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PMID: 30105226 Published · epublish English Journal Article Review

Molecular Basis of Human Sperm Capacitation.

Frontiers in cell and developmental biology ·Vol. 6 ·2018-00-00 ·Pages 72

Puga Molina LC, Luque GM, Balestrini PA, Marín-Briggiler CI, Romarowski A, Buffone MG

Abstract

In the early 1950s, Austin and Chang independently described the changes that are required for the sperm to fertilize oocytes in vivo. These changes were originally grouped under name of "capacitation" and were the first step in the development of in vitro fertilization (IVF) in humans. Following these initial and fundamental findings, a remarkable number of observations led to characterization of the molecular steps behind this process. The discovery of certain sperm-specific molecules and the possibility to record ion currents through patch-clamp approaches helped to integrate the initial biochemical observation with the activity of ion channels. This is of particular importance in the male gamete due to the fact that sperm are transcriptionally inactive. Therefore, sperm must control all these changes that occur during their transit through the male and female reproductive tracts by complex signaling cascades that include post-translational modifications. This review is focused on the principal molecular mechanisms that govern human sperm capacitation with particular emphasis on comparing all the reported pieces of evidence with the mouse model.

Keywords
acrosomal exocytosis capacitation fertilization human sperm hyperactivation
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Puga Molina Lis C
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
Luque Guillermina M
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
Balestrini Paula A
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
Marín-Briggiler Clara I
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
Romarowski Ana
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
Buffone Mariano G
Instituto de Biología y Medicina Experimental, Consejo Nacional de Investigaciones Científicas y Tecnológicas, Buenos Aires, Argentina.
References (349)
349 references, click to expand
  1. Molecular mechanism for human sperm chemotaxis mediated by progesterone.
    PLoS One. 2009 Dec 08;4(12):e8211 PMID: 19997608
  2. pH regulation in mouse sperm: identification of Na(+)-, Cl(-)-, and HCO3(-)-dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation.
    Dev Biol. 1996 Feb 1;173(2):510-20 PMID: 8606009
  3. Isolation and characterization of human plasma lipid transfer proteins.
    Arteriosclerosis. 1984 Jan-Feb;4(1):49-58 PMID: 6691846
  4. Ca2+ signalling in the control of motility and guidance in mammalian sperm.
    Front Biosci. 2008 May 01;13:5623-37 PMID: 18508611
  5. Different expression and activity of the alpha1 and alpha4 isoforms of the Na,K-ATPase during rat male germ cell ontogeny.
    Reproduction. 2005 Nov;130(5):627-41 PMID: 16264093
  6. Phosphorylation-regulated Cl- channel in CHO cells stably expressing the cystic fibrosis gene.
    Nature. 1991 Aug 15;352(6336):628-31 PMID: 1714039
  7. The physiology of bicarbonate transporters in mammalian reproduction.
    Biol Reprod. 2012 Apr 05;86(4):99 PMID: 22262691
  8. Hyperactivated sperm motility driven by CatSper2 is required for fertilization.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14869-74 PMID: 14657366
  9. A new sperm-specific Na+/H+ exchanger required for sperm motility and fertility.
    Nat Cell Biol. 2003 Dec;5(12):1117-22 PMID: 14634667
  10. Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation.
    Dev Biol. 1996 Nov 25;180(1):284-96 PMID: 8948591
  11. Analysis of the direct effects of prostaglandins on human sperm function.
    J Reprod Fertil. 1985 Jan;73(1):139-46 PMID: 3855460
  12. A high activity carbonic anhydrase isoenzyme (CA II) is present in mammalian spermatozoa.
    Histochemistry. 1991;95(5):477-82 PMID: 1907954
  13. A 31P NMR study of the epididymis and epididymal sperm of the bull and hamster.
    Biol Reprod. 1985 Dec;33(5):1029-40 PMID: 4074801
  14. Fertilization of rabbit ova in vitro.
    Nature. 1959 Aug 8;184(Suppl 7):466-7 PMID: 13809155
  15. Capacitation-associated protein tyrosine phosphorylation and membrane fluidity changes are impaired in the spermatozoa of asthenozoospermic patients.
    Reproduction. 2005 Jun;129(6):697-705 PMID: 15923385
  16. ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization.
    J Cell Biol. 1996 Aug;134(3):637-45 PMID: 8707844
  17. Segregation of micron-scale membrane sub-domains in live murine sperm.
    J Cell Physiol. 2006 Mar;206(3):636-46 PMID: 16222699
  18. ATPases, ion exchangers and human sperm motility.
    Reproduction. 2015 May;149(5):475-84 PMID: 25820902
  19. Phosphorus-31 nuclear magnetic resonance studies of spermatozoa from the boar, ram, goat and bull.
    Comp Biochem Physiol B. 1987;87(2):285-96 PMID: 3621898
  20. Direct action of endocrine disrupting chemicals on human sperm.
    EMBO Rep. 2014 Jul;15(7):758-65 PMID: 24820036
  21. Ion channels, phosphorylation and mammalian sperm capacitation.
    Asian J Androl. 2011 May;13(3):395-405 PMID: 21540868
  22. Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation.
    J Biol Chem. 2003 Feb 28;278(9):7001-9 PMID: 12496293
  23. SLO3 K+ channels control calcium entry through CATSPER channels in sperm.
    J Biol Chem. 2014 Nov 14;289(46):32266-75 PMID: 25271166
  24. Inwardly rectifying K(+) channels in spermatogenic cells: functional expression and implication in sperm capacitation.
    Dev Biol. 2001 Jun 1;234(1):261-74 PMID: 11356034
  25. Levels of cholesterol and phospholipids in freshly ejaculated sperm and Percoll-gradient-pelletted sperm from fertile and unexplained infertile men.
    Fertil Steril. 1991 Apr;55(4):820-7 PMID: 2010008
  26. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure.
    Physiol Rev. 2002 Jul;82(3):735-67 PMID: 12087134
  27. Intracellular pH regulates bovine sperm motility and protein phosphorylation.
    Biol Reprod. 1989 Nov;41(5):907-20 PMID: 2624855
  28. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm.
    FEBS Lett. 2001 Nov 30;509(1):119-25 PMID: 11734218
  29. Classification of mouse sperm motility patterns using an automated multiclass support vector machines model.
    Biol Reprod. 2011 Jun;84(6):1207-15 PMID: 21349820
  30. In vivo oxygen, temperature and pH dynamics in the female reproductive tract and their importance in human conception: a systematic review.
    Hum Reprod Update. 2018 Jan 1;24(1):15-34 PMID: 29077897
  31. Intracellular pH of bovine sperm increases during capacitation.
    Mol Reprod Dev. 1995 Apr;40(4):490-502 PMID: 7598914
  32. Cholesteryl sulfate and sterol sulfatase in the human reproductive tract.
    Steroids. 1976 Feb;27(2):247-60 PMID: 1273889
  33. Tissue-inherent fate of GPI revealed by GPI-anchored GFP transgenesis.
    FEBS Lett. 1999 Sep 24;458(3):299-303 PMID: 10570928
  34. The cell biology of mammalian fertilization.
    Development. 2013 Nov;140(22):4471-9 PMID: 24194470
  35. A genetic variant of the sperm-specific SLO3 K+ channel has altered pH and Ca2+ sensitivities.
    J Biol Chem. 2017 May 26;292(21):8978-8987 PMID: 28377504
  36. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization.
    Dev Cell. 2005 Aug;9(2):249-59 PMID: 16054031
  37. Purification and characterization of a human follicular fluid lipid transfer protein that stimulates human sperm capacitation.
    Biol Reprod. 1992 Dec;47(6):1126-33 PMID: 1493178
  38. Cholesterol and desmosterol in two sperm populations separated on Sil-Select gradient.
    Int J Androl. 2010 Jun 1;33(3):528-35 PMID: 19490187
  39. Action of steroids and plant triterpenoids on CatSper Ca2+ channels in human sperm.
    Proc Natl Acad Sci U S A. 2018 Jan 16;115(3):E344-E346 PMID: 29305558
  40. Effect of 2',4'-dichlorobenzamil hydrochloride, a Na(+)-Ca(2+) exchange inhibitor, on human spermatozoa.
    Eur J Pharmacol. 2001 Apr 20;418(1-2):153-5 PMID: 11334878
  41. Ion permeabilities in mouse sperm reveal an external trigger for SLO3-dependent hyperpolarization.
    PLoS One. 2013;8(4):e60578 PMID: 23577126
  42. Characterization of CA XIII, a novel member of the carbonic anhydrase isozyme family.
    J Biol Chem. 2004 Jan 23;279(4):2719-27 PMID: 14600151
  43. Dynamics of SNARE assembly and disassembly during sperm acrosomal exocytosis.
    PLoS Biol. 2005 Oct;3(10):e323 PMID: 16131227
  44. Post-translational cleavage of Hv1 in human sperm tunes pH- and voltage-dependent gating.
    J Physiol. 2017 Mar 1;595(5):1533-1546 PMID: 27859356
  45. Role of cholesterol in sperm capacitation.
    Biol Reprod. 1998 Jul;59(1):7-11 PMID: 9674986
  46. Signaling in Sperm: More Different than Similar.
    Trends Cell Biol. 2017 Feb;27(2):101-109 PMID: 27825709
  47. New insights into the regulation of cholesterol efflux from the sperm membrane.
    Asian J Androl. 2015 Jul-Aug;17(4):561-7 PMID: 25926609
  48. Genetic male infertility and mutation of CATSPER ion channels.
    Eur J Hum Genet. 2010 Nov;18(11):1178-84 PMID: 20648059
  49. Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex.
    PLoS One. 2008 Aug 22;3(8):e3040 PMID: 18725941
  50. Regulation of the cystic fibrosis transmembrane conductance regulator Cl- channel by specific protein kinases and protein phosphatases.
    J Biol Chem. 1993 Jan 25;268(3):2037-47 PMID: 7678414
  51. Ca2+ uptake during capacitation of mouse spermatozoa and the effect of an anion transport inhibitor on Ca2+ uptake.
    Mol Reprod Dev. 1990 May;26(1):63-8 PMID: 2112006
  52. A sperm-specific Na+/H+ exchanger (sNHE) is critical for expression and in vivo bicarbonate regulation of the soluble adenylyl cyclase (sAC).
    Proc Natl Acad Sci U S A. 2007 May 29;104(22):9325-30 PMID: 17517652
  53. Structure and Function of SLC4 Family [Formula: see text] Transporters.
    Front Physiol. 2015 Dec 01;6:355 PMID: 26648873
  54. Internal pH of human spermatozoa: effect of ions, human follicular fluid and progesterone.
    Mol Hum Reprod. 1996 Apr;2(4):219-24 PMID: 9238683
  55. A flagellar K(+)-dependent Na(+)/Ca(2+) exchanger keeps Ca(2+) low in sea urchin spermatozoa.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):6743-8 PMID: 12011436
  56. Ca(v)2.3 (alpha1E) Ca2+ channel participates in the control of sperm function.
    FEBS Lett. 2002 Apr 10;516(1-3):229-33 PMID: 11959138
  57. Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm.
    J Biol Chem. 2006 Mar 3;281(9):5623-33 PMID: 16407190
  58. Isoforms of the alpha subunit of Na,K-ATPase and their significance.
    Acta Physiol Scand Suppl. 1992;607:161-9 PMID: 1333149
  59. Control of human sperm intracellular pH by cholesterol and its relationship to the response of the acrosome to progesterone.
    Biol Reprod. 1997 May;56(5):1169-74 PMID: 9160715
  60. CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm.
    Proc Natl Acad Sci U S A. 2003 Dec 9;100(25):14864-8 PMID: 14657352
  61. Role of zinc in fertility and fecundity in the rat.
    Am J Physiol. 1958 Jun;193(3):505-8 PMID: 13533583
  62. Flow cytometry analysis reveals a decrease in intracellular sodium during sperm capacitation.
    J Cell Sci. 2012 Jan 15;125(Pt 2):473-85 PMID: 22302997
  63. Frequency of CFTR gene mutations in males participating in an ICSI programme.
    Hum Reprod. 1999 Jul;14(7):1833-4 PMID: 10402399
  64. Calcium requirements for human sperm function in vitro.
    Fertil Steril. 2003 Jun;79(6):1396-403 PMID: 12798888
  65. A novel gene required for male fertility and functional CATSPER channel formation in spermatozoa.
    Nat Commun. 2011 Jan 11;2:153 PMID: 21224844
  66. PGAP1 knock-out mice show otocephaly and male infertility.
    J Biol Chem. 2007 Oct 19;282(42):30373-80 PMID: 17711852
  67. Stimulation of human sperm capacitation by purified lipid transfer protein.
    J Exp Zool. 1995 May 1;272(1):78-83 PMID: 7738519
  68. Voltage-dependent calcium influx in human sperm assessed by simultaneous optical detection of intracellular calcium and membrane potential.
    Biochim Biophys Acta. 1998 Jun 24;1372(1):1-12 PMID: 9651467
  69. A-kinase anchoring proteins: from protein complexes to physiology and disease.
    IUBMB Life. 2009 Apr;61(4):394-406 PMID: 19319965
  70. Sperm membrane physiology and relevance for fertilization.
    Anim Reprod Sci. 2008 Sep;107(3-4):229-36 PMID: 18556155
  71. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel.
    Nature. 2006 Feb 9;439(7077):737-40 PMID: 16467839
  72. A review of the physical and chemical properties of human semen and the formulation of a semen simulant.
    J Androl. 2005 Jul-Aug;26(4):459-69 PMID: 15955884
  73. Anion exchanger 2 is essential for spermiogenesis in mice.
    Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):15847-52 PMID: 14673081
  74. Demonstration that CFTR is a chloride channel by alteration of its anion selectivity.
    Science. 1991 Jul 12;253(5016):202-5 PMID: 1712984
  75. Acidification of epididymal fluid in the boar.
    Int J Androl. 1990 Jun;13(3):238-43 PMID: 2387644
  76. Inhibition of Ser/Thr phosphatases induces capacitation-associated signaling in the presence of Src kinase inhibitors.
    J Biol Chem. 2010 Mar 12;285(11):7977-85 PMID: 20068039
  77. Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. Induction of [Ca(2+)](i) oscillations and cyclical transitions in flagellar beating.
    J Biol Chem. 2004 Oct 29;279(44):46315-25 PMID: 15322137
  78. Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm.
    J Cell Biol. 1998 Jul 27;142(2):473-84 PMID: 9679145
  79. Human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist, progesterone: cholesterol is the major inhibitor.
    Biol Reprod. 1996 Jan;54(1):138-45 PMID: 8838010
  80. Discrete regional distributions suggest diverse functional roles of calcium channel alpha1 subunits in sperm.
    Dev Biol. 1999 Mar 15;207(2):457-69 PMID: 10068476
  81. Intracellular pH in sperm physiology.
    Biochem Biophys Res Commun. 2014 Aug 1;450(3):1149-58 PMID: 24887564
  82. Capacitation-associated changes in protein tyrosine phosphorylation, hyperactivation and acrosome reaction in hamster spermatozoa.
    Andrologia. 2001 Mar;33(2):95-104 PMID: 11350373
  83. Ca(2+)/CaM-dependent kinases: from activation to function.
    Annu Rev Pharmacol Toxicol. 2001;41:471-505 PMID: 11264466
  84. The SLO3 sperm-specific potassium channel plays a vital role in male fertility.
    FEBS Lett. 2010 Mar 5;584(5):1041-6 PMID: 20138882
  85. Semi-automatized segmentation method using image-based flow cytometry to study sperm physiology: the case of capacitation-induced tyrosine phosphorylation.
    Mol Hum Reprod. 2018 Feb 1;24(2):64-73 PMID: 29186618
  86. Calcium regulation of the soluble adenylyl cyclase expressed in mammalian spermatozoa.
    Proc Natl Acad Sci U S A. 2003 Sep 16;100(19):10676-81 PMID: 12958208
  87. The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm.
    Nature. 2011 Mar 17;471(7338):382-6 PMID: 21412338
  88. Ca2+ ionophore A23187 can make mouse spermatozoa capable of fertilizing in vitro without activation of cAMP-dependent phosphorylation pathways.
    Proc Natl Acad Sci U S A. 2013 Nov 12;110(46):18543-8 PMID: 24128762
  89. Observations on the penetration of the sperm in the mammalian egg.
    Aust J Sci Res B. 1951 Nov;4(4):581-96 PMID: 14895481
  90. Participation of the Cl-/HCO(3)- exchangers SLC26A3 and SLC26A6, the Cl- channel CFTR, and the regulatory factor SLC9A3R1 in mouse sperm capacitation.
    Biol Reprod. 2012 Jan 19;86(1):1-14 PMID: 21976599
  91. Transient exposure to calcium ionophore enables in vitro fertilization in sterile mouse models.
    Sci Rep. 2016 Sep 15;6:33589 PMID: 27627854
  92. Function of calmodulin in mammalian sperm: presence of a calmodulin-dependent cyclic nucleotide phosphodiesterase associated with demembranated rat caudal epididymal sperm.
    Biochem Biophys Res Commun. 1984 Jan 30;118(2):636-42 PMID: 6322756
  93. Gating of CFTR by the STAS domain of SLC26 transporters.
    Nat Cell Biol. 2004 Apr;6(4):343-50 PMID: 15048129
  94. Phosphoproteome analysis of capacitated human sperm. Evidence of tyrosine phosphorylation of a kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation.
    J Biol Chem. 2003 Mar 28;278(13):11579-89 PMID: 12509440
  95. Blockade of epithelial sodium channels improves sperm motility in asthenospermia patients.
    Int J Androl. 2009 Aug;32(4):330-6 PMID: 18298571
  96. Mouse sperm K+ currents stimulated by pH and cAMP possibly coded by Slo3 channels.
    Biochem Biophys Res Commun. 2009 Apr 3;381(2):204-9 PMID: 19338774
  97. Characterization of Ca2+ uptake by guinea pig epididymal spermatozoa.
    Biol Reprod. 1987 Dec;37(5):1097-107 PMID: 3442689
  98. Hyperactivated sperm progress in the mouse oviduct.
    Biol Reprod. 1992 May;46(5):779-85 PMID: 1591334
  99. The epithelial Na+ channel: cell surface insertion and retrieval in Na+ homeostasis and hypertension.
    Endocr Rev. 2002 Apr;23(2):258-75 PMID: 11943747
  100. The functional role of beta subunits in oligomeric P-type ATPases.
    J Bioenerg Biomembr. 2001 Oct;33(5):425-38 PMID: 11762918
  101. 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
  102. Bovine oviductal fluid components and their potential role in sperm cholesterol efflux.
    Mol Reprod Dev. 1990 Feb;25(2):195-204 PMID: 2310569
  103. Fibroblast growth factor 2 (FGF2) is present in human spermatozoa and is related with sperm motility. The use of recombinant FGF2 to improve motile sperm recovery.
    Andrology. 2017 Sep;5(5):990-998 PMID: 28732140
  104. Ca2+ bursts occur around a local minimal concentration of attractant and trigger sperm chemotactic response.
    Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19312-7 PMID: 19047630
  105. Timing of CFTR pore opening and structure of its transition state.
    Cell. 2015 Oct 22;163(3):724-33 PMID: 26496611
  106. Isozymes of the Na-K-ATPase: heterogeneity in structure, diversity in function.
    Am J Physiol. 1998 Nov;275(5 Pt 2):F633-50 PMID: 9815123
  107. The CatSper channel: a polymodal chemosensor in human sperm.
    EMBO J. 2012 Apr 4;31(7):1654-65 PMID: 22354039
  108. ENaC is inhibited by an increase in the intracellular Cl(-) concentration mediated through activation of Cl(-) channels.
    Pflugers Arch. 2003 Jan;445(4):504-12 PMID: 12548397
  109. Fertilization potential in vitro is correlated with head-specific mannose-ligand receptor expression, acrosome status and membrane cholesterol content.
    Hum Reprod. 1993 Dec;8(12):2155-66 PMID: 8150918
  110. Regulation of the human sperm tyrosine kinase c-yes. Activation by cyclic adenosine 3',5'-monophosphate and inhibition by Ca(2+).
    Biol Reprod. 2002 Jul;67(1):301-7 PMID: 12080032
  111. Seminal vesicle protein SVS2 is required for sperm survival in the uterus.
    Proc Natl Acad Sci U S A. 2014 Mar 18;111(11):4145-50 PMID: 24591616
  112. Hv1 proton channels are required for high-level NADPH oxidase-dependent superoxide production during the phagocyte respiratory burst.
    Proc Natl Acad Sci U S A. 2009 May 5;106(18):7642-7 PMID: 19372380
  113. Plasma membrane Ca2+ ATPase 4 is required for sperm motility and male fertility.
    J Biol Chem. 2004 Jul 2;279(27):28220-6 PMID: 15078889
  114. Molecular cloning of a new sodium bicarbonate cotransporter cDNA from human retina.
    Biochem Biophys Res Commun. 1998 May 19;246(2):535-8 PMID: 9610397
  115. 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
  116. FERTILIZATION OF HAMSTER EGGS IN VITRO.
    Nature. 1963 Oct 19;200:281-2 PMID: 14085061
  117. Structurally distinct Ca(2+) signaling domains of sperm flagella orchestrate tyrosine phosphorylation and motility.
    Cell. 2014 May 8;157(4):808-22 PMID: 24813608
  118. Src Kinase Is the Connecting Player between Protein Kinase A (PKA) Activation and Hyperpolarization through SLO3 Potassium Channel Regulation in Mouse Sperm.
    J Biol Chem. 2015 Jul 24;290(30):18855-64 PMID: 26060254
  119. An adhesion-associated agonist from the zona pellucida activates G protein-promoted elevations of internal Ca2+ and pH that mediate mammalian sperm acrosomal exocytosis.
    Dev Biol. 1989 Sep;135(1):133-46 PMID: 2504631
  120. Patch clamp studies of human sperm under physiological ionic conditions reveal three functionally and pharmacologically distinct cation channels.
    Mol Hum Reprod. 2014 May;20(5):392-408 PMID: 24442342
  121. A plethora of interacting organellar Ca2+ stores.
    Curr Opin Cell Biol. 2005 Apr;17(2):135-40 PMID: 15780589
  122. Development changes occurring in the lipids of ram epididymal spermatozoa plasma membrane.
    Biol Reprod. 1985 Apr;32(3):653-68 PMID: 3158356
  123. A novel neuronal calcium sensor family protein, calaxin, is a potential Ca(2+)-dependent regulator for the outer arm dynein of metazoan cilia and flagella.
    Biol Cell. 2009 Feb;101(2):91-103 PMID: 18620543
  124. Calcium signaling.
    Cell. 2007 Dec 14;131(6):1047-58 PMID: 18083096
  125. Biphasic role of calcium in mouse sperm capacitation signaling pathways.
    J Cell Physiol. 2015 Aug;230(8):1758-1769 PMID: 25597298
  126. Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation.
    J Biol Chem. 2007 Aug 17;282(33):24397-406 PMID: 17588945
  127. Lipids of plasma membrane and outer acrosomal membrane from bovine spermatozoa.
    Biol Reprod. 1987 Dec;37(5):1249-58 PMID: 2832008
  128. Mouse models for genes involved in impaired spermatogenesis.
    Int J Androl. 2006 Feb;29(1):76-89; discussion 105-8 PMID: 16466527
  129. Slo3, a novel pH-sensitive K+ channel from mammalian spermatocytes.
    J Biol Chem. 1998 Feb 6;273(6):3509-16 PMID: 9452476
  130. Molecular basis of bicarbonate membrane transport in the male reproductive tract.
    Curr Med Chem. 2013;20(32):4037-49 PMID: 23931280
  131. CaV2.2 and CaV2.3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm.
    J Biol Chem. 2000 Jul 14;275(28):21210-7 PMID: 10791962
  132. p,p'-DDE activates CatSper and compromises human sperm function at environmentally relevant concentrations.
    Hum Reprod. 2013 Dec;28(12):3167-77 PMID: 24067601
  133. 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
  134. External ionic conditions, internal pH and motility of ram and boar spermatozoa.
    J Reprod Fertil. 1993 Jul;98(2):439-49 PMID: 8410809
  135. A detrimental effect of seminal plasma on the fertilizing capacity of sperm.
    Nature. 1957 Feb 2;179(4553):258-9 PMID: 13407696
  136. Progesterone activates the principal Ca2+ channel of human sperm.
    Nature. 2011 Mar 17;471(7338):387-91 PMID: 21412339
  137. Biophysical properties of the voltage gated proton channel H(V)1.
    Wiley Interdiscip Rev Membr Transp Signal. 2012 Sep 1;1(5):605-620 PMID: 23050239
  138. Prolonged survival of human sperm in chemically defined media at room temperatures.
    Nature. 1960 Nov 26;188:760 PMID: 13729568
  139. Central role of soluble adenylyl cyclase and cAMP in sperm physiology.
    Biochim Biophys Acta. 2014 Dec;1842(12 Pt B):2610-20 PMID: 25066614
  140. Membrane hyperpolarization during human sperm capacitation.
    Mol Hum Reprod. 2014 Jul;20(7):619-29 PMID: 24737063
  141. The tyrosine kinase FER is responsible for the capacitation-associated increase in tyrosine phosphorylation in murine sperm.
    Development. 2016 Jul 1;143(13):2325-33 PMID: 27226326
  142. Stimulation of protein tyrosine phosphorylation by platelet-activating factor and progesterone in human spermatozoa.
    Mol Cell Endocrinol. 1995 Feb 27;108(1-2):35-42 PMID: 7758838
  143. Carbonic anhydrase VII is S-glutathionylated without loss of catalytic activity and affinity for sulfonamide inhibitors.
    Bioorg Med Chem Lett. 2012 Feb 15;22(4):1560-4 PMID: 22277279
  144. Expression of antimicrobial defensins in the male reproductive tract of rats, mice, and humans.
    Biol Reprod. 2003 Jan;68(1):95-104 PMID: 12493700
  145. Green fluorescence protein driven by the Na,K-ATPase α4 isoform promoter is expressed only in male germ cells of mouse testis.
    J Assist Reprod Genet. 2012 Dec;29(12):1313-25 PMID: 23229519
  146. Ion channels in sperm physiology.
    Physiol Rev. 1999 Apr;79(2):481-510 PMID: 10221988
  147. Primary structure of a sperm cell anion exchanger and its messenger ribonucleic acid expression during spermatogenesis.
    Biol Reprod. 1999 Oct;61(4):981-6 PMID: 10491633
  148. Decreased protein tyrosine phosphorylation and membrane fluidity in spermatozoa from infertile men with varicocele.
    Mol Reprod Dev. 2006 Dec;73(12):1591-9 PMID: 16897700
  149. CCR6 is required for ligand-induced CatSper activation in human sperm.
    Oncotarget. 2017 Sep 5;8(53):91445-91458 PMID: 29207656
  150. Diacylglycerol stimulates acrosomal exocytosis by feeding into a PKC- and PLD1-dependent positive loop that continuously supplies phosphatidylinositol 4,5-bisphosphate.
    Biochim Biophys Acta. 2012 Sep;1821(9):1186-99 PMID: 22609963
  151. The movement of golden hamster spermatozoa before and after capacitation.
    J Reprod Fertil. 1970 Oct;23(1):193-6 PMID: 5472441
  152. Localization of sodium bicarbonate cotransporter (NBC) protein and messenger ribonucleic acid in rat epididymis.
    Biol Reprod. 1999 Mar;60(3):573-9 PMID: 10026101
  153. Behavior of Mouse Spermatozoa in the Female Reproductive Tract from Soon after Mating to the Beginning of Fertilization.
    Biol Reprod. 2016 Apr;94(4):80 PMID: 26962112
  154. A new prostaglandin E receptor mediates calcium influx and acrosome reaction in human spermatozoa.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3008-13 PMID: 9501206
  155. Picomolar gradients of progesterone select functional human sperm even in subfertile samples.
    Mol Hum Reprod. 2013 Sep;19(9):559-69 PMID: 23729411
  156. Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation.
    J Cell Sci. 2004 Jan 15;117(Pt 2):211-22 PMID: 14676274
  157. Bicarbonate secretion: it takes two to tango.
    Nat Cell Biol. 2004 Apr;6(4):292-4 PMID: 15057243
  158. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa.
    J Androl. 1991 Sep-Oct;12(5):323-30 PMID: 1765568
  159. Involvement of protein kinase A and A kinase anchoring protein in the progesterone-initiated human sperm acrosome reaction.
    Biol Reprod. 2000 Mar;62(3):811-20 PMID: 10684828
  160. Regulation and roles of Ca2+ stores in human sperm.
    Reproduction. 2015 Aug;150(2):R65-76 PMID: 25964382
  161. Intracellular calcium store depletion and acrosome reaction in human spermatozoa: role of calcium and plasma membrane potential.
    Mol Hum Reprod. 2001 Feb;7(2):119-28 PMID: 11160837
  162. Ion channels that control fertility in mammalian spermatozoa.
    Int J Dev Biol. 2008;52(5-6):607-13 PMID: 18649274
  163. CATSPER2, a human autosomal nonsyndromic male infertility gene.
    Eur J Hum Genet. 2003 Jul;11(7):497-502 PMID: 12825070
  164. Secretory pathway Ca(2+)-ATPase (SPCA1) Ca(2)+ pumps, not SERCAs, regulate complex [Ca(2+)](i) signals in human spermatozoa.
    J Cell Sci. 2005 Apr 15;118(Pt 8):1673-85 PMID: 15811949
  165. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):79-84 PMID: 9874775
  166. A novel, single, transmembrane protein CATSPERG is associated with CATSPER1 channel protein.
    Biol Reprod. 2009 Sep;81(3):539-44 PMID: 19516020
  167. CatSperζ regulates the structural continuity of sperm Ca2+ signaling domains and is required for normal fertility.
    Elife. 2017 Feb 23;6: PMID: 28226241
  168. An essential role for the extracellular domain of the Na,K-ATPase beta-subunit in cation occlusion.
    Biochemistry. 1993 Jul 6;32(26):6737-43 PMID: 8392370
  169. Strontium supports human sperm capacitation but not follicular fluid-induced acrosome reaction.
    Biol Reprod. 1999 Sep;61(3):673-80 PMID: 10456844
  170. Activation of spermatozoan adenylate cyclase by a low molecular weight factor in porcine seminal plasma.
    J Biol Chem. 1983 Nov 10;258(21):13056-62 PMID: 6630219
  171. Progesterone triggers a wave of increased free calcium during the human sperm acrosome reaction.
    Dev Biol. 1997 Feb 1;182(1):67-75 PMID: 9073447
  172. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2466-70 PMID: 2138778
  173. The Behavior and Acrosomal Status of Mouse Spermatozoa In Vitro, and Within the Oviduct During Fertilization after Natural Mating.
    Biol Reprod. 2016 Sep;95(3):50 PMID: 27417908
  174. Calcineurin: form and function.
    Physiol Rev. 2000 Oct;80(4):1483-521 PMID: 11015619
  175. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility.
    Proc Natl Acad Sci U S A. 2007 Jan 23;104(4):1219-23 PMID: 17227845
  176. Depolarization of sperm membrane potential is a common feature of men with subfertility and is associated with low fertilization rate at IVF.
    Hum Reprod. 2016 Jun;31(6):1147-57 PMID: 27052499
  177. Cholesterol, phospholipids and markers of the function of the accessory sex glands in the semen of men with hypercholesterolaemia.
    Int J Androl. 1995 Jun;18(3):151-6 PMID: 7558379
  178. Functional human sperm capacitation requires both bicarbonate-dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases.
    Mol Hum Reprod. 2013 Sep;19(9):570-80 PMID: 23630234
  179. KATP channels in mouse spermatogenic cells and sperm, and their role in capacitation.
    Dev Biol. 2006 Jan 15;289(2):395-405 PMID: 16343479
  180. Cell signaling in space and time: where proteins come together and when they're apart.
    Science. 2009 Nov 27;326(5957):1220-4 PMID: 19965465
  181. Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea.
    Mol Hum Reprod. 2006 Feb;12(2):107-11 PMID: 16421216
  182. Flow cytometry analysis reveals that only a subpopulation of mouse sperm undergoes hyperpolarization during capacitation.
    Biol Reprod. 2015 May;92(5):121 PMID: 25855261
  183. The control of male fertility by spermatozoan ion channels.
    Annu Rev Physiol. 2012;74:453-75 PMID: 22017176
  184. The capacitation of the mammalian sperm.
    Nature. 1952 Aug 23;170(4321):326 PMID: 12993150
  185. The BSA-induced Ca2+ influx during sperm capacitation is CATSPER channel-dependent.
    Reprod Biol Endocrinol. 2009 Oct 27;7:119 PMID: 19860887
  186. Intracellular Ca(2+)-Mg(2+)-ATPase regulates calcium influx and acrosomal exocytosis in bull and ram spermatozoa.
    Biol Reprod. 1999 Nov;61(5):1226-34 PMID: 10529268
  187. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3'5'-monophosphate-dependent pathway.
    Biol Reprod. 1997 Mar;56(3):707-19 PMID: 9047017
  188. Molecular cloning and functional expression of a novel amiloride-sensitive Na+ channel.
    J Biol Chem. 1995 Nov 17;270(46):27411-4 PMID: 7499195
  189. The intraacrosomal calcium pool plays a direct role in acrosomal exocytosis.
    J Biol Chem. 2002 Dec 20;277(51):49326-31 PMID: 12379648
  190. Crystal structure of the sodium-potassium pump.
    Nature. 2007 Dec 13;450(7172):1043-9 PMID: 18075585
  191. Structure and mechanism of Na,K-ATPase: functional sites and their interactions.
    Annu Rev Physiol. 2003;65:817-49 PMID: 12524462
  192. The influence of some cations on an adenosine triphosphatase from peripheral nerves.
    Biochim Biophys Acta. 1957 Feb;23(2):394-401 PMID: 13412736
  193. A sperm ion channel required for sperm motility and male fertility.
    Nature. 2001 Oct 11;413(6856):603-9 PMID: 11595941
  194. A role for the chemokine receptor CCR6 in mammalian sperm motility and chemotaxis.
    J Cell Physiol. 2014 Jan;229(1):68-78 PMID: 23765988
  195. Are TRP channels involved in sperm development and function?
    Cell Tissue Res. 2012 Sep;349(3):749-64 PMID: 22580508
  196. Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis.
    J Biol Chem. 2009 Sep 11;284(37):24825-39 PMID: 19546222
  197. CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir.
    Reprod Fertil Dev. 2009;21(2):345-50 PMID: 19210926
  198. Early stages of fertilization in vitro of human oocytes matured in vitro.
    Nature. 1969 Feb 15;221(5181):632-5 PMID: 4886881
  199. IDENTIFICATION OF SPERM STIMULATING FACTOR OF RABBIT OVIDUCT FLUID.
    Proc Soc Exp Biol Med. 1964 Oct;117:240-3 PMID: 14223281
  200. Plasma cholesteryl ester transfer protein.
    J Lipid Res. 1993 Aug;34(8):1255-74 PMID: 8409761
  201. Intracellular calcium reaches different levels of elevation in hyperactivated and acrosome-reacted hamster sperm.
    Mol Reprod Dev. 1995 Nov;42(3):325-33 PMID: 8579847
  202. Progesterone induces hyperpolarization after a transient depolarization phase in human spermatozoa.
    Biol Reprod. 2002 Jun;66(6):1775-80 PMID: 12021061
  203. Encoding of progesterone stimulus intensity by intracellular [Ca2+] ([Ca2+]i) in human spermatozoa.
    Biochem J. 2003 Jun 1;372(Pt 2):407-17 PMID: 12614198
  204. Deletion of the Slo3 gene abolishes alkalization-activated K+ current in mouse spermatozoa.
    Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5879-84 PMID: 21427226
  205. Identification and localisation of SERCA 2 isoforms in mammalian sperm.
    Mol Hum Reprod. 2007 May;13(5):307-16 PMID: 17376796
  206. Calcium channels in the development, maturation, and function of spermatozoa.
    Physiol Rev. 2011 Oct;91(4):1305-55 PMID: 22013213
  207. Disruption of the principal, progesterone-activated sperm Ca2+ channel in a CatSper2-deficient infertile patient.
    Proc Natl Acad Sci U S A. 2013 Apr 23;110(17):6823-8 PMID: 23530196
  208. Molecular expression of SLC4-derived Na+-dependent anion transporters in selected human tissues.
    Am J Physiol Regul Integr Comp Physiol. 2007 Nov;293(5):R2136-46 PMID: 17715183
  209. Structural features of sterols required to inhibit human sperm capacitation.
    Biol Reprod. 2003 Apr;68(4):1308-17 PMID: 12606419
  210. Regulation of the sperm calcium channel CatSper by endogenous steroids and plant triterpenoids.
    Proc Natl Acad Sci U S A. 2017 May 30;114(22):5743-5748 PMID: 28507119
  211. 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
  212. Cyclic adenosine 3',5'monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility.
    Biol Reprod. 1996 Sep;55(3):684-92 PMID: 8862788
  213. Dynamics of the mammalian sperm plasma membrane in the process of fertilization.
    Biochim Biophys Acta. 2000 Nov 10;1469(3):197-235 PMID: 11063883
  214. Relationship between calcium, cyclic AMP, ATP, and intracellular pH and the capacity of hamster spermatozoa to express hyperactivated motility.
    Gamete Res. 1989 Feb;22(2):163-77 PMID: 2540081
  215. Deficient human β-defensin 1 underlies male infertility associated with poor sperm motility and genital tract infection.
    Sci Transl Med. 2014 Aug 13;6(249):249ra108 PMID: 25122636
  216. Capacitation-associated changes in membrane fluidity in asthenozoospermic human spermatozoa.
    Int J Androl. 2009 Aug;32(4):360-75 PMID: 18399983
  217. The testis anion transporter TAT1 (SLC26A8) physically and functionally interacts with the cystic fibrosis transmembrane conductance regulator channel: a potential role during sperm capacitation.
    Hum Mol Genet. 2012 Mar 15;21(6):1287-98 PMID: 22121115
  218. Expression of TEX101, regulated by ACE, is essential for the production of fertile mouse spermatozoa.
    Proc Natl Acad Sci U S A. 2013 May 14;110(20):8111-6 PMID: 23633567
  219. Ca2+ signals generated by CatSper and Ca2+ stores regulate different behaviors in human sperm.
    J Biol Chem. 2013 Mar 1;288(9):6248-58 PMID: 23344959
  220. The ABC protein turned chloride channel whose failure causes cystic fibrosis.
    Nature. 2006 Mar 23;440(7083):477-83 PMID: 16554808
  221. Human sperm subpopulations: relationship between functional quality and protein tyrosine phosphorylation.
    Hum Reprod. 2004 Jan;19(1):139-46 PMID: 14688172
  222. The α4 isoform of the Na⁺,K⁺-ATPase is tuned for changing extracellular environments.
    FEBS J. 2016 Jan;283(2):282-93 PMID: 26476261
  223. Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm.
    Nat Cell Biol. 2003 Oct;5(10):902-6 PMID: 14515130
  224. 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
  225. Role of human Na,K-ATPase alpha 4 in sperm function, derived from studies in transgenic mice.
    Mol Reprod Dev. 2015 Mar;82(3):167-81 PMID: 25640246
  226. Biological basis for human capacitation-revisited.
    Hum Reprod Update. 2017 May 1;23(3):289-299 PMID: 28115407
  227. Human spermatozoa contain multiple targets for protein S-nitrosylation: an alternative mechanism of the modulation of sperm function by nitric oxide?
    Proteomics. 2007 Sep;7(17):3066-84 PMID: 17683036
  228. Purification and functional reconstitution of the cystic fibrosis transmembrane conductance regulator (CFTR).
    Cell. 1992 Feb 21;68(4):809-18 PMID: 1371239
  229. Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation.
    J Cell Sci. 2005 May 1;118(Pt 9):2013-22 PMID: 15840651
  230. A method for collecting motile spermatozoa from human semen.
    Fertil Steril. 1976 Jun;27(6):677-84 PMID: 1278462
  231. Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm.
    J Cell Biol. 1988 May;106(5):1625-33 PMID: 2836436
  232. Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes.
    Cryobiology. 1992 Apr;29(2):255-66 PMID: 1582232
  233. Flagellar ion channels of sperm: similarities and differences between species.
    Cell Calcium. 2015 Jul;58(1):105-13 PMID: 25465894
  234. Enhancement of motility and acrosome reaction in human spermatozoa: differential activation by type-specific phosphodiesterase inhibitors.
    Hum Reprod. 1998 May;13(5):1248-54 PMID: 9647555
  235. Increased calcium-ion influx is a component of capacitation of spermatozoa.
    Biochem J. 1978 Jun 15;172(3):549-56 PMID: 687358
  236. Rediscovering sperm ion channels with the patch-clamp technique.
    Mol Hum Reprod. 2011 Aug;17(8):478-99 PMID: 21642646
  237. Acrosomal exocytosis of mouse sperm progresses in a consistent direction in response to zona pellucida.
    J Cell Physiol. 2009 Sep;220(3):611-20 PMID: 19373867
  238. Albumin as a zinc carrier: properties of its high-affinity zinc-binding site.
    Biochem Soc Trans. 2008 Dec;36(Pt 6):1317-21 PMID: 19021548
  239. The sperm chemoattractant secreted from human cumulus cells is progesterone.
    Hum Reprod. 2008 Oct;23(10):2339-45 PMID: 18621752
  240. Voltage-dependent Ca(2+) channel subunit expression and immunolocalization in mouse spermatogenic cells and sperm.
    FEBS Lett. 1999 Nov 26;462(1-2):171-6 PMID: 10580114
  241. The pH and bicarbonate-ion content of the oviduct and uterine fluids.
    Fertil Steril. 1962 Sep-Oct;13:481-5 PMID: 13926247
  242. The Ca2+-activated K+ current of human sperm is mediated by Slo3.
    Elife. 2014 Mar 26;3:e01438 PMID: 24670955
  243. Hyperactivation of mammalian spermatozoa: function and regulation.
    Reproduction. 2001 Oct;122(4):519-26 PMID: 11570958
  244. High cholesterol content and decreased membrane fluidity in human spermatozoa are associated with protein tyrosine phosphorylation and functional deficiencies.
    J Androl. 2009 Sep-Oct;30(5):552-8 PMID: 19269935
  245. Structure and regulation of amiloride-sensitive sodium channels.
    Annu Rev Physiol. 2000;62:573-94 PMID: 10845103
  246. Increased frequency of cystic fibrosis transmembrane conductance regulator gene mutations in infertile males.
    Fertil Steril. 2006 Jan;85(1):135-8 PMID: 16412743
  247. Cystic fibrosis transmembrane conductance regulator is vital to sperm fertilizing capacity and male fertility.
    Proc Natl Acad Sci U S A. 2007 Jun 5;104(23):9816-21 PMID: 17519339
  248. Roles of the Na,K-ATPase alpha4 isoform and the Na+/H+ exchanger in sperm motility.
    Mol Reprod Dev. 2002 Jul;62(3):348-56 PMID: 12112599
  249. Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate.
    J Biol Chem. 2003 May 2;278(18):15922-6 PMID: 12609998
  250. Ion channels in sperm motility and capacitation.
    Soc Reprod Fertil Suppl. 2007;65:229-44 PMID: 17644965
  251. Lowered levels of bicarbonate in seminal plasma cause the poor sperm motility in human infertile patients.
    Fertil Steril. 1986 Feb;45(2):265-72 PMID: 3005051
  252. Lipocalin 2 binds to membrane phosphatidylethanolamine to induce lipid raft movement in a PKA-dependent manner and modulates sperm maturation.
    Development. 2014 May;141(10):2157-64 PMID: 24803661
  253. The pH as an important determinant of sperm-mucus interaction.
    Fertil Steril. 1993 Mar;59(3):617-28 PMID: 8458467
  254. Effects of extracellular adenosine 5'-triphosphate on human sperm motility.
    Reprod Sci. 2007 Oct;14(7):655-66 PMID: 18000227
  255. Localization patterns of the ganglioside GM1 in human sperm are indicative of male fertility and independent of traditional semen measures.
    Mol Reprod Dev. 2017 May;84(5):423-435 PMID: 28418610
  256. PKA, germ cells, and fertility.
    Physiology (Bethesda). 2007 Feb;22:40-6 PMID: 17289929
  257. Structure and function of the CFTR chloride channel.
    Physiol Rev. 1999 Jan;79(1 Suppl):S23-45 PMID: 9922375
  258. Development of new ganglioside probes and unraveling of raft domain structure by single-molecule imaging.
    Biochim Biophys Acta. 2017 Oct;1861(10):2494-2506 PMID: 28734966
  259. Assessment of the CFTR and ENaC association.
    Mol Biosyst. 2009 Feb;5(2):123-7 PMID: 19156256
  260. Expression of ion transport-associated proteins in human efferent and epididymal ducts.
    Reproduction. 2007 Apr;133(4):775-84 PMID: 17504921
  261. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel.
    Cell. 2010 Feb 5;140(3):327-37 PMID: 20144758
  262. Slo1 is the principal potassium channel of human spermatozoa.
    Elife. 2013 Oct 08;2:e01009 PMID: 24137539
  263. Identical phenotypes of CatSper1 and CatSper2 null sperm.
    J Biol Chem. 2005 Sep 16;280(37):32238-44 PMID: 16036917
  264. Direct sensing of intracellular pH by the cystic fibrosis transmembrane conductance regulator (CFTR) Cl- channel.
    J Biol Chem. 2009 Dec 18;284(51):35495-506 PMID: 19837660
  265. Hydrogen ion and carbon dioxide content of the oviductal fluid of the rhesus monkey (Macaca mulatta).
    Fertil Steril. 1977 Sep;28(9):981-5 PMID: 19307
  266. Role of the Na+/Ca2+ exchanger in calcium homeostasis and human sperm motility regulation.
    Cell Motil Cytoskeleton. 2006 Feb;63(2):66-76 PMID: 16374831
  267. Sodium-Hydrogen-Exchanger expression in human sperm and its relationship with semen parameters.
    J Assist Reprod Genet. 2017 Jun;34(6):795-801 PMID: 28432487
  268. Targeted ablation of plasma membrane Ca2+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4.
    J Biol Chem. 2004 Aug 6;279(32):33742-50 PMID: 15178683
  269. [Sperm reservoir in mice: involvement of ADAMs].
    Gynecol Obstet Fertil. 2011 Nov;39(11):630-2 PMID: 22000834
  270. CFTR/ENaC-dependent regulation of membrane potential during human sperm capacitation is initiated by bicarbonate uptake through NBC.
    J Biol Chem. 2018 Jun 22;293(25):9924-9936 PMID: 29743243
  271. Preliminary attempts to fertilize human oocytes matured in vitro.
    Am J Obstet Gynecol. 1966 Sep 15;96(2):192-200 PMID: 4958582
  272. Lipid raft dynamics linked to sperm competency for fertilization in mice.
    Genes Cells. 2017 May;22(5):493-500 PMID: 28425215
  273. The elemental composition of the environments of the gametes and preimplantation embryo during the initiation of pregnancy.
    Biol Reprod. 1977 Mar;16(2):147-57 PMID: 831844
  274. Polarized expression of a band 3-related protein in mammalian sperm cells.
    Biol Reprod. 1993 Aug;49(2):326-31 PMID: 8373956
  275. Changes in the distribution of intramembranous particles and filipin-reactive membrane sterols during in vitro capacitation of golden hamster spermatozoa.
    Gamete Res. 1989 Jul;23(3):335-47 PMID: 2777171
  276. Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation.
    Mol Hum Reprod. 1999 Nov;5(11):1017-26 PMID: 10541563
  277. Unresolved questions concerning mammalian sperm acrosomal exocytosis.
    Biol Reprod. 2014 May;90(5):112 PMID: 24671881
  278. FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa.
    Biol Reprod. 1999 Nov;61(5):1184-97 PMID: 10529264
  279. A putative fourth Na+,K(+)-ATPase alpha-subunit gene is expressed in testis.
    Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12952-6 PMID: 7809153
  280. Birth after the reimplantation of a human embryo.
    Lancet. 1978 Aug 12;2(8085):366 PMID: 79723
  281. Disruption of the SLC26A3-mediated anion transport is associated with male subfertility.
    Fertil Steril. 2006 Jan;85(1):232-5 PMID: 16412765
  282. Role of carbonic anhydrase IV in the bicarbonate-mediated activation of murine and human sperm.
    PLoS One. 2010 Nov 24;5(11):e15061 PMID: 21124840
  283. 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
  284. Dual effect of membrane cholesterol on simple and mediated transport processes in human erythrocytes.
    Biochim Biophys Acta. 1980 Aug 14;600(3):860-9 PMID: 7407148
  285. Direct evaluation of acidification by rat testis and epididymis: role of carbonic anhydrase.
    Am J Physiol. 1990 Jan;258(1 Pt 1):E143-50 PMID: 2105657
  286. Are there inositol 1,4,5-triphosphate (IP3) receptors in human sperm?
    Life Sci. 1999;65(2):135-43 PMID: 10416819
  287. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7266-70 PMID: 6950375
  288. Multi-ion pore behaviour in the CFTR chloride channel.
    Nature. 1993 Nov 4;366(6450):79-82 PMID: 7694154
  289. cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm.
    Mol Reprod Dev. 2000 Feb;55(2):220-8 PMID: 10618662
  290. CFTR is essential for sperm fertilizing capacity and is correlated with sperm quality in humans.
    Hum Reprod. 2010 Feb;25(2):317-27 PMID: 19923167
  291. Sensorineural deafness and male infertility: a contiguous gene deletion syndrome.
    J Med Genet. 2007 Apr;44(4):233-40 PMID: 17098888
  292. Measurement of intracellular pH in human spermatozoa by flow cytometry with the benzo[c]xanthene dye SNAFL-1: a novel, single excitation, dual emission, molecular probe.
    Mol Hum Reprod. 1996 Jan;2(1):18-25 PMID: 9238652
  293. Capacitation of mammalian spermatozoa.
    Nature. 1958 Mar 22;181(4612):851 PMID: 13526698
  294. GM1 dynamics as a marker for membrane changes associated with the process of capacitation in murine and bovine spermatozoa.
    J Androl. 2007 Jul-Aug;28(4):588-99 PMID: 17377143
  295. Fertilizing capacity of spermatozoa deposited into the fallopian tubes.
    Nature. 1951 Oct 20;168(4277):697-8 PMID: 14882325
  296. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor.
    Science. 2000 Jul 28;289(5479):625-8 PMID: 10915626
  297. Calmodulin-mediated adenylate cyclase from mammalian sperm.
    J Biol Chem. 1987 Jun 25;262(18):8672-6 PMID: 3597392
  298. Carbonic anhydrase isoenzymes CAI and CAII in semen, decidua, chorionic villi and various fetal tissues.
    Early Hum Dev. 1998 Jul 10;51(3):205-11 PMID: 9692790
  299. The cation composition of the seminal plasma and prostatic fluid and its correlation to semen quality.
    Fertil Steril. 1978 May;29(5):539-42 PMID: 27390
  300. Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa.
    Biol Reprod. 2008 Dec;79(6):1153-9 PMID: 18753612
  301. Modulation of Na-H antiporter activity in human lymphoblasts by altered membrane cholesterol.
    Am J Physiol. 1991 Dec;261(6 Pt 1):C1138-42 PMID: 1662905
  302. The role of Hv1 and CatSper channels in sperm activation.
    J Physiol. 2010 Dec 1;588(Pt 23):4667-72 PMID: 20679352
  303. Calcium signalling in human spermatozoa: a specialized 'toolkit' of channels, transporters and stores.
    Hum Reprod Update. 2006 May-Jun;12(3):253-67 PMID: 16338990
  304. Expression and differential cell distribution of low-threshold Ca(2+) channels in mammalian male germ cells and sperm.
    FEBS Lett. 2004 Apr 9;563(1-3):87-92 PMID: 15063728
  305. Endocervical pH measured in vivo through the normal menstrual cycle.
    Obstet Gynecol. 1970 Feb;35(2):202-6 PMID: 5414205
  306. The collection and analysis of human fallopian tubal fluid.
    Contraception. 1972 Feb;5(2):85-103 PMID: 4631126
  307. Unconventional endocannabinoid signaling governs sperm activation via the sex hormone progesterone.
    Science. 2016 Apr 29;352(6285):555-9 PMID: 26989199
  308. Molecular mechanism of Zn2+ inhibition of a voltage-gated proton channel.
    Proc Natl Acad Sci U S A. 2016 Oct 4;113(40):E5962-E5971 PMID: 27647906
  309. The concentration of some inorganic ions and organic compounds in the luminal fluid of the human ductus deferens.
    Int J Androl. 1981 Aug;4(4):457-61 PMID: 7298229
  310. Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway.
    J Biol Chem. 2006 Mar 31;281(13):8656-66 PMID: 16407249
  311. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.
    Development. 1995 Apr;121(4):1129-37 PMID: 7743926
  312. Chemical composition of human oviduct fluid.
    Fertil Steril. 1973 Jun;24(6):435-9 PMID: 4710008
  313. Angiotensin-converting enzyme is a GPI-anchored protein releasing factor crucial for fertilization.
    Nat Med. 2005 Feb;11(2):160-6 PMID: 15665832
  314. New insights into cystic fibrosis: molecular switches that regulate CFTR.
    Nat Rev Mol Cell Biol. 2006 Jun;7(6):426-36 PMID: 16723978
  315. Mouse sperm membrane potential: changes induced by Ca2+.
    FEBS Lett. 1995 Sep 18;372(1):119-25 PMID: 7556631
  316. Independent elevation of cytosolic [Ca2+] and pH of mammalian sperm by voltage-dependent and pH-sensitive mechanisms.
    J Biol Chem. 1987 Nov 5;262(31):15041-7 PMID: 3667622
  317. Sperm membrane potential: hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion.
    Dev Biol. 1995 Oct;171(2):554-63 PMID: 7556936
  318. Involvement of bicarbonate-induced radical signaling in oxysterol formation and sterol depletion of capacitating mammalian sperm during in vitro fertilization.
    Biol Reprod. 2013 Jan 25;88(1):21 PMID: 23115269
  319. Lipid modulation of calcium flux through CaV2.3 regulates acrosome exocytosis and fertilization.
    Dev Cell. 2014 Feb 10;28(3):310-21 PMID: 24525187
  320. Expression and localization of caveolin-1, and the presence of membrane rafts, in mouse and Guinea pig spermatozoa.
    Dev Biol. 2001 Dec 15;240(2):599-610 PMID: 11784086
  321. Activity of the Na,K-ATPase α4 isoform is regulated during sperm capacitation to support sperm motility.
    J Androl. 2012 Sep-Oct;33(5):1047-57 PMID: 22441762
  322. CatSperbeta, a novel transmembrane protein in the CatSper channel complex.
    J Biol Chem. 2007 Jun 29;282(26):18945-52 PMID: 17478420
  323. Ae4 (Slc4a9) is an electroneutral monovalent cation-dependent Cl-/HCO3- exchanger.
    J Gen Physiol. 2016 May;147(5):423-36 PMID: 27114614
  324. GPI-anchored proteins are organized in submicron domains at the cell surface.
    Nature. 1998 Aug 20;394(6695):798-801 PMID: 9723621
  325. Chloride Is essential for capacitation and for the capacitation-associated increase in tyrosine phosphorylation.
    J Biol Chem. 2008 Dec 19;283(51):35539-50 PMID: 18957426
  326. Sodium influx induced by external calcium chelation decreases human sperm motility.
    Hum Reprod. 2011 Oct;26(10):2626-35 PMID: 21810864
  327. 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
  328. Timing of sperm capacitation varies reproducibly among men.
    Mol Reprod Dev. 2018 May;85(5):387-396 PMID: 29521463
  329. Membrane lipid dynamics during human sperm capacitation.
    Front Biosci. 1996 Jul 01;1:d103-17 PMID: 9159218
  330. The Na,K-ATPase alpha4 isoform from humans has distinct enzymatic properties and is important for sperm motility.
    Mol Hum Reprod. 2006 Sep;12(9):565-76 PMID: 16861705
  331. Activation of protein kinase A during human sperm capacitation and acrosome reaction.
    J Androl. 2002 Sep-Oct;23(5):709-16 PMID: 12185106
  332. Only a subpopulation of mouse sperm displays a rapid increase in intracellular calcium during capacitation.
    J Cell Physiol. 2018 Jun 28;:null PMID: 29953592
  333. Defective function of membrane potential (psi) on sperm of infertile men.
    Arch Androl. 1997 Mar-Apr;38(2):151-5 PMID: 9049036
  334. Cyclic nucleotide-gated ion channels.
    Physiol Rev. 2002 Jul;82(3):769-824 PMID: 12087135
  335. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation.
    Proc Natl Acad Sci U S A. 1999 Jun 8;96(12):6757-62 PMID: 10359785
  336. Regulation of intracellular pH in capacitated human spermatozoa by a Na+/H+ exchanger.
    Mol Reprod Dev. 1999 Feb;52(2):189-95 PMID: 9890750
  337. Sperm motility is dependent on a unique isoform of the Na,K-ATPase.
    J Biol Chem. 2000 Jul 7;275(27):20693-9 PMID: 10764792
  338. Carbonic anhydrases and their functional differences in human and mouse sperm physiology.
    Biochem Biophys Res Commun. 2015 Dec 25;468(4):713-8 PMID: 26551457
  339. Missense mutations in SLC26A8, encoding a sperm-specific activator of CFTR, are associated with human asthenozoospermia.
    Am J Hum Genet. 2013 May 2;92(5):760-6 PMID: 23582645
  340. Disruption of ADAM3 impairs the migration of sperm into oviduct in mouse.
    Biol Reprod. 2009 Jul;81(1):142-6 PMID: 19339711
  341. Transient receptor potential (TRPC) channels in human sperm: expression, cellular localization and involvement in the regulation of flagellar motility.
    FEBS Lett. 2003 Apr 24;541(1-3):69-74 PMID: 12706821
  342. Evidence for the involvement of proline-rich tyrosine kinase 2 in tyrosine phosphorylation downstream of protein kinase A activation during human sperm capacitation.
    Mol Hum Reprod. 2014 Nov;20(11):1054-66 PMID: 25180269
  343. Calaxin drives sperm chemotaxis by Ca²⁺-mediated direct modulation of a dynein motor.
    Proc Natl Acad Sci U S A. 2012 Dec 11;109(50):20497-502 PMID: 23169663
  344. Changes in intracellular calcium of porcine sperm during in vitro incubation with seminal plasma and a capacitating medium.
    Biochem Biophys Res Commun. 1990 Oct 15;172(1):47-53 PMID: 2222481
  345. Mouse sperm begin to undergo acrosomal exocytosis in the upper isthmus of the oviduct.
    Dev Biol. 2016 Mar 15;411(2):172-182 PMID: 26872876
  346. Selective diffusion barriers separate membrane compartments.
    Biophys J. 2010 Jul 7;99(1):L1-3 PMID: 20655822
  347. Essential Role of CFTR in PKA-Dependent Phosphorylation, Alkalinization, and Hyperpolarization During Human Sperm Capacitation.
    J Cell Physiol. 2017 Jun;232(6):1404-1414 PMID: 27714810
  348. Evidence for the involvement of calmodulin in mouse sperm capacitation.
    Biol Reprod. 2000 May;62(5):1231-9 PMID: 10775171
  349. Mouse sperm membrane potential hyperpolarization is necessary and sufficient to prepare sperm for the acrosome reaction.
    J Biol Chem. 2012 Dec 28;287(53):44384-93 PMID: 23095755
Article Info
Journal
Frontiers in cell and developmental biology
Abbr.
Front Cell Dev Biol
ISSN
2296-634X
Published
2018-00-00
Epub
2018-00-27
Pages
72
Language
English
Region
Switzerland
NLM ID
101630250
PMCID
PMC6078053
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