Structure, Processing, and Polymerization of Rainbow Trout Egg Vitelline Envelope Proteins

Part of the NATO Science for Peace and Security Series A: Chemistry and Biology book series (NAPSA)


Mammalian and non-mammalian eggs are surrounded by a zona pellucida (ZP) and vitelline envelope (VE), respectively. The rainbow trout egg VE consists of three proteins, VEα, VEβ, and VEγ, which are related to mouse egg ZP proteins ZP1, ZP2, and ZP3. Mass spectrometry (MS) has been used extensively to identify the intramolecular disulfide linkages and the cellular site of proteolytic processing of trout VE proteins. Additionally, Blue Native-PAGE (BN-PAGE) has been used to investigate polymerization of purified trout VE proteins under non-denaturing conditions. Results of these experiments reveal that, despite ~400 million years separating the appearance of trout and mice, and the change from external to internal fertilization and development, VE and ZP proteins have a great deal in common.


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  1. Boja, E. S., T. Hoodbhoy, et al. (2003). “Structural characterization of native mouse zona pellu-cida proteins using mass spectrometry.” J Biol Chem 278(36): 34189-202.CrossRefPubMedGoogle Scholar
  2. Bourne, Y., M. H. Watson, et al. (2000). “Crystal structure and mutational analysis of the Sac-charomyces cerevisiae cell cycle regulatory protein Cks1: implications for domain swapping, anion binding and protein interactions.” Structure 8(8): 841-50.CrossRefPubMedGoogle Scholar
  3. Brivio, M. F., R. Bassi, et al. (1991). “Identification and characterization of the major compo-nents of the Oncorhynchus mykiss egg chorion.” Mol Reprod Dev 28(1): 85-93.CrossRefPubMedGoogle Scholar
  4. Carr, M. D., C. J. Bauer, et al. (1994). “Solution structure of a trefoil-motif-containing cell growth factor, porcine spasmolytic protein.” Proc Natl Acad Sci U S A 91(6): 2206-10.CrossRefPubMedGoogle Scholar
  5. Conner, S. J. and D. C. Hughes (2003). “Analysis of fish ZP1/ZPB homologous genes--evidence for both genome duplication and species-specific amplification models of evolution.” Repro-duction 126(3): 347-52.CrossRefGoogle Scholar
  6. Darie, C. C., M. L. Biniossek, et al. (2005). “Mass spectrometric evidence that proteolytic proc-essing of rainbow trout egg vitelline envelope proteins takes place on the egg.” J Biol Chem 280 (45): 37585-98.CrossRefPubMedGoogle Scholar
  7. Darie, C. C., M. L. Biniossek, et al. (2004). “Structural characterization of fish egg vitelline envelope proteins by mass spectrometry.” Biochemistry 43(23): 7459-78.CrossRefPubMedGoogle Scholar
  8. Darie, C. C., M. L. Biniossek, et al. (2005). “Isolation and structural characterization of the Ndh complex from mesophyll and bundle sheath chloroplasts of Zea mays.” Febs J 272(11): 2705-16.CrossRefPubMedGoogle Scholar
  9. Darie, C. C., W. G. Janssen, et al. (2007). “Purified trout egg vitelline envelope proteins VEbeta and VEgamma polymerize into homomeric fibrils from dimers in vitro.” Biochim Biophys Acta doi:10.1016/j.bbapap.2007.10.011.Google Scholar
  10. Dumont, J. N. and A. R. Brummett (1985). Egg envelopes in vertebrates. New York, Plenum press.Google Scholar
  11. Fujita, T., M. Shimizu, et al. (2002). “Purification of serum precursor proteins to vitelline envelope (choriogenins) in masu salmon, Oncorhynchus masou.” Comp Biochem Physiol B Biochem Mol Biol 132(3): 599-610.CrossRefPubMedGoogle Scholar
  12. Greve, J. M. and P. M. Wassarman (1985). “Mouse egg extracellular coat is a matrix of inter-connected filaments possessing a structural repeat.” J Mol Biol 181(2): 253-64.CrossRefPubMedGoogle Scholar
  13. Hagenmaier, H. E. (1973). “The hatching process in fish embryos. 3. The structure, poly-saccharide and protein cytochemistry of the chorion of the trout egg, Salmo gairdneri (Rich.).” Acta Histochem 47(1): 61-9.PubMedGoogle Scholar
  14. Handford, P. A., A. K. Downing, et al. (2000). “Fibrillin: from domain structure to supramole-cular assembly.” Matrix Biol 19(6): 457-70.CrossRefPubMedGoogle Scholar
  15. Hyllner, S. J. and C. Haux (1992). “Immunochemical detection of the major vitelline envelope proteins in the plasma and oocytes of the maturing female rainbow trout, Oncorhynchus mykiss.” J Endocrinol 135(2): 303-9.CrossRefPubMedGoogle Scholar
  16. Hyllner, S. J., D. O. Oppen-Berntsen, et al. (1991). “Oestradiol-17 beta induces the major vitel-line envelope proteins in both sexes in teleosts.” J Endocrinol 131(2): 229-36.CrossRefPubMedGoogle Scholar
  17. Hyllner, S. J., L. Westerlund, et al. (2001). “Cloning of rainbow trout egg envelope proteins: members of a unique group of structural proteins.” Biol Reprod 64(3): 805-11.CrossRefPubMedGoogle Scholar
  18. Iwamatsu, T., N. Yoshizaki, et al. (1997). “Changes in the chorion and sperm entry into the micropyle during fertilization in the teleostean fish, Oryzias latipes.” Dev Growth Differ 39 (1): 33-41.CrossRefPubMedGoogle Scholar
  19. Jovine, L., C. C. Darie, et al. (2005). “Zona pellucida domain proteins.” Annu Rev Biochem 74: 83-114.CrossRefPubMedGoogle Scholar
  20. Jovine, L., W. G. Janssen, et al. (2006). “The PLAC1-homology region of the ZP domain is suf-ficient for protein polymerisation.” BMC Biochem 7: 11.CrossRefPubMedGoogle Scholar
  21. Jovine, L., H. Qi, et al. (2002). “The ZP domain is a conserved module for polymerization of extracellular proteins.” Nat Cell Biol 4(6): 457-61.CrossRefPubMedGoogle Scholar
  22. Jovine, L., H. Qi, et al. (2006). Features that affect secretion and assembly of zona pellucidaglycoproteins during mammalian oogenesis. Nottingham, U. Press.Google Scholar
  23. Jovine, L., H. Qi, et al. (2004). “A duplicated motif controls assembly of zona pellucida domain proteins.” Proc Natl Acad Sci U S A 101(16): 5922-7.CrossRefPubMedGoogle Scholar
  24. Litscher, E. S., W. G. Janssen, et al. (2008). “Purified mouse egg zona pellucida glycoproteins polymerize into homomeric fibrils under non-denaturing conditions.” J Cell Physiol 214(1): 153-7.CrossRefPubMedGoogle Scholar
  25. Litscher, E. S., C. Liu, et al. (1999). “Zona pellucida glycoprotein mZP3 produced in milk of transgenic mice is active as a sperm receptor, but can be lethal to newborns.” Transgenic Res 8 (5): 361-9.CrossRefPubMedGoogle Scholar
  26. Litscher, E. S. and P. M. Wassarman (2007). “Egg extracellular coat proteins: from fish to mammals.” Histol Histopathol 22(3): 337-47.PubMedGoogle Scholar
  27. Llorca, O., A. Trujillo, et al. (2007). “Structural model of human endoglin, a transmembrane re-ceptor responsible for hereditary hemorrhagic telangiectasia.” J Mol Biol 365(3): 694-705.CrossRefPubMedGoogle Scholar
  28. Mosesson, M. W., K. R. Siebenlist, et al. (2001). “The structure and biological features of fi-brinogen and fibrin.” Ann N Y Acad Sci 936: 11-30.PubMedCrossRefGoogle Scholar
  29. Oppen-Berntsen, D. O., S. J. Hyllner, et al. (1992). “Eggshell zona radiata-proteins from cod (Gadus morhua): extra-ovarian origin and induction by estradiol-17 beta.” Int J Dev Biol 36 (2): 247-54.PubMedGoogle Scholar
  30. Sasanami, T., J. Pan, et al. (2002). “Secretion of egg envelope protein ZPC after C-terminal pro-teolytic processing in quail granulosa cells.” Eur J Biochem 269(8): 2223-31.CrossRefPubMedGoogle Scholar
  31. Schagger, H., W. A. Cramer, et al. (1994). “Analysis of molecular masses and oligomeric states of protein complexes by blue native electrophoresis and isolation of membrane protein com-plexes by two-dimensional native electrophoresis.” Anal Biochem 217(2): 220-30.CrossRefPubMedGoogle Scholar
  32. Schagger, H. and G. von Jagow (1991). “Blue native electrophoresis for isolation of membrane protein complexes in enzymatically active form.” Anal Biochem 199(2): 223-31.CrossRefPubMedGoogle Scholar
  33. Schneider, W. J. (1996). “Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family.” Int Rev Cytol 166: 103-37.CrossRefPubMedGoogle Scholar
  34. Shibata, Y., T. Iwamatsu, et al. (2000). “Identification and cDNA cloning of alveolin, an extracellular metalloproteinase, which induces chorion hardening of medaka (Oryzias latipes) eggs upon fertilization.” J Biol Chem 275(12): 8349-54.CrossRefPubMedGoogle Scholar
  35. Sugiyama, H., K. Murata, et al. (1999). “Formation of mature egg envelope subunit proteins from their precursors (choriogenins) in the fish, Oryzias latipes: loss of partial C-terminal sequences of the choriogenins.” J Biochem (Tokyo) 125(3): 469-75.Google Scholar
  36. Swamy, M., G. M. Siegers, et al. (2006). “Blue native polyacrylamide gel electrophoresis (BN-PAGE) for the identification and analysis of multiprotein complexes.” Sci STKE 2006 (345): p. l4.Google Scholar
  37. Taylor, K. M., A. R. Trimby, et al. (1997). “Mutation of recombinant complement component C9 reveals the significance of the N-terminal region for polymerization.” Immunology 91(1): 20-7.CrossRefPubMedGoogle Scholar
  38. Wallace, R. A. (1985). Vitellogenesis and oocyte growth in nonmammalian vertebrates. New York, Plenum Press.Google Scholar
  39. Wassarman, P. M. and S. Mortillo (1991). “Structure of the mouse egg extracellular coat, the zona pellucida.” Int Rev Cytol 130: 85-110.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science + Business Media B.V 2008

Authors and Affiliations

  1. 1.Department of Molecular, Cell and Developmental BiologyMount Sinai School of MedicineNew York10029-6574
  2. 2.Department of Structural Biology, Skirball Institute of Biomolecular MedicineNew York UniversityNew York

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