Identification of PLCγ-dependent and -independent events during fertilization of sea urchin eggs

Developmental Biology

Volumn 206, Issue 2, 1999, Pages 232-247

  Carroll, David J ^a   Albay, Diana T ^a   Terasaki, Mark ^b   Jaffe, Laurinda A ^b   Foltz, Kathy R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Activation; Calcium; DNA synthesis; Fertilization; MAP kinase; pH; Sea urchin; Signal transduction

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; CALCIUM ION; CHOLERA TOXIN; CYCLIC GMP; DEXTRAN; DIACYLGLYCEROL; DNA; FLUORESCEIN; HYBRID PROTEIN; INOSITOL TRISPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOLIPASE C; CALCIUM; ISOENZYME; PHOSPHOLIPASE C DELTA; PROTEIN KINASE (CALCIUM,CALMODULIN);

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL PH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEPHOSPHORYLATION; DNA SYNTHESIS; EGG; EXOCYTOSIS; FERTILIZATION; NONHUMAN; PRIORITY JOURNAL; SEA URCHIN; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CATTLE; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; FEMALE; INTRACELLULAR FLUID; MALE; METABOLISM; OOCYTE; PH; PHOSPHORYLATION; PHYSIOLOGY; SRC HOMOLOGY DOMAIN;

ACTION POTENTIALS; ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CATTLE; DNA; ENZYME ACTIVATION; FEMALE; FERTILIZATION; HYDROGEN-ION CONCENTRATION; INTRACELLULAR FLUID; ISOENZYMES; MALE; OVUM; PHOSPHOLIPASE C; PHOSPHORYLATION; RECOMBINANT FUSION PROTEINS; SEA URCHINS; SRC HOMOLOGY DOMAINS;

EID: 0033556702     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1998.9145     Document Type: Article

References (82)

1. Anderson D., Koch C. A., Grey L., Ellis C., Moran M. F., Pawson T. Binding of SH2 domains of phospholipase C gamma 1, GAP, and Src to activated growth factor receptors. Science. 250:1990;979-982.
2. Bestor T. H., Schatten G. Anti-tubulin immunofluorescence microscopy of microtubules present during the pronuclear movement of sea urchin fertilization. Dev. Biol. 88:1981;80-91.
3. Cameron L. A., Poccia D. L. In vitro. Dev. Biol. 162:1994;568-578.
4. Carroll D. J., Ramarao C. S., Mehlmann L. M., Roche S., Terasaki M., Jaffe L. A. Calcium release at fertilization in starfish eggs is mediated by phospholipase Cγ J. Cell Biol. 138:1997;1303-1311.
5. Carron C. P., Longo F. J. Relation of intracellular pH and pronuclear development in the sea urchin,Arbacia punctulata. Dev. Biol. 79:1980;478-487.
6. Chambers E. L., de Armendi J. Membrane potential, action potential and activation potential of eggs of the sea urchin. Lytechinus variegatus. Exp. Cell Res. 122:1979;203-218.
7. Chen P., Xie H., Sekar M. C., Gupta K., Wells A. 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. 127:1994;847-857.
8. Chiba K., Kado R. T., Jaffe L. A. Development of calcium release mechanisms during starfish oocyte maturation. Dev. Biol. 140:1990;300-306.
9. Cothren C. C., Poccia D. L. Two steps required for male pronucleus formation in the sea urchin egg. Exp. Cell Res. 205:1993;126-133.
10. 2+. Biochem. J. 316:1996;583-591.
11. Eisen A., Kiehart D. P., Wieland S. J., Reynolds G. T. Temporal sequence and spatial distribution of early events of fertilization in single sea urchin eggs. J. Cell Biol. 99:1984;1647-1654.
12. Epel D. The initiation of development at fertilization. Cell Differ. Dev. 29:1990;1-12.
13. Feng J.-F., Rhee S. G., Im M.-J. Evidence that phospholipase Cδ1 is the effector in the Gh(transglutaminase II)-mediated signaling. J. Biol. Chem. 271:1996;16451-16454.
14. Galione A., McDougall A., Busa W. B., Willmott N., Gillot I., Whitaker M. Redundant mechanisms of calcium-induced calcium release underlying calcium waves during fertilization of sea urchin eggs. Science. 261:1993;348-352.
15. Gish G., Larose L., Shen R., Pawson T. Biochemical analysis of SH2 domain-mediated protein interactions. Methods Enzymol. 254:1995;503-523.
16. Hepler J. R., Gilman A. G. G proteins. Trends Biochem. Sci. 17:1992;383-387.
17. Hiramoto Y. Microinjection of the live spermatozoa into sea urchin eggs. Exp. Cell Res. 27:1962;416-426.
18. Homma Y., Emori Y. A dual functional signal mediator showing RhoGAP and phospholipase C-delta stimulating activities. EMBO J. 14:1995;286-291.
19. Huang P. S., Davis L., Huber H., Goodhart P. J., Wegrzyn R. E., Oliff A., Heimbrook D. C. An SH3 domain is required for the mitogenic activity of microinjected phospholipase C-γ1. FEBS Lett. 358:1995;287-292.
20. Jaffe L. F. Sources of calcium in egg activation: A review and hypothesis. Dev. Biol. 99:1983;265-276.
21. Johnson J. D., Epel D., Paul D. Intracellular pH and activation of sea urchin eggs after fertilization. Nature. 262:1976;661-664.
22. Kiehart D. P. Microinjection of echinoderm eggs: Apparatus and procedures. Methods Cell Biol. 25:1982;13-31.
23. Kinsey W. H. Tyrosine kinase signaling at fertilization. Biochem. Biophys. Res. Commun. 240:1997;519-522.
24. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:1970;680-685.
25. Larose L., Gish G., Pawson T. Construction of an SH2 domain-binding site with mixed specificity. J. Biol. Chem. 270:1995;3858-3862.
26. ++. Exp. Cell Res. 22:1986;123-129.
27. Lee H. C., Aarhus R., Walseth T. F. Calcium mobilization by dual receptors during fertilization of sea urchin eggs. Science. 261:1993;352-355.
28. Lee S. J., Christenson L., Martin T., Shen S. S. The cyclic GMP-mediated calcium release pathway in sea urchin eggs is not required for the rise in calcium during fertilization. Dev. Biol. 180:1996;324-335.
29. Lee S. J., Shen S. S. The calcium transient in sea urchin eggs during fertilization requires the production of inositol 1,4,5-trisphosphate. Dev. Biol. 193:1998;195-208.
30. Lim N. F., Dascal N., Labarca C., Davidson N., Lester H. A. A G protein-gated K channel is activated via β2-adrenergic receptors and Gβγ subunits inXenopus. J. Gen. Physiol. 105:1995;421-4349.
31. Livingston B. T., VanWinkle C. E., Kinsey W. H. Protein tyrosine kinase activity following fertilization is required to complete gastrulation, but not for initial differentiation of endoderm and mesoderm in the sea urchin embryo. Dev. Biol. 193:1998;90-99.
32. Longo F. J. Effects of cytochalasin B on sperm-egg interactions. Dev. Biol. 67:1978;249-265.
33. Longo F. J., Anderson E. The fine structure of pronuclear development and fusion in the sea urchin,Arbacia punctulata. J. Cell Biol. 39:1968;339-368.
34. Luttmer S. J., Longo F. J. Rates of male pronuclear enlargement in sea urchin zygotes. J. Exp. Zool. 243:1987;289-298.
35. McCulloh D. H., Chambers E. L. Fusion of membranes during fertilization. Increases of the sea urchin egg's membrane capacitance and membrane conductance at the site of contact with the sperm. J. Gen. Physiol. 99:1992;137-175.
36. McDougall A., Gillot I., Whitaker M. Thimerosal reveals calcium-induced calcium release in unfertilised sea urchin eggs. Zygote. 1:1993;35-42.
37. McPherson S. M., McPherson P. S., Mathews L., Campbell K. P., Longo F. J. Cortical localization of a calcium release channel in sea urchin eggs. J. Cell. Biol. 116:1992;1111-1121.
38. 2+. Dev. Biol. 203:1998;221-232.
39. 2+2+. Science. 257:1992;251-255.
40. i. Dev. Biol. 159:1995;669-678.
41. Moore K. L., Kinsey W. H. Effects of protein tyrosine kinase inhibitors on egg activation and fertilization-dependent protein tyrosine kinase activity. Dev. Biol. 168:1995;1-10.
42. Muto Y., Nagao T., Urushidani T. The putative phospholipase C inhibitor U73122 and its negative control, U73343, elicit unexpected effects on the rabbit parietal cell. J. Pharmacol. Exp. Ther. 282:1997;1379-1388.
43. Nomura A., Maruyama Y. K., Yoneda M. Initiation of DNA replication cycle in fertilized eggs of the starfish,Asterina pectinifera. Dev. Biol. 143:1991;289-296.
44. 3. Dev. Biol. 158:1993;200-212.
45. Oberdorf J. A., Head J. F., Kaminer B. Calcium uptake and release by isolated cortices and microsomes from the unfertilized egg of the sea urchinStrongylocentrotus droebachiensis. J. Cell Biol. 102:1986;2205-2210.
46. Ottinger E. A., Botfield M. C., Shoelson S. E. Tandem SH2 domains confer high specificity in tyrosine kinase signaling. J. Biol. Chem. 273:1998;729-735.
47. Park D., Jhon D.-Y., Lee C.-W., Lee K.-H., Rhee S. G. Activation of phospholipase C isozymes by G protein βγ subunits. J. Biol. Chem. 268:1993;4573-4576.
48. Parys J. B., McPherson S. M., Mathews L., Campbell K. P., Longo F. J. Presence of inositol 1,4,5-trisphosphate receptor, calreticulin, and calsequestrin in eggs of sea urchins andXenopus laevis. Dev. Biol. 161:1994;466-476.
49. Payan P., Girard J. P., Ciapa B. Mechanisms regulating intracellular pH in sea urchin eggs. Dev. Biol. 100:1983;29-38.
50. Picard A., Galas S., Peaucellier G., Dorée M. Newly assembled cyclin B-cdc2 kinase is required to suppress DNA replication between meiosis I and meiosis II in starfish oocytes. EMBO J. 15:1996;3590-3598.
51. Poccia D., Collas P. Transforming sperm nuclei into male pronucleiin vivoin vitro. Curr. Top. Dev. Biol. 34:1996;25-88.
52. Poccia D., Collas P. Nuclear envelope dynamics during male pronuclear development. Dev. Growth Differ. 39:1997;541-550.
53. Raskin D. M., Wright D. J., Wright S. J. Sea urchin sperm nuclear enlargement and shape transformations are differentially regulated in vitro. J. Exp. Zool. 277:1997;401-416.
54. Rees B. B., Patton C., Grainger J. L., Epel D. Protein synthesis increases after fertilization of sea urchin eggs in the absence of an increase in intracellular pH. Dev. Biol. 169:1995;683-698.
55. Rhee S. G., Bae Y. S. Regulation of phosphoinositide-specific phospholipase C isozymes. J. Biol. Chem. 272:1997;15045-15048.
56. Roche S., McGlade J., Jones M., Gish G. D., Pawson T., Courtneidge S. A. Requirement of phospholipase Cγ, the tyrosine phosphatase Syp and the adapter proteins Shc and Nck for PDGF-induced DNA synthesis: Evidence for the existence of Ras-dependent and Ras-independent pathways. EMBO J. 15:1996;4940-4948.
57. Rotin D., Honegger A. M., Margolis B. L., Ullrich A., Schlessinger J. Presence of SH2 domains of phospholipase Cγ1 enhances substrate phosphorylation by increasing the affinity toward the epidermal growth factor receptor. J. Biol. Chem. 267:1992;9678-9683.
58. Sadler K. C., Ruderman J. V. Components of the signaling pathway linking the 1-methyladenine receptor to MPF activation and maturation in starfish oocytes. Dev. Biol. 197:1998;25-38.
59. ++. Biochem. Biophys. Res. Commun. 161:1989;1100-1108.
60. Shen S. S., Buck W. R. A synthetic peptide of the pseudosubstrate domain of protein kinase C blocks cytoplasmic alkalinization during activation of the sea urchin egg. J. Cell. Physiol. 127:1990;330-340.
61. Shen S. S., Buck W. R. Sources of calcium in sea urchin eggs during the fertilization response. Dev. Biol. 157:1993;157-169.
62. Shen S. S., Burgart L. J. 1,2-Diacylglycerols mimic phorbol 12-myristate 13-acetate activation of the sea urchin egg. J. Cell. Physiol. 127:1986;330-340.
63. Shen S. S., Steinhardt R. A. Direct measurement of intracellular pH during metabolic derepression of the sea urchin egg. Nature. 272:1978;253-254.
64. Shen S. S., Steinhardt R. A. Intracellular pH and the sodium requirement at fertilisation. Nature. 282:1979;87-89.
65. Shen S. S., Kinsey W. H., Lee S. J. Protein tyrosine kinase-dependent release of intracellular calcium in the sea urchin egg. Dev. Growth Differ. 1999.
66. Shilling F. M., Carroll D. J., Muslin A. J., Escobedo J. A., Williams L. T., Jaffe L. A. Evidence for both tyrosine kinase and G-protein-coupled pathways leading to starfish egg activation. Dev. Biol. 162:1994;590-599.
67. Smrcka A. V., Sternweis P. C. Regulation of purified subtypes of phosphatidylinositol-specific phospholipase Cβ by G protein α and βγ subunits. J. Biol. Chem. 268:1993;9667-9674.
68. Spiegel A. M. G protein α subunits: Diversity and range of expression. G Proteins. 1994;Landes, Austin. p. 25-31.
69. Steinhardt R., Zucker R., Schatten G. Intracellular calcium release at fertilization in the sea urchin egg. Dev. Biol. 58:1977;185-196.
70. Steinhardt R. A., Epel D. Activation of sea urchin eggs by a calcium ionophore. Proc. Natl. Acad. Sci. USA. 71:1974;1915-1919.
71. Swann K., Whitaker M. Stimulation of the Na/H exchanger of sea urchin eggs by phorbol ester. Nature. 314:1985;274-277.
72. Tachibana K., Machida T., Nomura Y., Kishimoto T. MAP kinase links the fertilization signal transduction pathway to the G1/S-phase transition in starfish eggs. EMBO J. 16:1997;4333-4339.
73. Terasaki M. Redistribution of cytoplasmic components during germinal vesicle breakdown in starfish oocytes. J. Cell Sci. 107:1994;1797-1805.
74. Terasaki M., Sardet C. Demonstration of calcium uptake and release by sea urchin egg cortical endoplasmic reticulum. J. Cell Biol. 115:1991;1031-1037.
75. Tilney L. G., Jaffe L. A. Actin, microvilli, and the fertilization cone of sea urchin eggs. J. Cell Biol. 87:1980;771-782.
76. Turner P. R., Jaffe L. A., Primakoff P. A cholera toxin-sensitive G-protein stimulates exocytosis in sea urchin eggs. Dev. Biol. 120:1987;577-583.
77. Wang Z., Gluck S., Zhang L., Moran M. F. Requirement for phospholipase C-gamma1 enzymatic activity in growth factor-induced mitogenesis. Mol. Cell Biol. 18:1998;590-597.
78. Whalley T., McDougall A., Crossley I., Swann K., Whitaker M. Internal calcium release and activation of sea urchin eggs by cGMP are independent of the phosphoinositide signaling pathway. Mol. Biol. Cell. 3:1992;373-383.
79. Wieland T., Schulze R., Jakobs K. H. Heterotrimeric guanine nucleotide binding proteins: Structure and function. Wirtz K. W. A. Molecular Mechanisms of Signaling and Membrane Transport. Nato ASI Series. 101:1997;1-24 Springer-Verlag, Berlin, Heidelberg.
80. 2+2+. Pflug. Arch. 427:1994;233-243.
81. Winkler M. M., Steinhardt R. A., Grainger J. L., Minning L. Dual ionic controls for the activation of protein synthesis at fertilization. Nature. 287:1980;558-560.
82. 2+. Development. 120:1994;1851-1859.