© The Rockefeller University Press,
0021-9525/1997//1303 $5.00
The Journal of Cell Biology, Volume 138, Number 6,
, 1997 1303-1311
Calcium Release at Fertilization in Starfish Eggs Is Mediated by Phospholipase C
David J. Carroll*,
Chodavarapu S. Ramarao*,
Lisa M. Mehlmann*,
Serge Roche
,
Mark Terasaki*, and
Laurinda A. Jaffe*
* Department of Physiology, University of Connecticut Health Center, Farmington, Connecticut 06032; and
Institut National de la Santé et de la Recherche Medicale CJF9207, Faculté de Pharmacie 15, F-34060 Montpellier, France
Although inositol trisphosphate (IP3) functions in releasing Ca2+ in eggs at fertilization, it is not known how fertilization activates the phospholipase C that produces IP3. To distinguish between a role for PLC
, which is activated when its two src homology-2 (SH2) domains bind to an activated tyrosine kinase, and PLCβ, which is activated by a G protein, we injected starfish eggs with a PLC
SH2 domain fusion protein that inhibits activation of PLC
. In these eggs, Ca2+ release at fertilization was delayed, or with a high concentration of protein and a low concentration of sperm, completely inhibited. The PLC
SH2 protein is a specific inhibitor of PLC
in the egg, since it did not inhibit PLCβ activation of Ca2+ release initiated by the serotonin 2c receptor, or activation of Ca2+ release by IP3 injection. Furthermore, injection of a PLC
SH2 domain protein mutated at its phosphotyrosine binding site, or the SH2 domains of another protein (the phosphatase SHP2), did not inhibit Ca2+ release at fertilization. These results indicate that during fertilization of starfish eggs, activation of phospholipase C
by an SH2 domain-mediated process stimulates the production of IP3 that causes intracellular Ca2+ release.
Abbreviations used in this paper: GST, glutathione-S-transferase; IP3, inositol trisphosphate; PLC, phospholipase C; PIP2, phosphatidylinositol 4,5-bisphosphate.
Address all correspondence to David J. Carroll or Laurinda A. Jaffe, Department of Physiology, University of Connecticut Health Center, Farmington, CT 06032. Tel.: (860) 679-2661. Fax: (860) 679-1661. E-mail: ljaffe{at}neuron.uchc.edu
D.J. Carroll's present address is Department of Molecular, Cellular, and Developmental Biology, University of California, Santa Barbara, CA 93106. e-mail: carroll{at}lifesci.lscf.ucsb.edu

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Whitaker, M.
(2008). Calcium signalling in early embryos. Phil Trans R Soc B
363: 1401-1418
[Abstract]
[Full Text]
-
Matsui, A., Okigaki, M., Amano, K., Adachi, Y., Jin, D., Takai, S., Yamashita, T., Kawashima, S., Kurihara, T., Miyazaki, M., Tateishi, K., Matsunaga, S., Katsume, A., Honshou, S., Takahashi, T., Matoba, S., Kusaba, T., Tatsumi, T., Matsubara, H.
(2007). Central Role of Calcium-Dependent Tyrosine Kinase PYK2 in Endothelial Nitric Oxide Synthase Mediated Angiogenic Response and Vascular Function. Circulation
116: 1041-1051
[Abstract]
[Full Text]
-
Whitaker, M.
(2006). Calcium at Fertilization and in Early Development. Physiol. Rev.
86: 25-88
[Abstract]
[Full Text]
-
Mehlmann, L. M, Jaffe, L. A
(2005). SH2 domain-mediated activation of an SRC family kinase is not required to initiate Ca2+ release at fertilization in mouse eggs. Reproduction
129: 557-564
[Abstract]
[Full Text]
-
Nishi, M., Werner, E. D., Oh, B.-C., Frantz, J. D., Dhe-Paganon, S., Hansen, L., Lee, J., Shoelson, S. E.
(2005). Kinase Activation through Dimerization by Human SH2-B. Mol. Cell. Biol.
25: 2607-2621
[Abstract]
[Full Text]
-
O'Neill, F. J., Gillett, J., Foltz, K. R.
(2004). Distinct roles for multiple Src family kinases at fertilization. J. Cell Sci.
117: 6227-6238
[Abstract]
[Full Text]
-
Voronina, E., Wessel, G. M.
(2004). {beta}{gamma} subunits of heterotrimeric G-proteins contribute to Ca2+ release at fertilization in the sea urchin. J. Cell Sci.
117: 5995-6005
[Abstract]
[Full Text]
-
Kurokawa, M., Sato, K.-i., Smyth, J., Wu, H., Fukami, K., Takenawa, T., Fissore, R. A
(2004). Evidence that activation of Src family kinase is not required for fertilization-associated [Ca2+]i oscillations in mouse eggs. Reproduction
127: 441-454
[Abstract]
[Full Text]
-
Sato, K.-i., Tokmakov, A. A., He, C.-L., Kurokawa, M., Iwasaki, T., Shirouzu, M., Fissore, R. A., Yokoyama, S., Fukami, Y.
(2003). Reconstitution of Src-dependent Phospholipase C{gamma} Phosphorylation and Transient Calcium Release by Using Membrane Rafts and Cell-free Extracts from Xenopus Eggs. J. Biol. Chem.
278: 38413-38420
[Abstract]
[Full Text]
-
Leckie, C., Empson, R., Becchetti, A., Thomas, J., Galione, A., Whitaker, M.
(2003). The NO Pathway Acts Late during the Fertilization Response in Sea Urchin Eggs. J. Biol. Chem.
278: 12247-12254
[Abstract]
[Full Text]
-
Tunquist, B. J., Maller, J. L.
(2003). Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev.
17: 683-710
[Full Text]
-
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: 367-376
[Abstract]
[Full Text]
-
LIM, D., LANGE, K., SANTELLA, L.
(2002). Activation of oocytes by latrunculin A. FASEB J.
16: 1050-1056
[Abstract]
[Full Text]
-
Halet, G., Tunwell, R., Balla, T., Swann, K., Carroll, J.
(2002). The dynamics of plasma membrane PtdIns(4,5)P2 at fertilization of mouse eggs. J. Cell Sci.
115: 2139-2149
[Abstract]
[Full Text]
-
Terasaki, M., Runft, L. L., Hand, A. R.
(2001). Changes in Organization of the Endoplasmic Reticulum during Xenopus Oocyte Maturation and Activation. Mol. Biol. Cell
12: 1103-1116
[Abstract]
[Full Text]
-
Rebecchi, M. J., Pentyala, S. N.
(2000). Structure, Function, and Control of Phosphoinositide-Specific Phospholipase C. Physiol. Rev.
80: 1291-1335
[Abstract]
[Full Text]
-
Morrison, T., Waggoner, L., Whitworth-Langley, L., Stith, B. J.
(2000). Nongenomic Action of Progesterone: Activation of XenopusOocyte Phospholipase C through a Plasma Membrane-Associated Tyrosine Kinase. Endocrinology
141: 2145-2152
[Abstract]
[Full Text]
-
Jaconi, M., Bony, C., Richards, S. M., Terzic, A., Arnaudeau, S., Vassort, G., Pucéat, M.
(2000). Inositol 1,4,5-Trisphosphate Directs Ca2+ Flow between Mitochondria and the Endoplasmic/Sarcoplasmic Reticulum: A Role in Regulating Cardiac Autonomic Ca2+ Spiking. Mol. Biol. Cell
11: 1845-1858
[Abstract]
[Full Text]
-
McDougall, A, Levasseur, M, O'Sullivan, A., Jones, K.
(2000). Cell cycle-dependent repetitive Ca(2+ )waves induced by a cytosolic sperm extract in mature ascidian eggs mimic those observed at fertilization. J. Cell Sci.
113: 3453-3462
[Abstract]
-
Runft, L., Jaffe, L.
(2000). Sperm extract injection into ascidian eggs signals Ca(2+) release by the same pathway as fertilization. Development
127: 3227-3236
[Abstract]
-
Giusti, A. F., Carroll, D. J., Abassi, Y. A., Terasaki, M., Foltz, K. R., Jaffe, L. A.
(1999). Requirement of a Src Family Kinase for Initiating Calcium Release at Fertilization in Starfish Eggs. J. Biol. Chem.
274: 29318-29322
[Abstract]
[Full Text]
-
Kobrinsky, E., Spielman, A. I., Rosenzweig, S., Marks, A. R.
(1999). Ceramide triggers intracellular calcium release via the IP3 receptor in Xenopus laevis oocytes. Am. J. Physiol. Cell Physiol.
277: C665-C672
[Abstract]
[Full Text]
-
Perry, A.C.F., Wakayama, T., Yanagimachi, R.
(1999). A Novel Trans-Complementation Assay Suggests Full Mammalian Oocyte Activation Is Coordinately Initiated by Multiple, Submembrane Sperm Components. Biol. Reprod.
60: 747-755
[Abstract]
[Full Text]
-
Shearer, J, De Nadai, C, Emily-Fenouil, F, Gache, C, Whitaker, M, Ciapa, B
(1999). Role of phospholipase Cgamma at fertilization and during mitosis in sea urchin eggs and embryos. Development
126: 2273-2284
[Abstract]
-
Sette, C., Bevilacqua, A., Geremia, R., Rossi, P.
(1998). Involvement of Phospholipase C{gamma}1 in Mouse Egg Activation Induced by a Truncated Form of the C-kit Tyrosine Kinase Present in Spermatozoa. JCB
142: 1063-1074
[Abstract]
[Full Text]
-
Giusti, A. F., Xu, W., Hinkle, B., Terasaki, M., Jaffe, L. A.
(2000). Evidence That Fertilization Activates Starfish Eggs by Sequential Activation of a Src-like Kinase and Phospholipase Cgamma. J. Biol. Chem.
275: 16788-16794
[Abstract]
[Full Text]
-
Iwasaki, H., Chiba, K., Uchiyama, T., Yoshikawa, F., Suzuki, F., Ikeda, M., Furuichi, T., Mikoshiba, K.
(2002). Molecular Characterization of the Starfish Inositol 1,4,5-Trisphosphate Receptor and Its Role during Oocyte Maturation and Fertilization. J. Biol. Chem.
277: 2763-2772
[Abstract]
[Full Text]