Intracellular Ca2+ increase induces post-fertilization events via MAP kinase dephosphorylation in eggs of the hydrozoan jellyfish Cladonema pacificum

Developmental Biology

Volumn 293, Issue 1, 2006, Pages 228-241

  Kondoh, Eri ^a   Tachibana, Kazunori ^b   Deguchi, Ryusaku ^a  

^a MIYAGI UNIVERSITY OF EDUCATION   (Japan)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

BAPTA; BrdU; Cell cycle; Intracellular calcium increase; IP3; Mitogen activated protein kinase; Mos; Sperm attraction; Surface adhesion; U0126

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; BROXURIDINE; CALCIUM ION; CELL ADHESION MOLECULE; DNA; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; 1,2-BIS(2-AMINOPHENOXY)ETHANE-N,N,N',N'-TETRAACETIC ACID; 1,3 BUTADIENE DERIVATIVE; CALCIUM; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; NITRILE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ARTIFICIAL INSEMINATION; CALCIUM CELL LEVEL; CELL CYCLE PROGRESSION; CELL NUCLEUS; CELL SURFACE; CONTROLLED STUDY; CYTOKINESIS; DNA SYNTHESIS; EMBRYO; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE CONTROL; HYDROZOA; INJECTION; JELLYFISH; NIDATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; SPERM; ANIMAL; CELL ADHESION; CELL CYCLE; DRUG EFFECT; ENZYMOLOGY; FERTILIZATION; METABOLISM; OOCYTE; PHOSPHORYLATION; PHYSIOLOGY;

CLADONEMA; CLADONEMA PACIFICUM; SCYPHOZOA;

ANIMALS; BUTADIENES; CALCIUM; CELL ADHESION; CELL CYCLE; CHELATING AGENTS; EGTAZIC ACID; FERTILIZATION; HYDROZOA; INOSITOL 1,4,5-TRISPHOSPHATE; MITOGEN-ACTIVATED PROTEIN KINASES; NITRILES; OVUM; PHOSPHORYLATION;

EID: 33744994769     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.02.005     Document Type: Article

References (74)

1. Abrieu A., Fisher D., Simon M., Dorée M., and Picard A. MAPK inactivation is required for the G2 to M-phase transition of the first mitotic cell cycle. EMBO J. 16 (1997) 6407-6413
2. Abrieu A., Dorée M., and Fisher D. The interplay between cyclin-B-Cdc2 kinase (MPF) and MAP kinase during maturation of oocytes. J. Cell Sci. 114 (2001) 257-267
3. 2+, and calmodulin. Cell. Signalling 14 (2002) 649-654
4. Carré D., and Sardet C. Sperm chemotaxis in siphonophores. Biol. Cell 40 (1981) 119-128
5. Carroll D.J., Albay D.T., Hoang K.M., O'Neill F.J., Kumano M., and Foltz K.R. The relationship between calcium, MAP kinase, and DNA synthesis in the sea urchin egg at fertilization. Dev. Biol. 217 (2000) 179-191
6. Chiri S., De Nadai C., and Ciapa B. Evidence for MAP kinase activation during mitotic division. J. Cell Sci. 111 (1998) 2519-2527
7. Collins A.G. Phylogeny of Medusozoa and the evolution of cnidarian life cycles. J. Evol. Biol. 15 (2002) 418-432
8. Coppolino M.G., and Dedhar S. Ligand-specific, transient interaction between integrins and calreticulin during cell adhesion to extracellular matrix proteins is dependent upon phosphorylation/dephosphorylation events. Biochem. J. 340 (1999) 41-50
9. Coppolino M.G., Woodside M.J., Demaurex N., Grinstein S., St-Arnaud R., and Dedhar S. Calreticulin is essential for integrin-mediated calcium signalling and cell adhesion. Nature 386 (1997) 843-847
10. Cosson J., Carré D., and Cosson M.P. Sperm chemotaxis in siphonophores: identification and biochemical properties of the attractant. Cell Motil. Cytoskeleton 6 (1986) 225-228
11. 2+ increases in fertilized oocytes of the marine bivalve Mactra chinensis. J. Cell Sci. 116 (2003) 367-376
12. 2+ oscillations in fertilized mouse eggs. Dev. Biol. 218 (2000) 299-313
13. 2+ increases at fertilization in eggs of jellyfish (Phylum Cnidaria, Class Hydrozoa). Dev. Biol. 279 (2005) 291-307
14. English J., Pearson G., Wilsbacher J., Swantek J., Karandikar M., Xu S., and Cobb M.H. New insights into the control of MAP kinase pathways. Exp. Cell Res. 253 (1999) 255-270
15. Fan H.-Y., and Sun Q.-Y. Involvement of mitogen-activated protein kinase cascade during oocyte maturation and fertilization in mammals. Biol. Reprod. 70 (2004) 535-547
16. Favata M.F., Horiuchi K.Y., Manos E.J., Daulerio A.J., Stradley D.A., Feeser W.S., Van Dyk D.E., Pitts W.J., Earl R.A., Hobbs F., Copeland R.A., Magolda R.L., Scherle P.A., and Trzaskos J.M. Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273 (1998) 18623-18632
17. 2-M phase transition in early embryogenesis cell cycles of the starfishes Marthasterias glacialis and Astropecten aranciacus. Dev. Biol. 202 (1998) 1-13
18. Freeman G. The role of oocyte maturation in the ontogeny of the fertilization site in the hydrozoan Hydractinia echinata. Roux's Arch. Dev. Biol. 196 (1987) 83-92
19. Freeman G., and Miller R.L. Hydrozoan eggs can only be fertilized at the site of polar body formation. Dev. Biol. 94 (1982) 142-152
20. Freeman G., and Ridgway E.B. Endogenous photoproteins as calcium indicators in hydrozoan eggs and larvae. Zool. Sci. 8 (1991) 225-233
21. Freeman G., and Ridgway E.B. The role of intracellular calcium and pH during fertilization and egg activation in the hydrozoan Phialidium. Dev. Biol. 156 (1993) 176-190
22. Gilbert S.F. Developmental Biology. 7th ed. (2003), Sinauer Associates, Sunderland
23. Gould M.C., and Stephano J.L. MAP kinase, meiosis, and sperm centrosome suppression in Urechis caupo. Dev. Biol. 216 (1999) 348-358
24. Harada K., Oita E., and Chiba K. Metaphase I arrest of starfish oocytes induced via the MAP kinase pathway is released by an increase of intracellular pH. Development 130 (2003) 4581-4586
25. Hinchcliffe E.H., Cassels G.O., Rieder C.L., and Sluder G. The coordination of centrosome reproduction with nuclear events of the cell cycle in the sea urchin zygote. J. Cell Biol. 140 (1998) 1417-1426
26. Hirai E., and Kakinuma Y. Developmental cycle of Cladonema radiatum var. mayeri Perkins reared in the laboratory. Bull. Mar. Biol. Stn. Asamushi, Tohoku Univ. 8 (1957) 49-54
27. Iwasaki H., Chiba K., Uchiyama T., Yoshikawa F., Suzuki F., Ikeda M., Furuichi T., and Mikoshiba K. Molecular characterization of the starfish inositol 1,4,5-trisphosphate receptor and its role during oocyte maturation and fertilization. J. Biol. Chem. 277 (2002) 2763-2772
28. 2+ signalling during fertilization of echinoderm eggs. Semin. Cell Dev. Biol. 12 (2001) 45-51
29. Kahl C.R., and Means A.R. Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr. Rev. 24 (2003) 719-736
30. Kishimoto T. More than G1 or G2 arrest: useful starfish oocyte system for investigating skillful MAP kinase. Biol. Cell 96 (2004) 241-244
31. Kültz D. Phylogenetic and functional classification of mitogen- and stress-activated protein kinases. J. Mol. Evol. 46 (1998) 571-588
32. Kumano M., Carroll D.J., Denu J.M., and Foltz K.R. Calcium-mediated inactivation of the MAP kinase pathway in sea urchin eggs at fertilization. Dev. Biol. 236 (2001) 244-257
33. Levasseur M., and McDougall A. Sperm-induced calcium oscillations at fertilisation in ascidians are controlled by cyclin B1-dependent kinase activity. Development 127 (2000) 631-641
34. Liu L., and Yang X. Interplay of maturation-promoting factor and mitogen-activated protein kinase inactivation during metaphase-to-interphase transition of activated bovine oocytes. Biol. Reprod. 61 (1999) 1-7
35. Marino M., Wilding M., and Dale B. Interaction of cell cycle kinases, microtubules, and chromatin in ascidian oocytes during meiosis. Mol. Reprod. Dev. 56 (2000) 155-162
36. Masui Y. Meiotic arrest in animal oocytes. In: Metz C.B., and Monroy A. (Eds). Biology of Fertilization vol. 1 (1985), Academic Press, New York 189-219
37. McDougall A., and Levasseur M. Sperm-triggered calcium oscillations during meiosis in ascidian oocytes first pause, restart, then stop: correlations with cell cycle kinase activity. Development 125 (1998) 4451-4459
38. Miller R.L. Site-specific sperm agglutination and the timed release of a sperm chemo-attractant by the egg of the leptomedusan, Orthopyxis caliculata. J. Exp. Zool. 205 (1978) 385-392
39. Miller R.L. Sperm chemotaxis in the hydromedusae: I. Species-specificity and sperm behavior. Mar. Biol. 53 (1979) 99-114
40. Miller R.L. Sperm chemo-orientation in the metazoa. In: Metz C.B., and Monroy A. (Eds). Biology of Fertilization vol. 2 (1985), Academic Press, New York 275-337
41. Moos J., Visconti P.E., Moore G.D., Schultz R.M., and Kopf G.S. Potential role of mitogen-activated protein kinase in pronuclear envelope assembly and disassembly following fertilization of mouse eggs. Biol. Reprod. 53 (1995) 692-699
42. Moreau J.-L., Marques F., Barakat A., Schatt P., Lozano J.-C., Peaucellier G., Picard A., and Genevière A.-M. Cdk2 activity is dispensable for the onset of DNA replication during the first mitotic cycles of the sea urchin early embryo. Dev. Biol. 200 (1998) 182-197
43. Murakami M.S., and Vande Woude G.F. Analysis of the early embryonic cell cycles of Xenopus; regulation of cell cycle length by Xe-wee1 and Mos. Development 125 (1998) 237-248
44. Philipova R., and Whitaker M. MAP kinase activity increases during mitosis in early sea urchin embryos. J. Cell Sci. 111 (1998) 2497-2505
45. Philipova R., Kisielewska J., Lu P., Larman M., Huang J.-Y., and Whitaker M. ERK1 activation is required for S-phase onset and cell cycle progression after fertilization in sea urchin embryos. Development 132 (2005) 579-589
46. Philippe H., Chenuil A., and Adoutte A. Can the Cambrian explosion be inferred through molecular phylogeny?. Development (1994) 15-25 (Suppl.)
47. Plows D., Briassouli P., Owen C., Zoumpourlis V., Garrett M.D., and Pintzas A. Ecdysone-inducible expression of oncogenic Ha-Ras in NIH 3T3 cells leads to transient nuclear localization of activated extracellular signal-regulated kinase regulated by mitogen-activated protein kinase phosphatase-1. Biochem. J. 362 (2002) 305-315
48. Portillo-López A., Gould M.C., and Stephano J.L. MAPK is involved in metaphase I arrest in oyster and mussel oocytes. Biol. Cell 95 (2003) 275-282
49. 1 phase cell cycle machinery. BioEssays 22 (2000) 818-826
50. Russo G.L., Kyozuka K., Antonazzo L., Tosti E., and Dale B. Maturation promoting factor in ascidian oocytes is regulated by different intracellular signals at meiosis I and II. Development 122 (1996) 1995-2003
51. Sadler K.C., and 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
52. Shibuya E.K., Boulton T.G., Cobb M.H., and Ruderman J.V. Activation of p42 MAP kinase and the release of oocytes from cell cycle arrest. EMBO J. 11 (1992) 3963-3975
53. Smythe T.L., and Stricker S.A. Germinal vesicle breakdown is not fully dependent on MAPK activation in maturing oocytes of marine nemertean worms. Mol. Reprod. Dev. 70 (2004) 91-102
54. Sohaskey M.L., and Ferrell Jr. J.E. Distinct, constitutively active MAPK phosphatases function in Xenopus oocytes: implication for p42 MAPK regulation in vivo. Mol. Biol. Cell 10 (1999) 3729-3743
55. Stephano J.L., and Gould M.C. MAP kinase, a universal suppressor of sperm centrosomes during meiosis?. Dev. Biol. 222 (2000) 420-428
56. Stricker S.A. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 211 (1999) 157-176
57. 2+ signaling in maturing and fertilized oocytes of marine protostome worms: the roles of MAPKs and MPF. Development 130 (2003) 2867-2879
58. Sumerel J.L., Moore J.C., Schnackenberg B.J., Nichols J.A., Canman J.C., Wessel G.M., and Marzluff W.F. Cyclin E and its associated cdk activity do not cycle during early embryogenesis of the sea urchin. Dev. Biol. 234 (2001) 425-440
59. Swann K., and Whitaker M. The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J. Cell Biol. 103 (1986) 2333-2342
60. Tachibana K., Machida T., Nomura Y., and 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
61. Tachibana K., Tanaka D., Isobe T., and Kishimoto T. c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 14301-14306
62. Tan X., Wang Y.-C., Sun Q.-Y., Peng A., Chen D.-Y., and Tang Y.-Z. Effects of MAP kinase pathway and other factors on meiosis of Urechis unicinctus eggs. Mol. Reprod. Dev. 71 (2005) 67-76
63. Tunquist B.J., and Maller J.L. Under arrest: cytostatic factor (CSF)-mediated metaphase arrest in vertebrate eggs. Genes Dev. 17 (2003) 683-710
64. Tutuncu L., Stein P., Ord T.S., Jorgez C.J., and Williams C.J. Calreticulin on the mouse egg surface mediates transmembrane signaling linked to cell cycle resumption. Dev. Biol. 270 (2004) 246-260
65. Verlhac M.-H., Kubiak J.Z., Clarke H.J., and Maro B. Microtubule and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120 (1994) 1017-1025
66. Watanabe N., Hunt T., Ikawa Y., and Sagata N. Independent inactivation of MPF and cytostatic factor (Mos) upon fertilization of Xenopus eggs. Nature 352 (1991) 247-248
67. Wessel G.M., Brooks J.M., Green E., Haley S., Voronina E., Wong J., Zaydfudim V., and Conner S. The biology of cortical granules. Int. Rev. Cytol. 209 (2001) 117-206
68. Widmann C., Gibson S., Jarpe M.B., and Johnson G.L. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79 (1999) 143-180
69. Wilding M., Wright E.M., Patel R., Ellis-Davies G., and Whitaker M. Local perinuclear calcium signals associated with mitosis-entry in early sea urchin embryos. J. Cell Biol. 135 (1996) 191-199
70. Yamashita M. A fine structural study of the fertilization process of the jellyfish Cladonema uchidai. Dev. Growth Differ. 30 (1987) 81-91
71. Yoshida M., Inaba K., and Morisawa M. Sperm chemotaxis during the process of fertilization in the ascidians Ciona savignyi and Ciona intestinalis. Dev. Biol. 157 (1993) 497-506
72. Yoshida M., Murata M., Inaba K., and Morisawa M. A chemoattractant for ascidian spermatozoa is a sulfated steroid. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 14831-14836
73. Zhang W., and Liu H.T. MAPK signal pathways in the regulation of cell proliferation in mammalian cells. Cell Res. 12 (2002) 9-18
74. Zhang W.L., Huitorel P., Glass R., Fernandez-Serra M., Arnone M.I., Chiri S., Picard A., and Ciapa B. A MAPK pathway is involved in the control of mitosis after fertilization of the sea urchin egg. Dev. Biol. 282 (2005) 192-206