Skip to main content
SpringerLink
Log in
Book cover

Reproductive and Developmental Strategies pp 569–589Cite as

Fertilization and Protein Tyrosine Kinase Signaling: Are They Merging or Emerging?

  • Chapter
  • First Online:

Part of the book series: Diversity and Commonality in Animals ((DCA))

Abstract

Fertilization is a unique form of cell–cell interaction allowing two gametes of the same species—the egg and sperm, which have distinctly different genetic compositions—to unite and give rise to the birth of the next generation of the species. Protein tyrosine phosphorylation, catalyzed by enzymes of a large family collectively called protein tyrosine kinases (PTKs), was initially discovered as a protein posttranslational modification system contributing to the onset, maintenance, and progression of malignant cell transformation, and it is now known to serve as a system that regulates a variety of cell–cell interaction events and multicellularity in living animals. As summarized here, a number of research projects using several model animals have been designed to examine how the egg and sperm interact and how the egg activates to initiate development, by highlighting the roles played by PTK in the egg. This chapter aims to provide the history of the study of fertilization and PTK signaling—most extensively studied using the African clawed frog, Xenopus laevis—and to discuss current problems.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

Introduction

  • Brown MT, Cooper JA (1996) Regulation, substrates and functions of src. Biochim Biophys Acta 1287(2–3):121–149

    PubMed  Google Scholar 

  • Ciapa B, Chiri S (2000) Egg activation: upstream of the fertilization calcium signal. Biol Cell 92(3–4):215–233

    Article  PubMed  CAS  Google Scholar 

  • de la Fuente van Bentem S, Hirt H (2009) Protein tyrosine phosphorylation in plants: more abundant than expected? Trends Plant Sci 14:71–76

    Article  PubMed  CAS  Google Scholar 

  • Ducibella T, Fissore R (2008) The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315(2):257–279

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hanks SK, Hunter T (1995) Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J 9(8):576–596

    Article  PubMed  CAS  Google Scholar 

  • Hunter T (2009) Tyrosine phosphorylation: thirty years and counting. Curr Opin Cell Biol 21(2):140–146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ijiri TW, Mahbub Hasan AK, Sato K (2012) Protein-tyrosine kinase signaling in the biological functions associated with sperm. J Signal Transduct 2012:181560

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, Marr M, Pincus D, Putnam N, Rokas A, Wright KJ, Zuzow R, Dirks W, Good M, Goodstein D, Lemons D, Li W, Lyons JB, Morris A, Nichols S, Richter DJ, Salamov A, Sequencing JG, Bork P, Lim WA, Manning G, Miller WT, McGinnis W, Shapiro H, Tjian R, Grigoriev IV, Rokhsar D (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451(7180):783–788

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kinsey WH (1997) Tyrosine kinase signaling at fertilization. Biochem Biophys Res Commun 240(3):519–522

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH (2014) SRC-family tyrosine kinases in oogenesis, oocyte maturation and fertilization: an evolutionary perspective. Adv Exp Med Biol 759:33–56

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee DC, Jia Z (2009) Emerging structural insights into bacterial tyrosine kinases. Trends Biochem Sci 34:351–357

    Article  PubMed  CAS  Google Scholar 

  • Lim WA, Pawson T (2010) Phosphotyrosine signaling: evolving a new cellular communication system. Cell 142:661–667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu BA, Nash PD (2012) Evolution of SH2 domains and phosphotyrosine signalling networks. Philos Trans R Soc Lond B Biol Sci 367:2556–2573

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Manning G, Young SL, Miller WT, Zhai Y (2008) The protist, Monosiga brevicollis, has a tyrosine kinase signaling network more elaborate and diverse than found in any known metazoan. Proc Natl Acad Sci U S A 105:9674–9679

    Article  PubMed  PubMed Central  Google Scholar 

  • McGinnis LK, Carroll DJ, Kinsey WH (2011) Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol Reprod Dev 78(10–11):831–845

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nuccitelli R (1991) How do sperm activate eggs? Curr Top Dev Biol 25:1–16

    Article  PubMed  CAS  Google Scholar 

  • Okabe M (2013) The cell biology of mammalian fertilization. Development 140(22):4471–4479

    Article  PubMed  CAS  Google Scholar 

  • Pincus D, Letunic I, Bork P, Lim WA (2008) Evolution of the phospho-tyrosine signaling machinery in premetazoan lineages. Proc Natl Acad Sci U S A 105(28):9680–9684

    Article  PubMed  PubMed Central  Google Scholar 

  • Robinson DR, Wu YM, Lin SF (2000) The protein tyrosine kinase family of the human genome. Oncogene 19(49):5548–5557

    Article  PubMed  CAS  Google Scholar 

  • Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254

    Article  PubMed  CAS  Google Scholar 

  • Santella L, Lim D, Moccia F (2004) Calcium and fertilization: the beginning of life. Trends Biochem Sci 29(8):400–408

    Article  PubMed  CAS  Google Scholar 

  • Segawa Y, Suga H, Iwabe N, Oneyama C, Akagi T, Miyata T, Okada M (2006) Functional development of Src tyrosine kinases during evolution from a unicellular ancestor to multicellular animals. Proc Natl Acad Sci U S A 103(32):12021–12026

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srivastava M, Simakov O, Chapman J, Fahey B, Gauthier ME, Mitros T, Richards GS, Conaco C, Dacre M, Hellsten U, Larroux C, Putnam NH, Stanke M, Adamska M, Darling A, Degnan SM, Oakley TH, Plachetzki DC, Zhai Y, Adamski M, Calcino A, Cummins SF, Goodstein DM, Harris C, Jackson DJ, Leys SP, Shu S, Woodcroft BJ, Vervoort M, Kosik KS, Manning G, Degnan BM, Rokhsar DS (2010) The Amphimedon queenslandica genome and the evolution of animal complexity. Nature 466(7307):720–726

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Suga H, Katoh K, Miyata T (2001) Sponge homologs of vertebrate protein tyrosine kinases and frequent domain shufflings in the early evolution of animals before the parazoan–eumetazoan split. Gene 280:195–201

    Article  PubMed  CAS  Google Scholar 

  • Suga H, Dacre M, de Mendoza A, Shalchian-Tabrizi K, Manning G, Ruiz-Trillo I (2012) Genomic survey of premetazoans shows deep conservation of cytoplasmic tyrosine kinases and multiple radiations of receptor tyrosine kinases. Sci Signal 5:ra35

    Article  PubMed  Google Scholar 

  • Thomas SM, Brugge JS (1997) Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513–609

    Article  PubMed  CAS  Google Scholar 

  • Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB (2002) Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 53(1–2):133–150

    Article  PubMed  CAS  Google Scholar 

  • Watari A, Iwabe N, Masuda H, Okada M (2010) Functional transition of Pak proto-oncogene during early evolution of metazoans. Oncogene 29(26):3815–3826

    Article  PubMed  CAS  Google Scholar 

Sea Urchin

  • Abassi YA, Foltz KR (1994) Tyrosine phosphorylation of the egg receptor for sperm at fertilization. Dev Biol 164(2):430–443

    Article  PubMed  CAS  Google Scholar 

  • Abassi YA, Carroll DJ, Giusti AF, Belton RJ Jr, 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 218(2):206–219

    Article  PubMed  CAS  Google Scholar 

  • Belton RJ Jr, Adams NL, Foltz KR (2001) Isolation and characterization of sea urchin egg lipid rafts and their possible function during fertilization. Mol Reprod Dev 59(3):294–305

    Article  PubMed  CAS  Google Scholar 

  • Carroll DJ, Albay DT, Terasaki M, Jaffe LA, Foltz KR (1999) Identification of PLCγ-dependent and -independent events during fertilization of sea urchin eggs. Dev Biol 206(2):232–247

    Article  PubMed  CAS  Google Scholar 

  • Ciapa B, Epel D (1991) A rapid change in phosphorylation on tyrosine accompanies fertilization of sea urchin eggs. FEBS Lett 295(1–3):167–170

    Article  PubMed  CAS  Google Scholar 

  • Dasgupta JD, Garbers DL (1983) Tyrosine protein kinase activity during embryogenesis. J Biol Chem 258(10):6174–6178

    PubMed  CAS  Google Scholar 

  • De Nadai C, Cailliau K, Epel D, Ciapa B (1998) Detection of phospholipase Cγ in sea urchin eggs. Develop Growth Differ 40(6):669–676

    Article  Google Scholar 

  • Giusti AF, O’Neill FJ, Yamasu K, Foltz KR, Jaffe LA (2003) Function of a sea urchin egg Src family kinase in initiating Ca2+ release at fertilization. Dev Biol 256(2):367–378

    Article  PubMed  CAS  Google Scholar 

  • Jiang WP, Veno PA, Wood RW, Peaucellier G, Kinsey WH (1991) pH regulation of an egg cortex tyrosine kinase. Dev Biol 146(1):81–88

    Article  PubMed  CAS  Google Scholar 

  • Kamel C, Veno PA, Kinsey WH (1986) Quantitation of a src-like tyrosine protein kinase during fertilization of the sea urchin egg. Biochem Biophys Res Commun 138(1):349–355

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH (1984) Regulation of tyrosine-specific kinase activity at fertilization. Dev Biol 105(1):137–143

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH (1995) Differential phosphorylation of a 57-KDa protein tyrosine kinase during egg activation. Biochem Biophys Res Commun 208(1):204–209

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH (1996) Biphasic activation of Fyn kinase upon fertilization of the sea urchin egg. Dev Biol 174(2):281–287

    Article  PubMed  CAS  Google Scholar 

  • Kinsey WH, Shen SS (2000) Role of the Fyn kinase in calcium release during fertilization of the sea urchin egg. Dev Biol 225(1):253–264

    Article  PubMed  CAS  Google Scholar 

  • Moore KL, Kinsey WH (1994) Identification of an abl-related protein tyrosine kinase in the cortex of the sea urchin egg: possible role at fertilization. Dev Biol 164(2):444–455

    Article  PubMed  CAS  Google Scholar 

  • Moore KL, Kinsey WH (1995) Effects of protein tyrosine kinase inhibitors on egg activation and fertilization-dependent protein tyrosine kinase activity. Dev Biol 168(1):1–10

    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 

  • Peaucellier G, Veno PA, Kinsey WH (1988) Protein tyrosine phosphorylation in response to fertilization. J Biol Chem 263(27):13806–13811

    PubMed  CAS  Google Scholar 

  • Ribot HD Jr, Eisenman EA, Kinsey WH (1984) Fertilization results in increased tyrosine phosphorylation of egg proteins. J Biol Chem 259(8):5333–5338

    PubMed  CAS  Google Scholar 

  • Rongish BJ, Wu W, Kinsey WH (1999) Fertilization-induced activation of phospholipase C in the sea urchin egg. Dev Biol 215(2):147–154

    Article  PubMed  CAS  Google Scholar 

  • Roux MM, Townley IK, Raisch M, Reade A, Bradham C, Humphreys G, Gunaratne HJ, Killian CE, Moy G, Su YH, Ettensohn CA, Wilt F, Vacquier VD, Burke RD, Wessel G, Foltz KR (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 MM, Radeke MJ, Goel M, Mushegian A, Foltz KR (2008) 2DE identification of proteins exhibiting turnover and phosphorylation dynamics during sea urchin egg activation. Dev Biol 313(2):630–647

    Article  PubMed  CAS  Google Scholar 

  • Satoh N, Garbers DL (1985) Protein tyrosine kinase activity of eggs of the sea urchin Strongylocentrotus purpuratus: the regulation of its increase after fertilization. Dev Biol 111(2):515–519

    Article  PubMed  CAS  Google Scholar 

  • Shearer J, De Nadai C, Emily-Fenouil F, Gache C, Whitaker M, Ciapa B (1999) Role of phospholipase Cγ at fertilization and during mitosis in sea urchin eggs and embryos. Development 126(10):2273–2284

    PubMed  CAS  Google Scholar 

  • Shen SS, Kinsey WH, Lee SJ (1999) Protein tyrosine kinase-dependent release of intracellular calcium in the sea urchin egg. Develop Growth Differ 41(3):345–355

    Article  CAS  Google Scholar 

  • Townley IK, Schuyler E, Parker-Gür M, Foltz KR (2009) Expression of multiple Src family kinases in sea urchin eggs and their function in Ca2+ release at fertilization. Dev Biol 327(2):465–477

    Article  PubMed  CAS  Google Scholar 

  • Wright SJ, Schatten G (1995) Protein tyrosine phosphorylation during sea urchin fertilization: microtubule dynamics require tyrosine kinase activity. Cell Motil Cytoskeleton 30(2):122–135

    Article  PubMed  CAS  Google Scholar 

Ascidians, Starfish, and Other Sea Animals

  • 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, Ramarao CS, Mehlmann LM, Roche S, Terasaki M, Jaffe LA (1997) Calcium release at fertilization in starfish eggs is mediated by phospholipase Cγ. J Cell Biol 138(6):1303–1311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Giusti AF, Carroll DJ, Abassi YA, Terasaki M, Foltz KR, Jaffe LA (1999a) 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, Carroll DJ, Abassi YA, Foltz KR (1999b) Evidence that a starfish egg Src family tyrosine kinase associates with PLC-γ1 SH2 domains at fertilization. Dev Biol 208(1):189–199

    Article  PubMed  CAS  Google Scholar 

  • Giusti AF, Xu W, Hinkle B, Terasaki M, Jaffe LA (2000) Evidence that fertilization activates starfish eggs by sequential activation of a Src-like kinase and phospholipase Cγ. J Biol Chem 275(22):16788–16794

    Article  PubMed  CAS  Google Scholar 

  • Harada Y, Takagaki Y, Sunagawa M, Saito T, Yamada L, Taniguchi H, Shoguchi E, Sawada H (2008) Mechanism of self-sterility in a hermaphroditic chordate. Science 320(5875):548–550

    Article  PubMed  CAS  Google Scholar 

  • Lim D, Kyozuka K, Gragnaniello G, Carafoli E, Santella L (2001) NAADP+ initiates the Ca2+ response during fertilization of starfish oocytes. FASEB J 15(12):2257–2267

    Article  PubMed  CAS  Google Scholar 

  • Peaucellier G, Andersen AC, Kinsey WH (1990) Protein tyrosine phosphorylation during meiotic divisions of starfish oocytes. Dev Biol 138(2):391–399

    Article  PubMed  CAS  Google Scholar 

  • 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(10):e3588

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Runft LL, Jaffe LA (2000) Sperm extract injection into ascidian eggs signals Ca2+ release by the same pathway as fertilization. Development 127(15):3227–3236

    PubMed  CAS  Google Scholar 

  • Runft LL, Carroll DJ, Gillett J, Giusti AF, O’Neill FJ, Foltz KR (2004) Identification of a starfish egg PLC-γ that regulates Ca2+ release at fertilization. Dev Biol 269(1):220–236

    Article  PubMed  CAS  Google Scholar 

  • Saito T, Shiba K, Inaba K, Yamada L, Sawada H (2012) Self-incompatibility response induced by calcium increase in sperm of the ascidian Ciona intestinalis. Proc Natl Acad Sci U S A 109(11):4158–4162

    Article  PubMed  PubMed Central  Google Scholar 

  • Santella L, Kyozuka K, De Riso L, Carafoli E (1998) Calcium, protease action, and the regulation of the cell cycle. Cell Calcium 23(2–3):123–130

    Article  PubMed  CAS  Google Scholar 

  • Sawada H, Sakai N, Abe Y, Tanaka E, Takahashi Y, Fujino J, Kodama E, Takizawa S, Yokosawa H (2002) Extracellular ubiquitination and proteasome-mediated degradation of the ascidian sperm receptor. Proc Natl Acad Sci U S A 99(3):1223–1228

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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(2):590–599

    Article  PubMed  CAS  Google Scholar 

  • Stricker SA, Carroll DJ, Tsui WL (2010) Roles of Src family kinase signaling during fertilization and the first cell cycle in the marine protostome worm Cerebratulus. Int J Dev Biol 54(5):787–793

    Article  PubMed  CAS  Google Scholar 

  • Ueki K, Yokosawa H (1997) Evidence for an erbstatin-sensitive tyrosine kinase functioning in ascidian egg activation. Biochem Biophys Res Commun 238(1):130–133

    Article  PubMed  CAS  Google Scholar 

  • Yin X, Eckberg WR (2009) Characterization of phospholipases Cβ and γ and their possible roles in Cerebratulus egg activation. Mol Reprod Dev 76(5):460–470

    Article  PubMed  CAS  Google Scholar 

Frog

  • Aoto M, Sato K, Takeba S, Horiuchi Y, Iwasaki T, Tokmakov AA, Fukami Y (1999) A 58-kDa Shc protein is present in Xenopus eggs and is phosphorylated on tyrosine residues upon egg activation. Biochem Biophys Res Commun 258(2):265–270

    Article  PubMed  CAS  Google Scholar 

  • Bates RC, Fees CP, Holland WL, Winger CC, Batbayar K, Ancar R, Bergren T, Petcoff D, Stith BJ (2014) Activation of Src and release of intracellular calcium by phosphatidic acid during Xenopus laevis fertilization. Dev Biol 386(1):165–180

    Article  PubMed  CAS  Google Scholar 

  • Brown DA, London E (1998) Functions of lipid rafts in biological membranes. Annu Rev Cell Dev Biol 14:111–136

    Article  PubMed  CAS  Google Scholar 

  • Ferrell JE Jr (1999a) Building a cellular switch: more lessons from a good egg. BioEssays 21(10):866–870

    Article  PubMed  Google Scholar 

  • Ferrell JE Jr (1999b) Xenopus oocyte maturation: new lessons from a good egg. BioEssays 21(10):833–842

    Article  PubMed  Google Scholar 

  • Fortini ME (2002) γ-Secretase-mediated proteolysis in cell-surface-receptor signalling. Nat Rev Mol Cell Biol 3(9):673–684

    Article  PubMed  CAS  Google Scholar 

  • Glahn D, Mark SD, Behr RK, Nuccitelli R (1999) Tyrosine kinase inhibitors block sperm-induced egg activation in Xenopus laevis. Dev Biol 205(1):171–180

    Article  PubMed  CAS  Google Scholar 

  • Hasan AK, Fukami Y, Sato K (2011) Gamete membrane microdomains and their associated molecules in fertilization signaling. Mol Reprod Dev 78(10–11):814–830

    Article  PubMed  CAS  Google Scholar 

  • Iwao Y, Fujimura T (1996) Activation of Xenopus eggs by RGD-containing peptides accompanied by intracellular Ca2+ release. Dev Biol 177(2):558–567

    Article  PubMed  CAS  Google Scholar 

  • Iwao Y, Jaffe LA (1989) Evidence that the voltage-dependent component in the fertilization process is contributed by the sperm. Dev Biol 134(2):446–451

    Article  PubMed  CAS  Google Scholar 

  • Iwao Y, Shiga K, Shiroshita A, Yoshikawa T, Sakiie M, Ueno T, Ueno S, Ijiri TW, Sato K (2014) The need of MMP-2 on the sperm surface for Xenopus fertilization: its role in a fast electrical block to polyspermy. Mech Dev 134:80–95

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki T, Sato K, Yoshino K, Itakura S, Kosuge K, Tokmakov AA, Owada K, Yonezawa K, Fukami Y (2006) Phylogeny of vertebrate Src tyrosine kinases revealed by the epitope region of mAb327. J Biochem 139(3):347–354

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki T, Koretomo Y, Fukuda T, Paronetto MP, Sette C, Fukami Y, Sato K (2008) Expression, phosphorylation, and mRNA-binding of heterogeneous nuclear ribonucleoprotein K in Xenopus oocytes, eggs, and early embryos. Develop Growth Differ 50(1):23–40

    Article  CAS  Google Scholar 

  • Jenkins D, Woolf AS (2007) Uroplakins: new molecular players in the biology of urinary tract malformations. Kidney Int 71(3):195–200

    Article  PubMed  CAS  Google Scholar 

  • Kushima S, Mammadova G, Mahbub Hasan AK, Fukami Y, Sato K (2011) Characterization of lipovitellin 2 as a tyrosine-phosphorylated protein in oocytes, eggs and early embryos of Xenopus laevis. Zool Sci 28(8):550–559

    Article  PubMed  CAS  Google Scholar 

  • Luria A, Vegelyte-Avery V, Stith B, Tsvetkova NM, Wolkers WF, Crowe JH, Tablin F, Nuccitelli R (2002) Detergent-free domain isolated from Xenopus egg plasma membrane with properties similar to those of detergent-resistant membranes. Biochemistry 41(44):13189–13197

    Article  PubMed  CAS  Google Scholar 

  • Mahbub Hasan AK, Sato K, Sakakibara K, Ou Z, Iwasaki T, Ueda Y, Fukami Y (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  PubMed  CAS  Google Scholar 

  • Mahbub Hasan AK, Ou Z, Sakakibara K, Hirahara S, Iwasaki T, Sato K, Fukami Y (2007) Characterization of Xenopus egg membrane microdomains containing uroplakin Ib/III complex: roles of their molecular interactions for subcellular localization and signal transduction. Genes Cells 12(2):251–267

    Article  PubMed  CAS  Google Scholar 

  • Mahbub Hasan AK, Hashimoto A, Maekawa Y, Matsumoto T, Kushima S, Ijiri TW, Fukami Y, Sato K (2014) Functional during oocyte maturation and is required for bidirectional gamete signaling at fertilization in Xenopus laevis. Development 141(8):1705–1714

    Article  PubMed  CAS  Google Scholar 

  • Mammadova G, Iwasaki T, Tokmakov AA, Fukami Y, Sato K (2009) Evidence that phosphatidylinositol 3-kinase is involved in sperm-induced tyrosine kinase signaling in Xenopus egg fertilization. BMC Dev Biol 9:68

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Masui Y (2000) The elusive cytostatic factor in the animal egg. Nat Rev Mol Cell Biol 1(3):228–232

    Article  PubMed  CAS  Google Scholar 

  • Mizote A, Okamoto S, Iwao Y (1999) Activation of Xenopus eggs by proteases: possible involvement of a sperm protease in fertilization. Dev Biol 208(1):79–92

    Article  PubMed  CAS  Google Scholar 

  • Nagano O, Saya H (2004) Mechanism and biological significance of CD44 cleavage. Cancer Sci 95(12):930–935

    Article  PubMed  CAS  Google Scholar 

  • Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). Garland Publishing, New York. ISBN: 0-8153-1896-0

    Google Scholar 

  • Nuccitelli R, Yim DL, Smart T (1993) The sperm-induced Ca2+ wave following fertilization of the Xenopus egg requires the production of Ins(1,4,5)P3. Dev Biol 158(1):200–212

    Article  PubMed  CAS  Google Scholar 

  • Runft LL, Watras J, Jaffe LA (1999) Calcium release at fertilization of Xenopus eggs requires type I IP3 receptors, but not SH2 domain–mediated activation of PLCγ or Gq-mediated activation of PLCbeta. Dev Biol 214(2):399–411

    Article  PubMed  CAS  Google Scholar 

  • Sakakibara K, Sato K, Yoshino K, Oshiro N, Hirahara S, Mahbub Hasan AK, Iwasaki T, Ueda Y, Iwao Y, Yonezawa K, Fukami Y (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 (2014) Transmembrane signal transduction in oocyte maturation and fertilization: focusing on Xenopus laevis as a model animal. Int J Mol Sci 16(1):114–134

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sato K, Aoto M, Mori K, Akasofu S, Tokmakov AA, Sahara S, Fukami Y (1996) Purification and characterization of a Src-related p57 protein-tyrosine kinase from Xenopus oocytes. Isolation of an inactive form of the enzyme and its activation and translocation upon fertilization. J Biol Chem 271(22):13250–13257

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Iwasaki T, Tamaki I, Aoto M, Tokmakov AA, Fukami Y (1998) Involvement of protein-tyrosine phosphorylation and dephosphorylation in sperm-induced Xenopus egg activation. FEBS Lett 424(1–2):113–118

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Iwao Y, Fujimura T, Tamaki I, Ogawa K, Iwasaki T, Tokmakov AA, Hatano O, Fukami Y (1999) Evidence for the involvement of a Src-related tyrosine kinase in Xenopus egg activation. Dev Biol 209(2):308–320

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Tokmakov AA, Fukami Y (2000a) Fertilization signalling and protein-tyrosine kinases. Comp Biochem Physiol B Biochem Mol Biol 126(2):129–148

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Tokmakov AA, Iwasaki T, Fukami Y (2000b) Tyrosine kinase-dependent activation of phospholipase Cγ is required for calcium transient in Xenopus egg fertilization. Dev Biol 224(2):453–469

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Ogawa K, Tokmakov AA, Iwasaki T, Fukami Y (2001) Hydrogen peroxide induces Src family tyrosine kinase-dependent activation of Xenopus eggs. Develop Growth Differ 43(1):55–72

    Article  CAS  Google Scholar 

  • Sato K, Iwasaki T, Ogawa K, Konishi M, Tokmakov AA, Fukami Y (2002) Low density detergent-insoluble membrane of Xenopus eggs: subcellular microdomain for tyrosine kinase signaling in fertilization. Development 129(4):885–896

    PubMed  CAS  Google Scholar 

  • Sato K, Tokmakov AA, He CL, Kurokawa M, Iwasaki T, Shirouzu M, Fissore RA, Yokoyama S, Fukami Y (2003) Reconstitution of Src-dependent phospholipase Cγ phosphorylation and transient calcium release by using membrane rafts and cell-free extracts from Xenopus eggs. J Biol Chem 278(40):38413–38420

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Iwasaki T, Hirahara S, Nishihira Y, Fukami Y (2004) Molecular dissection of egg fertilization signaling with the aid of tyrosine kinase-specific inhibitor and activator strategies. Biochim Biophys Acta 1697(1–2):103–121

    Article  PubMed  CAS  Google Scholar 

  • Sato K, Fukami Y, Stith BJ (2006a) 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 

  • Sato K, Yoshino K, Tokmakov AA, Iwasaki T, Yonezawa K, Fukami Y (2006b) Studying fertilization in cell-free extracts: focusing on membrane/lipid raft functions and proteomics. Methods Mol Biol 322:395–411

    Article  PubMed  CAS  Google Scholar 

  • Shilling FM, Krätzschmar J, Cai H, Weskamp G, Gayko U, Leibow J, Myles DG, Nuccitelli R, Blobel CP (1997) Identification of metalloprotease/disintegrins in Xenopus laevis testis with a potential role in fertilization. Dev Biol 186(2):155–164

    Article  PubMed  CAS  Google Scholar 

  • Shilling FM, Magie CR, Nuccitelli R (1998) Voltage-dependent activation of frog eggs by a sperm surface disintegrin peptide. Dev Biol 202(1):113–124

    Article  PubMed  CAS  Google Scholar 

  • Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387(6633):569–572

    Article  PubMed  CAS  Google Scholar 

  • Stith BJ (2015) Phospholipase C and D regulation of Src, calcium release and membrane fusion during Xenopus laevis development. Dev Biol 401(2):188–205

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tokmakov AA, Sato KI, Iwasaki T, Fukami Y (2002) Src kinase induces calcium release in Xenopus egg extracts via PLCγ and IP3-dependent mechanism. Cell Calcium 32(1):11–20

    Article  PubMed  CAS  Google Scholar 

  • Tu L, Sun TT, Kreibich G (2002) Specific heterodimer formation is a prerequisite for uroplakins to exit from the endoplasmic reticulum. Mol Biol Cell 13(12):4221–4230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vu TK, Hung DT, Wheaton VI, Coughlin SR (1991) Molecular cloning of a functional thrombin receptor reveals a novel proteolytic mechanism of receptor activation. Cell 64(6):1057–1068

    Article  PubMed  CAS  Google Scholar 

  • Wu XR, Kong XP, Pellicer A, Kreibich G, Sun TT (2009) Uroplakins in urothelial biology, function, and disease. Kidney Int 75(11):1153–1165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yim DL, Opresko LK, Wiley HS, Nuccitelli R (1994) Highly polarized EGF receptor tyrosine kinase activity initiates egg activation in Xenopus. Dev Biol 162(1):41–55

    Article  PubMed  CAS  Google Scholar 

Fish

  • Kinsey WH, Wu W, Macgregor E (2003) Activation of Src-family PTK activity at fertilization: role of the SH2 domain. Dev Biol 264(1):255–262

    Article  PubMed  CAS  Google Scholar 

  • Meyer A, Lydeard C (1993) The evolution of copulatory organs, internal fertilization, placentae and viviparity in killifishes (Cyprinodontiformes) inferred from a DNA phylogeny of the tyrosine kinase gene X-src. Proc Biol Sci 254(1340):153–162

    Article  PubMed  CAS  Google Scholar 

  • Sharma D, Kinsey WH (2006) Fertilization triggers localized activation of Src-family protein kinases in the zebrafish egg. Dev Biol 295(2):604–614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sharma D, Kinsey WH (2008) Regionalized calcium signaling in zebrafish fertilization. Int J Dev Biol 52(5–6):561–570

    Article  PubMed  Google Scholar 

  • Sharma D, Kinsey WH (2013) PYK2: a calcium-sensitive protein tyrosine kinase activated in response to fertilization of the zebrafish oocyte. Dev Biol 373(1):130–140

    Article  PubMed  CAS  Google Scholar 

  • Sides J, Lydeard C (2000) Phylogenetic utility of the tyrosine kinase gene X-src for assessing relationships among representative cichlid fishes. Mol Phylogenet Evol 14(1):51–74

    Article  PubMed  CAS  Google Scholar 

  • Tsai WB, Zhang X, Sharma D, Wu W, Kinsey WH (2005) Role of yes kinase during early zebrafish development. Dev Biol 277(1):129–141

    Article  PubMed  CAS  Google Scholar 

  • Wu W, Kinsey WH (2000) Fertilization triggers activation of Fyn kinase in the zebrafish egg. Int J Dev Biol 44(8):837–841

    PubMed  CAS  Google Scholar 

  • Wu W, Kinsey WH (2002) Role of PTPase(s) in regulating Fyn kinase at fertilization of the zebrafish egg. Dev Biol 247(2):286–294

    Article  PubMed  CAS  Google Scholar 

Mouse/Rat

  • Aarabi M, Balakier H, Bashar S, Moskovtsev SI, Sutovsky P, Librach CL, Oko R (2014) Sperm-derived WW domain–binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J 28(10):4434–4440

    Article  PubMed  CAS  Google Scholar 

  • Aarabi M, Sutovsky P, Oko R (2015) Re: is PAWP the ‘real’ sperm factor? Asian J Androl 17(3):446–449

    PubMed  PubMed Central  Google Scholar 

  • Ben-Yosef D, Talmor A, Shwartz L, Granot Y, Shalgi R (1998) Tyrosyl-phosphorylated proteins are involved in regulation of meiosis in the rat egg. Mol Reprod Dev 49(2):176–185

    Article  PubMed  CAS  Google Scholar 

  • Gonçalves RF, Wolinetz CD, Killian GJ (2007) Influence of arginine-glycine-aspartic acid (RGD), integrins (αV and α5) and osteopontin on bovine sperm–egg binding, and fertilization in vitro. Theriogenology 67(3):468–474

    Article  PubMed  CAS  Google Scholar 

  • Kim JH, Do HJ, Wang WH, Macháty Z, Han YM, Day BN, Prather RS (1999) A protein tyrosine phosphatase inhibitor, sodium orthovanadate, causes parthenogenetic activation of pig oocytes via an increase in protein tyrosine kinase activity. Biol Reprod 61(4):900–905

    Article  PubMed  CAS  Google Scholar 

  • Kurokawa M, Sato K, Smyth J, Wu H, Fukami K, Takenawa T, Fissore RA (2004) Evidence that activation of Src family kinase is not required for fertilization-associated [Ca2+]i oscillations in mouse eggs. Reproduction 127(4):441–454

    Article  PubMed  CAS  Google Scholar 

  • Kurokawa M, Sato K, Wu H, He C, Malcuit C, Black SJ, Fukami K, Fissore RA (2005) Functional, biochemical, and chromatographic characterization of the complete [Ca2+]i oscillation-inducing activity of porcine sperm. Dev Biol 285(2):376–392

    Article  PubMed  CAS  Google Scholar 

  • Levi M, Shalgi R (2010) The role of Fyn kinase in the release from metaphase in mammalian oocytes. Mol Cell Endocrinol 314(2):228–233

    Article  PubMed  CAS  Google Scholar 

  • Levi M, Maro B, Shalgi R (2010a) Fyn kinase is involved in cleavage furrow ingression during meiosis and mitosis. Reproduction 140(6):827–834

    Article  PubMed  CAS  Google Scholar 

  • Levi M, Maro B, Shalgi R (2010b) The involvement of Fyn kinase in resumption of the first meiotic division in mouse oocytes. Cell Cycle 9(8):1577–1589

    Article  PubMed  CAS  Google Scholar 

  • Levi M, Ninio-Mani L, Shalgi R (2012) Src protein kinases in mouse and rat oocytes and embryos. Results Probl Cell Differ 55:93–106

    Article  PubMed  CAS  Google Scholar 

  • Luo J, McGinnis LK, Kinsey WH (2009) Fyn kinase activity is required for normal organization and functional polarity of the mouse oocyte cortex. Mol Reprod Dev 76(9):819–831

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luo J, McGinnis LK, Carlton C, Beggs HE, Kinsey WH (2014) PTK2b function during fertilization of the mouse oocyte. Biochem Biophys Res Commun 450(3):1212–1217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Macias MJ, Hyvönen M, Baraldi E, Schultz J, Sudol M, Saraste M, Oschkinat H (1996) Structure of the WW domain of a kinase-associated protein complexed with a proline-rich peptide. Nature 382(6592):646–649

    Article  PubMed  CAS  Google Scholar 

  • McGinnis LK, Albertini DF, Kinsey WH (2007) Localized activation of Src-family protein kinases in the mouse egg. Dev Biol 306(1):241–254

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • McGinnis LK, Kinsey WH, Albertini DF (2009) Functions of Fyn kinase in the completion of meiosis in mouse oocytes. Dev Biol 327(2):280–287

    Article  PubMed  CAS  Google Scholar 

  • McGinnis LK, Hong X, Christenson LK, Kinsey WH (2011) Fer tyrosine kinase is required for germinal vesicle breakdown and meiosis-I in mouse oocytes. Mol Reprod Dev 78(1):33–47

    Article  PubMed  CAS  Google Scholar 

  • McGinnis LK, Luo J, Kinsey WH (2013) Protein tyrosine kinase signaling in the mouse oocyte cortex during sperm–egg interactions and anaphase resumption. Mol Reprod Dev 80(4):260–272

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mehlmann LM, Jaffe LA (2005) SH2 domain–mediated activation of an SRC family kinase is not required to initiate Ca2+ release at fertilization in mouse eggs. Reproduction 129(5):557–564

    Article  PubMed  CAS  Google Scholar 

  • Mehlmann LM, Carpenter G, Rhee SG, Jaffe LA (1998) SH2 domain–mediated activation of phospholipase Cγ is not required to initiate Ca2+ release at fertilization of mouse eggs. Dev Biol 203(1):221–232

    Article  PubMed  CAS  Google Scholar 

  • Mehlmann LM, Chattopadhyay A, Carpenter G, Jaffe LA (2001) Evidence that phospholipase C from the sperm is not responsible for initiating Ca2+ release at fertilization in mouse eggs. Dev Biol 236(2):492–501

    Article  PubMed  CAS  Google Scholar 

  • Meng L, Luo J, Li C, Kinsey WH (2006) Role of Src homology 2 domain–mediated PTK signaling in mouse zygotic development. Reproduction 132(3):413–421

    Article  PubMed  CAS  Google Scholar 

  • Mori T, Wu GM, Mori E (1991) Expression of CD4-like structure on murine egg vitelline membrane and its signal transductive roles through p56lck in fertilization. Am J Reprod Immunol 26(3):97–103

    Article  PubMed  CAS  Google Scholar 

  • Nomikos M, Sanders JR, Theodoridou M, Kashir J, Matthews E, Nounesis G, Lai FA, Swann K (2014) Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod 20(10):938–947

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paronetto MP, Venables JP, Elliott DJ, Geremia R, Rossi P, Sette C (2003) Tr-kit promotes the formation of a multimolecular complex composed by Fyn, PLCγ1 and Sam68. Oncogene 22(54):8707–8715

    Article  PubMed  CAS  Google Scholar 

  • Perry AC, Wakayama T, Cooke IM, Yanagimachi R (2000) Mammalian oocyte activation by the synergistic action of discrete sperm head components: induction of calcium transients and involvement of proteolysis. Dev Biol 217(2):386–393

    Article  PubMed  CAS  Google Scholar 

  • Saunders CM, Larman MG, Parrington J, Cox LJ, Royse J, Blayney LM, Swann K, Lai FA (2002) PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129(15):3533–3544

    PubMed  CAS  Google Scholar 

  • Sette C, Bevilacqua A, Bianchini A, Mangia F, Geremia R, Rossi P (1997) Parthenogenetic activation of mouse eggs by microinjection of a truncated c-kit tyrosine kinase present in spermatozoa. Development 124(11):2267–2274

    PubMed  CAS  Google Scholar 

  • Sette C, Bevilacqua A, Geremia R, Rossi P (1998) Involvement of phospholipase Cγ1 in mouse egg activation induced by a truncated form of the c-kit tyrosine kinase present in spermatozoa. J Cell Biol 142(4):1063–1074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sette C, Paronetto MP, Barchi M, Bevilacqua A, Geremia R, Rossi P (2002) Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. EMBO J 21(20):5386–5395

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sutovsky P, Manandhar G, Wu A, Oko R (2003) Interactions of sperm perinuclear theca with the oocyte: implications for oocyte activation, anti-polyspermy defense, and assisted reproduction. Microsc Res Tech 61(4):362–378

    Article  PubMed  Google Scholar 

  • Swann K (1996) Soluble sperm factors and Ca2+ release in eggs at fertilization. Rev Reprod 1(1):33–39

    Article  PubMed  CAS  Google Scholar 

  • Swann K, Larman MG, Saunders CM, Lai FA (2004) The cytosolic sperm factor that triggers Ca2+ oscillations and egg activation in mammals is a novel phospholipase C: PLCζ. Reproduction 127(4):431–439

    Article  PubMed  CAS  Google Scholar 

  • Talmor A, Kinsey WH, Shalgi R (1998) Expression and immunolocalization of p59c-fyn yrosine kinase in rat eggs. Dev Biol 194(1):38–46

    Article  PubMed  CAS  Google Scholar 

  • Talmor-Cohen A, Tomashov-Matar R, Eliyahu E, Shapiro R, Shalgi R (2004a) Are Src family kinases involved in cell cycle resumption in rat eggs? Reproduction 127(4):455–463

    Article  PubMed  CAS  Google Scholar 

  • Talmor-Cohen A, Tomashov-Matar R, Tsai WB, Kinsey WH, Shalgi R (2004b) Fyn kinase-tubulin interaction during meiosis of rat eggs. Reproduction 128(4):387–393

    Article  PubMed  CAS  Google Scholar 

  • Tatone C, Carbone MC (2006) Possible involvement of integrin-mediated signalling in oocyte activation: evidence that a cyclic RGD-containing peptide can stimulate protein kinase C and cortical granule exocytosis in mouse oocytes. Reprod Biol Endocrinol 4:48

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • White KL, Passipieri M, Bunch TD, Campbell KD, Pate B (2007) Effects of arginine-glycine-aspartic acid (RGD) containing snake venom peptides on parthenogenetic development and in vitro fertilization of bovine oocytes. Mol Reprod Dev 74(1):88–96

    Article  PubMed  CAS  Google Scholar 

  • Wu AT, Sutovsky P, Manandhar G, Xu W, Katayama M, Day BN, Park KW, Yi YJ, Xi YW, Prather RS, Oko R (2007) PAWP, a sperm-specific WW domain–binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282(16):12164–12175

    Article  PubMed  CAS  Google Scholar 

Perspective

  • Bianchi E, Doe B, Goulding D, Wright GJ (2014) Juno is the egg Izumo receptor and is essential for mammalian fertilization. Nature 508(7497):483–487

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Inoue N, Ikawa M, Isotani A, Okabe M (2005) The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 434(7030):234–238

    Article  PubMed  CAS  Google Scholar 

  • Inoue N, Hamada D, Kamikubo H, Hirata K, Kataoka M, Yamamoto M, Ikawa M, Okabe M, Hagihara Y (2013) Molecular dissection of IZUMO1, a sperm protein essential for sperm–egg fusion. Development 140(15):3221–3229

    Article  PubMed  CAS  Google Scholar 

  • Kaji K, Oda S, Shikano T, Ohnuki T, Uematsu Y, Sakagami J, Tada N, Miyazaki S, Kudo A (2000) The gamete fusion process is defective in eggs of Cd9-deficient mice. Nat Genet 24(3):279–282

    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 

  • Le Naour F, Rubinstein E, Jasmin C, Prenant M, Boucheix C (2000) Severely reduced female fertility in CD9-deficient mice. Science 287(5451):319–321

    Article  PubMed  Google Scholar 

  • Miyado K, Yamada G, Yamada S, Hasuwa H, Nakamura Y, Ryu F, Suzuki K, Kosai K, Inoue K, Ogura A, Okabe M, Mekada E (2000) Requirement of CD9 on the egg plasma membrane for fertilization. Science 287(5451):321–324

    Article  PubMed  CAS  Google Scholar 

  • Miyado K, Yoshida K, Yamagata K, Sakakibara K, Okabe M, Wang X, Miyamoto K, Akutsu H, Kondo T, Takahashi Y, Ban T, Ito C, Toshimori K, Nakamura A, Ito M, Miyado M, Mekada E, Umezawa A (2008) The fusing ability of sperm is bestowed by CD9-containing vesicles released from eggs in mice. Proc Natl Acad Sci U S A 105(35):12921–12926

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by a Grant-in-Aid for Scientific Research (C) from the Japan Society for the Promotion of Science (No. 15 K07083).

Author information

Authors and Affiliations

  1. Laboratory of Cell Signaling and Development Department of Molecular Biosciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan

    Ken-ichi Sato

Authors
  1. Ken-ichi Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ken-ichi Sato .

Editor information

Editors and Affiliations

  1. Department of Biology, Faculty of Agriculture and Life Science, Hirosaki University, Hirosaki, Japan

    Kazuya Kobayashi

  2. Department of Biological Sciences, Graduate School of Science and Technology Kumamoto University, Kumamoto, Japan

    Takeshi Kitano

  3. Laboratory of Reproductive Developmental Biology, Division of Earth Sciences, Biology, and Chemistry, Graduate School of Sciences and Technology for Innovation Yamaguchi University, Yamaguchi, Japan

    Yasuhiro Iwao

  4. Misaki Marine Biological Station, Graduate School of Science The University of Tokyo, Miura, Japan

    Mariko Kondo

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Japan KK, part of Springer Nature

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sato, Ki. (2018). Fertilization and Protein Tyrosine Kinase Signaling: Are They Merging or Emerging?. In: Kobayashi, K., Kitano, T., Iwao, Y., Kondo, M. (eds) Reproductive and Developmental Strategies. Diversity and Commonality in Animals. Springer, Tokyo. https://doi.org/10.1007/978-4-431-56609-0_27

Download citation

Publish with us

Policies and ethics

Search

Navigation