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PMID: 21042304 Published · ppublish English Journal Article Review

Cellular mechanisms regulating sperm-zona pellucida interaction.

Asian journal of andrology ·Vol. 13 ·No. 1 ·2011-01-00 ·Pages 88-96

Reid AT, Redgrove K, Aitken RJ, Nixon B

Abstract

For mammalian spermatozoa to exhibit the ability to bind the zona pellucida (ZP) they must undergo three distinct phases of maturation, namely, spermatogenesis (testis), epididymal maturation (epididymis) and capacitation (female reproductive tract). An impressive array of spermatozoa surface remodeling events accompany these phases of maturation and appear critical for recognition and adhesion of the outer vestments of the oocyte, a structure known as the ZP. It is becoming increasingly apparent that species-specific zona adhesion is not mediated by a single receptor. Instead, compelling evidence now points toward models implicating a multiplicity of receptor-ligand interactions. This notion is in keeping with emerging research that has shown that there is a dynamic aggregation of proteins believed to be important in sperm-ZP recognition to the regions of sperm that mediate this binding event. Such remodeling may in turn facilitate the assembly of a multimeric zona recognition complex (MZRC). Though formation of MZRCs raises questions regarding the nature of the block to polyspermy, formation and assembly of such a structure would no doubt explain the strenuous maturation process that sperm endure on their sojourn to functional maturity.

MeSH Terms
Animals Female Male Sperm Capacitation/physiology Sperm Maturation/physiology Sperm-Ovum Interactions/physiology Spermatozoa/physiology Zona Pellucida/physiology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Reid Andrew T
Reproductive Science Group, Discipline of Biological Sciences, School of Environmental and Life Sciences, University of Newcastle, Callaghan, NSW 2308, Australia.
Redgrove Kate
Aitken R John
Nixon Brett
References (156)
156 references, click to expand
  1. Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat.
    J Mol Biol. 1985 Jan 20;181(2):253-64 PMID: 3845123
  2. The biological significance of detergent-resistant membranes in spermatozoa.
    J Reprod Immunol. 2009 Dec;83(1-2):8-13 PMID: 19857901
  3. The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane.
    Development. 2000 Jun;127(11):2407-20 PMID: 10804182
  4. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition.
    J Cell Sci. 2004 Jul 15;117(Pt 16):3645-57 PMID: 15252132
  5. Differential release of soluble and matrix components: evidence for intermediate states of secretion during spontaneous acrosomal exocytosis in mouse sperm.
    Dev Biol. 2003 Dec 1;264(1):141-52 PMID: 14623237
  6. Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand.
    J Cell Sci. 2009 Nov 1;122(Pt 21):3894-906 PMID: 19808884
  7. A synthetic decapeptide from a conserved ZP3 protein domain induces the G protein-regulated acrosome reaction in bovine spermatozoa.
    Theriogenology. 2005 Apr 1;63(6):1682-94 PMID: 15763111
  8. Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7560-4 PMID: 6950397
  9. Arylsulfatase a is present on the pig sperm surface and is involved in sperm-zona pellucida binding.
    Dev Biol. 2002 Jul 1;247(1):182-96 PMID: 12074561
  10. Sperm capacitation induces an increase in lipid rafts having zona pellucida binding ability and containing sulfogalactosylglycerolipid.
    Dev Biol. 2006 Feb 1;290(1):220-35 PMID: 16387295
  11. Glycosidic residues involved in human sperm-zona pellucida binding in vitro.
    Mol Hum Reprod. 1997 May;3(5):399-404 PMID: 9239724
  12. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 5: intercellular junctions and contacts between germs cells and Sertoli cells and their regulatory interactions, testicular cholesterol, and genes/proteins associated with more than one germ cell generation.
    Microsc Res Tech. 2010 Apr;73(4):409-94 PMID: 19941291
  13. A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation.
    J Cell Sci. 1998 Mar;111 ( Pt 5):645-56 PMID: 9454738
  14. Receptor activity of the hamster and mouse solubilized zona pellucida before and after the zona reaction.
    J Reprod Fertil. 1977 Jan;49(1):55-9 PMID: 833789
  15. Observations on the penetration of the sperm in the mammalian egg.
    Aust J Sci Res B. 1951 Nov;4(4):581-96 PMID: 14895481
  16. The role of molecular chaperones in mouse sperm-egg interactions.
    Mol Cell Endocrinol. 2005 Aug 30;240(1-2):1-10 PMID: 16043280
  17. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.
    Development. 1995 Apr;121(4):1129-37 PMID: 7743926
  18. A mouse sperm decapacitation factor receptor is phosphatidylethanolamine-binding protein 1.
    Reproduction. 2005 Oct;130(4):497-508 PMID: 16183867
  19. Heat shock proteins on the human sperm surface.
    J Reprod Immunol. 2010 Jan;84(1):32-40 PMID: 19962198
  20. Bactericidal/Permeability-increasing protein is associated with the acrosome region of rodent epididymal spermatozoa.
    J Androl. 2010 Mar-Apr;31(2):201-14 PMID: 19745219
  21. Morphological changes in rabbit spermatozoa during passage through the epididymis.
    J Reprod Fertil. 1963 Apr;5:169-77 PMID: 13970203
  22. Interaction of mouse sperm with purified sperm receptors covalently linked to silica beads.
    J Cell Sci. 1989 Apr;92 ( Pt 4):713-22 PMID: 2557361
  23. Fertility of mammalian spermatozoa: its development and relativity.
    Zygote. 1994 Nov;2(4):371-2 PMID: 8665172
  24. Development of the fertilizing ability of spermatozoa in the epididymis of the Syrian hamster.
    J Reprod Fertil. 1972 Sep;30(3):417-23 PMID: 5073383
  25. Nature of the inhibitory effect of complex saccharide moieties on the tight binding of human spermatozoa to the human zona pellucida.
    Fertil Steril. 1991 Jan;55(1):165-9 PMID: 1702739
  26. Role of sperm surface arylsulfatase A in mouse sperm-zona pellucida binding.
    Biol Reprod. 2002 Jul;67(1):212-9 PMID: 12080020
  27. Structure and function of sphingolipid- and cholesterol-rich membrane rafts.
    J Biol Chem. 2000 Jun 9;275(23):17221-4 PMID: 10770957
  28. Localization and significance of molecular chaperones, heat shock protein 1, and tumor rejection antigen gp96 in the male reproductive tract and during capacitation and acrosome reaction.
    Biol Reprod. 2005 Feb;72(2):328-37 PMID: 15456702
  29. Changes in lipids and membrane anisotropy in human spermatozoa during epididymal maturation.
    Hum Reprod. 1997 Dec;12(12):2720-3 PMID: 9455842
  30. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor.
    Science. 2000 Jul 28;289(5479):625-8 PMID: 10915626
  31. Changes in the lipid content of boar sperm plasma membranes during epididymal maturation.
    Biochim Biophys Acta. 1985 May 28;815(3):486-98 PMID: 3995037
  32. Evidence for the capacitation-associated membrane priming of mouse spermatozoa.
    Histochem Cell Biol. 2003 Mar;119(3):179-87 PMID: 12649732
  33. Acrosin activation follows its surface exposure and precedes membrane fusion in human sperm acrosome reaction.
    Development. 1990 Oct;110(2):391-400 PMID: 2133545
  34. Model systems, lipid rafts, and cell membranes.
    Annu Rev Biophys Biomol Struct. 2004;33:269-95 PMID: 15139814
  35. Inhibition of hamster fertilization by phytoagglutinins.
    Exp Cell Res. 1974 Feb;83(2):239-46 PMID: 4593583
  36. Proteomic changes in mammalian spermatozoa during epididymal maturation.
    Asian J Androl. 2007 Jul;9(4):554-64 PMID: 17589795
  37. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 4: intercellular bridges, mitochondria, nuclear envelope, apoptosis, ubiquitination, membrane/voltage-gated channels, methylation/acetylation, and transcription factors.
    Microsc Res Tech. 2010 Apr;73(4):364-408 PMID: 19941288
  38. Functional morphology of the zona pellucida.
    Anat Histol Embryol. 2001 Oct;30(5):257-63 PMID: 11688734
  39. Glycosyltransferase function in core 2-type protein O glycosylation.
    Mol Cell Biol. 2009 Jul;29(13):3770-82 PMID: 19349303
  40. Rafts defined: a report on the Keystone Symposium on Lipid Rafts and Cell Function.
    J Lipid Res. 2006 Jul;47(7):1597-8 PMID: 16645198
  41. Effects of native human zona pellucida glycoproteins 3 and 4 on acrosome reaction and zona pellucida binding of human spermatozoa.
    Biol Reprod. 2008 Nov;79(5):869-77 PMID: 18667750
  42. Core 2 oligosaccharide biosynthesis distinguishes between selectin ligands essential for leukocyte homing and inflammation.
    Immunity. 1998 Dec;9(6):881-90 PMID: 9881978
  43. Antagonistic and agonistic properties of saccharide moieties in the hemizona assay.
    Fertil Steril. 1990 Jan;53(1):143-9 PMID: 2295334
  44. Mammalian fertilization: the egg's multifunctional zona pellucida.
    Int J Dev Biol. 2008;52(5-6):665-76 PMID: 18649280
  45. HongrES1, a cauda epididymis-specific protein, is involved in capacitation of guinea pig sperm.
    Mol Reprod Dev. 2009 Oct;76(10):984-93 PMID: 19565644
  46. 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
  47. Membrane lipid dynamics during human sperm capacitation.
    Front Biosci. 1996 Jul 01;1:d103-17 PMID: 9159218
  48. Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro.
    Biochemistry. 1995 Apr 11;34(14):4662-9 PMID: 7718569
  49. New insights into the molecular mechanisms of sperm-egg interaction.
    Cell Mol Life Sci. 2007 Jul;64(14):1805-23 PMID: 17447007
  50. Mammalian sperm acrosome: formation, contents, and function.
    Arch Biochem Biophys. 2000 Jul 15;379(2):173-82 PMID: 10898932
  51. Structure of the mouse egg extracellular coat, the zona pellucida.
    Int Rev Cytol. 1991;130:85-110 PMID: 1778730
  52. Purification and properties of aryl sulfatases from rabbit sperm acrosomes.
    Proc Soc Exp Biol Med. 1974 Feb;145(2):721-5 PMID: 4814165
  53. Enzymatic dissection of the functions of the mouse egg's receptor for sperm.
    Dev Biol. 1984 Nov;106(1):243-55 PMID: 6386571
  54. Characterization of the rabbit sperm membrane autoantigen, RSA, as a lectin-like zona binding protein.
    Dev Biol. 1988 Sep;129(1):231-40 PMID: 3410159
  55. Glioma pathogenesis-related 1-like 1 is testis enriched, dynamically modified, and redistributed during male germ cell maturation and has a potential role in sperm-oocyte binding.
    Endocrinology. 2010 May;151(5):2331-42 PMID: 20219979
  56. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 2: changes in spermatid organelles associated with development of spermatozoa.
    Microsc Res Tech. 2010 Apr;73(4):279-319 PMID: 19941292
  57. 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
  58. Resistance of cell membranes to different detergents.
    Proc Natl Acad Sci U S A. 2003 May 13;100(10):5795-800 PMID: 12721375
  59. Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro.
    Biochim Biophys Acta. 1979 Dec 12;558(3):257-66 PMID: 508748
  60. Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component.
    J Reprod Fertil. 1984 Nov;72(2):373-84 PMID: 6512763
  61. Investigating the role of murine epididymosomes and uterosomes in GPI-linked protein transfer to sperm using SPAM1 as a model.
    Mol Reprod Dev. 2008 Nov;75(11):1627-36 PMID: 18384048
  62. Molecular chaperones and protein quality control.
    Cell. 2006 May 5;125(3):443-51 PMID: 16678092
  63. Cholesterol efflux-mediated signal transduction in mammalian sperm. beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation.
    J Biol Chem. 1999 Jan 29;274(5):3235-42 PMID: 9915865
  64. 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
  65. Characterization of a decapacitation factor associated with epididymal mouse spermatozoa.
    J Reprod Fertil. 1990 May;89(1):135-48 PMID: 2197409
  66. Fertilizing capacity of spermatozoa deposited into the fallopian tubes.
    Nature. 1951 Oct 20;168(4277):697-8 PMID: 14882325
  67. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells.
    Biol Reprod. 2003 Jun;68(6):2122-34 PMID: 12606386
  68. 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
  69. Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions.
    Biol Reprod. 1991 May;44(5):806-13 PMID: 1907858
  70. Tracking diffusion of GM1 gangliosides and zona pellucida binding molecules in sperm plasma membranes following cholesterol efflux.
    Dev Biol. 2010 Mar 15;339(2):398-406 PMID: 20060391
  71. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 3: developmental changes in spermatid flagellum and cytoplasmic droplet and interaction of sperm with the zona pellucida and egg plasma membrane.
    Microsc Res Tech. 2010 Apr;73(4):320-63 PMID: 19941287
  72. Supramolecular organization of the sperm plasma membrane during maturation and capacitation.
    Asian J Androl. 2007 Jul;9(4):438-44 PMID: 17589780
  73. Evidence for Ca(2+)-dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm.
    Mol Reprod Dev. 1996 May;44(1):111-20 PMID: 8722699
  74. Human sperm plasma membranes possess alpha-D-mannosidase activity but no galactosyltransferase activity.
    Biol Reprod. 1990 May-Jun;42(5-6):843-58 PMID: 2116923
  75. Interactions between a decapacitation factor and mouse spermatozoa appear to involve fucose residues and a GPI-anchored receptor.
    Mol Reprod Dev. 1998 Oct;51(2):193-202 PMID: 9740327
  76. The role of carbohydrate in sperm-ZP3 adhesion.
    Mol Hum Reprod. 1996 Oct;2(10):767-74 PMID: 9239695
  77. Bicarbonate-induced membrane processing in sperm capacitation.
    Theriogenology. 2005 Jan 15;63(2):342-51 PMID: 15626403
  78. Lipid remodeling of murine epididymosomes and spermatozoa during epididymal maturation.
    Biol Reprod. 2006 Jun;74(6):1104-13 PMID: 16510839
  79. Composition and significance of detergent resistant membranes in mouse spermatozoa.
    J Cell Physiol. 2009 Jan;218(1):122-34 PMID: 18726997
  80. Mouse sperm protein sp56 is a component of the acrosomal matrix.
    Biol Reprod. 2001 Jan;64(1):36-43 PMID: 11133656
  81. Characterization of mouse ZP3-derived glycopeptide, gp55, that exhibits sperm receptor and acrosome reaction-inducing activity in vitro.
    Biochemistry. 1996 Apr 2;35(13):3980-5 PMID: 8672430
  82. Is sperm capacitation analogous to early phases of Ca2+-triggered membrane fusion in somatic cells and viruses?
    Bioessays. 2004 Mar;26(3):281-90 PMID: 14988929
  83. Identification of a region of mouse zona pellucida glycoprotein mZP3 that possesses sperm receptor activity.
    Dev Biol. 1992 Dec;154(2):309-17 PMID: 1330788
  84. 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
  85. 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
  86. Characterization of a novel ZP3-independent sperm-binding ligand that facilitates sperm adhesion to the egg coat.
    Development. 2004 Feb;131(3):503-12 PMID: 14695374
  87. Understanding the molecular basis of sperm capacitation through kinase design.
    Proc Natl Acad Sci U S A. 2009 Jan 20;106(3):667-8 PMID: 19144927
  88. Regulation of mammalian fertilization by zona pellucida glycoproteins.
    J Reprod Fertil Suppl. 1990;42:79-87 PMID: 2077130
  89. Approach to the infertile man.
    J Clin Endocrinol Metab. 2007 Jun;92(6):1995-2004 PMID: 17554051
  90. The polypeptide backbone of recombinant human zona pellucida glycoprotein-3 initiates acrosomal exocytosis in human spermatozoa in vitro.
    Biochem J. 1998 Mar 1;330 ( Pt 2):839-45 PMID: 9480899
  91. Dual role of heat shock proteins as regulators of apoptosis and innate immunity.
    J Innate Immun. 2010;2(3):238-47 PMID: 20375559
  92. Plasma membrane association, purification, and partial characterization of mouse sperm beta 1,4-galactosyltransferase.
    J Biol Chem. 1988 Nov 25;263(33):17706-14 PMID: 3141425
  93. Capacitation induces cyclic adenosine 3',5'-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells.
    Biol Reprod. 2002 Jul;67(1):340-50 PMID: 12080038
  94. Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation.
    Dev Biol. 1999 Oct 15;214(2):429-43 PMID: 10525345
  95. 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
  96. 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
  97. Fertilization defects in sperm from mice lacking fertilin beta.
    Science. 1998 Sep 18;281(5384):1857-9 PMID: 9743500
  98. Development of the ability to bind to zonae pellucidae during epididymal maturation: reversible immobilization of mouse-spermatozoa by lanthanum.
    Biol Reprod. 1982 Apr;26(3):429-36 PMID: 7200807
  99. Involvement of sperm sulphatases in early sperm-zona interactions in the hamster.
    J Cell Sci. 1985 Oct;78:247-61 PMID: 2936756
  100. Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa.
    Biol Reprod. 2004 Jul;71(1):253-65 PMID: 15028630
  101. Significance of D-mannose as a sperm receptor site on the zona pellucida in human fertilization.
    Am J Obstet Gynecol. 1989 Jul;161(1):207-11 PMID: 2750806
  102. Intracellular events and signaling pathways involved in sperm acquisition of fertilizing capacity and acrosome reaction.
    Front Biosci. 2000 Nov 01;5:E110-23 PMID: 11056077
  103. Sperm binding to the zona pellucida is not sufficient to induce acrosome exocytosis.
    Development. 2007 Mar;134(5):933-43 PMID: 17293534
  104. New insights into epididymal biology and function.
    Hum Reprod Update. 2009 Mar-Apr;15(2):213-27 PMID: 19136456
  105. Protein synthesis by isolated spermatozoa from cauda and caput epididymis of rat.
    Acta Physiol Lat Am. 1973;23(5):358-62 PMID: 4361620
  106. 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
  107. 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
  108. Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: background to spermatogenesis, spermatogonia, and spermatocytes.
    Microsc Res Tech. 2010 Apr;73(4):241-78 PMID: 19941293
  109. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  110. Structure and function of the N-linked carbohydrate chains of pig zona pellucida glycoproteins.
    J Reprod Fertil Suppl. 1996;50:25-34 PMID: 8984185
  111. Lipid rafts and signal transduction.
    Nat Rev Mol Cell Biol. 2000 Oct;1(1):31-9 PMID: 11413487
  112. Expression of mannose-binding sites on human spermatozoa and their role in sperm-zona pellucida binding.
    J Androl. 1995 Jan-Feb;16(1):55-63 PMID: 7768754
  113. Involvement of N-linked carbohydrate chains of pig zona pellucida in sperm-egg binding.
    Eur J Biochem. 1995 Oct 1;233(1):35-41 PMID: 7588766
  114. Acrosomal exocytosis, a special type of regulated secretion.
    IUBMB Life. 2007 Apr-May;59(4-5):286-92 PMID: 17505967
  115. 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
  116. 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
  117. Insights into the molecular basis of sperm-egg recognition in mammals.
    Reproduction. 2004 Apr;127(4):417-22 PMID: 15047932
  118. Novel alpha-D-mannosidase of rat sperm plasma membranes: characterization and potential role in sperm-egg interactions.
    J Cell Biol. 1989 Sep;109(3):1257-67 PMID: 2768341
  119. Glycodelin-A interacts with fucosyltransferase on human sperm plasma membrane to inhibit spermatozoa-zona pellucida binding.
    J Cell Sci. 2007 Jan 1;120(Pt 1):33-44 PMID: 17148576
  120. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway.
    Development. 1995 Apr;121(4):1139-50 PMID: 7538069
  121. Characterization of human zona pellucida glycoproteins.
    Mol Hum Reprod. 1999 Jun;5(6):534-40 PMID: 10341000
  122. Addition of androgens to cultured hamster epididymis increases zona recognition by immature spermatozoa.
    J Reprod Fertil. 1984 Mar;70(2):541-7 PMID: 6230444
  123. 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
  124. Hamster sperm antigen P26h is a phosphatidylinositol-anchored protein.
    Mol Reprod Dev. 1999 Feb;52(2):225-33 PMID: 9890754
  125. A plasma membrane-associated hyaluronidase is localized to the posterior acrosomal region of stallion sperm and is associated with spermatozoal function.
    Biol Reprod. 1999 Aug;61(2):444-51 PMID: 10411525
  126. The complexities of conception.
    Science. 1995 Jul 7;269(5220):39-40 PMID: 7604276
  127. Differential release of guinea pig sperm acrosomal components during exocytosis.
    Biol Reprod. 2001 Jan;64(1):148-56 PMID: 11133669
  128. Stimulation of partially purified adenylate cyclase from bull sperm by bicarbonate.
    FEBS Lett. 1987 Jun 22;218(1):148-52 PMID: 3036587
  129. Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase.
    J Biol Chem. 1985 Aug 15;260(17):9699-705 PMID: 2991260
  130. Characterization and cellular distribution of human spermatozoal heat shock proteins.
    Hum Reprod. 1992 May;7(5):637-45 PMID: 1639983
  131. Comparison between epididymosomes collected in the intraluminal compartment of the bovine caput and cauda epididymidis.
    Biol Reprod. 2006 Dec;75(6):885-90 PMID: 16943362
  132. Activation of a G protein complex by aggregation of beta-1,4-galactosyltransferase on the surface of sperm.
    Science. 1995 Sep 22;269(5231):1718-21 PMID: 7569899
  133. Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro.
    Biol Reprod. 1991 May;44(5):913-21 PMID: 1868148
  134. 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
  135. Elucidation of the signaling pathways that underpin capacitation-associated surface phosphotyrosine expression in mouse spermatozoa.
    J Cell Physiol. 2010 Jul;224(1):71-83 PMID: 20232304
  136. Molecular biology of sperm-egg interactions.
    Andrologia. 2005 Dec;37(6):198-9 PMID: 16336245
  137. Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse.
    Biol Reprod. 2008 Jun;78(6):983-93 PMID: 18276932
  138. Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane.
    J Cell Sci. 2001 Oct;114(Pt 19):3543-55 PMID: 11682613
  139. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm.
    Mol Cell Biol. 2003 Apr;23(7):2614-22 PMID: 12640142
  140. Reassessing the molecular biology of sperm-egg recognition with mouse genetics.
    Bioessays. 2004 Jan;26(1):29-38 PMID: 14696038
  141. The assembly of a zona pellucida binding protein complex in sperm.
    Reprod Domest Anim. 2008 Nov;43 Suppl 5:12-9 PMID: 19068028
  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. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  144. Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells.
    Mol Hum Reprod. 2005 Aug;11(8):583-90 PMID: 16051681
  145. The capacitation of the mammalian sperm.
    Nature. 1952 Aug 23;170(4321):326 PMID: 12993150
  146. 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
  147. Anti-SLIP1-reactive proteins exist on human spermatozoa and are involved in zona pellucida binding.
    Mol Hum Reprod. 2001 Jul;7(7):633-40 PMID: 11420386
  148. O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity.
    Cell. 1985 May;41(1):313-24 PMID: 2986849
  149. NYD-SP27, a novel intrinsic decapacitation factor in sperm.
    Asian J Androl. 2009 Mar;11(2):229-39 PMID: 19252507
  150. Differential binding of gold-labeled zona pellucida glycoproteins mZP2 and mZP3 to mouse sperm membrane compartments.
    Development. 1991 Sep;113(1):141-9 PMID: 1764991
  151. 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
  152. Molecular markers of human sperm functions.
    Int J Androl. 2009 Feb;32(1):25-45 PMID: 18298567
  153. Changes in fine structure of the rabbit sperm head during passage through the epididymis.
    J Anat. 1965 Oct;99(Pt 4):891-906 PMID: 5867174
  154. Identification of sterol acceptors that stimulate cholesterol efflux from human spermatozoa during in vitro capacitation.
    Gamete Res. 1988 Jun;20(2):185-201 PMID: 3235036
  155. Four zona pellucida glycoproteins are expressed in the human.
    Hum Reprod. 2004 Jul;19(7):1580-6 PMID: 15142998
  156. The role of carbohydrates in sperm-egg interaction in rats.
    Biol Reprod. 1986 Apr;34(3):446-52 PMID: 3008866
Article Info
Journal
Asian journal of andrology
Abbr.
Asian J Androl
ISSN
1745-7262
DOI
10.1038/aja.2010.74
Published
2011-01-00
Epub
2010-00-01
Pages
88-96
Language
English
Region
China
NLM ID
100942132
PMCID
PMC3739399
Subset
IM
External Links
PubMed source DOI: 10.1038/aja.2010.74 PMC Full Text View journal details
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