Evidence that G(q) family G proteins do not function in mouse egg activation at fertilization

Developmental Biology

Volumn 198, Issue 1, 1998, Pages 116-127

  Williams, Carmen J ^a   Mehlmann, Lisa M ^b   Jaffe, Laurinda A ^b   Kopf, Gregory S ^a   Schultz, Richard M ^a,c  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Egg activation; Fertilization; G protein; Mouse

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; ANTIBODY; CALCIUM; MESSENGER RNA; MUSCARINIC RECEPTOR;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL CYCLE; EMBRYO DEVELOPMENT; FERTILIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERM; ANIMAL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOLOGY; MALE; METABOLISM; MICROINJECTION; OOCYTE; PHYSIOLOGY; SPERMATOZOON; ZYGOTE;

ANIMALIA; VERTEBRATA;

ANIMALS; ANTIBODIES; CALCIUM; FERTILIZATION; FLUORESCENT ANTIBODY TECHNIQUE; GTP-BINDING PROTEINS; MALE; MICE; MICROINJECTIONS; OOCYTES; RECEPTORS, MUSCARINIC; RNA, MESSENGER; SPERMATOZOA; ZYGOTE;

EID: 0032084556     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1998.8892     Document Type: Article

References (79)

1. q-protein α-subunit. Nature 389, 296-299.
2. q/11, and phospholipase C-β1. J. Biol. Chem. 267, 8081-8088.
3. Bleil, J. D., and Wassarman, P.M. (1981). Mammalian sperm-egg interaction: Fertilization of mouse eggs triggers modifications of the major zona pellucida glycoprotein, ZP2. Dev. Biol. 86, 189-197.
4. Bonner, T. I., Buckley, N. J., Young, A. C., and Brann, M. R. (1987). Identification of a family of muscarinic acetylcholine receptor genes. Science 237, 527-532.
5. Camps, M., Carozzi, A., Schnabel, P., Scheer, A., Parker, P. J., and Gierschik, P. (1992). Isozyme-selective stimulation of phospholipase C-beta 2 by G protein beta gamma-subunits. Nature 360, 684-686.
6. 2+ release at fertilization in starfish eggs is mediated by phospholipase Cgamma. J. Cell Biol. 138, 1303-1311.
7. Chatot, C. L., Ziomek, C. A., Bavister, B. D., Lewis, J. L., and Torres, I. (1989). An improved culture medium supports development of random-bred 1-cell mouse embryos in vitro. J. Reprod. Fertil. 86, 679-688.
8. Cho, W. K., Stern, S., and Biggers, J. D. (1974). Inhibitory effect of dibutyryl cAMP on mouse oocyte maturation in vitro. J. Exp. Zool. 187, 383-386.
9. Ciapa, B., and Epel, D. (1991). A rapid change in phosphorylation on tyrosine accompanies fertilization of sea urchin eggs. FEBS Lett. 295, 167-170.
10. Cran, D. G., Moor, R. M., and Irvine, R. F. (1988). Initiation of the cortical reaction in hamster and sheep oocytes in response to inositol trisphosphate. J. Cell Sci. 91, 139-144.
11. Crossley, I., Whalley, T., and Whitaker, M. (1991). Guanosine 5′-thiotriphosphate may stimulate phosphoinositide messenger production in sea urchin eggs by a different route than the fertilizing sperm. Cell Regul. 2, 121-133.
12. 2+. Nature 316, 541-542.
13. Dale, B., DeFelice, L. J., and Ehrenstein, G. (1985). Injection of a soluble sperm fraction into sea urchin eggs triggers the cortical reaction. Experientia 41, 1068-1070.
14. 2+ transient in flowering plants at fertilization. Development 124, 2867-2874.
15. Ducibella, T., Kurasawa, S., Rangarajan, S., Kopf, G. S., and Schultz, R. M. (1990). Precocious loss of cortical granules during mouse oocyte meiotic maturation and correlation with an egg-induced modification of the zona pellucida. Dev. Biol. 137, 46-55.
16. 2+ spiking. Biochem. J. 316, 583-591.
17. Endo, Y., Kopf, G. S., and Schultz, R. M. (1986). Stage-specific changes in protein phosphorylation accompanying meiotic maturation of mouse oocytes and fertilization of mouse eggs. J. Exp. Zool. 239, 401-409.
18. Endo, Y., Mattei, P., Kopf, G. S., and Schultz, R. M. (1987). Effects of a phorbol ester on mouse eggs: Dissociation of sperm receptor activity from acrosome reaction-inducing activity of the mouse zona pellucida protein, ZP3. Dev. Biol. 123, 574-577.
19. Evans, J. P., Schultz, R. M., and Kopf, G. S. (1995). Identification and localization of integrin subunits in oocytes and eggs of the mouse. Mol. Reprod. Dev. 40, 211-220.
20. Gilman, A. G. (1987). G proteins: Transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615-649.
21. q subfamily of guanine nucleotide-binding regulatory protein α subunits attenuate activation of phosphatidylinositol 4,5-bisphosphate hydrolysis by hormones. J. Biol. Chem. 266, 20519-20524.
22. Hamm, H. E., Deretic, D., Arendt, A., Hargrave, P. A., Koenig, B., and Hofmann, K. P. (1988). Site of G protein binding to rhodopsin mapped with synthetic peptides from the α subunit. Science 241, 832-835.
23. Harlow, E., and Lane, D. (1988). Storing and purifying antibodies. In "Antibodies: A Laboratory Manual" (E. Harlow and D. Lane, Eds.), pp. 309-311. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Hepler, J. R., and Gilman, A. G. (1992). G proteins. TIBS 17, 383-387.
25. Hiramoto, Y. (1984). Micromanipulation. Cell Struct. Funct. 9(Suppl.), 139-144.
26. Jaffe, L. A. (1990). First messengers at fertilization. J. Reprod. Fertil. Suppl. 42, 107-116.
27. 2+ explosions, waves, and pulses in activating eggs. In "Biology of Fertilization" (C. B. Metz and A. Monroy, Eds.), Vol. 3, pp. 127-165. Academic Press, Orlando.
28. Jones, J., and Schultz, R. M. (1990). Pertussis toxin-catalyzed ADP-ribosylation of a G protein in mouse oocytes, eggs, and preimplantation embryos: Developmental changes and possible functional roles. Dev. Biol. 139, 250-262.
29. Kaneko, S., Takahashi, H., and Satoh, M. (1992). Metabotropic responses to acetylcholine and serotonin of Xenopus oocytes injected with rat brain mRNA are transduced by different G-protein subtypes. FEBS Lett. 299, 179-182.
30. Katz, A., Wu, D., and Simon, M. I. (1992). Subunits βγ of heterotrimeric G protein activate β2 isoform of phospholipase C. Nature 360, 686-689.
31. 2+ currents. Nature 353, 43-48.
32. 2+ in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149, 80-89.
33. Kline, D., Simoncini, L., Mandel, G., Maue, R. A., Kado, R. T., and Jaffe, L. A. (1988). Fertilization events induced by neurotransmitters after injection of mRNA in Xenopus eggs. Science 241, 464-467.
34. Kume, S., Muto, A., Inoue, T., Suga, K., Okano, H., and Mikoshiba, K. (1997). Role of inositol 1,4,5-trisphosphate receptor in ventral signaling in Xenopus embryos. Science 278, 1940-1943.
35. Kurasawa, S., Schultz, R. M., and Kopf, G. S. (1989). Egg-induced modifications of the zona pellucida of mouse eggs: Effects of microinjected inositol 1,4,5-trisphosphate. Dev. Biol. 133, 295-304.
36. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 221, 680-685.
37. 12. J. Cell Biol. 121, 91-99.
38. zα by site-directed mutagenesis. Sites and specificity of protein kinase C-dependent phosphorylation. J. Biol. Chem. 268, 3494-3498.
39. Machaty, Z., Mayes, M. A., Kovacs, L. G., Balatti, P. A., Kim, J. H., and Prather, R. S. (1997). Activation of porcine oocytes via an exogenously introduced rat muscarinic M1 receptor. Biol. Reprod. 57, 85-91.
40. Manejwala, F. M., Cragoe, E. J., Jr., and Schultz, R. M. (1989). Blastocoel expansion in the preimplantation mouse embryo: Role of extracellular sodium and chloride and possible apical routes of their entry. Dev. Biol. 133, 210-220.
41. 2+ release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol. Reprod. 51, 1088-1098.
42. s. J. Biol. Chem. 267, 13239-13245.
43. 2+ at fertilization of golden hamster eggs. Dev. Biol. 118, 259-267.
44. 2+ rises in golden hamster eggs. J. Cell Biol. 106, 345-353.
45. 2+ oscillations at fertilization of mammalian eggs. Dev. Biol. 158, 62-78.
46. 2+ oscillation by antibody to the inositol 1,4,5-trisphosphate receptor in fertilized hamster eggs. Science 257, 251-255.
47. α12 to the golgi by alternative spliced carboxyl-terminal region. Science 263, 95-98.
48. Moore, G. D., Ayabe, T., Visconti, P. E., Schultz, R. M., and Kopf, G. S. (1994). Roles of heterotrimeric and monomeric G proteins in sperm-induced activation of mouse eggs. Development 120, 3313-3323.
49. Moore, G. D., Kopf, G. S., and Schultz, R. M. (1993). Complete mouse egg activation in the absence of sperm by stimulation of an exogenous G protein-coupled receptor. Dev. Biol. 159, 669-678.
50. 3. Dev. Biol. 158, 200-212.
51. Offermanns, S., and Simon, M.I. (1995). G alpha 15 and G alpha 16 couple a wide variety of receptors to phospholipase C. J. Biol. Chem. 270, 15175-15180.
52. Offermanns, S., Wieland, T., Homann, D., Sandmann, J., Bombien, E., Spicher, K., Schultz, G., and Jakobs, K. H. (1994). Transfected muscarinic acetylcholine receptors selectively couple to Gi-type G proteins and Gq/11. Mol. Pharmacol. 45, 890-898.
53. Onrust, R., Herzmark, P., Chi, P., Garcia, P.D., Lichtarge, O., Kingsley, C., and Bourne, H. R. (1997). Receptor and βgamma binding sites in the α subunit of the retinal G protein transducin. Science 275, 381-384.
54. Pang, I. H., and Sternweis, P. C. (1990). Purification of unique alpha subunits of GTP-binding regulatory proteins (G proteins) by affinity chromatography with immobilized beta gamma subunits. J. Biol. Chem. 265, 18707-18712.
55. 2+ oscillations in mammalian eggs triggered by a soluble sperm protein. Nature 379, 364-368.
56. α13. J. Biol. Chem. 270, 18655-18659.
57. α13 induces Egr-1, c-fos, and transformation in NIH 3T3 cells. Oncogene 9, 2425-2429.
58. Rhee, S. G., and Choi, K. D. (1992). Regulation of inositol phospholipid-specific phospholipase C isozymes. J. Biol. Chem. 267, 12393-12396.
59. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). Extraction, purification and analysis of messenger RNA from eukaryotic cells. In "Molecular Cloning: A Laboratory Manual" (C. Nolan, Ed.), 2nd ed., pp. 7.43-7.45. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
60. Schultz, R. M., and Kopf, G. S. (1995). Molecular basis of mammalian egg activation. In "Current Topics in Developmental Biology" (R. A. Pederson and G. Schatten, Eds.), Vol. 30, pp. 21-62. Academic Press, San Diego.
61. Schultz, R. M., Montgomery, R. R., and Belanoff, J. R. (1983). Regulation of mouse oocyte meiotic maturation: Implication of a decrease in oocyte cAMP and protein dephosphorylation in commitment to resume meiosis. Dev. Biol. 97, 264-273.
62. Sette, C., Bevilacqua, A., Bianchini, A., Mangia, F., Geremia, R., and Rossi, P. (1997). Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development 124, 2267-2274.
63. Shilling, F., Mandel, G., and Jaffe, L. A. (1990). Activation by serotonin of starfish eggs expressing the rat serotonin 1c receptor. Cell Regul. 1, 465-469.
64. Shilling, F. M., Carroll, D. J., Muslin, A. J., Escobedo, J. A., Williams, L. T., and Jaffe, L. A. (1994). Evidence for both tyrosine kinase and G-protein-coupled pathways leading to starfish egg activation. Dev. Biol. 162, 590-599.
65. Strathmann, M., and Simon, M. I. (1990). G protein diversity: A distinct class of α subunits is present in vertebrates and invertebrates. Proc. Natl. Acad. Sci. USA 87, 9113-9117.
66. 2+ increases and mimics fertilization in hamster eggs. Development 110, 1295-1302.
67. Titus, D.E. (1991). Plasmid cloning and transcription in vitro. In "Promega Protocols and Applications Guide" (D. E. Titus, Ed.), 2nd ed., pp. 58-64. Promega Corp., Madison, WI.
68. 2+ independent in the mouse oocyte. J. Cell Biol. 117, 799-811.
69. van Biesen, T., Hawes, B. E., Luttrell, D. K., Krueger, K. M., Touhara, K., Porfiri, E., Sakaue, M., Luttrell, L. M., and Lefkowitz, R. J. (1995). Receptor-tyrosine-kinase-and Gβγ-mediated MAP kinase activation by a common signalling pathway. Nature 376, 781-784.
70. Whitten, W. K. (1971). Nutrient requirements for the culture of preimplantation embryos in vitro. Adv. Biosci. 6, 129-139.
71. q class: Expression in murine tissues and in stromal and hematopoietic cell lines. Proc. Natl. Acad. Sci. USA 88, 10049-10053.
72. 2f conversion and pronuclear formation in eggs expressing a functional m1 muscarinic receptor. Dev. Biol. 151, 288-296.
73. Williams, C. J., Schultz, R. M., and Kopf, G. S. (1996). G protein gene expression during mouse oocyte growth and maturation, and preimplantation embryo development. Mol. Reprod. Dev. 44, 315-323.
74. Wolosker, H., Kline, D., Bian, Y., Blackshaw, S., Cameron, A.M., Fralich, T. D., Schnaar, R. L., and Snyder, S. H. (1998). Molecularly cloned mammalian glucosamine-6-phosphate deaminase localizes to transporting epithelium and lacks oscillin activity. FASEB J. 12, 91-99.
75. 2+ oscillations in mouse oocytes and bovine eggs. Mol. Reprod. Dev. 46, 176-189.
76. 2+ release in early and late events of mouse egg activation. Development 120, 1851-1859.
77. 3-sensitivity. Biol. Reprod. 57, 743-750.
78. i-protein to activation of phospholipases in rat-cultured hepatocytes. J. Biol. Chem. 268, 3739-3746.
79. Zera, E. M., Molloy, D. P., Angleson, J. K., Lamture, J. B., Wensel, T. G., and Malinski, J. A. (1996). Low affinity interactions of GDPβS and ribose-or phosphoryl-substituted GTP analogues with the heterotrimeric G protein, transducin. J. Biol. Chem. 271, 12925-12931.