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

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Cyclic ADP-Ribose and NAADP

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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].

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References

  1. Hertwig O. 1876. Beiträge zur Kenntniss der Bildung, Befruchtung und theilung des thierischen Eies. Gegenbaurs Morph. Jb. 1: 347–434.

    Google Scholar 

  2. Fol H. 1877. Sur le commencement de l2019henogenie chez divers animaux. Arch. Sci. Gen. 58: 439–472.

    Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  5. Lee HC Aarhus R and Levitt D. 1994. The cristal structure of cADP-ribose. Nature Struct. Biol. 1: 143–144.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  19. Meijer L and Guerrier P. 1984. Maturation fertilization in starfish oocytes. Int. Rev. Cytol. 86: 129–196.

    Article  PubMed  CAS  Google Scholar 

  20. Meijer L and Mordret G. 1994. Starfish oocyte maturation: from prophase to metaphase. seminDev. Biol. 5: 165–171.

    CAS  Google Scholar 

  21. Kishimoto T, Kanatani H. 1976 Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocyte. Nature 260: 321–322.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  23. Kishimoto T. 1999. Activation of MPF at meiosis reinitiation in starfish oocytes. Dev. Biol. 214: 1–8.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  26. Nigg EA. 1993. Cellular substrates of p34cdc2 and its companion cyclin-dependent kinases. Trends Cell Biol. 3: 296–301.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  28. Schollmeyer JE. 1988 Calpain-II involvement in mitosis. Science 240: 911–913.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Chapter  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  38. Heil-Chapdelaine RA and Otto JJ. 1996. Characterization of changes in F-actin during maturation of starfish oocytes. Dev. Biol. 177: 204–216.

    Article  PubMed  CAS  Google Scholar 

  39. Schroeder TE and Strieker SA. 1983. Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev. Biol. 98: 373–384.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  45. Chiba K, Kado RT and Jaffe LA. 1990. Development of Ca2+ release mechanisms during starfish oocyte maturation. Dev. Biol. 140: 300–306.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  49. Kishimoto T. 1998. Cell cycle arrest and release in starfish oocytes and eggs. Sem. Dev. Biol. 9: 549–557.

    Article  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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. 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. Whitaker M and Patel R. 1990. Ca2+ and cell cycle control. Development 108: 525–542.

    PubMed  CAS  Google Scholar 

  54. Means AR. 1994. Calcium, calmodulin and cell cycle regulation. EEBS Lett. 347: 1–4.

    CAS  Google Scholar 

  55. Santella L. 1998. The role of calcioum in the cell cycle: facts and hypothesis. Biochem. Biophys. Res. Commun. 244: 317–324.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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. 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.

    Article  PubMed  CAS  Google Scholar 

  65. Galione A, Patel S and Churchill GC. 2000. NAADP+-induced Ca2+ release in sea urchin eggs. Biol. Cell. 92: 197–204.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  70. Dan JC. 1954. Studies on the acrosome. II. Acrosome reaction in starfish spermatozoa. Biol. Bull. 107:203–218.

    Article  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  72. Strieker SA. 1999. Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev. Biol. 15: 157–176.

    Article  Google Scholar 

  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: 2333–42

    Article  PubMed  CAS  Google Scholar 

  74. Ciapa B, Borg B, Whitaker M. 1992. Polyphosphoinositide metabolism during the fertilization wave in sea urchin eggs. Development 115: 187–95.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  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.

    Article  PubMed  CAS  Google Scholar 

  84. Lim D, Lange K and Santella L. 2002. Activation of oocytes by latrunculin A. FASEB J. (in press)

    Google Scholar 

  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.

    Article  PubMed  Google Scholar 

  86. Nilius B and Droogmans G. 2001. Ion channels and their functional role in vascularendothelium. Physiol. Rev. 81: 1415–1459.

    PubMed  Google Scholar 

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  1. Laboratory of Cell Biology, Stazione Zoologica “A. Dohrn”, Villa Comunale, I-80121, Naples, Italy

    Luigia Santella, Gilda A. Nusco & Dmitri Lim

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    Hon Cheung Lee

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Santella, L., Nusco, G.A., Lim, D. (2002). Calcium and Calcium-Linked Second Messengers are Main Actors in the Maturation and Fertilization of Starfish Oocytes. In: Lee, H.C. (eds) Cyclic ADP-Ribose and NAADP. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-0269-2_18

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