Advertisement

Calcium and Calcium-Linked Second Messengers are Main Actors in the Maturation and Fertilization of Starfish Oocytes

  • Luigia Santella
  • Gilda A. Nusco
  • Dmitri Lim

Abstract

Since the early studies on sea urchin egg activation [1] and on starfish oocytes [2], to the more recent discoveries of the Ca2+-mobilizing activities of cyclic ADP-ribose (cADPR) and nicotinic acid adenine dinucleotide phosphate (NAADP) in sea urchin egg homogenates [3–6], echinoderm gametes have remained a widely investigated system in the area of egg activation. In addition to fertilization, and at variance with sea urchin, starfish oocytes have also provided an exceptional model to investigate the re-initiation of the meiotic cycle (e.g., maturation) due to their synchrony, transparency and ease of handling. Maturation, which is induced by the hormone 1-methyladenine, takes these oocytes from the germinal vesicle stage (4n chromosomes, first prophase stage of meiosis) where they remain arrested to the spawning period at which they can be fertilized. During meiosis, reinitiated oocytes undergo a number of structural and biochemical changes, which prepare them for successful fertilization. Thus, oocytes have been a useful tool in investigations of the intracellular mechanisms regulating the prophase/metaphase transition. They are also a unique source of highly purified cell cycle control elements e.g., purified M-phase promoting factor [7, 8].

Keywords

Oocyte Maturation Germinal Vesicle Immature Oocyte Inositol Trisphosphate Meiotic Maturation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Hertwig O. 1876. Beiträge zur Kenntniss der Bildung, Befruchtung und theilung des thierischen Eies. Gegenbaurs Morph. Jb. 1: 347–434.Google Scholar
  2. 2.
    Fol H. 1877. Sur le commencement de l2019henogenie chez divers animaux. Arch. Sci. Gen. 58: 439–472.Google Scholar
  3. 3.
    Clapper DL, Walseth TF, Dargie PJ and Lee HC. 1987. Pyridine nucleotide metabolites stimulate Ca2+ release from sea urchin egg microsomes desensitized to inositol trisphosphate. J. Biol. Chem. 262: 9561–9568.PubMedGoogle Scholar
  4. 4.
    Lee HC, Walseth TF, Bratt GT, Hayes RN and Clapper DL. 1989. Structural determination of a cyclic metabolite of NAD+ with intracellular Ca2+-mobilizing activity. J. Biol. Chem. 264: 1608–1615.PubMedGoogle Scholar
  5. 5.
    Lee HC Aarhus R and Levitt D. 1994. The cristal structure of cADP-ribose. Nature Struct. Biol. 1: 143–144.PubMedCrossRefGoogle Scholar
  6. 6.
    Lee HC and Aarhus R. 1995. A derivative of NADP mobilizes Ca2+ stores insensitive to inositol trisphosphate and cyclic ADP-ribose. J. Biol. Chem. 270: 2152–2157.PubMedCrossRefGoogle Scholar
  7. 7.
    Labbée JC, Capony JP, Caput D, Cavadore JC, Derancourt J, Kaghad M, Lelias JM, Picard A and Doree M. 1989. MPF from starfish oocytes at first meiotic metaphase is a heterodimer containing one molecule of cdc2 and one molecule of cyclin B. EMBO J. 8: 3053–3058.Google Scholar
  8. 8.
    Pondaven P, Meijer L and Beach D. 1990. Activation of M-phase-speciflc histone HI kinase by modification of the phosphorylation of its p34cdc2 and cyclin components. Genes Dev. 4:9–17.PubMedCrossRefGoogle Scholar
  9. 9.
    Borgne A, Ostvold AC, Flament S and Meijer L. 1999. Intra-M phase-promoting factor phosphorylation of cyclin B at the prophase/metaphase transition. J. Biol. Chem. 23: 11977–11986.CrossRefGoogle Scholar
  10. 10.
    Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG and Moulinoux JP. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem. 243: 527–536.PubMedCrossRefGoogle Scholar
  11. 11.
    Kanatani H, Ikegami S, Shirai H, Oide H and Tamura S. 1971. Purification of gonad-stimulating substance obtained from radial nerves of the starfish, Asterias amurensis. Dev. Growth Differ. 13: 151–164.CrossRefGoogle Scholar
  12. 12.
    Schroeder TE. 1981. Microfilament-mediated surface change in starfish oocytes in response to 1-methyladenine: implications for identifying the pathway and receptor sites for maturation-inducing hormones. J. Cell Biol. 90: 362–371.PubMedCrossRefGoogle Scholar
  13. 13.
    Kanatani H, Shirai H, Nakanishi K and Kurosawa T. 1969. Isolation and identification of meiosis-inducing substance in starfish, Asterias amurensis. Nature 221: 273–274.Google Scholar
  14. 14.
    Kanatani H and Hiramoto Y. 1970. Site of action of 1-methyladenine in inducing oocyte maturation in starfish. Exp. Cell Res. 61: 280–284.PubMedCrossRefGoogle Scholar
  15. 15.
    Jaffe LA, Gallo CJ, Lee RH, Ho Y-K and Jones TLZ. 1993. Oocyte maturation in starfish is mediated by the βγ subunit complex of a G protein. J. Cell Biol. 121: 755–783.CrossRefGoogle Scholar
  16. 16.
    Chiba K, Kontani K, Tadenuma H, Katada T and Hoshi M. 1993. Induction of starfish oocyte maturation by the py subunit of starfish G protein and possible existence of the subsequent effector in cytoplasm. Mol. Biol. Cell. 4: 1027–1034.PubMedGoogle Scholar
  17. 17.
    Sadler KC and Ruderman JV. 1998. Components of the signaling pathway linking the 1-methyladenine receptor to MPF activation and maturation in starfish oocytes. Dev. Biol. 197:25–38.PubMedCrossRefGoogle Scholar
  18. 18.
    Meijer L and Zarutskie P. 1987. Starfish oocyte maturation: 1-methyladenine triggers a drop of cAMP concentration related to the hormone-dependent period. Dev. Biol. 121: 306–315.PubMedCrossRefGoogle Scholar
  19. 19.
    Meijer L and Guerrier P. 1984. Maturation fertilization in starfish oocytes. Int. Rev. Cytol. 86: 129–196.PubMedCrossRefGoogle Scholar
  20. 20.
    Meijer L and Mordret G. 1994. Starfish oocyte maturation: from prophase to metaphase. seminDev. Biol. 5: 165–171.Google Scholar
  21. 21.
    Kishimoto T, Kanatani H. 1976 Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocyte. Nature 260: 321–322.PubMedCrossRefGoogle Scholar
  22. 22.
    Guerrier P, Moreau M and Doree M. 1977. Hormonal control of meiosis in starfish: stimulation of protein phosphorylation induced by 1-methyladenine. Mol Cell Endocrinol. 7: 137–150.PubMedCrossRefGoogle Scholar
  23. 23.
    Kishimoto T. 1999. Activation of MPF at meiosis reinitiation in starfish oocytes. Dev. Biol. 214: 1–8.PubMedCrossRefGoogle Scholar
  24. 24.
    Ookata K, Hisanaga S, Okano T, Tachibana K and Kishimoto T. 1992. Relocation and distinct subcellular localization of p34cdc2-cyclin B complex at meiosis reinitiation in starfish oocytes. EMBO J. 11: 1763–1767.PubMedGoogle Scholar
  25. 25.
    Okumura E, Fukuhara T, Yoshida H, Hanada S, Kozutsumi R, Mori M, Tachibana K and Kishimoto T. 2002. Akt inhibits Mytl in the signalling pathway that leads to meiotic G2/M-phase transition. Nature Cell Biol. 4: 111–116.PubMedCrossRefGoogle Scholar
  26. 26.
    Nigg EA. 1993. Cellular substrates of p34cdc2 and its companion cyclin-dependent kinases. Trends Cell Biol. 3: 296–301.PubMedCrossRefGoogle Scholar
  27. 27.
    Santella L, Kyozuka K, Hoving S, Munchbach M, Quadroni M, Dainese P, Zamparelli C, James P and Carafoli E. 2000. Breakdown of cytoskeletal proteins during meiosis of starfish oocytes and proteolysis induced by calpain. Exp. Cell. Res. 259: 117–126.PubMedCrossRefGoogle Scholar
  28. 28.
    Schollmeyer JE. 1988 Calpain-II involvement in mitosis. Science 240: 911–913.PubMedCrossRefGoogle Scholar
  29. 29.
    Stevens M. 1970. Procedures for induction of spawning and meiotic maturation of starfish oocytes by treatment with 1 -methyladenine. Exp. Cell Res. 59: 482–484.PubMedCrossRefGoogle Scholar
  30. 30.
    Kanatani H. 1985. Oocyte growth and maturation in starfish. In Biology of fertilization, eds. CB Metz and A Monroy, vol. I, pp. 119–140. Academic Press, Inc Orlando, Florida.CrossRefGoogle Scholar
  31. 31.
    Dale B, de Santis A and Hoshi M. 1979. Membrane response to 1-methyladenine requires the presence of the nucleus. Nature 282: 89–90.PubMedCrossRefGoogle Scholar
  32. 32.
    Moody WJ and Bosma MM. 1985. Hormone-induced loss of surface membrane during maturation of starfish oocytes: differential effects on potassium and Ca2+ channels. Dev. Biol. 112:396–404.PubMedCrossRefGoogle Scholar
  33. 33.
    Moody WJ and Lansman JB. 1983. Developmental regulation of Ca2+ and K+ currents during hormone-induced maturation of starfish oocytes. Proc. Natl. Acad. Sci. USA. 80: 3096–3100.PubMedCrossRefGoogle Scholar
  34. 34.
    Miyazaki SI, Ohmori H and Sasaki S. 1975. Potassium rectifications of the starfish oocyte membrane and their changes during oocyte maturation. J. Physiol. 246: 55–78.PubMedGoogle Scholar
  35. 35.
    Longo FJ, Woerner M, Chiba K and Hoshi M. 1995. Cortical changes in starfish (Asterina pectinifera) oocytes during 1-methyladenine-induced maturation and fertilisation/activation. Zygote 3: 225–239.PubMedCrossRefGoogle Scholar
  36. 36.
    Santella L, De Riso L, Gragnaniello G and 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.PubMedCrossRefGoogle Scholar
  37. 37.
    Sardet C, Prodon F, Dumollard R, Chang P and Chenevert J. 2002. Structure and function of the egg cortex from oogenesis through fertilization. Dev. Biol. 241: 1–23.PubMedCrossRefGoogle Scholar
  38. 38.
    Heil-Chapdelaine RA and Otto JJ. 1996. Characterization of changes in F-actin during maturation of starfish oocytes. Dev. Biol. 177: 204–216.PubMedCrossRefGoogle Scholar
  39. 39.
    Schroeder TE and Strieker SA. 1983. Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev. Biol. 98: 373–384.PubMedCrossRefGoogle Scholar
  40. 40.
    Hirai H and Shida H. 1979. Shortening of microvilli during the maturation of starfish oocyte from which vitelline coat was removed. Bull. Mar. Biol. Sta. Asamushi, Tohoku, Univ. 16: 161–167.Google Scholar
  41. 41.
    Jaffe LA and Terasaki M. 1994. Structural changes in the endoplasmic reticulum of starfish oocytes during meiotic maturation and fertilization. Dev. Biol. 164: 579–587.PubMedCrossRefGoogle Scholar
  42. 42.
    Terasaki M, Runft LL and Hand AR. 2001. Changes in organization of the endoplasmic reticulum during Xenopus oocyte maturation and activation. Mol. Biol. Cell 12: 1103–1116.PubMedGoogle Scholar
  43. 43.
    Fujiwara T, Nakada K, Shirakawa H and Miyazaki S. 1993. Development of inositol trisphosphate-induced Ca2+ release mechanism during maturation of hamster oocytes. Dev. Biol. 156:69–79.PubMedCrossRefGoogle Scholar
  44. 44.
    Mehlmann LM and Kline D. 1994. Regulation of intracellular Ca2+ in the mouse egg: Ca2+ release in response to sperm or inositol trisphosphate is enhanced after meiotic maturation. Biol.Reprod. 51: 1088–1098.PubMedCrossRefGoogle Scholar
  45. 45.
    Chiba K, Kado RT and Jaffe LA. 1990. Development of Ca2+ release mechanisms during starfish oocyte maturation. Dev. Biol. 140: 300–306.PubMedCrossRefGoogle Scholar
  46. 46.
    Iwasaki H, Chiba K, Uchiyama T, Suzuki F, Ikeda M, Furuichi T and Mikoshiba K. 2002. Molecular characterization of the starfish InsP3 receptors and its role during oocyte maturation and fertilization. J. Biol. Chem. 211: 2763–2772.CrossRefGoogle Scholar
  47. 47.
    Schuetz AW and Longo FJ. 1981. Hormone-cytoplasmic interactions controlling sperm nuclear decondensation and male pronuclear development in starfish oocytes. J. Exp. Zooi 215: 107–111.CrossRefGoogle Scholar
  48. 48.
    Longo FJ, Cook S and Mathews L. 1991. Pronuclear formation in starfish eggs inseminated at different stages of meiotic maturation: correlation of sperm nuclear transformation and activity of the maternal chromatin. Dev. Biol. 147: 62–72.PubMedCrossRefGoogle Scholar
  49. 49.
    Kishimoto T. 1998. Cell cycle arrest and release in starfish oocytes and eggs. Sem. Dev. Biol. 9: 549–557.CrossRefGoogle Scholar
  50. 50.
    Tachibana K, Machida T, Nomura Y and Kishimoto T. 1997. MAP kinase links the fertilization signal transduction pathway to the Gl/S-phase transition in starfish eggs. EMBOJ. 16:4333–4339.CrossRefGoogle Scholar
  51. 51.
    Dalcq A. 1925. Recherches expérimentales et cytologiques sur la maturation et 1’ activation de 1’œfceuf d’Asterias glacialis. Arch. Biol. 34: 507–674.Google Scholar
  52. 52.
    Pasteels J. 1935. Recherches sur le déterminisme de l’entrée en maturation de 1’œuf chez divers Invertébrés marins. Arch. Biol. 46: 229–262.Google Scholar
  53. 53.
    Whitaker M and Patel R. 1990. Ca2+ and cell cycle control. Development 108: 525–542.PubMedGoogle Scholar
  54. 54.
    Means AR. 1994. Calcium, calmodulin and cell cycle regulation. EEBS Lett. 347: 1–4.Google Scholar
  55. 55.
    Santella L. 1998. The role of calcioum in the cell cycle: facts and hypothesis. Biochem. Biophys. Res. Commun. 244: 317–324.PubMedCrossRefGoogle Scholar
  56. 56.
    Moreau M, Guerrier P, Doree M and Ashley CC.1978. 1-methyladenine induced release of intracellular Ca2+ triggers meiosis in starfish oocytes. Nature 272: 251–253.PubMedCrossRefGoogle Scholar
  57. 57.
    Santella L and Kyozuka K. 1994. Reinitiation of meiosis in starfish oocytes requires an increase in nuclear Ca2+. Biochem. Biophys. Res. Commun. 203: 674–680.PubMedCrossRefGoogle Scholar
  58. 58.
    Santella L, De Riso L, Gragnaniello G and Kyozuka K. 1998. Separate activation of the cytoplasmic and nuclear Ca2+ pools in maturing starfish oocytes. Biochem. Biophys. Res. Commun. 252: 1–4.PubMedCrossRefGoogle Scholar
  59. 59.
    Santella L and Kyozuka K. 1997. Effects of 1-methyladenine on nuclear Ca2+ transients and meiosis resumption in starfish oocytes are mimicked by the nuclear injection of inositol 1,4,5-trisphosphate and cADP-ribose. Cell Calcium 22: 11–20.PubMedCrossRefGoogle Scholar
  60. 60.
    Nusco GA, Lim D, Sabala P and Santella L. 2002. Ca2+ response to cADPR during maturation and fertilization of starfish oocytes. Biochem. Biophys. Res. Commun. 290: 1015–1021.PubMedCrossRefGoogle Scholar
  61. 61.
    Santella L and Kyozuka K. 1997. Association of calmodulin with nuclear structures in starfish oocytes and its role in the resumption of meiosis. Eur. J. Biochem. 246: 602–610.PubMedCrossRefGoogle Scholar
  62. 62.
    Lee HC, Aarhus R and Graeff RM. 1995. Sensitization of Ca2+-induced Ca2+ release by cyclic ADP-ribose and calmodulin. J. Biol. Chem. 270: 9060–9066.PubMedCrossRefGoogle Scholar
  63. 63.
    Adebanjo OA, Anandatheerthavarada HK, Koval AP, Moonga BS, Biswas G, Sun L, Sodam BR, Bevis PJ, Huang CL, Epstein S, Lai FA, Avadhani NG and Zaidi M. 1999. A new function for CD38/ADP-ribosyl cyclase in nuclear Ca2+ homeostasis. Nature Cell Biol. 17:409–414.Google Scholar
  64. 64.
    Khoo KM, Han MK, Park JB, Chae SW, Kim UH, Lee HC, Bay BH and Chang CF. 2000. Localization of the cyclic ADP-ribose-dependent Ca2+ signaling pathway in hepatocyte nucleus. J. Biol. Chem. 275: 24807-24817.PubMedCrossRefGoogle Scholar
  65. 65.
    Galione A, Patel S and Churchill GC. 2000. NAADP+-induced Ca2+ release in sea urchin eggs. Biol. Cell. 92: 197–204.PubMedCrossRefGoogle Scholar
  66. 66.
    Albrieux M, Sardet C and Villaz M. 1997 The two intracellular Ca2+ release channels, ryanodine receptors and inositol 1,4,5-trisphosphate receptor, play different roles during fertilization in Ascidians. Dev. Biol. 189: 174–185.PubMedCrossRefGoogle Scholar
  67. 67.
    Albrieux M, Lee HC and Villaz M. 1998 Calcium signaling by cyclic ADP-ribose, NAADP, and inositol trisphosphate are involved in distinct functions in Ascidian oocytes. J. Biol. Chem. 273: 14566–14574.PubMedCrossRefGoogle Scholar
  68. 68.
    Santella L, Kyozuka K, Genazzani AA, De Riso L and Carafoli E. 2000b. Nicotinic acid adenine dinucleotide phosphate-induced Ca2+ release. FASEB J. 275: 8301–8306.Google Scholar
  69. 69.
    Hoshi M, Nishigaki T, Ushiyama A, Okinaga T, Chiba K and Matsumoto M. 1994. Egg-jelly signal molecules for triggering the acrosome reaction in starfish spermatozoa. Int. J. Dev. Biol. 38: 167–174.PubMedGoogle Scholar
  70. 70.
    Dan JC. 1954. Studies on the acrosome. II. Acrosome reaction in starfish spermatozoa. Biol. Bull. 107:203–218.CrossRefGoogle Scholar
  71. 71.
    Kyozuka K and Osanai K. 1988. Fertilization cone formation in starfish oocytes: the role of the egg cortex actin microfilaments in sperm incorporation. Gam. Res. 20: 275–285.CrossRefGoogle Scholar
  72. 72.
    Strieker SA. 1999. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 15: 157–176.CrossRefGoogle Scholar
  73. 73.
    Swann K, Whitaker M. 1986. The part played by inositol trisphosphate and calcium in the propagation of the fertilization wave in sea urchin eggs. J. Cell. Biol. 103: 2333–42PubMedCrossRefGoogle Scholar
  74. 74.
    Ciapa B, Borg B, Whitaker M. 1992. Polyphosphoinositide metabolism during the fertilization wave in sea urchin eggs. Development 115: 187–95.PubMedGoogle Scholar
  75. 75.
    Shilling FM, Carroll DJ, Muslin AJ, Escobedo JA, Williams LT, Jaffe LA. 1994. Evidence for both tyrosine kinase and G-protein-coupled pathways leading to starfish egg activation. Dev. Biol. 162: 590–599.PubMedCrossRefGoogle Scholar
  76. 76.
    Carroll DJ, Ramarao CS, Mehlmann LM, Roche S, Terasaki M and Jaffe LA. 1997. Calcium release at fertilization in starfish eggs is mediated by phospholipase Cy. J. Cell Biol. 138: 1303–1311.PubMedCrossRefGoogle Scholar
  77. 77.
    Giusti AF, Carroll DJ, Abassi YA and Foltz KR. 1999. Evidence that a starfish egg Src family tyrosine kinase associates with PLC-yl SH2 domains at fertilization. Dev. Biol. 208: 189–199.PubMedCrossRefGoogle Scholar
  78. 78.
    Abassi YA, Carroll DJ, Giusti AF, Belton RJ Jr and Foltz KR. 2000. Evidence that Src-type tyrosine kinase activity is necessary for initiation of calcium release at fertilization in sea urchin eggs. Dev. Biol. 15: 206–219.CrossRefGoogle Scholar
  79. 79.
    Galione A, Lee HC and Busa WB. 1991. Ca2+-induced Ca2+ release in sea urchin egg homogenates: modulation by cyclic ADP-ribose. Science 253: 1143–1146.PubMedCrossRefGoogle Scholar
  80. 80.
    Whalley T, McDougall A, Crossley I, Swann K and Whitaker M. 1992. Internal Ca2+ release and activation of sea urchin eggs by cGMP are independent of the phosphoinositide signaling pathway. Mol. Biol. Cell. 3: 373–383.PubMedGoogle Scholar
  81. 81.
    Willmott N, Sethi JK, Walseth TF, Lee HC, White AM and Galione A. 1996. Nitric oxide-induced mobilization of intracellular calcium via the cyclic ADP-ribose signaling pathway. J. Biol. Chem. 271: 3699–3705.PubMedCrossRefGoogle Scholar
  82. 82.
    Kuo RC, Baxter GT, Thompson SH, Strieker SA, Patton C, Bonaventura J and Epel D. 2000. NO is necessary and sufficient for egg activation at fertilization. Nature 406: 633–636.PubMedCrossRefGoogle Scholar
  83. 83.
    Lim D, Kyozuka K, Gragnaniello G, Carafoli E and Santella L. 2001. NAADPV initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J. 15: 2257–2267.PubMedCrossRefGoogle Scholar
  84. 84.
    Lim D, Lange K and Santella L. 2002. Activation of oocytes by latrunculin A. FASEB J. (in press)Google Scholar
  85. 85.
    Carafoli E, Santella L, Branca D and Brini M. 2001. Generation, control, and processing of cellular calcium signals. Crit. Rev. Biochem. Mol. Biol. 36: 107–260.PubMedCrossRefGoogle Scholar
  86. 86.
    Nilius B and Droogmans G. 2001. Ion channels and their functional role in vascularendothelium. Physiol. Rev. 81: 1415–1459.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Luigia Santella
    • 1
  • Gilda A. Nusco
    • 1
  • Dmitri Lim
    • 1
  1. 1.Laboratory of Cell BiologyStazione Zoologica “A. Dohrn”NaplesItaly

Personalised recommendations