Involvement of Rho family G protein in the cell signaling for sperm incorporation during fertilization of mouse eggs: Inhibition by Clostridium difficile toxin B

Developmental Biology

Volumn 260, Issue 2, 2003, Pages 522-535

  Kumakiri, Jun ^a,b   Oda, Shoji ^a   Kinoshita, Katsuyuki ^b   Miyazaki, Shunichi ^a  

^a TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Actin filament; Calcium oscillation; Clostridium difficile toxin B; Fertilization; Gamete fusion; Mouse egg; Rho family G protein; Sperm incorporation

Indexed keywords

ACTIN; CALCIUM ION; CELL CYCLE PROTEIN; CLOSTRIDIUM DIFFICILE TOXIN B; CYTOCHALASIN D; DYE; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL INSEMINATION; BRAIN CORTEX; CALCIUM CELL LEVEL; CLOSTRIDIUM DIFFICILE; CONTROLLED STUDY; CYTOPLASM; CYTOSKELETON; DOSE RESPONSE; EGG; FEMALE; FERTILIZATION; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPERM; SPERMATOZOON; STAINING;

CLOSTRIDIUM; CLOSTRIDIUM DIFFICILE;

EID: 0042061388     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0012-1606(03)00273-2     Document Type: Article

References (59)

1. Aida T., Oda S., Awaji T., Yoshida K., Miyazaki S. Expression of a green fluorescent protein variant in mouse oocytes by injection of RNA with an added long poly(A) tail. Mol. Hum. Reprod. 7:2001;1039-1046.
2. Aktories K., Schmidt G., Just I. Rho GTPases as targets of bacterial protein toxins. Biol. Chem. 381:2000;421-426.
3. Almeida E.A.C., Huovila A.P.J., Sutherland A.E., Stephens L.E., Calarco P.G., Shaw L.M., Mercurio A.M., Sonnenberg A., Primakoff P., Myles D.G., White J.M. Mouse egg integrin α6β1 functions as a sperm receptor. Cell. 81:1995;1095-1104.
4. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochem. J. 348:2000;241-255.
5. Chardin P., Boquet P., Madaule P., Popoff M.R., Rubin E.J., Gill D.M. The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO J. 8:1989;1087-1092.
6. Chaves-Olarte E., Weidmann M., von Eichel-Streiber C., Thelestam M. Toxins A and B from Clostridium difficile differ with respect to enzymatic potencies, cellular substrate specificities, and surface binding to cultured cells. J. Clin. Invest. 100:1997;1734-1741.
7. Cho C., Bunch D.O., Faure J.E., Goulding E.H., Eddy E.M., Primakoff P., Myles D.G. Fertilization defects in sperm from mice lacking fertilin β Science. 281:1998;1857-1859.
8. Chong L.D., Traynor-Kaplan A., Bokoch G.M., Schwartz M.A. The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell. 79:1994;507-513.
9. Connors S.A., Kanatsu-Shinohara M., Schultz R.M., Kopf G.S. Involvement of the cytoskeleton in the movement of cortical granules during oocyte maturation, and cortical granule anchoring in mouse eggs. Dev. Biol. 200:1998;103-115.
10. 2+ oscillations in fertilized mouse eggs. Dev. Biol. 218:2000;299-313.
11. Fulton B.P., Whittingham D.G. Activation of mammalian oocytes by intracellular injection of calcium. Nature. 273:1978;149-151.
12. Hartwig J.H., Bokoch G.M., Carpenter C.L., Janmey P.A., Taylor L.A., Toker A., Stossel T.P. Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets. Cell. 82:1995;643-653.
13. 2+ oscillations in the activation of the egg and development of the embryo in mammals. Int. J. Dev. Biol. 42:1998;1-10.
14. Just I., Selzer J., Wilm M., von Eichel-Streiber C., Mann M., Aktories K. Glucosylation of Rho proteins by Clostridium difficile toxin B. Nature. 375:1995;500-503.
15. Kaji K., Oda S., Shikano T., Ohnuki T., Uematsu Y., Sakagami J., Tada N., Miyazaki S., Kudo A. The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat. Genet. 24:2000;279-282.
16. 2+ increase at fertilization in the mouse. Development. 124:1997;233-241.
17. Le Naour F., Rubinstein E., Jasmin C., Prenant M., Boucheix C. Severely reduced female fertility in CD9-deficient mice. Science. 287:2000;319-321.
18. Li E., Stupack D., Bokoch G.M., Nemerow G.R. Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J. Virol. 72:1998;8806-8812.
19. Longo F.J. Effects of cytochalasin B on sperm-egg interactions. Dev. Biol. 67:1978;249-265.
20. Mabuchi I., Hamaguchi Y., Fujimoto H., Morii N., Mishima M., Narumiya S. A rho-like protein is involved in the organization of the contractile ring in dividing sand dollar eggs. Zygote. 1:1993;325-331.
21. Maro B., Johnson M.H., Pickering S.J., Flach G. Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81:1984;211-237.
22. Matozaki T., Nakanishi H., Takai Y. Small G-protein networks their crosstalk and signal cascades . Cell. Signal. 12:2000;515-524.
23. McAvey B.A., Wortzman G.B., Williams C.J., Evans J.P. Involvement of calcium signaling and the actin cytoskeleton in the membrane block to polyspermy in mouse eggs. Biol. Reprod. 67:2002;1342-1352.
24. Miller B.J., Georges-Labouesse E., Primakoff P., Myles D.G. Normal fertilization occurs with eggs lacking the integrin α6β1 and is CD9-dependent. J. Cell Biol. 149:2000;1289-1295.
25. Miyado K., Yamada G., Yamada S., Hasuwa H., Nakamura Y., Ryu F., Suzuki K., Kosai K., Inoue K., Ogura A., Okabe M., Mekada E. Requirement of CD9 on the egg plasma membrane for fertilization. Science. 287:2000;321-324.
26. 2+ oscillations at fertilization of mammalian eggs. Dev. Biol. 158:1993;62-78.
27. Moore G.D., Ayabe T., Visconti P.E., Schultz R.M., Kopf G.S. Roles of heterotrimeric and monomeric G proteins in sperm-induced activation of mouse eggs. Development. 120:1994;3313-3323.
28. Müller H., von Eichel-Streiber C., Habermann E. Morphological changes of cultured endothelial cells after microinjection of toxins that act on the cytoskeleton. Infect. Immun. 60:1992;3007-3010.
29. Nakano Y., Shirakawa H., Mitsuhashi N., Kuwabara Y., Miyazaki S. Spatiotemporal dynamics of intracellular calcium in the mouse egg injected with a spermatozoon. Mol. Hum. Reprod. 3:1997;1087-1093.
30. Nishimura H., Cho C., Branciforte D.R., Myles D.G., Primakoff P. Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin β Dev. Biol. 233:2001;204-213.
31. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell. 81:1995;53-62.
32. 2+ wave from the cortex mediated by the inositol 1,4,5-trisphosphate receptor . Dev. Biol. 209:1999;172-185.
33. Perry A.C.F., Wakayama T., Cooke I.M., Yanagimachi R. Mammalian oocyte activation by the synergistic action of discrete sperm head components induction of calcium transients and involvement of proteolysis . Dev. Biol. 217:2000;386-393.
34. Perry A.C.F., Wakayama T., Yanagimachi R. A novel trans-complementation assay suggests full mammalian oocyte activation is coordinately initiated by multiple, submembrane sperm components. Biol. Reprod. 60:1999;747-755.
35. Prepens U., Just I., von Eichel-Streiber C., Aktories K. Inhibition of FcεRI-mediated activation of rat basophilic leukemia cells by Clostridium difficile toxin B (monoglucosyltransferase). J. Biol. Chem. 271:1996;7324-7329.
36. Ridley A.J. Rho family proteins coordinating cell responses . Trends Cell Biol. 11:2001;471-477.
37. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell. 70:1992;389-399.
38. Ridley A.J., Paterson H.F., Johnston C.L., Diekmann D., Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:1992;401-410.
39. Rogers B.J., Bastias C., Coulson R.L., Russell L.D. Cytochalasin D inhibits penetration of hamster eggs by guinea pig and human spermatozoa. J. Androl. 10:1989;275-282.
40. 2+ oscillations in eggs and embryo development . Development. 129:2002;3533-3544.
41. Schatten H., Schatten G. Surface activity at the egg plasma membrane during sperm incorporation and its cytochalasin B sensitivity. Scanning electron microscopy and time-lapse video microscopy during fertilization of sea urchin Lytechinus variegatus. Dev. Biol. 78:1980;435-449.
42. Schmidt M., Bienek C., Rumenapp U., Zhang C., Lummen G., Jakobs K.H., Just I., Aktories K., Moos M., von Eichel-Streiber C. A role for Rho in receptor- and G protein-stimulated phospholipase C. Reduction in phosphatidylinositol 4,5-bisphosphate by Clostridium difficile toxin B. Naunyn Schmiedeberg's Arch. Pharmacol. 354:1996;87-94.
43. Schmitz A.A.P., Govek E.-E., Böttner B., Aelst L.V. Rho GTPases signaling, migration, and invasion . Exp. Cell Res. 261:2000;1-12.
44. Schwartz M.A., Shattil S.J. Signaling networks linking integrins and Rho family GTPases. Trends Biochem. Sci. 25:2000;388-391.
45. 2+ release during maturation of hamster oocytes. Dev. Biol. 170:1995;594-606.
46. Sun Q.-Y., Lai L., Park K.-W., Kühholzer B., Prather R.S., Schatten H. Dynamic events are differently mediated by microfilaments, microtubules, and mitogen-activated protein kinase during porcine oocyte maturation and fertilization in vitro. Biol. Reprod. 64:2001;879-889.
47. Sutovsky P., Navara C.S., Schatten G. Fate of the sperm mitochondria, and the incorporation, conversion, and disassembly of the sperm tail structures during bovine fertilization. Biol. Reprod. 55:1996;1195-1205.
48. 2+ release in eggs at fertilization. Rev. Reprod. 1:1996;33-39.
49. Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiol. Rev. 81:2001;153-208.
50. Talbot P., Shur B.D., Myles D.G. Cell adhesion, and fertilization steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion . Biol. Reprod. 68:2003;1-9.
51. Tilney L.G., Jaffe L.A. Actin, microvilli, and the fertilization cone of sea urchin eggs. J. Cell Biol. 87:1980;771-782.
52. Thelestam M., Chaves-Olarte E. Cytotoxic effects of the Clostridium difficile toxins. Curr. Top. Microbiol. Immunol. 250:2000;85-96.
53. Tsukita S., Yonemura S., Tsukita S. ERM (ezrin/radixin/moesin) family from cytoskeleton to signal transduction . Curr. Opin. Cell Biol. 9:1997;70-75.
54. Wang Y., Mattson M.P., Furukawa K. Endoplasmic reticulum calcium release is modulated by actin polymerization. J. Neurochem. 82:2002;945-952.
55. Whittingham D.G. Culture of mouse ova. J. Reprod. Fertil. Suppl. 14:1971;7-21.
56. Yamada K.M., Geiger B. Molecular interactions in cell adhesion complexes. Curr. Opin. Cell Biol. 9:1997;76-85.
57. Yanagimachi R. Mechanisms of fertilization in mammals. Mastroianni L., Biggers J.L. Fertilization and Embryonic Development in vitro. 1981;81-182 Plenum Press, New York.
58. Yanagimachi R. Mammalian fertilization. Knobland E., Neill J. Physiology of Reproduction. 1994;189-317 Raven Press, New York.
59. Yanagimachi R., Noda Y.D. Electron microscope studies of sperm incorporation into the golden hamster egg. Am. J. Anat. 128:1970;429-462.