Involvement of phospholipase Cγ1 in mouse egg activation induced by a truncated form of the C-kit tyrosine kinase present in spermatozoa

Journal of Cell Biology

Volumn 142, Issue 4, 1998, Pages 1063-1074

  Sette, Claudio ^a   Bevilacqua, Arturo ^b   Geremia, Raffaele ^a   Rossi, Pellegrino ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Egg activation; Phospholipase C 1; Spermatozoa; Src homology domains; Truncated c kit

Indexed keywords

DIACYLGLYCEROL; GLUTATHIONE TRANSFERASE; INOSITOL PHOSPHATE; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA1; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; ANTIBODY; GRB2 PROTEIN, MOUSE; GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; HYBRID PROTEIN; ISOENZYME; PHOSPHOLIPASE C GAMMA; PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; STEM CELL FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; ENZYME ANALYSIS; FEMALE; MALE; MOUSE; NONHUMAN; PARTHENOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; SPERMATOZOON; ANIMAL; CELL CYCLE; CELL STRAIN COS1; CHEMISTRY; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; MICROINJECTION; OOCYTE; PHYSIOLOGY; SRC HOMOLOGY DOMAIN;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIBODIES; CELL CYCLE; COS CELLS; DIGLYCERIDES; GRB2 ADAPTOR PROTEIN; INOSITOL PHOSPHATES; ISOENZYMES; MALE; MICE; MICROINJECTIONS; OOCYTES; PARTHENOGENESIS; PHOSPHOLIPASE C; PHOSPHOLIPASE C GAMMA; PROTEIN-TYROSINE KINASES; PROTEINS; PROTO-ONCOGENE PROTEINS C-KIT; RECOMBINANT FUSION PROTEINS; SPERMATOZOA; SRC HOMOLOGY DOMAINS; TRANSFECTION;

EID: 0032563387     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.4.1063     Document Type: Article

References (72)

1. Adamo, S., B.M. Zani, C. Nervi, M.I. Senni, M. Molinaro, and F. Eusebi. 1985. Acetylcholine stimulates phosphatidylinositol turnover at nicotinic receptors of cultured myotubes. FEBS (Fed. Eur. Biochem. Soc.) Lett. 190:161-164.
2. Albanesi, C., R. Geremia, M. Giorgio, S. Dolci, C. Sette, and P. Rossi. 1996. A cell- and developmental stage-specific promoter drives the expression of a truncated c-kit protein during mouse spermatid elongation. Development (Camb.). 122:1291-1302.
3. Andreotti, A.H., S.C. Bunnell, S. Feng, L.J. Berg, and S.L. Schreiber. 1997. Regulatory intramolecular association in a tyrosine kinase of the Tec family. Nature. 385:93-97.
4. Bae, Y.S., L.G. Cantley, C.S. Chen, S.R. Kirn, K.S. Kwon, and S.G. Rhee. 1998. Activation of phospholipase C-γ by phosphatydilinositol 3,4,5-trisphosphate. J. Biol. Chem. 273:4465-4469.
5. Bar-Sagi, D., D. Rotin, A. Batzer, V. Mandiyan, and J. Schlessinger. 1993. SH3 domains direct cellular localization of signaling molecules. Cell. 74:83-91.
6. Berridge, M.J. 1993. Inositol triphosphate and calcium signaling. Nature. 361: 315-325.
7. Berridge, M.J. 1996. Regulation of calcium spiking in mammalian oocytes through a combination of inositol triphosphate-dependent entry and release. Mol. Hum. Reprod. 2:386-388.
8. Blume-Jensen, P., L. Ronnstrand, I. Gout, M.D. Waterfield, and C.H. Heldin. 1994. Modulation of Kit/stem cell factor receptor-induced signaling by protein kinase C. J. Biol. Chem. 269:21793-21802.
9. Boukhchache, D., and M. Lagarde. 1982. Interaction between prostaglandin precursors during their oxygenation by human platelets. Biocham. Biophys. Acta. 713:386-392.
10. Bradford, M.M. 1976. A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
11. Carroll, D.J., C.S. Ramarao, L.M. Mehlmann, S. Roche, M. Terasaki, and L.A. Jaffe. 1997. Calcium release at fertilization in starfish eggs is mediated by phospholipase Cγ. J. Cell Biol. 138:1303-1311.
12. Chen, P., H. Xie, M.C. Sekar, K. Gupta, and A. Wells. 1994. Epidermal growth factor receptor-mediated cell motility: phospholipase C activity is required, but mitogen-activated protein kinase activity is not sufficient for induced cell movement. J. Cell Biol. 127:847-857.
13. Cohen, G.B., R. Ren, and D. Baltimore. 1995. Modular binding domains in signal transduction proteins. Cell. 80:237-248.
14. Colonna, R., C. Tatone, A. Francione, F. Rosati, G. Callaini, D. Corda, and L. Di Francesco. 1997. Protein kinase C is required for the disappearence of MPF upon artificial activation in mouse eggs. Mol. Reprod. Dev. 48:292-299.
15. Dozortsev, D., A. Rybouchkin, P. De Sutter, C. Qian, and M. Dhont. 1995. Human oocyte activation following intracytoplasmic injection: the role of the sperm cell. Hum. Reprod. 10:403-407.
16. Duchesne, M., F. Schweighoffer, F. Parker, F. Clerc, Y. Frobert, M.N. Thang, and B. Tocque. 1993. Identification of the SH3 domain of GAP as an essential sequence for ras-GAP-mediated signaling. Science. 259:525-528.
17. Ducibella, T., E. Anderson, D.F. Albertini, J. Aalberg, and S. Rangarajan. 1988. Quantitative studies of changes in cortical granule number and distribution in the mouse oocyte during meiotic maturation. Dev. Biol. 130:184-197.
18. 2+ spiking. Biochem. J. 316:53-591.
19. Exton, J.H. 1997. Phospholipase D: enzymology, mechanisms of regulation, and function. Physiol. Rev. 77:303-317.
20. Falasca, M., S.K. Logan, V.P. Lehto, G. Baccante, M.A. Lemmon, and J. Schlessinger. 1998. Activation of phospholipase C by PI 3-kinase-induced PH domain-mediated membrane targeting. EMBO (Eur. Mol. Biol. Organ.) J. 17:414-422.
21. Gallicano, G.I., M.C. Yousef, and D.G. Capco. 1997a. PKC: a pivotal regulator of early development. Bioessays. 19:29-36.
22. Gallicano, G.I., R.W. McGaughey, and D.G. Capco. 1997b. Activation of protein kinase C after fertilization is required for remodeling the mouse egg into the zygote. Mol. Reprod. Dev. 46:587-601.
23. Gish, G., M.L. McGlone, T. Pawson, and J.A. Adams. 1995. Bacterial expression, purification and preliminary kinetic description of the kinase domain of v-fps. Protein Eng. 8:609-614.
24. Gout, I., R. Dhand, I.D. Hiles, M.J. Fry, G. Panayotou, P. Das, O. Truong, N.F. Totty, J. Hsuan, G.W. Booker, I.D. Campbell, and M.D. Waterfield. 1993. The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell. 75:25-36.
25. Herbst, R., R. Lammers, J. Schlessinger, and A. Ullrich. 1991. Substrate phosphorylation specificity of the human c-kil receptor tyrosine kinase. J. Biol. Chem. 266:19908-19916.
26. Herbst, R., M.S. Shearman, B. Jallal, J. Schlessinger, and A. Ullrich. 1995. Formation of signal transfer complexes between stem cell and platelet-derived growth factor receptors and SH2 domain proteins in vitro. Biochemistry. 34: 5971-5979.
27. Hogan, B., R. Beddington, F. Costantini, and E. Lacy. 1994. Manipulating the Mouse Embryo. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY. 497 pp.
28. Homa, S.T., and K. Swann. 1994. A cytosolic sperm factor triggers calcium oscillations and membrane hyperpolarization in human oocytes. Hum. Reprod. 9:2356-2361.
29. Horie, K., K. Takakura, S. Taii, K. Narimoto, Y. Noda, S. Nishikawa, H. Nakayama, J. Fujita, and T. Mori. 1991. The expression of the c-kit protein during oogenesis and early embryonic development. Biol. Reprod. 45:547-552.
30. Horstman, D.A., K. DeStefano, and G. Carpenter. 1996. Enhanced phospholipase C-γ1 activity produced by association of independently expressed X and Y domain polypeptides. Proc. Natl. Acad. Sci. USA. 93:7518-7521.
31. Huang, P.S., L. Davis, H. Huber, P.J. Goodhart, R.E. Wergrzyn, A. Oliff, and D.C. Heimbrook. 1995. An SH3 domain is required for the mitogenic activity of microinjected phospholipase C-γ1. FEBS (Fed. Eur. Biochem. Soc.) Lett. 358:287-292.
32. Hwang, S.C., D.Y. Jhon, Y.S. Bae, J.H. Kim, and S.G. Rhee. 1996. Activation of phospholipase C-γ by the concerted action of tau proteins and arachidonic acid. J. Biol. Chem. 271:18342-18349.
33. Jones, G.A., and G. Carpenter. 1993. The regulation of phospholipase C-γ1 by phosphatidic acid. Assessment of kinetic parameters. J. Biol. Chem. 268: 20845-20850.
34. Kamat, A., and G. Carpenter. 1997. Phospholipase C-γ1: regulation of enzyme function and role in growth factor-dependent signal transduction. Cytokine Growth Factor Rev. 8: 109-117.
35. Kim, H.K., J.W. Kim, A. Zilberstein, B. Margolis, J.G. Kim, J. Schlessinger, and S.G. Rhee. 1991. PDGF stimulation of inositol phospholipid hydrolysis requires PLC-γ1 phosphorylation on tyrosine residues 783 and 1254. Cell. 65: 435-441.
36. Kinsey, W.H. 1996. Biphasic activation of fyn kinase upon fertilization of the sea urchin egg. Dev. Biol. 174:281-287.
37. Kline, D., and J.T. Kline. 1992. Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149: 80-89.
38. Koike, T., K. Hirai, Y. Morita, and Y. Nozawa. 1993. Stem cell factor-induced signal transduction in rat mast cells. Activation of phospholipase D but not phosphoinositide-specific phospholipase C in c-kit receptor stimulation. J. Immnnol. 151:359-366.
39. Kozawa, O., P. Blume-Jensen, C.H. Heldin, and L. Ronnstrand. 1997. Involvement of phosphatidylinositol 3′-kinase in stem-cell-factor-induced phospholipase D activation and arachidonic acid release. Eur. J. Biochem. 248:149-155.
40. 2+ increase at fertilization in the mouse. Development (Camb.). 124:233-241.
41. 2 hydrolysis and regulation of phospholipase C isozymes. Curr. Opin. Cell Biol. 7:183-189.
42. Lev, S., D. Givol, and Y. Yarden. 1991. A specific combination of substrates is involved in signal transduction by the kit-encoded receptor. EMBO (Eur. Mol. Biol. Organ.) J. 10:647-654.
43. Li, W., R. Nishimura, A. Kashishian, A.G. Batzer, W.J. Kim, J.A. Cooper, and J. Schlessinger. 1994. A new function for a phosphotyrosine phosphatase: linking GRB2-Sos to a receptor tyrosine kinase. Mol. Cell. Biol. 14:509-517.
44. Manova, K., K. Nocka, P. Besmer, and R.F. Bachvarova. 1990. Gonadal expression of c-kit encoded at the W locus of the mouse. Development (Camb.). 110:1057-1069.
45. 2+ oscillation by antibody to the inositol 1,4,5-triphosphate receptor in fertilized hamster eggs. Science. 257:251-255.
46. 2+ oscillations at fertilization of mammalian eggs. Dev. Biol. 158:62-78.
47. Moarefi, I., M. LaFevre-Bernt, F. Sicheri, M. Huse, C.H. Lee, J. Kuriyan, and W.T. Miller. 1997. Activation of the Src-family tyrosine kinase Hck by SH3 domain displacement. Nature. 385:650-653.
48. Mohammadi, M., A.M. Honegger, D. Rotin, R. Fischer, F. Bellot, W. Li, C.A. Dionne, M. Jaye, M. Rubinstein, and J. Schlessinger. 1991. A tyrosine-phosphorylated carboxy-terminal peptide of the fibroblast growth factor receptor(Flg) is a binding site for the SH2 domain of phospholipase C-γ1. Mol. Cell. Biol. 11:5068-5078.
49. Moore, K.L., and W.H. Kinsey. 1994. Identification of an abl-related protein kinase in the cortex of the sea urchin egg: possible role at fertilization. Dev. Biol. 164:444-455.
50. Moore, K.L., and W.H. Kinsey. 1995. Effects of protein tyrosine kinase inhibitors on egg activation and fertilization-dependent protein tyrosine kinase activity. Dev. Biol. 168:1-10.
51. Mori, C., H. Hashimoto, and K. Hoshino. 1988. Fluorescence microscopy of nuclear DNA in oocytes and zygotes during in vitro fertilization and development of early embryos in mice. Biol. Reprod. 39:737-742.
52. Motto, D.G., M.A. Musci, S.E. Ross, amd G.A. Koretzky. 1996. Tyrosine phosphorylation of Grb2-associated proteins correlates with phospholipase C γ1 activation in T cells. Mol. Cell. Biol. 16:2823-2829.
53. 3. Dev. Biol. 158:200-212.
54. Parrington, J., K. Swann, V.I. Shevchenko, A.K. Sesay, and F.A. Lai. 1996. Calcium oscillations in mammalian eggs triggered by a soluble sperm protein. Nature. 379:364-368.
55. Pawson, T. 1995. Protein modules and signaling networks. Nature. 373:573-580.
56. Rhee, S.G., and Y.S. Bae. 1997. Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272:15045-15048.
57. Rossi, P., G. Marziali, C. Albanesi, A. Charlesworth, R. Geremia, and V. Sorrentino. 1992. A novel c-kit transcript, potentially encoding a truncated receptor, originates within a kit gone intron in mouse spermatids. Dev. Biol. 152:203-207.
58. Rottapel, R., M. Reedijk, D.E. Williams, S.D. Lyman, D.M. Anderson, T. Pawson, and A. Bernstein. 1991. The Steel/W transduction pathway: kit auto-phosphorylation and its association with a unique subset of cytoplasmic signaling proteins is induced by the Steel factor. Mol. Cell Biol. 11:3043-3051.
59. Sato, K., M. Aoto, K. Mori, S. Akasofu, A.A. Tokmakov, S. Sahara, and Y. Fukami. 1996. Purification and characterization of a src-related p57 protein-tyrosine kinase from Xenopus oocytes. Isolation of an inactive form of the enzyme and its activation and translocation upon fertilization. J. Biol. Chem. 271:13250-13257.
60. Sette, C., A. Bevilacqua, A. Bianchini, F. Mangia, R. Geremia, and P. Rossi. 1997. Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development (Camb.). 124:2267-2274.
61. Shilling, P.M., D.J. Carroll, A.J. Muslin, J.A. Escobedo, L.T. Williams, and L.A. Jaffe. 1994. Evidence for both tyrosine kinase and G protein-coupled pathways leading to starfish egg activation. Dev. Biol. 162:590-599.
62. Sorrentino, V., M. Giorgi, R. Geremia, P. Besmer, and P. Rossi. 1991. Expression of the c-kit proto-oncogene in the murine male germ cells. Oncogene. 6:149-151.
63. Slice, S.L., and J.M. Robl. 1990. Activation of mammalian oocytes by a factor obtained from rabbit sperm. Mol. Reprod. Dev. 25:272-280.
64. Stricker, S.A. 1997. Intracellular injections of a soluble sperm factor trigger calcium oscillations and meiotic maturation in unfertilized oocytes of a marine worm. Dev. Biol. 186:185-201.
65. Swann, K. 1990. A cytosolic sperm factor stimulates repetitive calcium increases and mimics fertilization in hamster eggs. Development (Camb.). 110: 1295-1302.
66. Valius, M., J.P. Secrist, and A. Kazlauskas. 1995. The GTPase-activating protein of ras suppresses platelet-derived growth factor β receptor signaling by silencing phospholipase C-γ1. Mol. Cell. Biol. 15:3058-3071.
67. Whitaker, M., and K. Swann. 1993. Lighting the fuse at fertilization. Development (Camb.). 117:1-12.
68. Wolosker, H., D. Kline, Y. Bian, S. Blackshaw, A.M. Cameron, T.D. Fralich, R.L. Schnaar, and S.H. Snyder. 1998. Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB (Fed. Am. Soc. Exp. Biol.) J. 12:91-99.
69. Wu, H., C.L. He, and R.A. Fissore. 1997. Injection of a porcine sperm factor triggers calcium oscillations in mouse oocytes and bovine eggs. Mol. Reprod. Dev. 46:176-189.
70. 2- release in early and late events of mouse egg activation. Development (Camb.). 120:1851-1859.
71. Yim, D.L., L.K. Opresko, H.S. Wiley, and R. Nuccitelli. 1994. Highly polarized EGF receptor tyrosine kinase activity initiates egg activation in Xenopus. Dev. Biol. 162:41-55.
72. Yoshinaga, K., S. Nishikawa, M. Ogawa, S. Hayashi, T. Kunisada, T. Fujimoto, and S.-I. Nishikawa. 1991. Role of c-kit in mouse spermatogenesis: identification of spermatogonia as a specific site of c-kit expression and function. Development (Camb.). 113:689-699.