Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T15:53:21.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Role of phospholipase A2 pathway in regulating activation of Bufo arenarum oocytes

Published online by Cambridge University Press:  02 February 2012

M.T. Ajmat ,
F. Bonilla ,
P.C. Hermosilla ,
L. Zelarayán  and
M.I. Bühler
M.T. Ajmat
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
F. Bonilla
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
P.C. Hermosilla
Affiliation:
Instituto de Biología Facultad de Bioquímica, Química y Farmacia Universidad Nacional de Tucumán, Argentina.
L. Zelarayán
Affiliation:
Instituto Superior de Investigaciones Biológicas (INSIBIO) Universidad Nacional de Tucumán Chacabuco 461 (4000) S.M. de Tucumán. Argentina.
M.I. Bühler*
Affiliation:
Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000- San Miguel de Tucumán, Argentina.
*
All correspondence to: Marta Bühler. Departamento de Biología del Desarrollo (INSIBIO), Chacabuco 461, 4000- San Miguel de Tucumán, Argentina. Fax: +54 381 4247752 (ext. 7004). e-mail: mbuhler@fbqf.unt.edu.ar
Get access Rights & Permissions [Opens in a new window]

Summary

Transient increases in the concentration of cytosolic Ca2+ are essential for triggering egg activation events. Increased Ca2+ results from its rapid release from intracellular stores, mainly mediated by one or both intracellular calcium channels: the inositol trisphosphate receptor (IP3R) and the ryanodine receptor (RyR). Several regulatory pathways that tailor the response of these channels to the specific cell type have been proposed. Among its many modulatory actions, calcium can serve as an activator of a cytosolic phospholipase A2 (cPLA2), which releases arachidonic acid from phospholipids of the endoplasmic reticulum as well as from the nuclear envelope. Previous studies have suggested that arachidonic acid and/or its metabolites were able to modulate the activity of several ion channels. Based on these findings, we have studied the participation of the phospholipase A2 (PLA2) pathway in the process of Bufo arenarum oocyte activation and the interrelation between any of its metabolites and the ion channels involved in the calcium release from the intracellular reservoirs at fertilization. We found that addition of both melittin, a potent PLA2 activator, and arachidonic acid, the main PLA2 reaction metabolite, was able to induce activation events in a bell-shaped manner. Differential regulation of IP3Rs and RyRs by arachidonic acid and its products could explain melittin and arachidonic acid behaviour in Bufo arenarum egg activation. The concerted action of arachidonic acid and/or its metabolites could provide controlled mobilization of calcium from intracellular reservoirs and useful tools for understanding calcium homeostasis in eggs that express both types of receptors.

Keywords

Bufo arenarumOocytes activationPhospholipase A2
Type
Research Article
Information
Zygote , Volume 21 , Issue 3 , August 2013 , pp. 214 - 220
Copyright
Copyright © Cambridge University Press 2012 

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

Abbott, A.L. & Ducibella, T. (2001). Calcium and the control of mammalian cortical granule exocytosis. Front. Biosci. 6, D792–806.CrossRefGoogle ScholarPubMed
Ajmat, M.T., Bonilla, F., Zelarayán, L., Oterino, J. & Bühler, M.I. (2010). Participation of inositol-trisphosphate and ryanodine receptors in Bufo arenarum oocyte activation. Zygote, 19, 181–9.Google ScholarPubMed
Albrieux, M., Sardet, C. & Villaz, M. (1997). The two intracellular Ca2+ release channels, ryanodine receptor and inositol 1,4,5-trisphosphate receptor, play different roles during fertilization in ascidians. Dev. Biol. 189, 174–85.CrossRefGoogle ScholarPubMed
Ayabe, T., Kopf, G.S. & Schultz, R.M. (1995). Regulation of mouse egg activation: presence of ryanodine receptors and effects of microinjected ryanodine and cyclic ADP ribose on uninseminated and inseminated eggs. Development 121, 2233–44.CrossRefGoogle ScholarPubMed
Balakier, H., Dziak, E., Sojecki, A., Librach, C., Michalak, M. & Opas, M. (2002). Calcium-binding proteins and calcium-release channels in human maturing oocytes, pronuclear zygotes and early preimplantation embryos. Hum. Reprod. 17, 2938–47.CrossRefGoogle ScholarPubMed
Clark, J.D., Lin, L.L., Kriz, R.W., Ramesha, C.S., Sultzman, L.A., Lin, A.Y., Milona, N. & Knopf, J.L. (1991). A novel arachidonic acid-selective cytosolic PLA2 contains a Ca2+-dependent translocation domain with homology to PKC and GAP. Cell 14, 65, 1043–51.CrossRefGoogle Scholar
Chen, W.Y., Ni, Y., Pan, Y.M., Shi, Q.X., Yuan, Y.Y., Chen, A.J., Mao, L.Z., Yu, S.Q. & Roldan, E.R. (2005). GABA, progesterone and zona pellucida activation of PLA2 and regulation by MEK-ERK1/2 during acrosomal exocytosis in guinea pig spermatozoa. FEBS Lett. 579, 4692–700.CrossRefGoogle ScholarPubMed
Ferguson, J.E. & Shen, S.S. (1984). Evidence of phospholipase A2 in the sea urchin egg: Its possible involvement in the cortical granule reaction. Gamete Res. 9, 329–38.CrossRefGoogle Scholar
Fissore, R.A. & Robl, J.M. (1993). Sperm, inositol trisphosphate and thimerosal-induced intracellular calcium elevations in rabbit eggs. Dev. Biol. 159, 122–30.CrossRefGoogle ScholarPubMed
Galione, A., Lee, H.C. & Busa, W.B. (1991). Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253, 1143–6.CrossRefGoogle Scholar
Galione, A., McDougall, A., Busa, W.B., Willmott, N., Gillot, I. & Whitaker, M. (1993a). Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science 261, 348–52.CrossRefGoogle ScholarPubMed
Galione, A., White, A., Willmott, N., Turner, M., Potter, B.V. & Watson, S.P. (1993b). cGMP mobilizes intracellular Ca2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis. Nature 365, 456–9.CrossRefGoogle ScholarPubMed
Herbert, M., Gillespie, J.I. & Murdoch, A.P. (1997). Development of calcium signalling mechanisms during maturation of human oocytes. Mol. Hum. Reprod. 3, 965–73.CrossRefGoogle ScholarPubMed
Horner, V.L. & Wolfner, M.F. (2008). Transitioning from egg to embryo: triggers and mechanisms of egg activation. Dev. Dynam. 237, 527–44.CrossRefGoogle ScholarPubMed
Kamata, Y., Mita, M., Fujiwara, A., Tojo, T., Takano, J., Ide, A. & Yasumasu, I. (1997). Probable participation of phospholipase A2 reaction in the process of fertilization-induced activation sea urchin eggs. Develop. Growth Differ. 39, 419–28.CrossRefGoogle ScholarPubMed
Keyser, D.O. & Alger, B.E. (1990). Arachidonic acid modulates hippocampal calcium current via protein kinase C and oxygen radicals. Neuron 5, 545–53.CrossRefGoogle ScholarPubMed
Kline, J.T. & Kline, D. (1994). Regulation of intracellular calcium in the mouse egg: evidence for inositol trisphosphate-induced calcium release, but not calcium-induced calcium release. Biol. Reprod. 50, 193–203.CrossRefGoogle Scholar
Lee, H.C., Aarhus, R. & Walseth, T.F. (1993). Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science 261, 352–5.CrossRefGoogle ScholarPubMed
Macháty, Z., Funahashi, H., Day, B.N. & Prather, R.S. (1997). Developmental changes in the intracellular Ca2+ release mechanisms in porcine oocytes. Biol. Reprod. 56, 921–30.CrossRefGoogle ScholarPubMed
Maruyama, Y. (1993). Control of inositol polyphosphate–mediated calcium mobilization by arachidonic acid in pancreatic acinar cells of rats. J. Physiol. 463, 729–46.CrossRefGoogle ScholarPubMed
McPherson, S.M., McPherson, P.S., Mathews, L., Campbell, K.P. & Longo, F.J. (1992). Cortical localization of a calcium release channel in sea urchin eggs. J Cell Biol. 116, 1111–21CrossRefGoogle ScholarPubMed
Nuccitelli, R. (1991). How do sperm activate eggs? Curr. Top. Dev. Biol. 25, 1–16.CrossRefGoogle ScholarPubMed
Nuccitelli, R., Yim, D.L. & Smart, T. (1993). The sperm-induced Ca2+ wave following fertilization of the Xenopus egg requires the production of Ins(1,4,5)P3. Dev Biol. 158, 200–12.CrossRefGoogle ScholarPubMed
Oterino, J, Sánchez Toranzo, G., Zelarayán, L., Valz-Gianinet, J.N. & Bühler, M.I (2001). Cortical granule exocytosis in Bufo arenarum oocytes matured in vitro. Zygote 9, 251–9.CrossRefGoogle ScholarPubMed
Petcoff, D.W., Holland, W.L. & Stith, B.J. (2008). Lipid levels in sperm, eggs and during fertilization in Xenopus laevis. J. Lipid Res. 49, 2365–78.CrossRefGoogle ScholarPubMed
Petit-Jacques, J. & Hartzell, H.C. (1996). Effect of arachidonic acid on the L-type calcium current in frog cardiac myocytes. J. Physiol. 493 (Pt 1), 67–81.CrossRefGoogle ScholarPubMed
Petr, J., Urbánková, D., Tománek, M., Rozinek, J. & Jílek, F. (2002). Activation of in vitro matured pig oocytes using activators of inositol triphosphate or ryanodine receptors Anim. Reprod. Sci. 70 (3–4), 235–49.CrossRefGoogle ScholarPubMed
Riffo, M.S. & Párraga, M. (1997). Role of phospholipase A2 in mammalian sperm-egg fusion: development of hamster oolemma fusibility by lysophosphatidylcholine. J. Exp. Zool. 279, 81–8.3.0.CO;2-Y>CrossRefGoogle ScholarPubMed
Roldan, E.R. & Shi, Q.X. (2007). Sperm phospholipases and acrosomal exocytosis. Front. Biosci. 12, 89–104.CrossRefGoogle ScholarPubMed
Rowles, S.J. & Gallacher, D.V. (1996). Ins(1,3,4,5)P4 is effective in mobilizing Ca2+ in mouse exocrine pancreatic acinar cells if phospholipase A2 is inhibited. Biochem. J. 319, 913–8.CrossRefGoogle ScholarPubMed
Runft, L.L., Jaffe, L.A. & Mehlmann, L.M. (2002). Egg activation at fertilization: where it all begins. Dev. Biol. 245, 237–54.CrossRefGoogle ScholarPubMed
Schultz, R.M. & Kopf, G.S. (1995). Molecular basis of mammalian egg activation. Curr. Top. Dev. Biol. 30, 21–62.CrossRefGoogle ScholarPubMed
Silver, R.B., Oblak, J.B., Jeun, G.S., Sung, J.J. & Dutta, T.C. (1994). Biol. Bull. 187, 242–4.CrossRefGoogle Scholar
Sousa, M., Barros, A. & Tesarik, J. (1996). The role of ryanodine-sensitive Ca2+ stores in the Ca2+ oscillation machine of human oocytes. Mol. Hum. Reprod. 2, 265–72.CrossRefGoogle ScholarPubMed
Stricker, S.A. (1999). Comparative biology of calcium signalling during fertilization and egg activation in animals. Dev. Biol. 211, 157–76.CrossRefGoogle ScholarPubMed
Swann, K. (1992). Different triggers for calcium oscillations in mouse eggs involve a ryanodine-sensitive calcium store. Biochem J. 287, 79–84.CrossRefGoogle ScholarPubMed
Striggow, F. & Erlich, B.E. (1997). Regulation of intracellular calcium release channel function by arachidonic acid and leukotriene B4. Biochem. Biophys. Res. Commun. 237, 413–7.CrossRefGoogle ScholarPubMed
Tesarik, J. (2002). Calcium signalling in human oocytes and embryos: two-store model revival. Hum. Reprod. 17, 2948–9.CrossRefGoogle ScholarPubMed
Whitaker, M. & Swann, K. (1993). Lighting the fuse at fertilization. Development 117, 1–12.CrossRefGoogle Scholar
Wang, L., White, K.L., Reed, W.A. & Campbell, K.D. (2005). Dynamic changes to the inositol 1,4,5-trisphosphate and ryanodine receptors during maturation of bovine oocytes Cloning Stem Cells 7, 306–20.CrossRefGoogle Scholar
Woolcott, O.O., Gustafsson, A.J., Dzabic, M., Pierro, C., Tedeschi, P., Sandgren, J., Bari, M.R., Nguyen, K.H., Bianchi, M., Rakonjac, M., Rådmark, O., Ostenson, C.G. & Islam, M.S. (2006). Arachidonic acid is a physiological activator of the ryanodine receptor in pancreatic beta-cells. Cell Calcium 39, 529–37.CrossRefGoogle ScholarPubMed
Yue, C., White, K.L., Reed, W.A. & Bunch, T.D. (1995). The existence of inositol 1,4,5-trisphosphate and ryanodine receptors in mature bovine oocytes. Development 121, 2645–54.CrossRefGoogle ScholarPubMed
Yue, C., White, K.L., Reed, W.A. & King, E. (1998). Localization and regulation of ryanodine receptor in bovine oocytes. Biol. Reprod. 58, 608–14.CrossRefGoogle ScholarPubMed