Avian Egg and Egg Coat

  • Hiroki OkumuraEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1001)


An ovulated egg of vertebrates is surrounded by unique extracellular matrix, the egg coat or zona pellucida, playing important roles in fertilization and early development. The vertebrate egg coat is composed of two to six zona pellucida (ZP) glycoproteins that are characterized by the evolutionarily conserved ZP-domain module and classified into six subfamilies based on phylogenetic analyses. Interestingly, investigations of biochemical and functional features of the ZP glycoproteins show that the roles of each ZP-glycoprotein family member in the egg-coat formation and the egg–sperm interactions seemingly vary across vertebrates. This might be one reason why comprehensive understandings of the molecular basis of either architecture or physiological functions of egg coat still remain elusive despite more than 3 decades of intensive investigations. In this chapter, an overview of avian egg focusing on the oogenesis are provided in the first section, and unique features of avian egg coat, i.e., perivitelline layer, including the morphology, biogenesis pathway, and physiological functions are discussed mainly on chicken and quail in terms of the characteristics of ZP glycoproteins in the following sections. In addition, these features of avian egg coat are compared to mammalian zona pellucida, from the viewpoint that the structural and functional varieties of ZP glycoproteins might be associated with the evolutionary adaptation to their reproductive strategies. By comparing the egg coat of birds and mammals whose reproductive strategies are largely different, new insights into the molecular mechanisms of vertebrate egg–sperm interactions might be provided.


Egg coat Zona pellucida Sperm–zona interaction ZP glycoprotein Extracellular matrix Evolution 


  1. Adkins-Regan E, Banerjee SB, Correa SM, Schweitzer C. Maternal effects in quail and zebra finches: behavior and hormones. Gen Comp Endocrinol. 2013;190:34–41. doi: 10.1016/j.ygcen.2013.03.002.PubMedCrossRefGoogle Scholar
  2. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997;25(17):3389–402.PubMedPubMedCentralCrossRefGoogle Scholar
  3. Avella MA, Baibakov B, Dean J. A single domain of the ZP2 zona pellucida protein mediates gamete recognition in mice and humans. J Cell Biol. 2014;205(6):801–9. doi: 10.1083/jcb.201404025.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Baba T, Niida Y, Michikawa Y, Kashiwabara S, Kodaira K, Takenaka M, Kohno N, Gerton GL, Arai Y. An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. J Biol Chem. 1994;269(13):10133–40.PubMedGoogle Scholar
  5. Bakst MR, Howarth B Jr. The fine structure of the hen’s ovum at ovulation. Biol Reprod. 1977a;17(3):361–9.PubMedCrossRefGoogle Scholar
  6. Bakst MR, Howarth B Jr. Hydrolysis of the hen’s perivitelline layer by cock sperm in vitro. Biol Reprod. 1977b;17(3):370–9.PubMedCrossRefGoogle Scholar
  7. Bansal P, Chakrabarti K, Gupta SK. Functional activity of human ZP3 primary sperm receptor resides toward its C-terminus. Biol Reprod. 2009;81(1):7–15. doi: 10.1095/biolreprod.108.074716.PubMedCrossRefGoogle Scholar
  8. Bausek N, Waclawek M, Schneider WJ, Wohlrab F. The major chicken egg envelope protein ZP1 is different from ZPB and is synthesized in the liver. J Biol Chem. 2000;275(37):28866–72.PubMedCrossRefGoogle Scholar
  9. Benson AP, Christensen VL, Fairchild BD, Davis AJ. The mRNA for zona pellucida proteins B1, C and D in two genetic lines of turkey hens that differ in fertility. Anim Reprod Sci. 2009;111(2–4):149–59. doi: 10.1016/j.anireprosci.2008.02.013.PubMedCrossRefGoogle Scholar
  10. Birkhead TR, Sheldon BC, Fletcher F. A comparative study of sperm–egg interactions in birds. J Reprod Fertil. 1994;101(2):353–61.PubMedCrossRefGoogle Scholar
  11. Blackmore DG, Baillie LR, Holt JE, Dierkx L, Aitken RJ, McLaughlin EA. Biosynthesis of the canine zona pellucida requires the integrated participation of both oocytes and granulosa cells. Biol Reprod. 2004;71(2):661–8. doi: 10.1095/biolreprod.104.028779.PubMedCrossRefGoogle Scholar
  12. Bleil JD, Greve JM, Wassarman PM. Identification of a secondary sperm receptor in the mouse egg zona pellucida: role in maintenance of binding of acrosome-reacted sperm to eggs. Dev Biol. 1988;128(2):376–85.PubMedCrossRefGoogle Scholar
  13. Bleil JD, Wassarman PM. Mammalian sperm–egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm. Cell. 1980;20(3):873–82.PubMedCrossRefGoogle Scholar
  14. Bokhove M, Nishimura K, Brunati M, Han L, de Sanctis D, Rampoldi L, Jovine L. A structured interdomain linker directs self-polymerization of human uromodulin. Proc Natl Acad Sci U S A. 2016;113(6):1552–7. doi: 10.1073/pnas.1519803113.PubMedPubMedCentralCrossRefGoogle Scholar
  15. Bork P, Sander C. A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor. FEBS Lett. 1992;300(3):237–40.PubMedCrossRefGoogle Scholar
  16. Bramwell RK, Howarth B Jr. Preferential attachment of cock spermatozoa to the perivitelline layer directly over the germinal disc of the hen’s ovum. Biol Reprod. 1992;47(6):1113–7.PubMedCrossRefGoogle Scholar
  17. Burkart AD, Xiong B, Baibakov B, Jimenez-Movilla M, Dean J. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy. J Cell Biol. 2012;197(1):37–44. doi: 10.1083/jcb.201112094.PubMedPubMedCentralCrossRefGoogle Scholar
  18. Callebaut I, Mornon JP, Monget P. Isolated ZP-N domains constitute the N-terminal extensions of Zona Pellucida proteins. Bioinformatics. 2007;23(15):1871–4. doi: 10.1093/bioinformatics/btm265.PubMedCrossRefGoogle Scholar
  19. Clark GF. The role of carbohydrate recognition during human sperm–egg binding. Hum Reprod. 2013;28(3):566–77. doi: 10.1093/humrep/des447.PubMedCrossRefGoogle Scholar
  20. Correa SM, Adkins-Regan E, Johnson PA. High progesterone during avian meiosis biases sex ratios toward females. Biol Lett. 2005;1(2):215–8. doi: 10.1098/rsbl.2004.0283.PubMedPubMedCentralCrossRefGoogle Scholar
  21. Darie CC, Biniossek ML, Jovine L, Litscher ES, Wassarman PM. Structural characterization of fish egg vitelline envelope proteins by mass spectrometry. Biochemistry. 2004;43(23):7459–78. doi: 10.1021/bi0495937.PubMedCrossRefGoogle Scholar
  22. Dean J. Reassessing the molecular biology of sperm–egg recognition with mouse genetics. BioEssays. 2004;26(1):29–38. doi: 10.1002/bies.10412.PubMedCrossRefGoogle Scholar
  23. Dias da Silva W, Tambourgi DV. IgY: a promising antibody for use in immunodiagnostic and in immunotherapy. Vet Immunol Immunopathol. 2010;135(3–4):173–80. doi: 10.1016/j.vetimm.2009.12.011.PubMedCrossRefGoogle Scholar
  24. Diestel U, Resch M, Meinhardt K, Weiler S, Hellmann TV, Mueller TD, Nickel J, Eichler J, Muller YA. Identification of a novel TGF-beta-binding site in the Zona Pellucida C-terminal (ZP-C) domain of TGF-beta-Receptor-3 (TGFR-3). PLoS One. 2013;8(6):e67214. doi: 10.1371/journal.pone.0067214.PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ensslin MA, Shur BD. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm–egg binding. Cell. 2003;114(4):405–17.PubMedCrossRefGoogle Scholar
  26. Epifano O, Liang LF, Familari M, Moos MC Jr, Dean J. Coordinate expression of the three zona pellucida genes during mouse oogenesis. Development. 1995;121(7):1947–56.PubMedGoogle Scholar
  27. Florman HM, Storey BT. Mouse gamete interactions: the zona pellucida is the site of the acrosome reaction leading to fertilization in vitro. Dev Biol. 1982;91(1):121–30.PubMedCrossRefGoogle Scholar
  28. Florman HM, Wassarman PM. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell. 1985;41(1):313–24.PubMedCrossRefGoogle Scholar
  29. Gao Z, Garbers DL. Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains. J Biol Chem. 1998;273(6):3415–21.PubMedCrossRefGoogle Scholar
  30. Goudet G, Mugnier S, Callebaut I, Monget P. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates. Biol Reprod. 2008;78(5):796–806. doi: 10.1095/biolreprod.107.064568.PubMedCrossRefGoogle Scholar
  31. Greve JM, Wassarman PM. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. J Mol Biol. 1985;181(2):253–64.PubMedCrossRefGoogle Scholar
  32. Gwatkin RB, Williams DT. Receptor activity of the hamster and mouse solubilized zona pellucida before and after the zona reaction. J Reprod Fertil. 1977;49(1):55–9.PubMedCrossRefGoogle Scholar
  33. Gwatkin RB, Williams DT, Hartmann JF, Kniazuk M. The zona reaction of hamster and mouse eggs: production in vitro by a trypsin-like protease from cortical granules. J Reprod Fertil. 1973;32(2):259–65.PubMedCrossRefGoogle Scholar
  34. Han L, Monné M, Okumura H, Schwend T, Cherry AL, Flot D, Matsuda T, Jovine L. Insights into egg coat assembly and egg–sperm interaction from the X-ray structure of full-length ZP3. Cell. 2010;143(3):404–15. doi: 10.1016/j.cell.2010.09.041.PubMedCrossRefGoogle Scholar
  35. Hanada A, Chang MC. Penetration of zone-free eggs by spermatozoa of different species. Biol Reprod. 1972;6(2):300–9.PubMedCrossRefGoogle Scholar
  36. Hanafy AM, Sasanami T, Mori M. Sensitivity of expression of perivitelline membrane glycoprotein ZP1 mRNA in the liver of Japanese quail (Coturnix japonica) to estrogenic compounds. Comp Biochem Physiol C Toxicol Pharmacol. 2007;144(4):356–62. doi: 10.1016/j.cbpc.2006.11.007.PubMedCrossRefGoogle Scholar
  37. Hardy DM, Garbers DL. A sperm membrane protein that binds in a species-specific manner to the egg extracellular matrix is homologous to von Willebrand factor. J Biol Chem. 1995;270(44):26025–8.PubMedCrossRefGoogle Scholar
  38. Hartmann JF, Gwatkin RB. Alteration of sites on the mammalian sperm surface following capacitation. Nature. 1971;234(5330):479–81.PubMedCrossRefGoogle Scholar
  39. Hartmann JF, Gwatkin RB, Hutchison CF. Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida. Proc Natl Acad Sci U S A. 1972;69(10):2767–9.PubMedPubMedCentralCrossRefGoogle Scholar
  40. Hoodbhoy T, Joshi S, Boja ES, Williams SA, Stanley P, Dean J. Human sperm do not bind to rat zonae pellucidae despite the presence of four homologous glycoproteins. J Biol Chem. 2005;280(13):12721–31. doi: 10.1074/jbc.M413569200.PubMedCrossRefGoogle Scholar
  41. Hoodbhoy T, Talbot P. Mammalian cortical granules: contents, fate, and function. Mol Reprod Dev. 1994;39(4):439–48. doi: 10.1002/mrd.1080390413.PubMedCrossRefGoogle Scholar
  42. Hughes GC. The population of germ cells in the developing female chick. J Embryol Exp Morphol. 1963;11:513–36.PubMedGoogle Scholar
  43. Inoue N, Satouh Y, Ikawa M, Okabe M, Yanagimachi R. Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc Natl Acad Sci U S A. 2011;108(50):20008–11. doi: 10.1073/pnas.1116965108.PubMedPubMedCentralCrossRefGoogle Scholar
  44. Izquierdo-Rico MJ, Jiménez-Movilla M, Llop E, Pérez-Oliva AB, Ballesta J, Gutiérrez-Gallego R, Jiménez-Cervantes C, Avilés M. Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4. J Proteome Res. 2009;8(2):926–41. doi: 10.1021/pr800568x.PubMedCrossRefGoogle Scholar
  45. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci U S A. 2011;108(12):4892–6. doi: 10.1073/pnas.1018202108.PubMedPubMedCentralCrossRefGoogle Scholar
  46. Johnson AL. Ovarian follicle selection and granulosa cell differentiation. Poult Sci. 2015;94(4):781–5. doi: 10.3382/ps/peu008.PubMedCrossRefGoogle Scholar
  47. Jones R. Evidence for boar sperm proacrosin as a carbohydrate binding protein. Cell Biol Int Rep. 1987;11(11):833.PubMedCrossRefGoogle Scholar
  48. Jovine L, Darie CC, Litscher ES, Wassarman PM. Zona pellucida domain proteins. Annu Rev Biochem. 2005;74:83–114. doi: 10.1146/annurev.biochem.74.082803.133039.PubMedCrossRefGoogle Scholar
  49. Jovine L, Qi H, Williams Z, Litscher ES, Wassarman PM. A duplicated motif controls assembly of zona pellucida domain proteins. Proc Natl Acad Sci U S A. 2004;101(16):5922–7. doi: 10.1073/pnas.0401600101.PubMedPubMedCentralCrossRefGoogle Scholar
  50. Kanai S, Yonezawa N, Ishii Y, Tanokura M, Nakano M. Recombinant bovine zona pellucida glycoproteins ZP3 and ZP4 coexpressed in Sf9 cells form a sperm-binding active hetero-complex. FEBS J. 2007;274(20):5390–405. doi: 10.1111/j.1742-4658.2007.06065.x.PubMedCrossRefGoogle Scholar
  51. Kim E, Baba D, Kimura M, Yamashita M, Kashiwabara S, Baba T. Identification of a hyaluronidase, Hyal5, involved in penetration of mouse sperm through cumulus mass. Proc Natl Acad Sci U S A. 2005;102(50):18028–33. doi: 10.1073/pnas.0506825102.PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kinoshita M, Mizui K, Ishiguro T, Ohtsuki M, Kansaku N, Ogawa H, Tsukada A, Sato T, Sasanami T. Incorporation of ZP1 into perivitelline membrane after in vivo treatment with exogenous ZP1 in Japanese quail (Coturnix japonica). FEBS J. 2008;275(14):3580–9. doi: 10.1111/j.1742-4658.2008.06503.x.PubMedCrossRefGoogle Scholar
  53. Kinoshita M, Rodler D, Sugiura K, Matsushima K, Kansaku N, Tahara K, Tsukada A, Ono H, Yoshimura T, Yoshizaki N, Tanaka R, Kohsaka T, Sasanami T. Zona pellucida protein ZP2 is expressed in the oocyte of Japanese quail (Coturnix japonica). Reproduction. 2010;139(2):359–71. doi: 10.1530/REP-09-0222.PubMedCrossRefGoogle Scholar
  54. Koyanagi F, Masuda S, Nishiyama H. Acrosome reaction of cock spermatozoa incubated with the perivitelline layer of the hen’s ovum. Poult Sci. 1988;67(12):1770–4.PubMedCrossRefGoogle Scholar
  55. Kudo K, Yonezawa N, Katsumata T, Aoki H, Nakano M. Localization of carbohydrate chains of pig sperm ligand in the glycoprotein ZPB of egg zona pellucida. Eur J Biochem/FEBS. 1998;252(3):492–9.CrossRefGoogle Scholar
  56. Lefiévre L, Conner SJ, Salpekar A, Olufowobi O, Ashton P, Pavlovic B, Lenton W, Afnan M, Brewis IA, Monk M, Hughes DC, Barratt CL. Four zona pellucida glycoproteins are expressed in the human. Hum Reprod. 2004;19(7):1580–6. doi: 10.1093/humrep/deh301.PubMedCrossRefGoogle Scholar
  57. Leyton L, Saling P. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction. J Cell Biol. 1989;108(6):2163–8.PubMedCrossRefGoogle Scholar
  58. Li J, Leghari IH, He B, Zeng W, Mi Y, Zhang C. Estrogen stimulates expression of chicken hepatic vitellogenin II and very low-density apolipoprotein II through ER-alpha. Theriogenology. 2014;82(3):517–24. doi: 10.1016/j.theriogenology.2014.05.003.PubMedCrossRefGoogle Scholar
  59. Liang LF, Chamow SM, Dean J. Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes. Mol Cell Biol. 1990;10(4):1507–15.PubMedPubMedCentralCrossRefGoogle Scholar
  60. Lin SJ, Hu Y, Zhu J, Woodruff TK, Jardetzky TS. Structure of betaglycan zona pellucida (ZP)-C domain provides insights into ZP-mediated protein polymerization and TGF-beta binding. Proc Natl Acad Sci U S A. 2011;108(13):5232–6. doi: 10.1073/pnas.1010689108.PubMedPubMedCentralCrossRefGoogle Scholar
  61. Lindsay LL, Wallace MA, Hedrick JL. A hatching enzyme substrate in the Xenopus laevis egg envelope is a high molecular weight ZPA homolog. Develop Growth Differ. 2001;43(3):305–13.CrossRefGoogle Scholar
  62. Lindsay LL, Yang JC, Hedrick JL. Identification and characterization of a unique Xenopus laevis egg envelope component, ZPD. Develop Growth Differ. 2002;44(3):205–12.CrossRefGoogle Scholar
  63. Louros NN, Chrysina ED, Baltatzis GE, Patsouris ES, Hamodrakas SJ, Iconomidou VA. A common “aggregation-prone” interface possibly participates in the self-assembly of human zona pellucida proteins. FEBS Lett. 2016; doi: 10.1002/1873-3468.12099.
  64. Maldera JA, Weigel Munoz M, Chirinos M, Busso D, G E Raffo F, Battistone MA, Blaquier JA, Larrea F, Cuasnicu PS. Human fertilization: epididymal hCRISP1 mediates sperm–zona pellucida binding through its interaction with ZP3. Mol Hum Reprod. 2014;20(4):341–9. doi: 10.1093/molehr/gat092.PubMedCrossRefGoogle Scholar
  65. Mann K. Proteomic analysis of the chicken egg vitelline membrane. Proteomics. 2008;8(11):2322–32. doi: 10.1002/pmic.200800032.PubMedCrossRefGoogle Scholar
  66. Mann K, Mann M. The chicken egg yolk plasma and granule proteomes. Proteomics. 2008;8(1):178–91. doi: 10.1002/pmic.200700790.PubMedCrossRefGoogle Scholar
  67. Margalit M, Paz G, Yavetz H, Yogev L, Amit A, Hevlin-Schwartz T, Gupta SK, Kleiman SE. Genetic and physiological study of morphologically abnormal human zona pellucida. Eur J Obstet Gynecol Reprod Biol. 2012;165(1):70–6. doi: 10.1016/j.ejogrb.2012.07.022.PubMedCrossRefGoogle Scholar
  68. Menkhorst E, Selwood L. Vertebrate extracellular preovulatory and postovulatory egg coats. Biol Reprod. 2008;79(5):790–7. doi: 10.1095/biolreprod.108.068551.PubMedCrossRefGoogle Scholar
  69. Monné M, Han L, Jovine L. Tracking down the ZP domain: from the mammalian zona pellucida to the molluscan vitelline envelope. Semin Reprod Med. 2006;24(4):204–16. doi: 10.1055/s-2006-948550.PubMedCrossRefGoogle Scholar
  70. Monné M, Han L, Schwend T, Burendahl S, Jovine L. Crystal structure of the ZP-N domain of ZP3 reveals the core fold of animal egg coats. Nature. 2008;456(7222):653–7. doi: 10.1038/nature07599.PubMedCrossRefGoogle Scholar
  71. Nakamura Y, Kagami H, Tagami T. Development, differentiation and manipulation of chicken germ cells. Develop Growth Differ. 2013;55(1):20–40. doi: 10.1111/dgd.12026.CrossRefGoogle Scholar
  72. Nishio S, Kohno Y, Iwata Y, Arai M, Okumura H, Oshima K, Nadano D, Matsuda T. Glycosylated chicken ZP2 accumulates in the egg coat of immature oocytes and remains localized to the germinal disc region of mature eggs. Biol Reprod. 2014;91(5):107. doi: 10.1095/biolreprod.114.119826.PubMedCrossRefGoogle Scholar
  73. Ohtsuki M, Hanafy AM, Mori M, Sasanami T. Involvement of interaction of ZP1 and ZPC in the formation of quail perivitelline membrane. Cell Tissue Res. 2004;318(3):565–70. doi: 10.1007/s00441-004-1000-9.PubMedCrossRefGoogle Scholar
  74. Okumura H, Aoki N, Sato C, Nadano D, Matsuda T. Heterocomplex formation and cell-surface accumulation of hen’s serum zona pellucida B1 (ZPB1)with ZPC expressed by a mammalian cell line (COS-7): a possible initiating step of egg-envelope matrix construction. Biol Reprod. 2007a;76(1):9–18. doi: 10.1095/biolreprod.106.056267.PubMedCrossRefGoogle Scholar
  75. Okumura H, Fukushima H, Momoda M, Ima Y, Matsuda T, Ujita M. Diverse lectin-binding specificity of four ZP3 glycoprotein isoforms with a discrete isoelectric point in chicken egg coat. Biochem Biophys Res Commun. 2012;424(3):586–92. doi: 10.1016/j.bbrc.2012.06.157.PubMedCrossRefGoogle Scholar
  76. Okumura H, Kohno Y, Iwata Y, Mori H, Aoki N, Sato C, Kitajima K, Nadano D, Matsuda T. A newly identified zona pellucida glycoprotein, ZPD, and dimeric ZP1 of chicken egg envelope are involved in sperm activation on sperm–egg interaction. Biochem J. 2004;384(Pt 1):191–9. doi: 10.1042/BJ20040299.PubMedPubMedCentralCrossRefGoogle Scholar
  77. Okumura H, Okajima T, Nadano D, Matsuda T. Association of chicken zona pellucida glycoprotein (ZP) B1 with ZPC induces formation of ZPB1–ZPC fibrous aggregates containing disulfide-bridged ZPB1 dimer. Biochem Biophys Res Commun. 2007b;364(3):682–8. doi: 10.1016/j.bbrc.2007.10.072.PubMedCrossRefGoogle Scholar
  78. Okumura H, Sato T, Sakuma R, Fukushima H, Matsuda T, Ujita M. Identification of distinctive interdomain interactions among ZP-N, ZP-C and other domains of zona pellucida glycoproteins underlying association of chicken egg-coat matrix. FEBS Open Bio. 2015;5:454–65. doi: 10.1016/j.fob.2015.05.005.PubMedPubMedCentralCrossRefGoogle Scholar
  79. Pan J, Sasanami T, Kono Y, Matsuda T, Mori M. Effects of testosterone on production of perivitelline membrane glycoprotein ZPC by granulosa cells of Japanese quail (Coturnix japonica). Biol Reprod. 2001;64(1):310–6.PubMedCrossRefGoogle Scholar
  80. Pan J, Sasanami T, Nakajima S, Kido S, Doi Y, Mori M. Characterization of progressive changes in ZPC of the vitelline membrane of quail oocyte following oviductal transport. Mol Reprod Dev. 2000;55(2):175–81. doi:10.1002/(SICI)1098-2795(200002)55:2<175::AID-MRD6>3.0.CO;2-6.PubMedCrossRefGoogle Scholar
  81. Perry MM. Nuclear events from fertilisation to the early cleavage stages in the domestic fowl (Gallus domesticus). J Anat. 1987;150:99–109.PubMedPubMedCentralGoogle Scholar
  82. Perry MM, Gilbert AB, Evans AJ. The structure of the germinal disc region of the hen’s ovarian follicle during the rapid growth phase. J Anat. 1978;127(Pt 2):379–92.PubMedPubMedCentralGoogle Scholar
  83. Petrie M, Schwabl H, Brande-Lavridsen N, Burke T. Maternal investment. Sex differences in avian yolk hormone levels. Nature. 2001;412(6846):498–9. doi: 10.1038/35087652.PubMedCrossRefGoogle Scholar
  84. Pike TW, Petrie M. Experimental evidence that corticosterone affects offspring sex ratios in quail. Proc Biol Sci. 2006;273(1590):1093–8. doi: 10.1098/rspb.2005.3422.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Pökkylä RM, Lakkakorpi JT, Nuojua-Huttunen SH, Tapanainen JS. Sequence variations in human ZP genes as potential modifiers of zona pellucida architecture. Fertil Steril. 2011;95(8):2669–72. doi: 10.1016/j.fertnstert.2011.01.168.PubMedCrossRefGoogle Scholar
  86. Rankin T, Dean J. The zona pellucida: using molecular genetics to study the mammalian egg coat. Rev Reprod. 2000;5(2):114–21.PubMedCrossRefGoogle Scholar
  87. Rankin T, Familari M, Lee E, Ginsberg A, Dwyer N, Blanchette-Mackie J, Drago J, Westphal H, Dean J. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile. Development. 1996;122(9):2903–10.PubMedGoogle Scholar
  88. Rankin T, Talbot P, Lee E, Dean J. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss. Development. 1999;126(17):3847–55.PubMedGoogle Scholar
  89. Rankin TL, O’Brien M, Lee E, Wigglesworth K, Eppig J, Dean J. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development. Development. 2001;128(7):1119–26.PubMedGoogle Scholar
  90. Ringuette MJ, Sobieski DA, Chamow SM, Dean J. Oocyte-specific gene expression: molecular characterization of a cDNA coding for ZP-3, the sperm receptor of the mouse zona pellucida. Proc Natl Acad Sci U S A. 1986;83(12):4341–5.PubMedPubMedCentralCrossRefGoogle Scholar
  91. Rodler D, Sasanami T, Sinowatz F. Assembly of the inner perivitelline layer, a homolog of the mammalian zona pellucida: an immunohistochemical and ultrastructural study. Cells Tissues Organs. 2012;195(4):330–9. doi: 10.1159/000327013.PubMedCrossRefGoogle Scholar
  92. Säemann MD, Weichhart T, Horl WH, Zlabinger GJ. Tamm–Horsfall protein: a multilayered defence molecule against urinary tract infection. Eur J Clin Investig. 2005;35(4):227–35. doi: 10.1111/j.1365-2362.2005.01483.x.CrossRefGoogle Scholar
  93. Saling PM, Sowinski J, Storey BT. An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: sequential relationship to the acrosome reaction. J Exp Zool. 1979;209(2):229–38. doi: 10.1002/jez.1402090205.PubMedCrossRefGoogle Scholar
  94. Saling PM, Storey BT. Mouse gamete interactions during fertilization in vitro. Chlortetracycline as a fluorescent probe for the mouse sperm acrosome reaction. J Cell Biol. 1979;83(3):544–55.PubMedCrossRefGoogle Scholar
  95. Sano K, Kawaguchi M, Watanabe S, Nagakura Y, Hiraki T, Yasumasu S. Inferring the evolution of teleostean zp genes based on their sites of expression. J Exp Zool B Mol Dev Evol. 2013;320(5):332–43. doi: 10.1002/jez.b.22507.PubMedCrossRefGoogle Scholar
  96. Sano K, Kawaguchi M, Yoshikawa M, Iuchi I, Yasumasu S. Evolution of the teleostean zona pellucida gene inferred from the egg envelope protein genes of the Japanese eel, Anguilla japonica. FEBS J. 2010;277(22):4674–84. doi: 10.1111/j.1742-4658.2010.07874.x.PubMedCrossRefGoogle Scholar
  97. Santambrogio S, Cattaneo A, Bernascone I, Schwend T, Jovine L, Bachi A, Rampoldi L. Urinary uromodulin carries an intact ZP domain generated by a conserved C-terminal proteolytic cleavage. Biochem Biophys Res Commun. 2008;370(3):410–3. doi: 10.1016/j.bbrc.2008.03.099.PubMedCrossRefGoogle Scholar
  98. Sasanami T, Atsumi E, Toriyama M, Mori M. Asparagine-linked oligosaccharide-independent secretion of egg envelope glycoprotein ZPC of the Japanese quail (Coturnix japonica). Comp Biochem Physiol A Mol Integr Physiol. 2003a;134(3):631–8.PubMedCrossRefGoogle Scholar
  99. Sasanami T, Matsushima K, Ohtsuki M, Kansaku N, Hiyama G, Mori M. Vectorial secretion of perivitelline membrane glycoprotein ZPC of Japanese quail (Coturnix japonica) in polarized Madin–Darby canine kidney cells. Cells Tissues Organs. 2005;180(3):169–77. doi: 10.1159/000088245.PubMedCrossRefGoogle Scholar
  100. Sasanami T, Murata T, Ohtsuki M, Matsushima K, Hiyama G, Kansaku N, Mori M. Induction of sperm acrosome reaction by perivitelline membrane glycoprotein ZP1 in Japanese quail (Coturnix japonica). Reproduction. 2007;133(1):41–9. doi: 10.1530/REP-06-0104.PubMedCrossRefGoogle Scholar
  101. Sasanami T, Pan J, Doi Y, Hisada M, Kohsaka T, Toriyama M. Secretion of egg envelope protein ZPC after C-terminal proteolytic processing in quail granulosa cells. Eur J Biochem/FEBS. 2002;269(8):2223–31.CrossRefGoogle Scholar
  102. Sasanami T, Pan J, Mori M. Expression of perivitelline membrane glycoprotein ZP1 in the liver of Japanese quail (Coturnix japonica) after in vivo treatment with diethylstilbestrol. J Steroid Biochem Mol Biol. 2003b;84(1):109–16.PubMedCrossRefGoogle Scholar
  103. Sasanami T, Toriyama M, Mori M. Carboxy-terminal proteolytic processing at a consensus furin cleavage site is a prerequisite event for quail ZPC secretion. Biol Reprod. 2003c;68(5):1613–9. doi: 10.1095/biolreprod.102.011841.PubMedCrossRefGoogle Scholar
  104. Sato T, Kinoshita M, Kansaku N, Tahara K, Tsukada A, Ono H, Yoshimura T, Dohra H, Sasanami T. Molecular characterization of egg envelope glycoprotein ZPD in the ovary of Japanese quail (Coturnix japonica). Reproduction. 2009;137(2):333–43. doi: 10.1530/REP-08-0057.PubMedCrossRefGoogle Scholar
  105. Schneider WJ. Low density lipoprotein receptor relatives in chicken ovarian follicle and oocyte development. Cytogenet Genome Res. 2007;117(1–4):248–55. doi: 10.1159/000103186.PubMedCrossRefGoogle Scholar
  106. Serizawa M, Kinoshita M, Rodler D, Tsukada A, Ono H, Yoshimura T, Kansaku N, Sasanami T. Oocytic expression of zona pellucida protein ZP4 in Japanese quail (Coturnix japonica). Anim Sci J. 2011;82(2):227–35. doi: 10.1111/j.1740-0929.2010.00830.x.PubMedCrossRefGoogle Scholar
  107. Sousa M, Teixeira da Silva J, Silva J, Cunha M, Viana P, Oliveira E, Sa R, Soares C, Oliveira C, Barros A. Embryological, clinical and ultrastructural study of human oocytes presenting indented zona pellucida. Zygote. 2015;23(1):145–57. doi: 10.1017/S0967199413000403.PubMedCrossRefGoogle Scholar
  108. Spargo SC, Hope RM. Evolution and nomenclature of the zona pellucida gene family. Biol Reprod. 2003;68(2):358–62.PubMedCrossRefGoogle Scholar
  109. Stetson I, Aviles M, Moros C, Garcia-Vazquez FA, Gimeno L, Torrecillas A, Aliaga C, Bernardo-Pisa MV, Ballesta J, Izquierdo-Rico MJ. Four glycoproteins are expressed in the cat zona pellucida. Theriogenology. 2015;83(7):1162–73. doi: 10.1016/j.theriogenology.2014.12.019.PubMedCrossRefGoogle Scholar
  110. Stewart SG, Bausek N, Wohlrab F, Schneider WJ, Janet Horrocks A, Wishart GJ. Species specificity in avian sperm:perivitelline interaction. Comp Biochem Physiol A Mol Integr Physiol. 2004;137(4):657–63. doi: 10.1016/j.cbpb.2004.01.027.PubMedCrossRefGoogle Scholar
  111. Stifani S, Barber DL, Nimpf J, Schneider WJ. A single chicken oocyte plasma membrane protein mediates uptake of very low density lipoprotein and vitellogenin. Proc Natl Acad Sci U S A. 1990;87(5):1955–9.PubMedPubMedCentralCrossRefGoogle Scholar
  112. Takeuchi Y, Nishimura K, Aoki N, Adachi T, Sato C, Kitajima K, Matsuda T. A 42-kDa glycoprotein from chicken egg-envelope, an avian homolog of the ZPC family glycoproteins in mammalian Zona pellucida. Its first identification, cDNA cloning and granulosa cell-specific expression. Eur J Biochem/FEBS. 1999;260(3):736–42.CrossRefGoogle Scholar
  113. Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A. Minireview: functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev. 2002;61(3):414–24. doi: 10.1002/mrd.10102.PubMedCrossRefGoogle Scholar
  114. Uto N, Yoshimatsu N, Lopata A, Yanagimachi R. Zona-induced acrosome reaction of hamster spermatozoa. J Exp Zool. 1988;248(1):113–20. doi: 10.1002/jez.1402480115.PubMedCrossRefGoogle Scholar
  115. Visconti PE, Florman HM. Mechanisms of sperm–egg interactions: between sugars and broken bonds. Sci Signal. 2010;3(142):pe35. doi: 10.1126/scisignal.3142pe35.PubMedPubMedCentralCrossRefGoogle Scholar
  116. Waclawek M, Foisner R, Nimpf J, Schneider WJ. The chicken homologue of zona pellucida protein-3 is synthesized by granulosa cells. Biol Reprod. 1998;59(5):1230–9.PubMedCrossRefGoogle Scholar
  117. Wassarman PM. Zona pellucida glycoproteins. Annu Rev Biochem. 1988;57:415–42. doi: 10.1146/ Scholar
  118. Williams Z, Litscher ES, Jovine L, Wassarman PM. Polypeptide encoded by mouse ZP3 exon-7 is necessary and sufficient for binding of mouse sperm in vitro. J Cell Physiol. 2006;207(1):30–9. doi: 10.1002/jcp.20532.PubMedCrossRefGoogle Scholar
  119. Wyburn GM, Aitken RN, Johnston HS. The ultrastructure of the zona radiata of the ovarian follicle of the domestic fowl. J Anat. 1965;99(Pt 3):469–84.PubMedPubMedCentralGoogle Scholar
  120. Yamaguchi R, Yamagata K, Ikawa M, Moss SB, Okabe M. Aberrant distribution of ADAM3 in sperm from both angiotensin-converting enzyme (Ace)- and calmegin (Clgn)-deficient mice. Biol Reprod. 2006;75(5):760–6. doi: 10.1095/biolreprod.106.052977.PubMedCrossRefGoogle Scholar
  121. Yanagimachi R. Mammalian sperm acrosome reaction: where does it begin before fertilization? Biol Reprod. 2011;85(1):4–5. doi: 10.1095/biolreprod.111.092601.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2017

Authors and Affiliations

  1. 1.Department of Applied Biological ChemistryFaculty of Agriculture, Meijo UniversityNagoyaJapan

Personalised recommendations