Effects of ionomycin on egg activation and early development in starfish

PLoS ONE

Volumn 7, Issue 6, 2012, Pages

  Vasilev, Filip ^a   Chun, Jong T ^a   Gragnaniello, Giovanni ^a   Garante, Ezio ^a   Santella, Luigia ^a  

^a STAZIONE ZOOLOGICA ANTON DOHRN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; IONOMYCIN;

ACTIN FILAMENT; ANALYTIC METHOD; ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM IMAGING; CELL DISRUPTION; CELL DIVISION; CELL FUSION; CELL GRANULE; CELL NUCLEUS MEMBRANE; CELL VACUOLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOPLASM; DEPOLYMERIZATION; EMBRYO; FEMALE; FERTILIZATION; MICROINJECTION; MICROVILLUS; NONHUMAN; OOCYTE CORTEX; OOCYTE DEVELOPMENT; OOCYTE MATURATION; POLYMERIZATION; STARFISH; TRANSMISSION ELECTRON MICROSCOPY; ZYGOTE;

ACTINS; ANIMALS; CALCIUM; CALCIUM SIGNALING; EMBRYONIC DEVELOPMENT; EXOCYTOSIS; FEMALE; FERTILIZATION; INTRACELLULAR SPACE; IONOMYCIN; MICROINJECTIONS; MICROVILLI; OOCYTES; OVUM; STARFISH;

EID: 84862499642     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0039231     Document Type: Article

References (64)

1. Trimmer JS, Vacquier VD, (1986) Activation of sea urchin gametes. Annu Rev Cell Biol 2: 1-26.
2. Epel D, (1990) The initiation of development at fertilization. Cell Differ Dev 29: 1-12.
3. Ridgway EB, Gilkey JC, Jaffe LF, (1977) Free calcium increases explosively in activating medaka eggs. Proc Natl Acad U S A 74: 623-627.
4. Miyazaki S, (1991) Repetitive calcium transients in hamster oocytes. Cell Calcium 12: 205-216.
5. Jaffe LF, (2002) On the conservation of fast calcium wave speeds. Cell Calcium 32: 217-229.
6. Steinhardt RA, Epel D, (1974) Activation of sea urchin eggs by a calcium ionophore. Proc Natl Acad Sci U S A 71: 1915-1919.
7. Steinhardt RA, Epel D, Carroll EJ, Yanagimachi R, (1974) Is calcium ionophore a universal activator for unfertilized eggs? Nature 252: 41-43.
8. Ciapa B, Arnoult C, (2011) Could modifications of signalling pathways activated after ICSI induce a potential risk of epigenetic defects? Int J Dev Biol 55: 143-152.
9. Santella L, Kyozuka K, Genazzani AA, De Riso L, Carafoli E, (2000) Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. Interactions among distinct Ca2+ mobilizing mechanisms in starfish oocytes. J Biol Chem 275: 8301-8306.
10. Santella L, Lim D, Moccia F, (2004) Calcium and fertilization: the beginning of life. Trends Biochem Sci 29: 400-408.
11. Whitaker M, (2006) Calcium at fertilization and in early development. Physiol Rev 86: 25-88.
12. Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L, (2001) NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J 15: 2257-2267.
13. Liu WC, Slusarchyk DS, Astle G, Trejo WH, Brown WE, Meyers E, (1978) Ionomycin, a new polyether antibiotic. J Antibiot (Tokyo) 31: 815-819.
14. Liu C, Hermann TE, (1978) Characterization of ionomycin as a calcium ionophore. J Biol Chem 253: 5892-5894.
15. Erdahl WL, Chapman CJ, Taylor RW, Pfeiffer DR, (1994) Ca2+ transport properties of ionophores A23187, ionomycin, and 4-BrA23187 in a well defined model system. Biophys J 66: 1678-1693.
16. Kauffman RF, Taylor RW, Pfeiffer DR, (1980) Cation transport and specificity of ionomycin - comparison with ionophore A23187 in rat liver mitochondria. J Biol Chem 255: 2735-2739.
17. Morgan AJ, Jacob R, (1994) Ionomycin enhances Ca2+ influx by stimulating store-regulated cation entry and not by a direct action at the plasma membrane. Biochem J 300: 665-672.
18. Mason MJ, Grinstein S, (1993) Ionomycin activates electrogenic Ca2+ influx in rat thymic lymphocytes. Biochem J 296: 22-39.
19. Moreau M, Guerrier P, Doree M, Ashley CC, (1978) Hormone-induced release of intracellular Ca2+ triggers meiosis in starfish oocytes. Nature 272: 251-253.
20. Santella L, Kyozuka K, (1994) Reinitiation of meiosis in starfish oocytes requires an increase in nuclear Ca2+. Biochem Biophys Res Commun 203: 674-680.
21. Kyozuka K, Chun JT, Puppo A, Gragnaniello G, Garante E, et al. (2008) Actin cytoskeleton modulates calcium signaling during maturation of starfish oocytes. Dev Biol 320: 426-435.
22. Santella L, De Riso L, Gragnaniello G, Kyozuka K, (1999) Cortical granule translocation during maturation of starfish oocytes requires cytoskeletal rearrangement triggered by InsP3-mediated Ca2+ release. Exp Cell Res 248: 567-574.
23. Wessel GM, Conner SD, Berg L, (2002) Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte. Development 129: 4315-4325.
24. Schuetz AW, (1975) Cytoplasmic activation of starfish oocytes by sperm and divalent ionophore A-23187. J Cell Biol 66: 86-94.
25. Kater SB, Mattson MP, Cohan C, Connor J, (1988) Calcium regulation of the neuronal growth cone. Trends Neurosci 11: 315-321.
26. Forscher P, (1989) Calcium and polyphosphoinositide control of cytoskeletal dynamics. Trends Neurosci 12: 468-474.
27. Spira ME, Oren R, Dormann A, Ilouz N, Lev S, (2001) Calcium, protease activation, and cytoskeleton remodeling underlie growth cone formation and neuronal regeneration. Cell Mol Neurobiol 21: 591-604.
28. Hirohashi N, Harada K, Chiba K, (2008) Hormone-induced cortical maturation ensures the slow block to polyspermy and does not couple with meiotic maturation in starfish. Dev Biol 318: 194-202.
29. Terasaki M, Runft L, (2010) Two-stage dependence for 1-methyladenine induced reinitiation of meiotic maturation in starfish oocytes. Exp Cell Res 316: 2654-2663.
30. Moccia F, Lim D, Nusco GA, Ercolano E, Santella L, (2003) NAADP activates a Ca2+ current that is dependent on F-actin cytoskeleton. FASEB J 17: 1907-1909.
31. Churchill GC, O'Neill JS, Masgrau R, Patel S, Thomas JM, et al. (2003) Sperm deliver a new second messenger: NAADP. Curr Biol 13: 125-128.
32. Muallem S, Kwiatkowska K, Xu X, Yin HL, (1995) Actin filament disassembly is a sufficient final trigger for exocytosis in nonexcitable cells. J Cell Biol 128: 589-598.
33. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, Bader MF, (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15: 520-531.
34. Malacombe M, Bader MF, Gasman S, (2006) Exocytosis in neuroendocrine cells: new tasks for actin. Biochim Biophys Acta 1763: 1175-1183.
35. Puppo A, Chun JT, Gragnaniello G, Garante E, Santella L, (2008) Alteration of the cortical actin cytoskeleton deregulates Ca2+ signaling, monospermic fertilization, and sperm entry. PLoS One 3: e3588.
36. Chun JT, Puppo A, Vasilev F, Gragnaniello G, Garante E, et al. (2010) The biphasic increase of PIP2 in the fertilized eggs of starfish: new roles in actin polymerization and Ca2+ signaling. PLoS One 5: e14100.
37. Terasaki M, (1996) Actin filament translocations in sea urchin eggs. Cell Motil Cytoskeleton 34: 48-56.
38. Terada Y, Hasegawa H, Takahashi A, Ugajin T, Yaegashi N, et al. (2009) Successful pregnancy after oocyte activation by a calcium ionophore for a patient with recurrent intracytoplasmic sperm injection failure, with an assessment of oocyte activation and sperm centrosomal function using bovine eggs. Fertil Steril 91: 935.e11-14.
39. Heytens E, Schmitt-John T, Moser JM, Jensen NM, Soleimani R, et al. (2010) Reduced fertilization after ICSI and abnormal phospholipase C zeta presence in spermatozoa from the wobbler mouse. Reprod Biomed Online 21: 742-749.
40. Burtnick LD, Urosev D, Irobi E, Narayan K, Robinson RC, (2004) Structure of the N-terminal half of gelsolin bound to actin: roles in severing, apoptosis and FAF. EMBO J 23: 2713-2722.
41. Carlier MF, Pantaloni D, Korn ED, (1986) Fluorescence measurements of the binding of cations to high-affinity and low-affinity sites on ATP-G-actin. J Biol Chem 261: 10778-10784.
42. Gershman LC, Selden LA, Estes JE, (1986) High affinity binding of divalent cation to actin monomer is much stronger than previously reported. Biochem Biophys Res Commun 135: 607-614.
43. Kasai M, Oosawa F, (1969) Behavior of divalent cations and nucleotides bound to F-actin. Biochim Biophys Acta 172: 300-310.
44. Lange K, Gartzke J, (2006) F-actin-based Ca signaling-a critical comparison with the current concept of Ca signaling. J Cell Physiol 209: 270-287.
45. Santella L, Chun JT, (2011) Actin, more than just a housekeeping protein at the scene of fertilization. Sci China Life Sci 54: 733-743.
46. Darbellay B, Arnaudeau S, Bader CR, Konig S, Bernheim L, (2011) STIM1L is a new actin-binding splice variant involved in fast repetitive Ca2+ release. J Cell Biol 194: 335-346.
47. Reunova AA, Crawford BJ, (2010) An ultrastructural study of oocyte atresia in the starfish Pisaster ochraceus. Zoology 113: 295-300.
48. Ramos IB, Miranda K, Pace DA, Verbist KC, Lin FY, et al. (2010) Calcium- and polyphosphate-containing acidic granules of sea urchin eggs are similar to acidocalcisomes, but are not the targets for NAADP. Biochem J 429: 485-495.
49. Yoshida S, Plant S, (1992) Mechanism of release of Ca2+ from intracellular stores in response to ionomycin in oocytes of the frog Xenopus laevis. J Physiol 458: 307-318.
50. Chiba K, Kado RT, Jaffe LA, (1990) Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol 140: 300-306.
51. Lim D, Ercolano E, Kyozuka K, Nusco GA, Moccia F, et al. (2003) The M-phase-promoting factor modulates the sensitivity of the Ca2+ stores to inositol 1,4,5-trisphosphate via the actin cytoskeleton. J Biol Chem 278: 42505-42514.
52. Gillot I, Ciapa B, Payan P, Sardet C, (1991) The calcium content of cortical granules and the loss of calcium from sea urchin eggs at fertilization. Dev Biol 146: 396-405.
53. Rizzuto R, Pozzan T, (2006) Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev 86: 369-408.
54. McPherson SM, McPherson PS, Mathews L, Campbell KP, Longo FJ, (1992) Cortical localization of a calcium release channel in sea urchin eggs. J Cell Biol 116: 1111-1121.
55. Oberdorf JA, Head JF, Kaminer B, (1986) Calcium uptake and release by isolated cortices and microsomes from the unfertilized egg of the sea urchin Strongylocentrotus droebachiensis. J Cell Biol 102: 2205-2210.
56. Calcraft PJ, Ruas M, Pan Z, Cheng X, Arredouani A, et al. (2009) NAADP mobilizes calcium from acidic organelles through two-pore channels. Nature 459: 596-600.
57. Nusco GA, Chun JT, Ercolano E, Lim D, Gragnaniello G, et al. (2006) Modulation of calcium signalling by the actin-binding protein cofilin. Biochem Biophys Res Commun 348: 109-114.
58. Chun JT, Santella L, (2009) Roles of the actin-binding proteins in intracellular Ca2+ signalling. Acta Physiol 195: 61-70.
59. Lee HK, Yang Y, Su Z, Hyeon C, Lee TS, et al. (2010) Dynamic Ca2+-dependent stimulation of vesicle fusion by membrane-anchored synaptotagmin. Science 328: 760-763.
60. Morgan AJ, (2011) Sea urchin eggs in the acid reign. Cell Calcium 50: 147-156.
61. van Rheenen J, Jalink K, (2002) Agonist-induced PIP2 hydrolysis inhibits cortical actin dynamics: regulation at a global but not at a micrometer scale. Mol Biol Cell 13: 3257-3267.
62. Runge KE, Evans JE, He ZY, Gupta S, McDonald KL, et al. (2007) Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 304: 317-325.
63. Dale B, De Santis A, (1981) The effect of cytochalasin B and D on the fertilization of sea urchins. Dev Biol. 83: 232-7.
64. Nasr-Esfahani MH, Razavi S, Javdan Z, Tavalaee M, (2008) Artificial oocyte activation in severe teratozoospermia undergoing intracytoplasmic sperm injection. Fertil Steril 90: 2231-2237.