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PMID: 23335731 Published · ppublish English Journal Article Research Support, N.I.H., Intramural Review

The molecular basis of gamete recognition in mice and humans.

Molecular human reproduction ·Vol. 19 ·No. 5 ·2013-05-00 ·Pages 279-89

Avella MA, Xiong B, Dean J

Abstract

Successful fertilization heralds the onset of development and requires both gamete recognition and a definitive block to polyspermy. Sperm initially bind and penetrate the extracellular zona pellucida (ZP) that surrounds ovulated eggs, but are unable to bind the zona surrounding preimplantation embryos. The ZP of humans is composed of four (ZP1-4) and that of mouse three (ZP1-3) glycoproteins. Models for gamete recognition developed in mice had proposed that sperm bind to ZP3 glycans. However, phenotypes observed in genetically engineered mice are not consistent with this widely accepted model. More recently, taking advantage of the observation that human sperm do not bind to mouse eggs, human ZP2 was defined as the zona ligand in transgenic mouse models using gain-of-function assays. The sperm-binding site is an N-terminal domain of ZP2 that is cleaved by ovastacin, a metalloendoprotease released from egg cortical granules following fertilization. Proteolysis of this docking site provides a definitive block to polyspermy as sperm bind to uncleaved, but not cleaved ZP2 even after fertilization and cortical granule exocytosis. While progress has been made in defining the ZP ligand, less headway has been made in identifying the cognate sperm receptor. Although a number of sperm receptor candidates have been documented to interact with specific proteins in the ZP in vitro, continued fertility after genetic ablation of the cognate gene indicates that none are essential for gamete recognition. These on-going investigations inform reproductive medicine and suggest new therapies to improve fertility and/or provide contraception, thus expanding reproductive choices for human couples.

MeSH Terms
Animals Egg Proteins/genetics,metabolism Female Gene Expression Regulation, Developmental Humans Male Membrane Glycoproteins/genetics,metabolism Metalloproteases/metabolism Mice Mice, Transgenic Protein Structure, Tertiary Proteolysis Receptors, Cell Surface/genetics,metabolism Sperm-Ovum Interactions/physiology Spermatozoa/growth & development,metabolism Zona Pellucida/metabolism Zona Pellucida Glycoproteins Zygote/cytology,growth & development,metabolism
Chemicals
Egg Proteins Membrane Glycoproteins Receptors, Cell Surface ZP1 protein, human ZP2 protein, human ZP3 protein, human Zona Pellucida Glycoproteins Zp1 protein, mouse Zp2 protein, mouse Zp3 protein, mouse Metalloproteases ASTL protein, human
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Avella Matteo A
Laboratory of Cellular and Developmental Biology, NIDDK, National Institutes of Health, Bethesda, MD 20892, USA. [email protected]
Xiong Bo
Dean Jurrien
References (148)
148 references, click to expand
  1. Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome.
    Biochem J. 2003 Oct 15;375(Pt 2):477-88 PMID: 12882646
  2. Interaction of zona pellucida glycoproteins, sulphated carbohydrates and synthetic polymers with proacrosin, the putative egg-binding protein from mammalian spermatozoa.
    Development. 1991 Apr;111(4):1155-63 PMID: 1652426
  3. Receptor function of mouse sperm surface galactosyltransferase during fertilization.
    J Cell Biol. 1985 Oct;101(4):1501-10 PMID: 2995408
  4. New insights into the t-complex and control of sperm function.
    Bioessays. 1999 Apr;21(4):304-12 PMID: 10377892
  5. International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care.
    Hum Reprod. 2007 Jun;22(6):1506-12 PMID: 17376819
  6. The human sperm protein PH-20 has hyaluronidase activity.
    FEBS Lett. 1993 Dec 28;336(3):545-8 PMID: 8282124
  7. Successful fertilization in vitro of fresh intact oocytes by perivitelline (acrosome-reacted) spermatozoa of the rabbit.
    Fertil Steril. 1984 May;41(5):766-70 PMID: 6714454
  8. Characterization of the human zona pellucida from fertilized and unfertilized eggs.
    J Reprod Fertil. 1988 Jan;82(1):151-61 PMID: 3339577
  9. Cloning and characterization of zona pellucida genes and cDNAs from a variety of mammalian species: the ZPA, ZPB and ZPC gene families.
    DNA Seq. 1994;4(6):361-93 PMID: 7841460
  10. Oocyte-specific expression of mouse Zp-2: developmental regulation of the zona pellucida genes.
    Mol Cell Biol. 1990 Apr;10(4):1507-15 PMID: 1690843
  11. Fertilization: a sperm's journey to and interaction with the oocyte.
    J Clin Invest. 2010 Apr;120(4):984-94 PMID: 20364096
  12. Porcine zona pellucida glycoprotein ZP4 is responsible for the sperm-binding activity of the ZP3/ZP4 complex.
    Zygote. 2012 Nov;20(4):389-97 PMID: 22008510
  13. Growth retardation and early death of beta-1,4-galactosyltransferase knockout mice with augmented proliferation and abnormal differentiation of epithelial cells.
    EMBO J. 1997 Apr 15;16(8):1850-7 PMID: 9155011
  14. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice.
    Science. 2004 May 21;304(5674):1147-50 PMID: 15155946
  15. Defective zonae pellucidae in Zp2-null mice disrupt folliculogenesis, fertility and development.
    Development. 2001 Apr;128(7):1119-26 PMID: 11245577
  16. Human sperm bind to the N-terminal domain of ZP2 in humanized zonae pellucidae in transgenic mice.
    J Cell Biol. 2012 Jun 25;197(7):897-905 PMID: 22734000
  17. Human cyritestin genes (CYRN1 and CYRN2) are non-functional.
    Biochem J. 2001 Jul 15;357(Pt 2):551-6 PMID: 11439107
  18. Polyspermy-preventing mechanisms in mouse eggs fertilized in vitro.
    J Exp Zool. 1979 Nov;210(2):353-9 PMID: 541603
  19. Native human zona pellucida glycoproteins: purification and binding properties.
    Hum Reprod. 2008 Jun;23(6):1385-93 PMID: 18332087
  20. Species-specific binding of sperm proteins to the extracellular matrix (zona pellucida) of the egg.
    J Biol Chem. 1994 Jul 22;269(29):19000-4 PMID: 8034657
  21. Reassessing the role of protein-carbohydrate complementarity during sperm-egg interactions in the mouse.
    Int J Dev Biol. 2008;52(5-6):703-15 PMID: 18649283
  22. 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 Aug;128(2):376-85 PMID: 3396765
  23. Gamete recognition in mice depends on the cleavage status of an egg's zona pellucida protein.
    Science. 2010 Jul 9;329(5988):216-9 PMID: 20616279
  24. Galactosyltransferase activities on mouse sperm bearing multiple tlethal and tviable haplotypes of the T/t-complex.
    Genet Res. 1981 Dec;38(3):225-36 PMID: 6800883
  25. Protein disulfide isomerase homolog PDILT is required for quality control of sperm membrane protein ADAM3 and male fertility [corrected].
    Proc Natl Acad Sci U S A. 2012 Mar 6;109(10):3850-5 PMID: 22357757
  26. Mammalian glycosyltransferases: genomic organization and protein structure.
    Glycobiology. 1992 Aug;2(4):271-7 PMID: 1421748
  27. Molecular cloning and characterization of P47, a novel boar sperm-associated zona pellucida-binding protein homologous to a family of mammalian secretory proteins.
    Biol Reprod. 1998 Apr;58(4):1057-64 PMID: 9546740
  28. Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein.
    Dev Biol. 1983 Feb;95(2):317-24 PMID: 6402397
  29. In vitro biosynthesis of three sulfated glycoproteins of murine zonae pellucidae by oocytes grown in follicle culture.
    J Biol Chem. 1983 May 10;258(9):5858-63 PMID: 6853551
  30. Oocyte Gal alpha 1,3Gal epitopes implicated in sperm adhesion to the zona pellucida glycoprotein ZP3 are not required for fertilization in the mouse.
    J Biol Chem. 1995 Sep 15;270(37):21437-40 PMID: 7545161
  31. The synthesis of complex carbohydrates by multiglycosyltransferase systems and their potential function in intercellular adhesion.
    Chem Phys Lipids. 1970 Oct;5(1):270-97 PMID: 5476326
  32. Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding.
    Biol Reprod. 1996 Jul;55(1):80-6 PMID: 8793062
  33. MFG-E8/lactadherin promotes tumor growth in an angiogenesis-dependent transgenic mouse model of multistage carcinogenesis.
    Cancer Res. 2007 Jul 15;67(14):6777-85 PMID: 17638889
  34. An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: sequential relationship to the acrosome reaction.
    J Exp Zool. 1979 Aug;209(2):229-38 PMID: 512592
  35. Species diversity in the structure of zonadhesin, a sperm-specific membrane protein containing multiple cell adhesion molecule-like domains.
    J Biol Chem. 1998 Feb 6;273(6):3415-21 PMID: 9452463
  36. Complementarity between sperm surface beta-1,4-galactosyltransferase and egg-coat ZP3 mediates sperm-egg binding.
    Nature. 1992 Jun 18;357(6379):589-93 PMID: 1608469
  37. A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg.
    J Cell Biol. 1994 Jun;125(5):1157-63 PMID: 8195297
  38. Lactadherin promotes VEGF-dependent neovascularization.
    Nat Med. 2005 May;11(5):499-506 PMID: 15834428
  39. Expression of recombinant human zona pellucida protein 2 and its binding capacity to spermatozoa.
    Biol Reprod. 1999 Dec;61(6):1649-54 PMID: 10570015
  40. Enzymatic dissection of the functions of the mouse egg's receptor for sperm.
    Dev Biol. 1984 Nov;106(1):243-55 PMID: 6386571
  41. Proteolysis of Xenopus laevis egg envelope ZPA triggers envelope hardening.
    Biochem Biophys Res Commun. 2004 Nov 12;324(2):648-54 PMID: 15474476
  42. Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm.
    Proc Natl Acad Sci U S A. 1998 May 26;95(11):6193-7 PMID: 9600940
  43. Site-directed mutagenesis of rabbit proacrosin. Identification of residues involved in zona pellucida binding.
    J Biol Chem. 1996 Sep 27;271(39):24069-74 PMID: 8798644
  44. Antibodies to human ZP3 induce reversible contraception in transgenic mice with 'humanized' zonae pellucidae.
    Hum Reprod. 1999 Mar;14(3):593-600 PMID: 10221681
  45. In humans, zona pellucida glycoprotein-1 binds to spermatozoa and induces acrosomal exocytosis.
    Hum Reprod. 2010 Jul;25(7):1643-56 PMID: 20504872
  46. Binding of zona pellucida proteins to a boar sperm polypeptide of Mr 53,000 and identification of zona moieties involved.
    Development. 1987 Mar;99(3):333-9 PMID: 3653005
  47. Factors regulating sperm capacitation.
    Syst Biol Reprod Med. 2010 Oct;56(5):334-48 PMID: 20849222
  48. AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins.
    J Biol Chem. 1997 May 9;272(19):12714-22 PMID: 9139729
  49. Fertile life of acrosome-reacted guinea pig spermatozoa.
    J Exp Zool. 1982 Mar 1;220(1):109-15 PMID: 7077263
  50. Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking.
    Proc Natl Acad Sci U S A. 1990 Jul;87(14):5563-7 PMID: 2371290
  51. Mechanistic studies of the plasma membrane block to polyspermy in mouse eggs.
    Mol Reprod Dev. 1993 Jan;34(1):65-72 PMID: 8418819
  52. Fertilization with acrosome-reacted mouse sperm: implications for the site of exocytosis.
    Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):19843-4 PMID: 22143800
  53. The ZP domain is a conserved module for polymerization of extracellular proteins.
    Nat Cell Biol. 2002 Jun;4(6):457-61 PMID: 12021773
  54. Male-female differences in fertility and blood pressure in ACE-deficient mice.
    Nature. 1995 May 11;375(6527):146-8 PMID: 7753170
  55. Abnormal zonae pellucidae in mice lacking ZP1 result in early embryonic loss.
    Development. 1999 Sep;126(17):3847-55 PMID: 10433913
  56. Transgenic mice with reduced numbers of functional sperm receptors on their eggs reproduce normally.
    Mol Biol Cell. 1995 May;6(5):577-85 PMID: 7663023
  57. A trefoil domain in the major rabbit zona pellucida protein.
    Protein Sci. 1993 Apr;2(4):669-70 PMID: 8518738
  58. Possible function of the ADAM1a/ADAM2 Fertilin complex in the appearance of ADAM3 on the sperm surface.
    J Biol Chem. 2004 Aug 13;279(33):34957-62 PMID: 15194697
  59. Mammalian zona pellucida glycoproteins: structure and function during fertilization.
    Cell Tissue Res. 2012 Sep;349(3):665-78 PMID: 22298023
  60. The role of the zona pellucida in the development of mouse eggs in vivo.
    J Embryol Exp Morphol. 1970 Jun;23(3):539-47 PMID: 5473304
  61. Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta.
    Dev Biol. 2001 May 1;233(1):204-13 PMID: 11319869
  62. Sperm/egg interaction: the specificity of human spermatozoa.
    Anat Rec. 1977 Aug;188(4):477-87 PMID: 409311
  63. Absence of an electrical polyspermy block in the mouse.
    Dev Biol. 1983 Apr;96(2):317-23 PMID: 6832474
  64. Studies on acrosomal proteinase of rabbit spermatozoa.
    Biochim Biophys Acta. 1972 Oct 12;284(2):473-7 PMID: 4635825
  65. A duplicated motif controls assembly of zona pellucida domain proteins.
    Proc Natl Acad Sci U S A. 2004 Apr 20;101(16):5922-7 PMID: 15079052
  66. Evidence for the presence of high-mannose/hybrid oligosaccharide chain(s) on the mouse ZP2 and ZP3.
    Biol Reprod. 1992 Jan;46(1):93-100 PMID: 1547319
  67. Mouse sperm protein sp56 is a component of the acrosomal matrix.
    Biol Reprod. 2001 Jan;64(1):36-43 PMID: 11133656
  68. Galactose at the nonreducing terminus of O-linked oligosaccharides of mouse egg zona pellucida glycoprotein ZP3 is essential for the glycoprotein's sperm receptor activity.
    Proc Natl Acad Sci U S A. 1988 Sep;85(18):6778-82 PMID: 2842789
  69. Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction.
    J Cell Biol. 1989 Jun;108(6):2163-8 PMID: 2544604
  70. Inactivation of the Mgat1 gene in oocytes impairs oogenesis, but embryos lacking complex and hybrid N-glycans develop and implant.
    Mol Cell Biol. 2004 Nov;24(22):9920-9 PMID: 15509794
  71. ZP2 and ZP3 cytoplasmic tails prevent premature interactions and ensure incorporation into the zona pellucida.
    J Cell Sci. 2011 Mar 15;124(Pt 6):940-50 PMID: 21378311
  72. Mouse sperm lacking cell surface hyaluronidase PH-20 can pass through the layer of cumulus cells and fertilize the egg.
    J Biol Chem. 2002 Aug 16;277(33):30310-4 PMID: 12065596
  73. ZP2 and ZP3 traffic independently within oocytes prior to assembly into the extracellular zona pellucida.
    Mol Cell Biol. 2006 Nov;26(21):7991-8 PMID: 17047254
  74. 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 Nov 3;270(44):26025-8 PMID: 7592795
  75. Zona pellucida-binding and fucose-binding of boar sperm acrosin is not correlated with proteolytic activity.
    Biol Chem Hoppe Seyler. 1988 Jan;369(1):69-76 PMID: 3162367
  76. Structural characterization of native mouse zona pellucida proteins using mass spectrometry.
    J Biol Chem. 2003 Sep 5;278(36):34189-202 PMID: 12799386
  77. Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs.
    Dev Cell. 2003 Jul;5(1):33-43 PMID: 12852850
  78. Human homolog of the mouse sperm receptor.
    Proc Natl Acad Sci U S A. 1990 Aug;87(16):6014-8 PMID: 2385582
  79. Fully effective contraception in male and female guinea pigs immunized with the sperm protein PH-20.
    Nature. 1988 Oct 6;335(6190):543-6 PMID: 3419530
  80. Fertilization defects in sperm from mice lacking fertilin beta.
    Science. 1998 Sep 18;281(5384):1857-9 PMID: 9743500
  81. Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice.
    Proc Natl Acad Sci U S A. 1996 May 28;93(11):5431-6 PMID: 8643592
  82. Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida.
    Dev Biol. 1980 Apr;76(1):185-202 PMID: 7380091
  83. Identification of a zona-binding protein from boar spermatozoa as proacrosin.
    Exp Cell Res. 1987 Aug;171(2):503-8 PMID: 3113989
  84. Zonadhesin: characterization, localization, and zona pellucida binding.
    Biol Reprod. 2001 Dec;65(6):1691-700 PMID: 11717130
  85. Birth after the reimplantation of a human embryo.
    Lancet. 1978 Aug 12;2(8085):366 PMID: 79723
  86. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis.
    Development. 2007 Mar;134(5):933-43 PMID: 17293534
  87. Function of the acrosomal matrix: zona pellucida 3 receptor (ZP3R/sp56) is not essential for mouse fertilization.
    Biol Reprod. 2012 Jan 30;86(1):1-6 PMID: 21998167
  88. Human sperm binding is mediated by the sialyl-Lewis(x) oligosaccharide on the zona pellucida.
    Science. 2011 Sep 23;333(6050):1761-4 PMID: 21852454
  89. Structural conservation of mouse and rat zona pellucida glycoproteins. Probing the native rat zona pellucida proteome by mass spectrometry.
    Biochemistry. 2005 Dec 20;44(50):16445-60 PMID: 16342937
  90. A genetic approach to Mammalian glycan function.
    Annu Rev Biochem. 2003;72:643-91 PMID: 12676797
  91. Evolution and nomenclature of the zona pellucida gene family.
    Biol Reprod. 2003 Feb;68(2):358-62 PMID: 12533396
  92. Acrosin shows zona and fucose binding, novel properties for a serine proteinase.
    FEBS Lett. 1987 Dec 21;226(1):38-42 PMID: 3480243
  93. Ovastacin, a cortical granule protease, cleaves ZP2 in the zona pellucida to prevent polyspermy.
    J Cell Biol. 2012 Apr 2;197(1):37-44 PMID: 22472438
  94. Oocyte specific oolemmal SAS1B involved in sperm binding through intra-acrosomal SLLP1 during fertilization.
    Dev Biol. 2012 Mar 1;363(1):40-51 PMID: 22206759
  95. Sperm-egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3.
    J Cell Biol. 1994 May;125(4):867-78 PMID: 8188752
  96. Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm.
    Cell. 1980 Jul;20(3):873-82 PMID: 7418009
  97. Anuran and pig egg zona pellucida glycoproteins in fertilization and early development.
    Int J Dev Biol. 2008;52(5-6):683-701 PMID: 18649282
  98. Novel cell surface receptors during mammalian fertilization and development.
    Bioessays. 1988 Nov;9(5):153-8 PMID: 3149196
  99. Fertilization in mouse does not require terminal galactose or N-acetylglucosamine on the zona pellucida glycans.
    J Cell Sci. 2007 Apr 15;120(Pt 8):1341-9 PMID: 17374637
  100. Male mice deficient for germ-cell cyritestin are infertile.
    Biol Reprod. 1999 Dec;61(6):1445-51 PMID: 10569988
  101. Human ZP4 is not sufficient for taxon-specific sperm recognition of the zona pellucida in transgenic mice.
    Reproduction. 2011 Mar;141(3):313-9 PMID: 21173071
  102. Epididymal protein Rnase10 is required for post-testicular sperm maturation and male fertility.
    FASEB J. 2012 Oct;26(10):4198-209 PMID: 22750516
  103. Calsperin is a testis-specific chaperone required for sperm fertility.
    J Biol Chem. 2011 Feb 18;286(7):5639-46 PMID: 21131354
  104. Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs.
    Proc Natl Acad Sci U S A. 2011 Dec 13;108(50):20008-11 PMID: 22084105
  105. The putative chaperone calmegin is required for sperm fertility.
    Nature. 1997 Jun 5;387(6633):607-11 PMID: 9177349
  106. Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile.
    Development. 1996 Sep;122(9):2903-10 PMID: 8787763
  107. Purification of rabbit testis proacrosin and studies of its active form.
    Biol Reprod. 1975 Mar;12(2):232-8 PMID: 235333
  108. Recombinant mouse sperm ZP3-binding protein (ZP3R/sp56) forms a high order oligomer that binds eggs and inhibits mouse fertilization in vitro.
    J Biol Chem. 2008 May 2;283(18):12438-45 PMID: 18316377
  109. Identification and characterization of human and mouse ovastacin: a novel metalloproteinase similar to hatching enzymes from arthropods, birds, amphibians, and fish.
    J Biol Chem. 2004 Jun 18;279(25):26627-34 PMID: 15087446
  110. Identification of mouse sperm SED1, a bimotif EGF repeat and discoidin-domain protein involved in sperm-egg binding.
    Cell. 2003 Aug 22;114(4):405-17 PMID: 12941270
  111. Lack of tyrosylprotein sulfotransferase-2 activity results in altered sperm-egg interactions and loss of ADAM3 and ADAM6 in epididymal sperm.
    J Biol Chem. 2011 Apr 15;286(15):13060-70 PMID: 21339297
  112. Relevance of glycosylation of human zona pellucida glycoproteins for their binding to capacitated human spermatozoa and subsequent induction of acrosomal exocytosis.
    Mol Reprod Dev. 2008 Jan;75(1):75-88 PMID: 17486637
  113. Conservation of mammalian secondary sperm receptor genes enables the promoter of the human gene to function in mouse oocytes.
    Dev Biol. 1993 Apr;156(2):399-408 PMID: 8385033
  114. 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 Mar 22;108(12):4892-6 PMID: 21383182
  115. The interaction of boar sperm proacrosin with its natural substrate, the zona pellucida, and with polysulfated polysaccharides.
    Development. 1991 Apr;111(4):1165-72 PMID: 1908770
  116. Insights into egg coat assembly and egg-sperm interaction from the X-ray structure of full-length ZP3.
    Cell. 2010 Oct 29;143(3):404-15 PMID: 20970175
  117. Activation of boar proacrosin is effected by processing at both N- and C-terminal portions of the zymogen molecule.
    FEBS Lett. 1989 Feb 13;244(1):132-6 PMID: 2494060
  118. Heterogeneous processing and zona pellucida binding activity of pig zonadhesin.
    J Biol Chem. 2001 Nov 2;276(44):41502-9 PMID: 11526117
  119. Gamete interactions in Xenopus laevis: identification of sperm binding glycoproteins in the egg vitelline envelope.
    J Cell Biol. 1997 Mar 10;136(5):1099-108 PMID: 9060474
  120. Mice expressing aberrant sperm-specific protein PMIS2 produce normal-looking but fertilization-incompetent spermatozoa.
    Mol Biol Cell. 2012 Jul;23(14):2671-9 PMID: 22621904
  121. Heads or tails? Structural events and molecular mechanisms that promote mammalian sperm acrosomal exocytosis and motility.
    Mol Reprod Dev. 2012 Jan;79(1):4-18 PMID: 22031228
  122. A cell surface block to polyspermy occurs in golden hamster eggs.
    Dev Biol. 1988 Jul;128(1):150-7 PMID: 2454853
  123. Tissue- and species-specific expression of sp56, a mouse sperm fertilization protein.
    Science. 1995 Jul 7;269(5220):86-9 PMID: 7604284
  124. Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida.
    J Biol Chem. 2010 Aug 6;285(32):24863-70 PMID: 20529856
  125. A structural view of egg coat architecture and function in fertilization.
    Biol Reprod. 2011 Oct;85(4):661-9 PMID: 21715714
  126. Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida.
    Dev Biol. 1988 Jun;127(2):287-95 PMID: 3378665
  127. A large domain common to sperm receptors (Zp2 and Zp3) and TGF-beta type III receptor.
    FEBS Lett. 1992 Apr 6;300(3):237-40 PMID: 1313375
  128. Identification by affinity chromatography of boar sperm membrane-associated proteins bound to immobilized porcine zona pellucida. Mapping of the phosphorylethanolamine-binding region of spermadhesin AWN.
    Biol Chem Hoppe Seyler. 1995 Dec;376(12):733-8 PMID: 9072049
  129. Acrosin accelerates the dispersal of sperm acrosomal proteins during acrosome reaction.
    J Biol Chem. 1998 Apr 24;273(17):10470-4 PMID: 9553106
  130. Failure of human spermatozoa to penetrate zona free mouse and rat ova in vitro.
    J Exp Zool. 1979 Dec;210(3):497-505 PMID: 541604
  131. Phylogenetic analysis and identification of pseudogenes reveal a progressive loss of zona pellucida genes during evolution of vertebrates.
    Biol Reprod. 2008 May;78(5):796-806 PMID: 18046012
  132. Mammalian sperm-egg interaction: fertilization of mouse eggs triggers modification of the major zona pellucida glycoprotein, ZP2.
    Dev Biol. 1981 Aug;86(1):189-97 PMID: 6793422
  133. Tracing the evolutionary origin of the TFF-domain, an ancient motif at mucous surfaces.
    Gene. 1999 Aug 5;236(1):133-6 PMID: 10433974
  134. Immuno-colloidal gold labeled surface replica, and its application to detect sp56, the egg recognition and binding protein, on the mouse spermatozoon.
    J Electron Microsc (Tokyo). 1995 Jun;44(3):135-9 PMID: 7673811
  135. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization.
    J Biol Chem. 1994 Dec 16;269(50):31845-9 PMID: 7989357
  136. Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte.
    Lancet. 1992 Jul 4;340(8810):17-8 PMID: 1351601
  137. Transfer to the mouse oviduct of eggs with and without the zona pellucida.
    J Reprod Fertil. 1970 Jun;22(1):129-37 PMID: 5421101
  138. Characterization of zona pellucida glycoprotein 3 (ZP3) and ZP2 binding sites on acrosome-intact mouse sperm.
    Biol Reprod. 2002 Jun;66(6):1585-95 PMID: 12021035
  139. Binding of both acrosome-intact and acrosome-reacted guinea pig sperm to the zona pellucida during in vitro fertilization.
    Dev Biol. 1987 Jun;121(2):559-67 PMID: 3582740
  140. Interactions between mouse ZP2 glycoprotein and proacrosin; a mechanism for secondary binding of sperm to the zona pellucida during fertilization.
    J Cell Sci. 2001 Nov;114(Pt 22):4127-36 PMID: 11739644
  141. A role for the migrating sperm surface antigen PH-20 in guinea pig sperm binding to the egg zona pellucida.
    J Cell Biol. 1985 Dec;101(6):2239-44 PMID: 4066757
  142. Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly.
    Development. 1997 Oct;124(20):4121-31 PMID: 9374408
  143. Mouse Zp1 encodes a zona pellucida protein homologous to egg envelope proteins in mammals and fish.
    J Biol Chem. 1995 Nov 10;270(45):27254-8 PMID: 7592984
  144. A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida.
    J Cell Biol. 1982 Nov;95(2 Pt 1):574-9 PMID: 6815212
  145. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity.
    Cell. 1985 May;41(1):313-24 PMID: 2986849
  146. Four zona pellucida glycoproteins are expressed in the human.
    Hum Reprod. 2004 Jul;19(7):1580-6 PMID: 15142998
  147. Structural analysis of murine zona pellucida glycans. Evidence for the expression of core 2-type O-glycans and the Sd(a) antigen.
    J Biol Chem. 2000 Mar 17;275(11):7731-42 PMID: 10713085
  148. O-linked trisaccharide and N-linked poly-N-acetyllactosaminyl glycans are present on mouse ZP2 and ZP3.
    Biol Reprod. 1994 Aug;51(2):262-72 PMID: 7948482
Article Info
Journal
Molecular human reproduction
Abbr.
Mol Hum Reprod
ISSN
1460-2407
DOI
10.1093/molehr/gat004
Email
[email protected]
Published
2013-05-00
Epub
2013-00-17
Pages
279-89
Language
English
Region
England
NLM ID
9513710
PMCID
PMC3632220
Subset
IM
Grants
Intramural NIH HHS · United States
External Links
PubMed source DOI: 10.1093/molehr/gat004 PMC Full Text View journal details
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