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Starfish as a Model System for Analyzing Signal Transduction During Fertilization

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Marine Organisms as Model Systems in Biology and Medicine

Part of the book series: Results and Problems in Cell Differentiation ((RESULTS,volume 65))

Abstract

The starfish oocyte and egg offer advantages for use as a model system for signal transduction research. Some of these have been recognized for over a century, including the ease of procuring gametes, in vitro fertilization, and culturing the embryos. New advances, particularly in genomics, have also opened up opportunities for the use of these animals. In this chapter, we give a few examples of the historical use of the starfish for research in cell biology and then describe some new areas in which we believe the starfish can contribute to our understanding of signal transduction—particularly in fertilization.

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References

  • Angerer LM, Angerer RC (2004) Disruption of gene function using antisense morpholinos. Methods Cell Biol 74:699–711

    Article  PubMed  CAS  Google Scholar 

  • Belton RJ, Adams NL, Foltz KR (2001) Isolation and characterization of sea urchin egg lipid rafts and their possible function during fertilization. Mol Reprod Dev 305:294–305

    Article  Google Scholar 

  • Brayboy LM, Wessel GM (2016) The double-edged sword of the mammalian oocyte – advantages, drawbacks and approaches for basic and clinical analysis at the single cell level. Mol Hum Reprod 22(3):200–207

    Article  PubMed  CAS  Google Scholar 

  • Briggs E, Wessel GM (2006) In the beginning… Animal fertilization and sea urchin development. Dev Biol 300(1):15–26

    Article  PubMed  CAS  Google Scholar 

  • Cameron RA et al (2009) SpBase: the sea urchin genome database and web site. Nucleic Acids Res 37(Database):D750–D754

    Article  PubMed  CAS  Google Scholar 

  • Carroll DJ, Hua W (2009) Combining microinjection and immunoblotting to analyze MAP kinase phosphorylation in single starfish oocytes and eggs. Methods Mol Biol 518:57–66

    Article  PubMed  CAS  Google Scholar 

  • Carroll DJ, Jaffe LA (1995) Proteases stimulate fertilization-like responses in starfish eggs. Dev Biol 170(2):690–700

    Article  PubMed  CAS  Google Scholar 

  • Carroll DJ et al (1997) Calcium release at fertilization in starfish eggs is mediated by phospholipase Cgamma. J Cell Biol 138(6):1303–1311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chalbi M et al (2014) Binding of sperm protein Izumo1 and its egg receptor Juno drives Cd9 accumulation in the intercellular contact area prior to fusion during mammalian fertilization. Development 141(19):3732–3739

    Article  PubMed  CAS  Google Scholar 

  • Chiba K, Kado RT, Jaffe LA (1990) Development of calcium release mechanisms during starfish oocyte maturation. Dev Biol 140(2):300–306

    Article  PubMed  CAS  Google Scholar 

  • Cui M, Lin C-Y, Su Y-H (2017) Recent advances in functional perturbation and genome editing techniques in studying sea urchin development. Brief Funct Genomics 16(5):309–318

    Article  PubMed  Google Scholar 

  • Evans T et al (1983) Cyclin: a protein specified by maternal mRNA in sea urchin eggs that is destroyed at each cleavage division. Cell 33(2):389–396

    Article  PubMed  CAS  Google Scholar 

  • Fol H (1879) Recherches sur la fĂ©condation et le commencement de l’hĂ©nogĂ©nie chez divers animaux. Mem Soc Phys Hist Nat Genève 26:92–397

    Google Scholar 

  • Giusti AF, Hoang KM, Foltz KR (1997) Surface localization of the sea urchin egg receptor for sperm. Dev Biol 184(1):10–24

    Article  PubMed  CAS  Google Scholar 

  • Giusti AF, Carroll DJ, Abassi YA, Foltz KR (1999a) Evidence that a starfish egg Src family tyrosine kinase associates with PLC-gamma1 SH2 domains at fertilization. Dev Biol 208(1):189–199

    Article  PubMed  CAS  Google Scholar 

  • Giusti AF, Carroll DJ, Abassi YA, Terasaki M et al (1999b) Requirement of a Src family kinase for initiating calcium release at fertilization in starfish eggs. J Biol Chem 274(41):29318–29322

    Article  PubMed  CAS  Google Scholar 

  • Giusti AF et al (2000) Evidence that fertilization activates starfish eggs by sequential activation of a Src-like kinase and phospholipase cgamma. J Biol Chem 275(22):16788–16794

    Article  PubMed  CAS  Google Scholar 

  • György P et al (1941) Egg-white injury as the result of nonabsorption or inactivation of biotin. Science 93(2420):477–478

    Article  PubMed  Google Scholar 

  • Hara M et al (2012) Greatwall kinase and cyclin B-Cdk1 are both critical constituents of M-phase-promoting factor. Nat Commun 3:1059

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hasan AKMM et al (2005) Uroplakin III, a novel Src substrate in Xenopus egg rafts, is a target for sperm protease essential for fertilization. Dev Biol 286(2):483–492

    Article  CAS  Google Scholar 

  • Hiramoto Y (1962) Microinjection of the live spermatozoa into sea urchin eggs. Exp Cell Res 27(3):416–426

    Article  PubMed  CAS  Google Scholar 

  • Hiramoto Y (1974) A method of microinjection. Exp Cell Res 87(2):403–406

    Article  PubMed  CAS  Google Scholar 

  • Hoshi M, Moriyama H, Matsumoto M (2012) Structure of acrosome reaction-inducing substance in the jelly coat of starfish eggs: a mini review. Biochem Biophys Res Commun 425(3):595–598

    Article  PubMed  CAS  Google Scholar 

  • Inoue N (2017) Novel insights into the molecular mechanism of sperm–egg fusion via IZUMO1. J Plant Res 130(3):475–478

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LA, Egbert JR (2017) Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Annu Rev Physiol 79:237–260

    Article  PubMed  CAS  Google Scholar 

  • Jaffe LA, Terasaki M (2004) Quantitative microinjection of oocytes, eggs, and embryos. Methods Cell Biol 74:219–242

    Article  PubMed  PubMed Central  Google Scholar 

  • Jahromi S, Shamsir M (2013) Construction and analysis of the cell surface’s protein network for human sperm-egg interaction. ISRN Bioinform 2013:962760

    Google Scholar 

  • Kadandale P et al (2005) The egg surface LDL receptor repeat-containing proteins EGG-1 and EGG-2 are required for fertilization in Caenorhabditis elegans. Curr Biol 15(24):2222–2229

    Article  PubMed  CAS  Google Scholar 

  • Kalinowski RR et al (2003) A receptor linked to a Gi-family G-protein functions in initiating oocyte maturation in starfish but not frogs. Dev Biol 253(1):139–149

    Article  PubMed  CAS  Google Scholar 

  • Kamei N, Glabe CG (2003) The species-specific egg receptor for sea urchin sperm adhesion is EBR1, a novel ADAMTS protein. Genes Dev 17(20):2502–2507

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kishimoto T (2015) Entry into mitosis: a solution to the decades-long enigma of MPF. Chromosoma 124(4):417–428

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kishimoto T, Kanatani H (1976) Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocyte. Nature 260(5549):321–322

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto T, Hirai S, Kanatani H (1981) Role of germinal vesicle material in producing maturation-promoting factor in starfish oocyte. Dev Biol 81(1):177–181

    Article  PubMed  CAS  Google Scholar 

  • Kishimoto T et al (1982) Generality of the action of various maturation-promoting factors. Exp Cell Res 137(1):121–126

    Article  PubMed  CAS  Google Scholar 

  • Klinovska K, Sebkova N, Dvorakova-hortova K (2014) Sperm-egg fusion: a molecular enigma of mammalian reproduction. Int J Mol Sci 15:10652–10668

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kudtarkar P, Cameron RA (2017) Echinobase: an expanding resource for echinoderm genomic information. Database 2017:bax074

    Article  PubMed Central  CAS  Google Scholar 

  • Lazaridis T, Masunov A, Gandolfo F (2002) Contributions to the binding free energy of ligands to avidin and streptavidin. Proteins Struct Funct Genet 47(2):194–208

    Article  PubMed  CAS  Google Scholar 

  • Levental I, Veatch SL (2016) The continuing mystery of lipid rafts. J Mol Biol 428(24):4749–4764

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin C-Y, Su Y-H (2016) Genome editing in sea urchin embryos by using a CRISPR/Cas9 system. Dev Biol 409(2):420–428

    Article  PubMed  CAS  Google Scholar 

  • Mabuchi I, Okuno M (1977) The effect of myosin antibody on the division of starfish blastomeres. J Cell Biol 74(1):251–263

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masui Y, Markert CL (1971) Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool 177(2):129–145

    Article  PubMed  CAS  Google Scholar 

  • Morin R et al (2008) Profiling the HeLa S3 transcriptome using randomly primed cDNA and massively parallel short-read sequencing. BioTechniques 45(1):81–94

    Article  PubMed  CAS  Google Scholar 

  • Musacchia F et al (2017) De novo assembly of a transcriptome from the eggs and early embryos of Astropecten aranciacus. PLoS One 12(9):e0184090

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • NCBI Resource Coordinators (2017) Database resources of the national center for biotechnology information. Nucleic Acids Res 45(D1):D12–D17

    Article  CAS  Google Scholar 

  • Nurse P, Bissett Y (1981) Gene required in G1 for commitment to cell cycle and in G2 for control of mitosis in fission yeast. Nature 292(5823):558–560

    Article  PubMed  CAS  Google Scholar 

  • O’Neill FJ, Gillett J, Foltz KR (2004) Distinct roles for multiple Src family kinases at fertilization. J Cell Sci 117(Pt 25):6227–6238

    Article  PubMed  CAS  Google Scholar 

  • Ohto U et al (2016) Structure of IZUMO1–JUNO reveals sperm–oocyte recognition during mammalian fertilization. Nature 534(7608):566–569

    Article  PubMed  CAS  Google Scholar 

  • Okumura E et al (2014) Cyclin B–Cdk1 inhibits protein phosphatase PP2A-B55 via a Greatwall kinase–independent mechanism. J Cell Biol 204(6):881–889

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Oren-Suissa M, Podbilewicz B (2007) Cell fusion during development. Trends Cell Biol 17(11):537–546

    Article  PubMed  CAS  Google Scholar 

  • Picard A, Labbe J-C, Doree M (1988) Normal embryogenesis occurs in starfish eggs induced to mature by microinjection of cytoplasm containing maturation-promoting factor (MPF). Development 103:575–579

    CAS  Google Scholar 

  • Pike LJ (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. J Lipid Res 47(7):1597–1598

    Article  PubMed  CAS  Google Scholar 

  • Ramos I, Wessel GM (2013) Calcium pathway machinery at fertilization in echinoderms. Cell Calcium 53(1):16–23

    Article  PubMed  CAS  Google Scholar 

  • Ramos I, Reich A, Wessel GM (2014) Two-pore channels function in calcium regulation in sea star oocytes and embryos. Development 141(23):4598–4609

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rotin D et al (1992) SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. EMBO J 11(2):559–567

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roux MM et al (2006) A functional genomic and proteomic perspective of sea urchin calcium signaling and egg activation. Dev Biol 300(1):416–433

    Article  PubMed  CAS  Google Scholar 

  • Roux-Osovitz MM, Foltz KR (2014) Isolation and assessment of signaling proteins from synchronized cultures during egg activation and through the egg-to-embryo transition in sea urchins. Methods Mol Biol 1128:277–294

    Article  PubMed  CAS  Google Scholar 

  • Runft LL et al (2004) Identification of a starfish egg PLC-g that regulates Ca2+ release at fertilization. Dev Biol 269:220–236

    Article  PubMed  CAS  Google Scholar 

  • Sakakibara K et al (2005) Molecular identification and characterization of Xenopus egg uroplakin III, an egg raft-associated transmembrane protein that is tyrosine-phosphorylated upon fertilization. J Biol Chem 280(15):15029–15037

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Fukami Y, Stith BJ (2006) Signal transduction pathways leading to Ca2+ release in a vertebrate model system: lessons from Xenopus eggs. Semin Cell Dev Biol 17(2):285–292

    Article  PubMed  CAS  Google Scholar 

  • Schroeder TE, Stricker SA (1983) Morphological changes during maturation of starfish oocytes: surface ultrastructure and cortical actin. Dev Biol 98(2):373–384

    Article  PubMed  CAS  Google Scholar 

  • Shevidi S et al (2017) Single nucleotide editing without DNA cleavage using CRISPR/Cas9-deaminase in the sea urchin embryo. Dev Dyn 246(12):1036–1046

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Simons K, Toomre D (2000) Lipid rafts and signal transduction. Nat Rev Mol Cell Biol 1(1):31–39

    Article  PubMed  CAS  Google Scholar 

  • Sodergren E et al (2006) The genome of the sea urchin Strongylocentrotus purpuratus. Science 314(5801):941–952

    Article  PubMed  Google Scholar 

  • Steptoe PC, Edwards RG (1978) Birth after the reimplantation of a human embryo. Lancet 2(8085):366

    Article  PubMed  CAS  Google Scholar 

  • Strathmann M (1987) Reproduction and development of marine invertebrates of the Northern Pacific Coast. University of Washington, Seattle

    Google Scholar 

  • Stricker SA (1995) Time-lapse confocal imaging of calcium dynamics in starfish embryos. Dev Biol 170(2):496–518

    Article  PubMed  CAS  Google Scholar 

  • Stricker SA, Centonze VE, Melendez RF (1994) Calcium dynamics during starfish oocyte maturation and fertilization. Dev Biol 166(1):34–58

    Article  PubMed  CAS  Google Scholar 

  • Swalla BJ, Smith AB (2008) Deciphering deuterostome phylogeny: molecular, morphological and palaeontological perspectives. Philos Trans R Soc Lond Ser B Biol Sci 363(1496):1557–1568

    Article  Google Scholar 

  • Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Genetics 3(February):137–144

    PubMed  CAS  Google Scholar 

  • Tilney LG et al (1973) The polymerization of actin: its role in the generation of the acrosomal process of certain echinoderm sperm. J Cell Biol 59(1):109–126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vacquier VD (2012) The quest for the sea urchin egg receptor for sperm. Biochem Biophys Res Commun 425(3):583–587

    Article  PubMed  CAS  Google Scholar 

  • Vacquier VD, Moy GW (1977) Isolation of bindin: the protein responsible for adhesion of sperm to sea urchin eggs. Cell Biol 74(6):2456–2460

    CAS  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wessel GM, Reich AM, Klatsky PC (2010) Use of sea stars to study basic reproductive processes. Syst Biol Reprod Med 56(3):236–245

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Whitaker M (2006) Calcium at fertilization and in early development. Physiol Rev 86(1):25–88

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wong JL et al (2007) Membrane hemifusion is a stable intermediate of exocytosis. Dev Cell 12(4):653–659

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Author notes

  1. Emily Wiseman and Lauren Bates contributed equally.

Authors and Affiliations

  1. Department of Biological Sciences, Florida Institute of Technology, Melbourne, FL, USA

    Emily Wiseman, Lauren Bates, Altair Dubé & David J. Carroll

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  1. Emily Wiseman
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  2. Lauren Bates
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  3. Altair Dubé
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  4. David J. Carroll
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Corresponding author

Correspondence to David J. Carroll .

Editor information

Editors and Affiliations

  1. Houston Methodist Research Institute, Houston, Texas, USA

    Malgorzata Kloc

  2. Institute of Genetics and Development of Rennes, Université de Rennes, Rennes, France

    Jacek Z. Kubiak

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Wiseman, E., Bates, L., Dubé, A., Carroll, D.J. (2018). Starfish as a Model System for Analyzing Signal Transduction During Fertilization. In: Kloc, M., Kubiak, J. (eds) Marine Organisms as Model Systems in Biology and Medicine. Results and Problems in Cell Differentiation, vol 65. Springer, Cham. https://doi.org/10.1007/978-3-319-92486-1_4

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