More Than a Simple Lock and Key Mechanism: Unraveling the Intricacies of Sperm-Zona Pellucida Binding

© 2012 Nixon et al., licensee InTech. This is an open access chapter distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. More Than a Simple Lock and Key Mechanism: Unraveling the Intricacies of Sperm-Zona Pellucida Binding

[1]  J. Bleil,et al.  Tissue- and species-specific expression of sp56, a mouse sperm fertilization protein. , 1995, Science.

[2]  R. Yanagimachi,et al.  Fertility of mammalian spermatozoa: its development and relativity , 1994, Zygote.

[3]  M. Capecchi,et al.  Mice lacking angiotensin-converting enzyme have low blood pressure, renal pathology, and reduced male fertility. , 1996, Laboratory investigation; a journal of technical methods and pathology.

[4]  R. Aitken,et al.  Proteomic and functional analysis of human sperm detergent resistant membranes , 2011, Journal of cellular physiology.

[5]  J. Bedford.  Effects of duct ligation on the fertilizing ability of spermatozoa from different regions of the rabbit epididymis. , 1967, The Journal of experimental zoology.

[6]  T. Nakanishi,et al.  Mouse Sperm Lacking ADAM1b/ADAM2 Fertilin Can Fuse with the Egg Plasma Membrane and Effect Fertilization* , 2006, Journal of Biological Chemistry.

[7]  J. Dean,et al.  Insights into the molecular basis of sperm-egg recognition in mammals. , 2004, Reproduction.

[8]  D. Garbers,et al.  A Sperm Membrane Protein That Binds in a Species-specific Manner to the Egg Extracellular Matrix Is Homologous to von Willebrand Factor (*) , 1995, The Journal of Biological Chemistry.

[9]  J. Arribas,et al.  Phosphorylation of C8 and C9 subunits of the multicatalytic proteinase by casein kinase II and identification of the C8 phosphorylation sites by direct mutagenesis. , 1996, Biochemistry.

[10]  J. Brouwers,et al.  Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. , 2001, Journal of cell science.

[11]  Susan S Suarez,et al.  Control of hyperactivation in sperm. , 2008, Human reproduction update.

[12]  Paul D. Dunne,et al.  Tracking diffusion of GM1 gangliosides and zona pellucida binding molecules in sperm plasma membranes following cholesterol efflux. , 2010, Developmental biology.

[13]  A. Walsh,et al.  Elucidation of the signaling pathways that underpin capacitation‐associated surface phosphotyrosine expression in mouse spermatozoa , 2010, Journal of cellular physiology.

[14]  M. Ikawa,et al.  Calmegin is required for fertilin alpha/beta heterodimerization and sperm fertility. , 2001, Developmental biology.

[15]  C. Soler,et al.  Development of sperm motility patterns in the murine epididymis. , 1994, International journal of andrology.

[16]  M. Ikawa,et al.  Calsperin Is a Testis-specific Chaperone Required for Sperm Fertility* , 2010, The Journal of Biological Chemistry.

[17]  P. Kloetzel,et al.  Phosphoamino acids in proteasome subunits. , 1996, Biological chemistry.

[18]  D. Garbers,et al.  Species Diversity in the Structure of Zonadhesin, a Sperm-specific Membrane Protein Containing Multiple Cell Adhesion Molecule-like Domains* , 1998, The Journal of Biological Chemistry.

[19]  I. Adham,et al.  Male mice deficient for germ-cell cyritestin are infertile. , 1999, Biology of reproduction.

[20]  H. Florman,et al.  Mechanisms of Sperm-Egg Interactions: Between Sugars and Broken Bonds , 2010, Science Signaling.

[21]  C. Gagnon,et al.  Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. , 1997, Free radical biology & medicine.

[22]  M. O’Bryan,et al.  Human sperm NADH and NADPH diaphorase cytochemistry: correlation with sperm motility. , 1998, Urology.

[23]  M. Orgebin-Crist,et al.  Maturation of spermatozoa in the rabbit epididymis: delayed fertilization in does inseminated with epididymal spermatozoa. , 1968, Journal of reproduction and fertility.

[24]  G. Huszar,et al.  Incomplete development of human spermatozoa is associated with increased creatine phosphokinase concentration and abnormal head morphology , 1993, Molecular reproduction and development.

[25]  S. Naaby-Hansen,et al.  Heat shock proteins on the human sperm surface. , 2010, Journal of reproductive immunology.

[26]  P. Wassarman,et al.  Inactivation of the mouse sperm receptor, mZP3, by site-directed mutagenesis of individual serine residues located at the combining site for sperm. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  L. Altucci,et al.  A Gradient of 2-Arachidonoylglycerol Regulates Mouse Epididymal Sperm Cell Start-Up1 , 2010, Biology of reproduction.

[28]  J. Garin,et al.  Post-meiotic Shifts in HSPA2/HSP70.2 Chaperone Activity during Mouse Spermatogenesis* , 2006, Journal of Biological Chemistry.

[29]  R. Shope,et al.  Semen changes in boars after experimental infection with pseudorabies virus. , 1980, American journal of veterinary research.

[30]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[31]  H. Moore,et al.  In vitro maturation of mammalian spermatozoa. , 1996, Reviews of reproduction.

[32]  M. Belghazi,et al.  Human epididymal secretome and proteome , 2006, Molecular and Cellular Endocrinology.

[33]  E. S. Díaz,et al.  Participation of the Human Sperm Proteasome in the Capacitation Process and Its Regulation by Protein Kinase A and Tyrosine Kinase1 , 2009, Biology of reproduction.

[34]  E. Seren,et al.  Immunolocalization of heat shock protein 70 (Hsp 70) in boar spermatozoa and its role during fertilization , 2005, Molecular reproduction and development.

[35]  M. Ollero,et al.  Variation of docosahexaenoic acid content in subsets of human spermatozoa at different stages of maturation: Implications for sperm lipoperoxidative damage , 2000, Molecular reproduction and development.

[36]  G. Clark.  Molecular models for mouse sperm-oocyte binding. , 2011, Glycobiology.

[37]  M. Orgebin-Crist,et al.  Studies on the function of the epididymis. , 1969, Biology of reproduction.

[38]  C. Hardy,et al.  Development of mouse-specific contraceptive vaccines: infertility in mice immunized with peptide and polyepitope antigens. , 2004, Reproduction.

[39]  M. Cann,et al.  Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. , 2000, Science.

[40]  D. Buckingham,et al.  Relationships between biochemical markers for residual sperm cytoplasm, reactive oxygen species generation, and the presence of leukocytes and precursor germ cells in human sperm suspensions , 1994, Molecular reproduction and development.

[41]  P. Sutovsky,et al.  Interference with the 19S proteasomal regulatory complex subunit PSMD4 on the sperm surface inhibits sperm-zona pellucida penetration during porcine fertilization , 2010, Cell and Tissue Research.

[42]  R. Aitken,et al.  Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function. , 1996, Journal of andrology.

[43]  V. Winfrey,et al.  Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. , 2003, The Biochemical journal.

[44]  T. Baba,et al.  Synthesis, processing, and subcellular localization of mouse ADAM3 during spermatogenesis and epididymal sperm transport. , 2004, The Journal of reproduction and development.

[45]  P. Wassarman,et al.  Zona Pellucida Glycoproteins* , 2008, Journal of Biological Chemistry.

[46]  J. Tesarik,et al.  Stimulation of protein tyrosine phosphorylation by a progesterone receptor on the cell surface of human sperm. , 1993, Endocrinology.

[47]  R. Jones.  Plasma membrane structure and remodelling during sperm maturation in the epididymis. , 1998, Journal of reproduction and fertility. Supplement.

[48]  R. Aitken,et al.  A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. , 1998, Journal of cell science.

[49]  M. El‐Alfy,et al.  Cytoplasmic localization during testicular biogenesis of the murine mRNA for Spam1 (PH‐20), a protein involved in acrosomal exocytosis , 2004, Molecular reproduction and development.

[50]  William Arbuthnot Sir Lane,et al.  Proteomic analysis of sperm regions that mediate sperm‐egg interactions , 2006, Proteomics.

[51]  William D. Willis,et al.  Phosphoglycerate Kinase 2 (PGK2) Is Essential for Sperm Function and Male Fertility in Mice1 , 2010, Biology of reproduction.

[52]  David J. Miller,et al.  Sperm Proteasomes Degrade Sperm Receptor on the Egg Zona Pellucida during Mammalian Fertilization , 2011, PloS one.

[53]  S. Coonrod,et al.  Monoclonal antibody to human fertilization antigen-1 (FA-1) inhibits bovine fertilization in vitro: application in immunocontraception. , 1994, Biology of reproduction.

[54]  R. Aitken,et al.  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 Reaction1 , 2005, Biology of reproduction.

[55]  R. Naz,et al.  Expression and function of ras proto-oncogene proteins in human sperm cells. , 1992, Journal of cell science.

[56]  R. Aitken,et al.  Phosphorylation and consequent stimulation of the tyrosine kinase c-Abl by PKA in mouse spermatozoa; its implications during capacitation. , 2009, Developmental biology.

[57]  A. Salicioni,et al.  Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. , 2008, The International journal of developmental biology.

[58]  B. Gadella,et al.  The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. , 2000, Development.

[59]  M. Orgebin-Crist,et al.  The Effect of Epididymal and Testicular Fluids on the Fertilising Capacity of Testicular and Epididymal Spermatozoa , 2009, Andrologia.

[60]  J. Marth,et al.  Inactivation of the Mgat1 Gene in Oocytes Impairs Oogenesis, but Embryos Lacking Complex and Hybrid N-Glycans Develop and Implant , 2004, Molecular and Cellular Biology.

[61]  D. Brown,et al.  Functions of lipid rafts in biological membranes. , 1998, Annual review of cell and developmental biology.

[62]  Zuo-min Zhou,et al.  NYD-SP27, a novel intrinsic decapacitation factor in sperm. , 2009, Asian journal of andrology.

[63]  R. Gibbons,et al.  A mouse sperm decapacitation factor receptor is phosphatidylethanolamine-binding protein 1. , 2005, Reproduction.

[64]  B. Shur,et al.  Sperm surface galactosyltransferase activities during in vitro capacitation , 1982, The Journal of cell biology.

[65]  G. Gerton,et al.  Differential Release of Guinea Pig Sperm Acrosomal Components During Exocytosis1 , 2001, Biology of reproduction.

[66]  C. López-Otín,et al.  Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies. , 2004, The International journal of developmental biology.

[67]  N. García-Gil,et al.  Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction. , 2008, Theriogenology.

[68]  E. Töpfer‐Petersen.  Carbohydrate-based interactions on the route of a spermatozoon to fertilization. , 1999, Human reproduction update.

[69]  D. Sakkas,et al.  Protein Tyrosine Phosphorylation in Sperm During Gamete Interaction in the Mouse: The Influence of Glucose1 , 2001, Biology of reproduction.

[70]  P. Wassarman,et al.  Interaction of mouse sperm with purified sperm receptors covalently linked to silica beads. , 1989, Journal of cell science.

[71]  M. Miyake,et al.  Fructose stimulates shedding of cytoplasmic droplets from epididymal boar spermatozoa. , 1996, Reproduction, fertility, and development.

[72]  L. Leyton,et al.  Evidence that aggregation of mouse sperm receptors by ZP3 triggers the acrosome reaction , 1989, The Journal of cell biology.

[73]  R. Schultz,et al.  Effects of a phorbol ester on mouse eggs: dissociation of sperm receptor activity from acrosome reaction-inducing activity of the mouse zona pellucida protein, ZP3. , 1987, Developmental biology.

[74]  Angshumoy Roy,et al.  Loss of Zona Pellucida Binding Proteins in the Acrosomal Matrix Disrupts Acrosome Biogenesis and Sperm Morphogenesis , 2007, Molecular and Cellular Biology.

[75]  J. Keating,et al.  Investigation of the association between the presence of cytoplasmic residues on the human sperm midpiece and defective sperm function. , 1997, Journal of reproduction and fertility.

[76]  E. M. Eddy,et al.  Male germ cell gene expression. , 2002, Recent progress in hormone research.

[77]  M. J. Kornblatt.  Synthesis and turnover of sulfogalactoglycerolipid, a membrane lipid, during spermatogenesis. , 1979, Canadian journal of biochemistry.

[78]  T. Nakanishi,et al.  Possible Function of the ADAM1a/ADAM2 Fertilin Complex in the Appearance of ADAM3 on the Sperm Surface* , 2004, Journal of Biological Chemistry.

[79]  Y. Salomon,et al.  Stimulation of partially purified adenylate cyclase from bull sperm by bicarbonate , 1987, FEBS letters.

[80]  P. James,et al.  Cholesterol Efflux Alters Lipid Raft Stability and Distribution During Capacitation of Boar Spermatozoa1 , 2004, Biology of reproduction.

[81]  Bedford Jm.  Changes in fine structure of the rabbit sperm head during passage through the epididymis. , 1965 .

[82]  R. Sullivan,et al.  Hamster sperm antigen P26h is a phosphatidylinositol‐anchored protein , 1999, Molecular reproduction and development.

[83]  P. Wassarman,et al.  Mammalian fertilization: the egg's multifunctional zona pellucida. , 2008, The International journal of developmental biology.

[84]  J. Bedford.  Ultrastructural changes in the sperm head during fertilization in the rabbit. , 1968, The American journal of anatomy.

[85]  M. Buffone,et al.  Recombinant Mouse Sperm ZP3-binding Protein (ZP3R/sp56) Forms a High Order Oligomer That Binds Eggs and Inhibits Mouse Fertilization in Vitro* , 2008, Journal of Biological Chemistry.

[86]  Deborah A. Brown,et al.  Structure and Function of Sphingolipid- and Cholesterol-rich Membrane Rafts* , 2000, The Journal of Biological Chemistry.

[87]  B. Hille,et al.  External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility. , 2007, Developmental biology.

[88]  A. Lobley,et al.  Reproductive Biology and Endocrinology Identification of Human and Mouse Catsper3 and Catsper4 Genes: Characterisation of a Common Interaction Domain and Evidence for Expression in Testis , 2022 .

[89]  P. Wassarman,et al.  O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity , 1985, Cell.

[90]  G. Hale,et al.  Cell-to-cell transfer of glycosylphosphatidylinositol-anchored membrane proteins during sperm maturation. , 1996, Molecular human reproduction.

[91]  P. Martin-DeLeon,et al.  Mouse epididymal Spam1 (pH-20) is released in the luminal fluid with its lipid anchor. , 2003, Journal of andrology.

[92]  L. Fraser.  Mouse sperm capacitation in vitro involves loss of a surface-associated inhibitory component. , 1984, Journal of reproduction and fertility.

[93]  M. Ikawa,et al.  Disruption of ADAM3 Impairs the Migration of Sperm into Oviduct in Mouse1 , 2009, Biology of reproduction.

[94]  B. Shur,et al.  A specific defect in galactosyltransferase regulation on sperm bearing mutant alleles of the T/t locus. , 1979, Developmental biology.

[95]  Kai Simons,et al.  Lipid rafts and signal transduction , 2000, Nature Reviews Molecular Cell Biology.

[96]  B. Dunbar,et al.  Specificity of sperm-zona interaction. , 1982, The Journal of experimental zoology.

[97]  M. C. CHANG,et al.  Fertilizing Capacity of Spermatozoa deposited into the Fallopian Tubes , 1951, Nature.

[98]  Sara Linse,et al.  Methods for the detection and analysis of protein–protein interactions , 2007, Proteomics.

[99]  R. Sullivan,et al.  Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. , 2011, International journal of andrology.

[100]  G. Cornwall,et al.  The effect of sulfhydryl oxidation on the morphology of immature hamster epididymal spermatozoa induced to acquire motility in vitro. , 1988, Biology of reproduction.

[101]  Dennis Brown,et al.  Regulation of luminal acidification in the male reproductive tract via cell–cell crosstalk , 2009, Journal of Experimental Biology.

[102]  B. T. Storey,et al.  Mouse gamete interactions: the zona pellucida is the site of the acrosome reaction leading to fertilization in vitro. , 1982, Developmental biology.

[103]  D. Wolf,et al.  Fertilization-associated changes in the murine zona pellucida: a time sequence study. , 1975, Biology of reproduction.

[104]  N. Tanphaichitr,et al.  Role of Sperm Surface Arylsulfatase A in Mouse Sperm-Zona Pellucida Binding1 , 2002, Biology of reproduction.

[105]  E. Schwoebel,et al.  The mammalian zona pellucida: its biochemistry, immunochemistry, molecular biology, and developmental expression. , 1994, Reproduction, fertility, and development.

[106]  M. O'Rand,et al.  Expression of the rabbit sperm protein Sp17 in cos cells and interaction of recombinant Sp17 with the rabbit zona pellucida , 1995, Molecular reproduction and development.

[107]  N. Tanphaichitr,et al.  Binding of Arylsulfatase A to Mouse Sperm Inhibits Gamete Interaction and Induces the Acrosome Reaction1 , 2002, Biology of reproduction.

[108]  H. Scrable,et al.  Isolation and Proteomic Analysis of Mouse Sperm Detergent-Resistant Membrane Fractions: Evidence for Dissociation of Lipid Rafts During Capacitation1 , 2005, Biology of reproduction.

[109]  R. Aitken,et al.  Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa , 2006, Journal of Cell Science.

[110]  A. Agarwal,et al.  Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. , 2000, Human reproduction.

[111]  J. Gatti,et al.  Post-testicular sperm environment and fertility. , 2004, Animal reproduction science.

[112]  B. Jaiswal,et al.  Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[113]  D. Jay,et al.  Extracellular Heat Shock Protein (Hsp)70 and Hsp90α Assist in Matrix Metalloproteinase-2 Activation and Breast Cancer Cell Migration and Invasion , 2011, PloS one.

[114]  B. Shur,et al.  Receptor function of mouse sperm surface galactosyltransferase during fertilization , 1985, The Journal of cell biology.

[115]  Matthew D. Dun,et al.  Involvement of multimeric protein complexes in mediating the capacitation-dependent binding of human spermatozoa to homologous zonae pellucidae. , 2011, Developmental biology.

[116]  D. Hardy,et al.  Heterogeneous Processing and Zona Pellucida Binding Activity of Pig Zonadhesin* , 2001, The Journal of Biological Chemistry.

[117]  J. Calvete,et al.  Spermadhesins: A new protein family. Facts, hypotheses and perspectives , 2009, Andrologia.

[118]  B. Shur,et al.  Mouse oviduct-specific glycoprotein is an egg-associated ZP3-independent sperm-adhesion ligand , 2009, Journal of Cell Science.

[119]  D. Cyr,et al.  Gene Expression Profiling and Its Relevance to the Blood-Epididymal Barrier in the Human Epididymis1 , 2007, Biology of reproduction.

[120]  V. Labas,et al.  Mammalian epididymal proteome , 2009, Molecular and Cellular Endocrinology.

[121]  N. Nakamura,et al.  Cleavage of Disulfide Bonds in Mouse Spermatogenic Cell-Specific Type 1 Hexokinase Isozyme Is Associated with Increased Hexokinase Activity and Initiation of Sperm Motility1 , 2008, Biology of reproduction.

[122]  G S Kopf,et al.  Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. , 1995, Development.

[123]  N. Tanphaichitr,et al.  Sulfogalactosylglycerolipid is involved in human gamete interaction , 2001, Molecular reproduction and development.

[124]  P. Wassarman,et al.  Structure and function of the zona pellucida: identification and characterization of the proteins of the mouse oocyte's zona pellucida. , 1980, Developmental biology.

[125]  E. Delpiano,et al.  Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. , 2007, Reproductive biomedicine online.

[126]  B. Gadella,et al.  Capacitation Induces Cyclic Adenosine 3′,5′-Monophosphate-Dependent, but Apoptosis-Unrelated, Exposure of Aminophospholipids at the Apical Head Plasma Membrane of Boar Sperm Cells1 , 2002, Biology of reproduction.

[127]  Dennis Brown,et al.  Bicarbonate-regulated Adenylyl Cyclase (sAC) Is a Sensor That Regulates pH-dependent V-ATPase Recycling* , 2003, Journal of Biological Chemistry.

[128]  C. Weber,et al.  The tight junction protein complex undergoes rapid and continuous molecular remodeling at steady state , 2008, The Journal of cell biology.

[129]  D. Chan,et al.  Secretion of extracellular hsp90α via exosomes increases cancer cell motility: a role for plasminogen activation , 2010, BMC Cancer.

[130]  J. Bedford,et al.  Formation of disulphide bonds in the nucleus and accessory structures of mammalian spermatozoa during maturation in the epididymis. , 1971, Journal of reproduction and fertility. Supplement.

[131]  W. Engel,et al.  Interactions between mouse ZP2 glycoprotein and proacrosin; a mechanism for secondary binding of sperm to the zona pellucida during fertilization. , 2001, Journal of cell science.

[132]  B. T. Storey,et al.  An ultrastructural study of epididymal mouse spermatozoa binding to zonae pellucidae in vitro: sequential relationship to the acrosome reaction. , 1979, The Journal of experimental zoology.

[133]  R. Gwatkin,et al.  Early contact interactions between mammalian gametes in vitro: evidence that the vitellus influences adherence between sperm and zona pellucida. , 1972, Proceedings of the National Academy of Sciences of the United States of America.

[134]  T. Cooper,et al.  Effect of aging on the fertilizing capacity of testicular spermatozoa from the rabbit. , 1977, Biology of reproduction.

[135]  D. Kretser,et al.  Male infertility: the case for continued research , 2001, The Medical journal of Australia.

[136]  G. Berruti,et al.  Acrosome biogenesis , 2011, Spermatogenesis.

[137]  A. Petrunkina,et al.  Only low levels of spermadhesin AWN are detectable on the surface of live ejaculated boar spermatozoa. , 2000, Reproduction, fertility, and development.

[138]  R. Yanagimachi.  Germ Cell Research: A Personal Perspective , 2009, Biology of reproduction.

[139]  A. Sanjay,et al.  Inhibition of Ser/Thr Phosphatases Induces Capacitation-associated Signaling in the Presence of Src Kinase Inhibitors* , 2010, The Journal of Biological Chemistry.

[140]  D. Liu,et al.  Morphology of spermatozoa bound to the zona pellucida of human oocytes that failed to fertilize in vitro. , 1992, Journal of reproduction and fertility.

[141]  D. Cyr,et al.  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 , 2009, Microscopy research and technique.

[142]  T. Cooper.  The human epididymis--is it necessary? , 1993, International journal of andrology.

[143]  R. Brinster,et al.  Spermatogonial stem cells. , 2006, Methods in enzymology.

[144]  W. Willis,et al.  Glyceraldehyde 3-phosphate dehydrogenase-S, a sperm-specific glycolytic enzyme, is required for sperm motility and male fertility. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[145]  G. Cornwall,et al.  Inhibition of the mouse sperm surface alpha-D-mannosidase inhibits sperm-egg binding in vitro. , 1991, Biology of reproduction.

[146]  G. Clark.  The Mammalian Zona Pellucida: A Matrix That Mediates Both Gamete Binding and Immune Recognition? , 2010, Systems biology in reproductive medicine.

[147]  R. Sackstein.  The lymphocyte homing receptors: gatekeepers of the multistep paradigm , 2005, Current opinion in hematology.

[148]  B. Shur,et al.  Sperm from beta 1,4-galactosyltransferase-null mice are refractory to ZP3-induced acrosome reactions and penetrate the zona pellucida poorly. , 1997, Development.

[149]  C. Celik-Ozenci,et al.  Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: selection of sperm for intracytoplasmic sperm injection , 2006, Current opinion in obstetrics & gynecology.

[150]  S. Oehninger,et al.  Creatine kinase immunocytochemistry of human sperm‐hemizona complexes: Selective binding of sperm with mature creatine kinase‐staining pattern , 1994, Fertility and sterility.

[151]  D. Tulsiani,et al.  Rat sperm surface mannosidase is first expressed on the plasma membrane of testicular germ cells. , 1998, Biology of reproduction.

[152]  C. R. Austin,et al.  The ‘Capacitation’ of the Mammalian Sperm , 1952, Nature.

[153]  M. Ensslin,et al.  Identification of Mouse Sperm SED1, a Bimotif EGF Repeat and Discoidin-Domain Protein Involved in Sperm-Egg Binding , 2003, Cell.

[154]  D. Garbers,et al.  Species-specific binding of sperm proteins to the extracellular matrix (zona pellucida) of the egg. , 1994, The Journal of biological chemistry.

[155]  Michael D. Wilson,et al.  Zonadhesin Is Essential for Species Specificity of Sperm Adhesion to the Egg Zona Pellucida* , 2010, The Journal of Biological Chemistry.

[156]  H. Iida,et al.  Bactericidal/Permeability-increasing protein is associated with the acrosome region of rodent epididymal spermatozoa. , 2010, Journal of andrology.

[157]  M. Kong,et al.  Role of the sperm proteasome during fertilization and gamete interaction in the mouse , 2005, Molecular reproduction and development.

[158]  A. Dell,et al.  Differential O-glycosylation of a conserved domain expressed in murine and human ZP3. , 2006, Biochemistry.

[159]  M. Ikawa,et al.  Calmegin Is Required for Fertilin α/β Heterodimerization and Sperm Fertility , 2001 .

[160]  M. Okabe,et al.  Function of the Acrosomal Matrix: Zona Pellucida 3 Receptor (ZP3R/sp56) Is Not Essential for Mouse Fertilization1 , 2012, Biology of reproduction.

[161]  B. Gadella,et al.  Bicarbonate-induced membrane processing in sperm capacitation. , 2005, Theriogenology.

[162]  H. Koistinen,et al.  Binding of Zona Binding Inhibitory Factor-1 (ZIF-1) from Human Follicular Fluid on Spermatozoa* , 2003, The Journal of Biological Chemistry.

[163]  M. Takenaka,et al.  An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. , 1994, The Journal of biological chemistry.

[164]  R. Aitken,et al.  Investigation of the role of SRC in capacitation-associated tyrosine phosphorylation of human spermatozoa. , 2008, Molecular human reproduction.

[165]  E. M. Eddy,et al.  Fertilization defects in sperm from mice lacking fertilin beta. , 1998, Science.

[166]  H. Koistinen,et al.  The Contribution of d-Mannose, l-Fucose, N-Acetylglucosamine, and Selectin Residues on the Binding of Glycodelin Isoforms to Human Spermatozoa1 , 2004, Biology of reproduction.

[167]  S. Nagdas,et al.  Zonadhesin Assembly into the Hamster Sperm Acrosomal Matrix Occurs by Distinct Targeting Strategies During Spermiogenesis and Maturation in the Epididymis1 , 2004, Biology of reproduction.

[168]  E. Bosmans,et al.  Sperm morphology assessment: diagnostic potential and comparative analysis of strict or WHO criteria in a fertile and a subfertile population. , 1998, International journal of andrology.

[169]  M. Mahony,et al.  Modulation of sperm tail protein tyrosine phosphorylation by pentoxifylline and its correlation with hyperactivated motility. , 1999, Fertility and sterility.

[170]  R. Aitken,et al.  Relationship between calcium, cyclic AMP, ATP, and intracellular pH and the capacity of hamster spermatozoa to express hyperactivated motility. , 1989, Gamete research.

[171]  R. Cardullo,et al.  Distinct Membrane Fractions from Mouse Sperm Bind Different Zona Pellucida Glycoproteins1 , 2002, Biology of reproduction.

[172]  T. Cooper,et al.  Acquisition of volume regulatory response of sperm upon maturation in the epididymis and the role of the cytoplasmic droplet , 2003, Microscopy research and technique.

[173]  D. Fawcett.  Gametogenesis in the male: prospects for its control. , 1975, The ... Symposium. Society for Developmental Biology. Symposium.

[174]  P. Wassarman,et al.  Mouse gamete adhesion molecules. , 1992, Biology of reproduction.

[175]  A. Campana,et al.  Localization of Tyrosine Phosphorylated Proteins in Human Sperm and Relation to Capacitation and Zona Pellucida Binding1 , 2003, Biology of reproduction.

[176]  P. Donner,et al.  Characterization of human zona pellucida glycoproteins. , 1999, Molecular human reproduction.

[177]  J. Jarow.  A sperm ion channel required for sperm motility and male fertility. , 2002, The Journal of urology.

[178]  E. Cosmi,et al.  Morphometric assessment of mature and diminished-maturity human spermatozoa: sperm regions that reflect differences in maturity. , 1999, Human reproduction.

[179]  A. Rivett,et al.  Phosphorylation of proteasomes in mammalian cells , 1999, Molecular Biology Reports.

[180]  C. P. Leblond,et al.  Spermiogenesis of rat, mouse, hamster and guinea pig as revealed by the periodic acid-fuchsin sulfurous acid technique. , 1952, The American journal of anatomy.

[181]  R. Cardullo,et al.  The Initial Molecular Interaction between Mouse Sperm and the Zona Pellucida Is a Complex Binding Event* , 1996, The Journal of Biological Chemistry.

[182]  G. Kopf,et al.  The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. , 2005, Developmental cell.

[183]  P. Hermonat,et al.  Immunolocalization of Sperm Protein 17 in Human Testis and Ejaculated Spermatozoa , 2003, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[184]  G. Kopf,et al.  Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. , 1999, Developmental biology.

[185]  D. Katz.  Characteristics of Sperm Motility , 1991, Annals of the New York Academy of Sciences.

[186]  K. Stone,et al.  Putative Creatine Kinase M-Isoform in Human Sperm Is Identifiedas the 70-Kilodalton Heat Shock Protein HspA21 , 2000, Biology of reproduction.

[187]  N. Kosower,et al.  Tyrosine Phosphorylation, Thiol Status, and Protein Tyrosine Phosphatase in Rat Epididymal Spermatozoa , 2004, Biology of reproduction.

[188]  R. Aitken,et al.  The Identification of Mouse Sperm-Surface-Associated Proteins and Characterization of Their Ability to Act as Decapacitation Factors1 , 2006, Biology of reproduction.

[189]  J. Overstreet,et al.  Effects of antibodies to sperm surface fertilization antigen-1 on human sperm-zona pellucida interaction. , 1992, Fertility and sterility.

[190]  Roy Jones,et al.  Interactions between zona pellucida glycoproteins and sperm proacrosin/acrosin during fertilization. , 2002, Journal of reproductive immunology.

[191]  L. Fraser.  Interactions between a decapacitation factor and mouse spermatozoa appear to involve fucose residues and a GPI‐anchored receptor , 1998, Molecular reproduction and development.

[192]  M. Mahony,et al.  Protein tyrosine phosphorylation during hyperactivated motility of cynomolgus monkey (Macaca fascicularis) spermatozoa. , 1999, Biology of reproduction.

[193]  U. A. Urch,et al.  The interaction of boar sperm proacrosin with its natural substrate, the zona pellucida, and with polysulfated polysaccharides. , 1991, Development.

[194]  Kai Simons,et al.  Model systems, lipid rafts, and cell membranes. , 2004, Annual review of biophysics and biomolecular structure.

[195]  G. Clark.  The molecular basis of mouse sperm-zona pellucida binding: a still unresolved issue in developmental biology. , 2011, Reproduction.

[196]  Germán L. Rosano,et al.  D-Mannose-binding sites are putative sperm determinants of human oocyte recognition and fertilization. , 2007, Reproductive biomedicine online.

[197]  S. Oehninger,et al.  Predictive value of the hemizona assay for pregnancy outcome in patients undergoing controlled ovarian hyperstimulation with intrauterine insemination. , 2006, Fertility and sterility.

[198]  T. Cooper.  Cytoplasmic droplets: the good, the bad or just confusing? , 2005, Human Reproduction.

[199]  N. Tanphaichitr,et al.  Role of a gamete-specific sulfoglycolipid immobilizing protein on mouse sperm-egg binding. , 1993, Developmental biology.

[200]  R. Sullivan,et al.  Aldose Reductase and Macrophage Migration Inhibitory Factor Are Associated with Epididymosomes and Spermatozoa in the Bovine Epididymis1 , 2003, Biology of reproduction.

[201]  L. Fraser.  The “switching on” of mammalian spermatozoa: Molecular events involved in promotion and regulation of capacitation , 2010, Molecular reproduction and development.

[202]  P. Castle,et al.  Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. , 2003, Developmental cell.

[203]  B. Shur,et al.  Redistribution of mouse sperm surface galactosyltransferase after the acrosome reaction , 1987, The Journal of cell biology.

[204]  M. Dym.  Spermatogonial stem cells of the testis. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[205]  J. Shabanowitz,et al.  Phosphoproteome Analysis of Capacitated Human Sperm , 2003, The Journal of Biological Chemistry.

[206]  B. Gulyas,et al.  Mammalian sperm-egg recognition and binding in vitro. I. Specificity of sperm interactions with live and fixed eggs in homologous and heterologous inseminations of hamster, mouse, and guinea pig oocytes. , 1980, Biology of reproduction.

[207]  J. Gatti,et al.  The epididymal transcriptome and proteome provide some insights into new epididymal regulations. , 2011, Journal of andrology.

[208]  R. Aitken,et al.  Identification of post‐translational modifications that occur during sperm maturation using difference in two‐dimensional gel electrophoresis , 2005, Proteomics.

[209]  J. Wilcox,et al.  Regulated expression of testis angiotensin-converting enzyme during spermatogenesis in mice. , 1993, Biology of reproduction.

[210]  R. Aitken,et al.  Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition , 2004, Journal of Cell Science.

[211]  W. Schill,et al.  Release of angiotensin-converting enzyme (ACE) from human spermatozoa during capacitation and acrosome reaction. , 1995, Journal of andrology.

[212]  N. Tanphaichitr,et al.  Role of Sperm Sulfogalactosylglycerolipid in Mouse Sperm-Zona Pellucida Binding1 , 2000, Biology of reproduction.

[213]  M. Paquignon,et al.  Relations between the fertilizing ability, motility and metabolism of epididymal spermatozoa. , 1980, Reproduction, nutrition, developpement.

[214]  A. Dokras,et al.  Sperm maturity and treatment choice of in vitro fertilization (IVF) or intracytoplasmic sperm injection: diminished sperm HspA2 chaperone levels predict IVF failure. , 2002, Fertility and sterility.

[215]  R. Cardullo,et al.  The acrosomal vesicle of mouse sperm is a calcium store , 2005, Journal of cellular physiology.

[216]  G. Cornwall.  New insights into epididymal biology and function. , 2008, Human reproduction update.

[217]  L. Pike.  Rafts defined: a report on the Keystone symposium on lipid rafts and cell function Published, JLR Papers in Press, April 27, 2006. , 2006, Journal of Lipid Research.

[218]  R. Brinster.  Germline Stem Cell Transplantation and Transgenesis , 2002, Science.

[219]  D. H. Kim,et al.  Expression and Relationship of Male Reproductive ADAMs in Mouse1 , 2006, Biology of reproduction.

[220]  Cecil Han,et al.  ADAM7 is associated with epididymosomes and integrated into sperm plasma membrane , 2009, Molecules and cells.

[221]  J. Fujii,et al.  Localization and physiological implication of aldose reductase and sorbitol dehydrogenase in reproductive tracts and spermatozoa of male rats. , 2002, Journal of andrology.

[222]  P. Wassarman,et al.  Sperm-egg recognition in the mouse: characterization of sp56, a sperm protein having specific affinity for ZP3 , 1994, The Journal of cell biology.

[223]  E. Donetti,et al.  Sperm protein 17 is expressed in the sperm fibrous sheath , 2009, Journal of Translational Medicine.

[224]  M. Ikawa,et al.  Mouse Sperm Lacking Cell Surface Hyaluronidase PH-20 Can Pass through the Layer of Cumulus Cells and Fertilize the Egg* , 2002, The Journal of Biological Chemistry.

[225]  B. K. Davis.  Timing of fertilization in mammals: sperm cholesterol/phospholipid ratio as a determinant of the capacitation interval. , 1981, Proceedings of the National Academy of Sciences of the United States of America.

[226]  P. Wassarman,et al.  Mammalian sperm-egg interaction: Identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm , 1980, Cell.

[227]  P. Wassarman,et al.  Sperm-egg interactions in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. , 1983, Developmental biology.

[228]  B. Nixon,et al.  Galactosyltransferase Function during Mammalian Fertilization , 2000, Cells Tissues Organs.

[229]  P. Wassarman,et al.  Enzymatic dissection of the functions of the mouse egg's receptor for sperm. , 1984, Developmental biology.

[230]  R. Sullivan,et al.  Protein composition of human epididymosomes collected during surgical vasectomy reversal: a proteomic and genomic approach. , 2008, Human reproduction.

[231]  S. Brough,et al.  Characterization and cellular distribution of human spermatozoal heat shock proteins. , 1992, Human reproduction.

[232]  M. Okabe,et al.  Mechanisms of fertilization--a view from the study of gene-manipulated mice. , 2011, Journal of andrology.

[233]  R. Sullivan,et al.  Prostasome‐like particles are involved in the transfer of P25b from the bovine epididymal fluid to the sperm surface , 2001, Molecular reproduction and development.

[234]  L. Russell,et al.  Boar sperm cytoplasmic droplets: their ultrastructure, their numbers in the epididymis and at ejaculation and their removal during isolation of sperm plasma membranes. , 1984, Tissue & cell.

[235]  C. Barros,et al.  The polysulphate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction , 1998, Zygote.

[236]  P. Primakoff,et al.  Why did the sperm cross the cumulus? To get to the oocyte. Functions of the sperm surface proteins PH-20 and fertilin in arriving at, and fusing with, the egg. , 1997, Biology of reproduction.

[237]  M. Okuno,et al.  Role of tyrosine phosphorylation of flagellar proteins in hamster sperm hyperactivation. , 1999, Biology of reproduction.

[238]  M. Sibony,et al.  Gene expression and tissue localization of the two isoforms of angiotensin I converting enzyme. , 1993, Hypertension.

[239]  P. Primakoff,et al.  Identification of an ADAM2-ADAM3 Complex on the Surface of Mouse Testicular Germ Cells and Cauda Epididymal Sperm* , 2007, Journal of Biological Chemistry.

[240]  D. Tulsiani,et al.  The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. , 1998, Experimental cell research.

[241]  P. Wassarman,et al.  Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. , 1995, Biochemistry.

[242]  P. Hasty,et al.  Targeted mutation in beta1,4-galactosyltransferase leads to pituitary insufficiency and neonatal lethality. , 1997, Developmental biology.

[243]  D. Veeramachaneni,et al.  The epididymis and sperm maturation: a perspective. , 1993, Reproduction, fertility, and development.

[244]  A. Walsh,et al.  Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. , 2008, Biology of reproduction.

[245]  D. Friend,et al.  A mechanism for differential release of acrosomal enzymes during the acrosome reaction. , 1991, The Biochemical journal.

[246]  B. K. Davis,et al.  Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro. , 1979, Biochimica et biophysica acta.

[247]  H. Zischler,et al.  The molecular evolution of sperm zonadhesin. , 2008, The International journal of developmental biology.

[248]  D. Boatman,et al.  Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions. , 1991, Biology of reproduction.

[249]  M. Orgebin-Crist,et al.  Sperm Maturation in Rabbit Epididymis , 1967, Nature.

[250]  D. Blei.  Autoradiographic Visualization of the Mouse Egg's Sperm Receptor Bound to Sperm , 2002 .

[251]  I. Braakman,et al.  Quality control in the endoplasmic reticulum protein factory , 2003, Nature.

[252]  R. Aitken,et al.  Analysis of chaperone proteins associated with human spermatozoa during capacitation. , 2007, Molecular human reproduction.

[253]  J. Bedford.  Morphological changes in rabbit spermatozoa during passage through the epididymis. , 1963, Journal of reproduction and fertility.

[254]  R. Naz.  c‐Abl proto‐oncoprotein is expressed and tyrosine phosphorylated in human sperm cell , 1998, Molecular Reproduction and Development.

[255]  Brett Nixon,et al.  The role of molecular chaperones in mouse sperm–egg interactions , 2005, Molecular and Cellular Endocrinology.

[256]  R. D'Hooge,et al.  Phenotype of arylsulfatase A-deficient mice: relationship to human metachromatic leukodystrophy. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[257]  J. Brouwers,et al.  Capacitation-dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. , 2005, Molecular human reproduction.

[258]  Denny Sakkas,et al.  Protein phosphorylation in mammalian spermatozoa. , 2003, Reproduction.

[259]  P. Hansen,et al.  Immunolocalization of heat shock protein 70 in bovine spermatozoa , 2004, Andrologia.

[260]  P. Primakoff,et al.  A hyaluronidase activity of the sperm plasma membrane protein PH-20 enables sperm to penetrate the cumulus cell layer surrounding the egg , 1994, The Journal of cell biology.

[261]  D. Tulsiani,et al.  Mannose-binding molecules of rat spermatozoa and sperm–egg interaction , 1999, Zygote.

[262]  R. Carballada,et al.  Molecules involved in mammalian sperm-egg interaction. , 1998, International review of cytology.

[263]  C. V. D. van de Lest,et al.  Capacitation dependent activation of tyrosine phosphorylation generates two sperm head plasma membrane proteins with high primary binding affinity for the zona pellucida , 2001, Molecular reproduction and development.

[264]  J. Bailey.  Factors Regulating Sperm Capacitation , 2010, Systems biology in reproductive medicine.

[265]  B. Shur,et al.  Sperm plasma membrane remodeling during spermiogenetic maturation in men: relationship among plasma membrane beta 1,4-galactosyltransferase, cytoplasmic creatine phosphokinase, and creatine phosphokinase isoform ratios. , 1997, Biology of reproduction.

[266]  R. Aitken,et al.  Composition and significance of detergent resistant membranes in mouse spermatozoa , 2009, Journal of cellular physiology.

[267]  M. Monk,et al.  Four zona pellucida glycoproteins are expressed in the human. , 2004, Human reproduction.

[268]  P. Leclerc,et al.  Increased Activity of the Human Sperm Tyrosine Kinase SRC by the cAMP-Dependent Pathway in the Presence of Calcium1 , 2008, Biology of reproduction.

[269]  R. Sullivan,et al.  Epididymosomes and prostasomes: their roles in posttesticular maturation of the sperm cells. , 2003, Journal of andrology.

[270]  E. Brown,et al.  The Rat Epididymal Transcriptome: Comparison of Segmental Gene Expression in the Rat and Mouse Epididymides1 , 2007, Biology of reproduction.

[271]  P. Wassarman,et al.  Association of egg zona pellucida glycoprotein mZP3 with sperm protein sp56 during fertilization in mice. , 2001, The International journal of developmental biology.

[272]  D. Clapham,et al.  All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility , 2007, Proceedings of the National Academy of Sciences.

[273]  D. H. Kim,et al.  Identification of heat shock protein 5, calnexin and integral membrane protein 2B as Adam7‐interacting membrane proteins in mouse sperm , 2011, Journal of cellular physiology.

[274]  R. Harrison,et al.  Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. , 1990, Journal of reproduction and fertility.

[275]  N. Okamura,et al.  Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. , 1985, The Journal of biological chemistry.

[276]  P. Wassarman,et al.  Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat. , 1985, Journal of molecular biology.

[277]  J. Gatti,et al.  Characterization and identification of proteins secreted in the various regions of the adult boar epididymis. , 1996, Biology of reproduction.

[278]  B. N. Day,et al.  Proteasomal Interference Prevents Zona Pellucida Penetration and Fertilization in Mammals1 , 2004, Biology of reproduction.

[279]  E. Boja,et al.  Structural Characterization of Native Mouse Zona Pellucida Proteins Using Mass Spectrometry* , 2003, Journal of Biological Chemistry.

[280]  C. Foresta,et al.  Evidence for the involvement of sperm angiotensin converting enzyme in fertilization. , 1991, International journal of andrology.

[281]  Matthew D. Dun,et al.  The Chaperonin Containing TCP1 Complex (CCT/TRiC) Is Involved in Mediating Sperm-Oocyte Interaction , 2011, The Journal of Biological Chemistry.

[282]  J. Calvete,et al.  Immunohistochemical localization of spermadhesin AWN in the porcine male genital tract , 1995, Cell and Tissue Research.

[283]  R. Naz,et al.  Characterization of a membrane antigen from rabbit testis and sperm isolated by using monoclonal antibodies and effect of its antiserum on fertility. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[284]  J. Calvete,et al.  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. , 1995, Biological chemistry Hoppe-Seyler.

[285]  T. Motyl,et al.  Matrix metalloproteinase-2 involvement in breast cancer progression: a mini-review. , 2009, Medical science monitor : international medical journal of experimental and clinical research.

[286]  W. Swanson,et al.  Molecular population genetics of the gene encoding the human fertilization protein zonadhesin reveals rapid adaptive evolution. , 2006, American journal of human genetics.

[287]  Kazuo Yamagata,et al.  Sperm from the calmegin-deficient mouse have normal abilities for binding and fusion to the egg plasma membrane. , 2002, Developmental biology.

[288]  S. Suarez,et al.  Characterization of the Intracellular Calcium Store at the Base of the Sperm Flagellum That Regulates Hyperactivated Motility1 , 2003, Biology of reproduction.

[289]  P. Wassarman,et al.  Structure of the mouse egg extracellular coat, the zona pellucida. , 1991, International review of cytology.

[290]  G. Gerton,et al.  The sperm acrosomal matrix contains a novel member of the pentaxin family of calcium-dependent binding proteins. , 1994, The Journal of biological chemistry.

[291]  M. Wade,et al.  Acquisition of Arylsulfatase A onto the Mouse Sperm Surface During Epididymal Transit1 , 2003, Biology of reproduction.

[292]  A. Chenn,et al.  Activity of the β-catenin phosphodestruction complex at cell–cell contacts is enhanced by cadherin-based adhesion , 2009, The Journal of cell biology.

[293]  G. Hunnicutt,et al.  Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. , 1996, Biology of reproduction.

[294]  A. Shevchenko,et al.  Resistance of cell membranes to different detergents , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[295]  B. Hille,et al.  Identical Phenotypes of CatSper1 and CatSper2 Null Sperm* , 2005, Journal of Biological Chemistry.

[296]  G. Schatten,et al.  Membrane trafficking machinery components associated with the mammalian acrosome during spermiogenesis. , 2001, Experimental cell research.

[297]  T. Baba,et al.  Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. , 1994, The Journal of biological chemistry.

[298]  H. Koistinen,et al.  Zona-Binding Inhibitory Factor-1 from Human Follicular Fluid Is an Isoform of Glycodelin1 , 2003, Biology of reproduction.

[299]  B. Nixon,et al.  Rabbit Epididymal Secretory Proteins. I. Characterization and Hormonal Regulation1 , 2002, Biology of reproduction.

[300]  D. Klenerman,et al.  Supramolecular organization of the sperm plasma membrane during maturation and capacitation. , 2007, Asian journal of andrology.

[301]  J. Bedford.  Changes in fine structure of the rabbit sperm head during passage through the epididymis. , 1965, Journal of anatomy.

[302]  Wei Yan,et al.  Catsper3 and Catsper4 Are Essential for Sperm Hyperactivated Motility and Male Fertility in the Mouse1 , 2007, Biology of reproduction.

[303]  G. Christman,et al.  Fertilization antigen-1 removes antisperm autoantibodies from spermatozoa of infertile men and results in increased rates of acrosome reaction. , 1999, Fertility and sterility.

[304]  R. Sullivan,et al.  Polyol pathway along the bovine epididymis , 2004, Molecular reproduction and development.

[305]  M. Buffone,et al.  The role of the acrosomal matrix in fertilization. , 2008, The International journal of developmental biology.

[306]  D. Carrier,et al.  Sperm capacitation induces an increase in lipid rafts having zona pellucida binding ability and containing sulfogalactosylglycerolipid. , 2006, Developmental biology.

[307]  L. Neckers,et al.  Functional proteomic screens reveal an essential extracellular role for hsp90α in cancer cell invasiveness , 2004, Nature Cell Biology.

[308]  P. Wassarman,et al.  Mammalian fertilization: the strange case of sperm protein 56 , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[309]  J. Langlais,et al.  Identification of sterol acceptors that stimulate cholesterol efflux from human spermatozoa during in vitro capacitation. , 1988, Gamete research.

[310]  D. Clapham,et al.  Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel , 2006, Nature.

[311]  V. Winfrey,et al.  Characterization of two antigenically related integral membrane proteins of the guinea pig sperm periacrosomal plasma membrane , 1994, Molecular reproduction and development.

[312]  D. Johnston,et al.  Identification of epididymis-specific transcripts in the mouse and rat by transcriptional profiling. , 2007, Asian journal of andrology.

[313]  M. Kates,et al.  Levels of sulfogalactosylglycerolipid in capacitated motile and immotile mouse spermatozoa. , 1990, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[314]  L. Levin,et al.  Kinetic Properties of “Soluble” Adenylyl Cyclase , 2003, The Journal of Biological Chemistry.

[315]  R. Naz,et al.  Recombinant fertilization antigen-1 causes a contraceptive effect in actively immunized mice. , 1998, Biology of reproduction.

[316]  I. Vattulainen,et al.  Interplay of unsaturated phospholipids and cholesterol in membranes: effect of the double-bond position. , 2008, Biophysical journal.

[317]  D. Tulsiani,et al.  Novel alpha-D-mannosidase of rat sperm plasma membranes: characterization and potential role in sperm-egg interactions , 1989, The Journal of cell biology.

[318]  S. Tsuboi,et al.  Core 2 oligosaccharide biosynthesis distinguishes between selectin ligands essential for leukocyte homing and inflammation. , 1998, Immunity.

[319]  D. Clapham,et al.  A voltage-gated ion channel expressed specifically in spermatozoa , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[320]  N. Cormier,et al.  Role of zonadhesin during sperm-egg interaction: a species-specific acrosomal molecule with multiple functions. , 2011, Molecular human reproduction.

[321]  G. Kopf,et al.  Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. , 1995, Development.

[322]  S. Nagdas,et al.  Purification and characterization of rat epididymal-fluid alpha-D-mannosidase: similarities to sperm plasma-membrane alpha-D-mannosidase. , 1993, Biochemical Journal.

[323]  M. Kong,et al.  Participation of the sperm proteasome in human fertilization. , 2003, Human reproduction.

[324]  R. Bucala,et al.  Purification and Characterization of Macrophage Migration Inhibitory Factor as a Secretory Protein from Rat Epididymis: Evidences for Alternative Release and Transfer to Spermatozoa , 2001, Molecular medicine.

[325]  B. Shur,et al.  A role for mouse sperm surface galactosyltransferase in sperm binding to the egg zona pellucida , 1982, The Journal of cell biology.

[326]  J. Dean.  Reassessing the molecular biology of sperm-egg recognition with mouse genetics. , 2004, BioEssays : news and reviews in molecular, cellular and developmental biology.

[327]  G. Hunnicutt,et al.  Structural relationship of sperm soluble hyaluronidase to the sperm membrane protein PH-20. , 1996, Biology of reproduction.

[328]  R. Sullivan,et al.  Polyol pathway in human epididymis and semen. , 2006, Journal of andrology.

[329]  B. Robaire,et al.  Dynamic Changes in Gene Expression along the Rat Epididymis1 , 2001, Biology of reproduction.

[330]  R. Aitken,et al.  New insights into the molecular mechanisms of sperm-egg interaction , 2007, Cellular and Molecular Life Sciences.

[331]  J. Kirkman-Brown,et al.  Ca2+-stores in sperm: their identities and functions. , 2009, Reproduction.

[332]  A. Petrunkina,et al.  Dynamic quantification of the tyrosine phosphorylation of the sperm surface proteins during capacitation , 2006, Cytometry. Part A : the journal of the International Society for Analytical Cytology.

[333]  West Ap,et al.  Brefeldin A and mannose 6-phosphate regulation of acrosomic related vesicular trafficking. , 1996 .

[334]  D. Cyr,et al.  Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 1: Background to spermatogenesis, spermatogonia, and spermatocytes , 2010, Microscopy research and technique.

[335]  D. G. Rooij.  Proliferation and differentiation of spermatogonial stem cells , 2001 .

[336]  H. Reiss.  Population study of causes, treatment and outcome of infertility. , 1986, British medical journal.