian oocyte maturation: model systems and their physiological relevance. Adv. Exp. Med. Biol. 112, 269–81.CrossRefGoogle ScholarPubMed
Tsafriri, A. & Dekel, N. (2010). Intra- and intercellular molecular mechanisms in regulation of meiosis in murid rodents. In Oocyte maturation and fertilization: a long history for a short event (eds. Tosti, E. & Boni, R.), in press. Karachi: Bentham Scientific Publishers.Google Scholar
Vaccari, S., Corner, K., Mehlmann, L.M. & Conti, M. (2008). Generation of mouse oocytes defective in cAMP synthesis and degradation: endogenous cyclic AMP is essential for meiotic arrest. Dev. Biol. 316, 124–34.CrossRefGoogle ScholarPubMed
Voronina, E. & Wessel, G.M. (2003). The regulation of oocyte maturation. Curr. Top. Dev. Biol. 58, 53–110.CrossRefGoogle ScholarPubMed
Wessel, G.M., Brooks, J.M., Green, E., Haley, S., Voronina, E., Wong, J., Zaydfudim, V. & Conner, S. (2001). The biology of cortical granules. Int. Rev. Cytol. 209, 117–206.CrossRefGoogle ScholarPubMed
Whitaker, M. (1996). Control of meiotic arrest. Rev. Repr. 1, 127–35.CrossRefGoogle ScholarPubMed
Whitaker, M. & Patel, R. (1990). Calcium and cell cycle control. Development 108, 525–42.CrossRefGoogle ScholarPubMed
Yamashita, M. (1988). Involvement of cAMP in initiating maturation of the brittle star Amphipholis kochii oocytes: induction of oocyte maturation by inhibitors of cyclic nucleotide phosphodiesterases and activators of adenylate cyclase. Dev. Biol. 125, 109–14.CrossRefGoogle Scholar
Yi, J.H., Lefevre, L., Gagnon, C., Anctil, M. & Dube, F. (2002). Increase of cAMP upon release from prophase arrest in surf clam oocytes. J. Cell. Sci. 115, 311–20.CrossRefGoogle ScholarPubMed