Egg activation events are regulated by the duration of a sustained [Ca 2+]cyt signal in the mouse

Developmental Biology

Volumn 282, Issue 1, 2005, Pages 39-54

  Ozil, Jean Pierre ^a   Markoulaki, Styliani ^b,c   Toth, Szabolcs ^a   Matson, Sara ^b,c   Banrezes, Bernadette ^a   Knott, Jason G ^d   Schultz, Richard M ^d   Huneau, Daniel ^a   Ducibella, Tom ^b,c  

^a INRA Institut National de la Recherche Agronomique   (France)

^b TUFTS MEDICAL CENTER   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Ca2+ signal duration; CaMKII; Egg activation; Electropermeabilization; Phosphoinositide; Preimplantation mouse embryo

Indexed keywords

MESSENGER RNA; PROTEIN KINASE (CALCIUM,CALMODULIN) II;

ANIMAL CELL; ANIMAL EMBRYO; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; BLASTOCYST; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL CYCLE; CELL DEATH; CONTROLLED STUDY; DOWN REGULATION; EGG; ELECTROPORATION; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVITY; EXOCYTOSIS; FEMALE; FERTILIZATION; MOUSE; NONHUMAN; PRIORITY JOURNAL;

MAMMALIA;

EID: 20344385241     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.02.035     Document Type: Article

References (53)

1. A.L. Abbott, R.A. Fissore, and T. Ducibella Incompetence of preovulatory mouse oocytes to undergo cortical granule exocytosis following induced calcium oscillations Dev. Biol. 207 1999 38 48
2. B. Banrezes, S. Toth, D. Huneau, R.M. Schultz, and J.P. Ozil A method to drive calcium signalling dynamics in fertilized eggs Reprod. Fertil. Dev. 16 2004 268
3. M.J. Berridge, and A. Galione Cytosolic calcium oscillators FASEB J. 2 1988 3074 3082
4. M.J. Berridge, M.D. Bootman, and H.L. Roderick Calcium signalling: dynamics, homeostasis and remodelling Nat. Rev., Mol. Cell Biol. 4 2003 517 529
5. A. Bos-Mikich, D.G. Whittingham, and K.T. Jones Meiotic and mitotic Ca2+ oscillations affect cell composition in resulting blastocysts Dev. Biol. 182 1997 172 179
6. R. Caroppo, M. Colella, A. Colasuonno, A. DeLuisi, L. Debellis, S. Curci, and A.M. Hofer A reassessment of the effects of luminal [Ca2+] on inositol 1,4,5-trisphosphate-induced Ca2+ release from internal stores J. Biol. Chem. 278 2003 39503 39508
7. K.S. Cuthbertson Parthenogenetic activation of mouse oocytes in vitro with ethanol and benzyl alcohol J. Exp. Zool. 226 1983 311 314
8. R.E. Dolmetsch, R.S. Lewis, C.C. Goodnow, and J.I. Healy Differential activation of transcription factors induced by Ca2+ response amplitude and duration Nature 386 1997 855 858
9. M.R. Duchen Mitochondria and calcium: from cell signalling to cell death J. Physiol. 529 Pt. 1 2000 57 68
10. T. Ducibella Biochemical and cellular insights into the temporal window of normal fertilization Theriogenology 49 1998 53 65
11. T. Ducibella, D. Huneau, E. Angelichio, Z. Xu, R. Schultz, G. Kopf, R. Fissore, S. Madoux, and J.-P. Ozil Egg-to-embryo transition is driven by differential responses to Ca(2+) oscillation number Dev. Biol. 250 2002 280
12. G. Dupont, M.J. Berridge, and A. Goldbeter Signal-induced Ca2+ oscillations: properties of a model based on Ca(2+)-induced Ca2+ release Cell Calcium 12 1991 73 85
13. A. Goldbeter, G. Dupont, and M.J. Berridge Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation Proc. Natl. Acad. Sci. U. S. A. 87 1990 1461 1465
14. G. Grynkiewicz, M. Poenie, and R.Y. Tsien A new generation of Ca2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
15. T. Higo, M. Hattori, T. Nakamura, T. Natsume, T. Michikawa, and K. Mikoshiba Subtype-specific and ER lumenal environment-dependent regulation of inositol 1,4,5-trisphosphate receptor type 1 by ERp44 Cell 120 2005 85 98
16. Y. Igusa, and S. Miyazaki Effects of altered extracellular and intracellular calcium concentration on hyperpolarizing responses of the hamster egg J. Physiol. 340 1983 611 632
17. D.P. Kiehart Studies on the in vivo sensitivity of spindle microtubules to calcium ions and evidence for a vesicular calcium-sequestering system J. Cell Biol. 88 1981 604 617
18. Y. Kimura, and R. Yanagimachi Mouse oocytes injected with testicular spermatozoa or round spermatids can develop into normal offspring Development 121 1995 2397 2405
19. D. Kline, and J.T. Kline Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg Dev. Biol. 149 1992 80 89
20. J.G. Knott, M. Kurokawa, R.A. Fissore, R.M. Schultz, and C.J. Williams Transgenic RNAi reveals role for mouse sperm phospholipase Cz in triggering Ca2+ oscillations during fertilization Biol. Reprod. 72 2005 992 996
21. Z. Kouchi, K. Fukami, T. Shikano, S. Oda, Y. Nakamura, T. Takenawa, and S. Miyazaki Recombinant phospholipase Czeta has high Ca2+ sensitivity and induces Ca2+ oscillations in mouse eggs J. Biol. Chem. 279 2004 10408 10412
22. M. Kurokawa, and R.A. Fissore ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development Mol. Hum. Reprod. 9 2003 523 533
23. M. Kurokawa, K. Sato, and R.A. Fissore Mammalian fertilization: from sperm factor to phospholipase Czeta Biol. Cell 96 2004 37 45
24. Y. Lawrence, J.P. Ozil, and K. Swann The effects of a Ca2+ chelator and heavy-metal-ion chelators upon Ca2+ oscillations and activation at fertilization in mouse eggs suggest a role for repetitive Ca2+ increases Biochem. J. 335 Pt. 2 1998 335 342
25. S.J. Lee, and S.S. Shen The calcium transient in sea urchin eggs during fertilization requires the production of inositol 1,4,5-trisphosphate Dev. Biol. 193 1998 195 208
26. Y. Li, and P. Camacho Ca2+-dependent redox modulation of SERCA 2b by ERp57 J. Cell Biol. 164 2004 35 46
27. T. Lorca, F.H. Cruzalegui, D. Fesquet, J.C. Cavadore, J. Mery, A. Means, and M. Doree Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs Nature 366 1993 270 273
28. S. Markoulaki, S. Matson, A.L. Abbott, and T. Ducibella Oscillatory CaMKII activity in mouse egg activation Dev. Biol. 258 2003 464 474
29. S. Markoulaki, S. Matson, and T. Ducibella Fertilization stimulates long-lasting oscillations of CaMKII activity in mouse eggs Dev. Biol. 272 2004 15 25
30. T. Meyer, and L. Stryer Calcium spiking Annu. Rev. Biophys. Biophys. Chem. 20 1991 153 174
31. S. Miyazaki, H. Shirakawa, K. Nakada, and Y. Honda Essential role of the inositol 1,4,5-trisphosphate receptor/Ca2+ release channel in Ca2+ waves and Ca2+ oscillations at fertilization of mammalian eggs Dev. Biol. 158 1993 62 78
32. J. Moos, P.E. Visconti, G.D. Moore, R.M. Schultz, and G.S. Kopf Potential role of mitogen-activated protein kinase in pronuclear envelope assembly and disassembly following fertilization of mouse eggs Biol. Reprod. 53 1995 692 699
33. P. Nicotera, and S. Orrenius The role of calcium in apoptosis Cell Calcium 23 1998 173 180
34. V.L. Nixon, M. Levasseur, A. McDougall, and K.T. Jones Ca(2+) oscillations promote APC/C-dependent cyclin B1 degradation during metaphase arrest and completion of meiosis in fertilizing mouse eggs Curr. Biol. 12 2002 746 750
35. B. Oh, S.Y. Hwang, D. Solter, and B.B. Knowles Spindlin, a major maternal transcript expressed in the mouse during the transition from oocyte to embryo Development 124 1997 493 503
36. J.-P. Ozil Role of calcium oscillations in mammalian egg activation: experimental approach Biophys. Chem. 72 1998 141 152
37. J.-P. Ozil, and D. Huneau Activation of rabbit oocytes: the impact of the Ca2+ signal regime on development Development 128 2001 917 928
38. J.-P. Ozil, and K. Swann Stimulation of repetitive calcium transients in mouse eggs J. Physiol. 483 Pt. 2 1995 331 346
39. P.E. Rapp, A.I. Mees, and C.T. Sparrow Frequency encoded biochemical regulation is more accurate than amplitude dependent control J. Theor. Biol. 90 1981 531 544
40. C.M. Saunders, M.G. Larman, J. Parrington, L.J. Cox, J. Royse, L.M. Blayney, K. Swann, and F.A. Lai PLC zeta: a sperm-specific trigger of Ca(2+) oscillations in eggs and embryo development Development 129 2002 3533 3544
41. R.M. Schultz The molecular foundations of the maternal to zygotic transition in the preimplantation embryo Hum. Reprod. Updat. 8 2002 323 331
42. S.A. Stricker Comparative biology of calcium signaling during fertilization and egg activation in animals Dev. Biol. 211 1999 157 176
43. M.A. Surani, S.C. Barton, and M.L. Norris Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis Nature 308 1984 548 550
44. K. Swann, and J.P. Ozil Dynamics of the calcium signal that triggers mammalian egg activation Int. Rev. Cytol. 152 1994 183 222
45. K. Swann, D.H. McCulloh, A. McDougall, E.L. Chambers, and M. Whitaker Sperm-induced currents at fertilization in sea urchin eggs injected with EGTA and neomycin Dev. Biol. 151 1992 552 563
46. K. Swann, M.G. Larman, C.M. Saunders, and F.A. Lai The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLC{zeta} Reproduction 127 2004 431 439
47. R.R. Swezey, and D. Epel Stable, resealable pores formed in sea urchin eggs by electric discharge (electroporation) permit substrate loading for assay of enzymes in vivo Cell Regul. 1 1989 65 74
48. C. Tatone, S. Delle Monache, R. Iorio, D. Caserta, M. Di Cola, and R. Colonna Possible role for Ca(2+) calmodulin-dependent protein kinase II as an effector of the fertilization Ca(2+) signal in mouse oocyte activation Mol. Hum. Reprod. 8 2002 750 757
49. T. Whalley, A. McDougall, I. Crossley, K. Swann, and M. Whitaker 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
50. D.G. Whittingham Parthenognesis in mammals Oxf. Rev. Reprod. Biol. 2 1980 205 231
51. Z. Xu, L. Lefevre, T. Ducibella, R.M. Schultz, and G.S. Kopf Effects of calcium-BAPTA buffers and the calmodulin antagonist W-7 on mouse egg activation Dev. Biol. 180 1996 594 604
52. Z. Xu, A. Abbott, G.S. Kopf, R.M. Schultz, and T. Ducibella Spontaneous activation of ovulated mouse eggs: time-dependent effects on M-phase exit, cortical granule exocytosis, maternal messenger ribonucleic acid recruitment, and inositol 1,4,5-trisphosphate sensitivity Biol. Reprod. 57 1997 743 750
53. Z. Xu, C.J. Williams, G.S. Kopf, and R.M. Schultz Maturation-associated increase in IP3 receptor type 1: role in conferring increased IP3 sensitivity and Ca2+ oscillatory behavior in mouse eggs Dev. Biol. 254 2003 163 171