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Role of arachidonic acid cascade in Rhinella arenarum oocyte maturation

Published online by Cambridge University Press:  25 June 2014

Maria Eugenia Ortiz
Affiliation:
Centro de Referencia para Lactobacilos (CERELA)-CONICET, Chacabuco 145, Tucumán, Argentina.
Ana Josefina Arias-Torres
Affiliation:
Instituto de Biología, Facultad de Bioqca., Qca. y Farmacia, UNT. INSIBIO-CONICET, Chacabuco 461, Tucumán, Argentina.
Liliana Isabel Zelarayán*
Affiliation:
Instituto de Biología, Facultad de Bioqca., Qca. y Farmacia, UNT. INSIBIO-CONICET, Chacabuco 461, 4000 San Miguel de Tucumán, Tucumán, Argentina.
*
All correspondence to: Liliana Isabel Zelarayán. Instituto de Biología, Facultad de Bioqca., Qca. y Farmacia, UNT. INSIBIO-CONICET, Chacabuco 461, 4000 San Miguel de Tucumán, Tucumán, Argentina. Tel: +549 381 4247752 x7093. Fax: +549 381 4247752 x7004. e-mail: [email protected]

Summary

There are no studies that document the production of prostaglandins (PGs) or their role in Rhinella arenarum oocyte maturation. In this study, we analysed the effect of arachidonic acid (AA) and prostaglandins (PGs) on maturation, activation and pronuclear formation in R. arenarum oocytes. Our results demonstrated that AA was capable of inducing maturation in time-dependent and dose-dependent manner. Arachidonic acid-induced maturation was inhibited by indomethacin. PGs from AA hydrolysis, such as prostaglandin F (PGF) and, to a lesser extent, PGE2, induced meiosis resumption. Oocyte maturation in response to PGF was similar to that produced by progesterone (P4). Oocyte response to PGE1 was scarce. Rhinella arenarum oocyte PGF-induced maturation showed seasonal variation. From February to June, oocytes presented low sensitivity to PGF. In following periods, this response increased until a maximum was reached during October to January, a close temporal correlation with oocyte response to P4 being observed. The effect of PGF on maturation was verified by analysing the capacity of oocytes to activate and form pronuclei after being injected with homologous sperm. The cytological analysis of activated oocytes demonstrated the absence of cortical granules in oocytes, suggesting that PGF induces germinal vesicle breakdown (GVBD) and meiosis resumption up to metaphase II. In turn, oocytes matured by the action of PGF were able to form pronuclei after fertilization in a similar way to oocyte maturated by P4. In microinjection of mature cytoplasm experiments, the transformation of pre-maturation promoting factor (pre-MPF) to MPF was observed when oocytes were treated with PGF. In summary, our results illustrated the participation of the AA cascade and its metabolites in maturation, activation and pronuclei formation in R. arenarum.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2014 

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References

Albertini, D.F. & Carabatsos, M.J. (1998). Comparative aspects of meiotic cell cycle control in mammals. J. Mol. Med. 76, 795–9.CrossRefGoogle ScholarPubMed
Bonilla, F., Ajmat, M.T., Sánchez Toranzo, G., Zelarayán, L.I., Oterino, J. & Bühler, M.I. (2008). Activation of amphibian oocyte by sperm extracts. Zygote 16, 303–8.CrossRefGoogle ScholarPubMed
Brunet, S. & Maro, B. (2005). Cytoskeleton and cell cycle control during meiotic maturation of the mouse oocyte: integrating time and space. Reproduction 130, 801–11.CrossRefGoogle ScholarPubMed
Bühler, M.I. & Petrino, T. (1983). Simplified technique for the observation of asters in amphibian eggs stratified by centrifugation. Mikroskopie 40, 344–6.Google ScholarPubMed
Bühler, M.I., Petrino, T. & Legname, A.H. (1987). Sperm nuclear transformation and aster formation related to metabolic behaviour in amphibian eggs. Dev. Growth Differ. 29, 177–84.CrossRefGoogle ScholarPubMed
Buschiazzo, J. & Alonso, T.S. (2005). Effect of meiotic maturation on yolk platelet lipids from Bufo arenarum oocytes. J. Exp. Zool. 303A (9), 813–22.CrossRefGoogle Scholar
Downs, S.M. & Longo, F.J. (1983). Prostaglandins and preovulatory follicular maturation in mice. J. Exp. Zool. 228, 99108.CrossRefGoogle ScholarPubMed
Grosser, T., Yusuff, S., Cheskis, E., Pack, M.A. & FitzGerald, G.A. (2002). Developmental expression of functional cyclooxygenases in zebrafish. Proc. Natl. Acad. Sci. USA. 99, 8418–23.CrossRefGoogle ScholarPubMed
Kwon, H.B., Lin, Y.P., Choi, M.J. & Ahn, R.S. (1989). Spontaneous maturation of follicular oocytes in Rana dybowskii in vitro: seasonal influences, progesterone production and involvement of cAMP. J. Exp. Zool. 252, 190–9.CrossRefGoogle ScholarPubMed
Lister, A.L. & Van Der Kraak, G. (2008). An investigation into the role of prostaglandins in zebrafish oocyte maturation and ovulation. Gen. Comp. Endocrinol. 159, 4657.CrossRefGoogle ScholarPubMed
Liu, X.S., Ma, C., Hamam, A.W. & Liu, X.J. (2005). Transcription-dependent and transcription-independent functions of the classical progesterone receptor in Xenopus ovaries. Dev. Biol. 283, 180–90.CrossRefGoogle ScholarPubMed
Maller, J.L. (2001). The elusive progesterone receptor in Xenopus oocytes. Proc. Nat. Acad. Sci. USA 98 (1), 810.CrossRefGoogle ScholarPubMed
Manes, M.E. & Nieto, O.L. (1983). A fast and reliable celloidin paraffin embedding technique for yolked amphibian embryos. Mikroskopie (Wien) 40, 341–3.Google ScholarPubMed
Medina, M., Ramos, I., Crespo, C.A., Gonzalez-Calvar, S. & Fernandez, S.N. (2004). Changes in serum sex steroid levels throughout the reproductive cycle of Bufo arenarum females. Gen. Comp. Endocrinol. 136, 143–51.CrossRefGoogle ScholarPubMed
Meijer, L., Guerrier, P. & Maclouf, J. (1984). Arachidonic acid, 12- and 15-hydroxyeicosatetraenoic acids, eicosapentaenoic acid, and phospholipase A2 induce starfish oocyte maturation. Dev. Biol. 106, 368–78.CrossRefGoogle ScholarPubMed
Meijer, L., Maclouf, J. & Bryant, R.W. (1986). Contrasting effects of fatty acids on oocyte maturation in several starfish species. Prostaglandins Leukot. Med. 23, 179184.CrossRefGoogle ScholarPubMed
Melien, O., Thoresen, G.H., Sandnes, D., Ostby, E. & Christoffersen, T. (1998). Activation of p42/p44 mitogen-activated protein kinase by angiotensin II, vasopressin, norepinephrine, and prostaglandin F2a in hepatocytes is sustained, and like the effect of epidermal growth factor, mediated through pertussis toxin-sensitive mechanisms. J. Cell Physiol. 175 (3), 348–58.3.0.CO;2-1>CrossRefGoogle ScholarPubMed
Mercure, F. & Van Der Kraak, G. (1995). Inhibition of gonadotropin-stimulated ovarian steroid production by polyunsaturated fatty acids in teleost fish. Lipids 30, 547–54.CrossRefGoogle ScholarPubMed
Morrill, G.A., Ma, G-Y. & Kostellow, A. (2000). Molecular species analysis of 1,2-diacylglycerol released in response to progesterone binding to the amphibian oocyte plasma membrane. Cell Signal. 12, 787–96.CrossRefGoogle Scholar
Murdoch, W.J. (1988). Disruption of cellular associations within the granulosal compartment of periovulatory ovine follicles: relationship to maturation of the oocyte and regulation by prostaglandins. Cell Tissue Res. 252, 459–62.CrossRefGoogle ScholarPubMed
Ortiz, M.E., Bühler, M.I. & Zelarayán, L.I. (2013). Involvement of PLA2, COX and LOX in Rhinella arenarum oocyte maturation. Zygote 27, 516–23.Google Scholar
Oterino, J., Sánchez Toranzo, G., Zelarayán, L. & Bühler, M.I. (1997). Polyspermy in Bufo arenarum oocytes matured in vitro. Zygote 5, 267–71.CrossRefGoogle ScholarPubMed
Oterino, J.M. (2003). Mecanismos celulares involucrados en el bloqueo de la polispermia en ovocitos de Bufo arenarum. Tesis doctoral. Facultad de Bioquímica, Química y Farmacia. UNT.Google Scholar
Patiño, R., Yoshizaki, G., Bolamba, D. & Thomas, P. (2003). Role of arachidonic acid and protein kinase C during maturation-inducing hormone-dependent meiotic resumption and ovulation in ovarian follicles of Atlantic croaker. Biol. Reprod. 68, 516–23.CrossRefGoogle ScholarPubMed
Sánchez Toranzo, G., Bonilla, F., Zelarayán, L., Oterino, J. & Bühler, M.I. (2006). Activation of maturation promoting factor in Bufo arenarum oocytes: injection of mature cytoplasm and germinal vesicle contents. Zygote 14, 305–16.CrossRefGoogle Scholar
Sena, J. & Liu, Z. (2008). Expression of cyclooxygenase genes and production of prostaglandins during ovulation in the ovarian follicles of Xenopus laevis. Gen. Comp. Endocrinol. 157, 165–73.CrossRefGoogle ScholarPubMed
Sirois, J., Sayasith, K., Brown, K.A., Stock, A.E., Bouchard, N. & Doré, M. (2004). Cyclooxygenase-2 and its role in ovulation: a 2004 account. Hum. Reprod. Update 10, 373–85.CrossRefGoogle ScholarPubMed
Sorbera, L.A., Asturiano, J.F. & Zanuy, S. (1998). A role for polyunsaturated fatty acids and prostaglandins in oocyte maturation in the sea bass (Dicentrarchus labrax). Ann. N. Y. Acad. Sci. 839, 535–8.CrossRefGoogle Scholar
Sorbera, L.A., Asturiano, J.F., Carrillo, M. & Zanuy, S. (2001). Effects of polyunsaturated fatty acids and prostaglandins on oocyte maturation in a marine teleost, the European sea bass (Dicentrarchus labrax). Biol. Reprod. 64, 382–9.CrossRefGoogle Scholar
Toranzo, G.S., Bonilla, F., Bühler, M.C. & Bühler, M.I. (2011). Participation of MAPK, PKA and PP2A in the regulation of MPF activity in Bufo arenarum oocytes. Zygote 19, 181–9.CrossRefGoogle ScholarPubMed
Törnquist, K., Ekokoski, E. & Forse, L. (1994) TRH-evoked entry of extracellular calcium in GH4C1 cells: possible importance of arachidonic acid metabolites. Mol. Cell. Endocrinol. 102 (1–2), 103–10.CrossRefGoogle ScholarPubMed
Valdéz Toledo, C.L. & Pisanó, A. (1980). Studies of oogenesis in Bufo arenarum. Reproduction 4, 315–30.Google ScholarPubMed
Van Der Kraak, G. & Chang, J.P. (1990). Arachidonic acid stimulates steroidogenesis in goldfish preovulatory ovarian follicles. Gen. Comp. Endocrinol. 77, 221–8.CrossRefGoogle ScholarPubMed
Zelarayán, L., Oterino, J., Sánchez Toranzo, G. & Bühler, M.I. (2004). The role of calcium in the nuclear maturation in Bufo arenarum oocytes. Zygote 12, 4956.CrossRefGoogle ScholarPubMed
Zelarayán, L.I., Ajmat, M.T., Bonilla, F. & Bühler, M.I. (2012). Involvement of G protein and purines in Rhinella arenarum oocyte maturation. Zygote 2, 110.Google Scholar
Zelarayán, L.I., Ajmat, M.T., Unías, L., Bonilla, F., Sánchez Toranzo, G. & Bühler, M.I. (2007). Cyclooxygenase participation on amphibian oocyte maturation. Biocell 31, 252.Google Scholar
Zelarayán, L.I., Oterino, J. & Bühler, M.I. (1995). Spontaneous maturation in Bufo arenarum oocytes: follicle wall involvment, respiratory activity and seasonal influences. J. Exp. Zool. 272, 356–62.CrossRefGoogle ScholarPubMed
Zelarayán, L.I., Oterino, J., Sánchez Toranzo, G. & Bühler, M.I. (2000). Involvement of purines and phosphoinositides in spontaneous and progesterone-induced nuclear maturation of Bufo arenarum oocytes. J. Exp. Zool. 287, 151–7.3.0.CO;2-S>CrossRefGoogle ScholarPubMed