Home LiteratureArticle Details
PMID: 21540868 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review

Ion channels, phosphorylation and mammalian sperm capacitation.

Asian journal of andrology ·Vol. 13 ·No. 3 ·2011-05-00 ·Pages 395-405

Visconti PE, Krapf D, de la Vega-Beltrán JL, Acevedo JJ, Darszon A

Abstract

Sexually reproducing animals require an orchestrated communication between spermatozoa and the egg to generate a new individual. Capacitation, a maturational complex phenomenon that occurs in the female reproductive tract, renders spermatozoa capable of binding and fusing with the oocyte, and it is a requirement for mammalian fertilization. Capacitation encompasses plasma membrane reorganization, ion permeability regulation, cholesterol loss and changes in the phosphorylation state of many proteins. Novel tools to study sperm ion channels, image intracellular ionic changes and proteins with better spatial and temporal resolution, are unraveling how modifications in sperm ion transport and phosphorylation states lead to capacitation. Recent evidence indicates that two parallel pathways regulate phosphorylation events leading to capacitation, one of them requiring activation of protein kinase A and the second one involving inactivation of ser/thr phosphatases. This review examines the involvement of ion transporters and phosphorylation signaling processes needed for spermatozoa to achieve capacitation. Understanding the molecular mechanisms leading to fertilization is central for societies to deal with rising male infertility rates, to develop safe male gamete-based contraceptives and to preserve biodiversity through better assisted fertilization strategies.

MeSH Terms
Animals Calcium/metabolism Calcium Channels Cyclic AMP-Dependent Protein Kinases/metabolism Cystic Fibrosis Transmembrane Conductance Regulator/physiology Epithelial Sodium Channels/physiology Female Fertilization Hydrogen-Ion Concentration Ion Channels/physiology Male Membrane Microdomains/physiology Phospholipid Transfer Proteins/physiology Phosphoprotein Phosphatases/metabolism Phosphorylation Potassium Channels, Inwardly Rectifying/physiology Signal Transduction/physiology Sperm Capacitation/physiology Spermatozoa/physiology src-Family Kinases/physiology
Chemicals
Calcium Channels Catsper1 protein, mouse Epithelial Sodium Channels Ion Channels Phospholipid Transfer Proteins Potassium Channels, Inwardly Rectifying Cystic Fibrosis Transmembrane Conductance Regulator src-Family Kinases Cyclic AMP-Dependent Protein Kinases Phosphoprotein Phosphatases Calcium
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Visconti Pablo E
Department of Veterinary and Animal Science, Paige Labs, University of Massachusets, Amherst, MA 01003, USA.
Krapf Dario
de la Vega-Beltrán José Luis
Acevedo Juan José
Darszon Alberto
References (167)
167 references, click to expand
  1. 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
  2. Protein kinase C is present in human sperm: possible role in flagellar motility.
    Proc Natl Acad Sci U S A. 1990 Sep;87(18):7305-8 PMID: 2402510
  3. Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein.
    Biol Reprod. 1997 Nov;57(5):1080-8 PMID: 9369174
  4. Subcellular distribution of protein kinase C alpha and betaI in bovine spermatozoa, and their regulation by calcium and phorbol esters.
    Biol Reprod. 1997 Feb;56(2):454-9 PMID: 9116146
  5. Ion channels in sperm physiology.
    Physiol Rev. 1999 Apr;79(2):481-510 PMID: 10221988
  6. Novelty of the pyruvate metabolic enzyme dihydrolipoamide dehydrogenase in spermatozoa: correlation of its localization, tyrosine phosphorylation, and activity during sperm capacitation.
    J Biol Chem. 2005 Jul 8;280(27):25743-53 PMID: 15888450
  7. Casein kinase II activity of buffalo sperm chromatin.
    Mol Reprod Dev. 1998 Jun;50(2):178-84 PMID: 9590534
  8. ATP-sensitive potassium channels: metabolic sensing and cardioprotection.
    J Appl Physiol (1985). 2007 Nov;103(5):1888-93 PMID: 17641217
  9. A novel, single, transmembrane protein CATSPERG is associated with CATSPER1 channel protein.
    Biol Reprod. 2009 Sep;81(3):539-44 PMID: 19516020
  10. 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
  11. The SLO3 sperm-specific potassium channel plays a vital role in male fertility.
    FEBS Lett. 2010 Mar 5;584(5):1041-6 PMID: 20138882
  12. cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm.
    Mol Reprod Dev. 2000 Feb;55(2):220-8 PMID: 10618662
  13. Leptin secretion by human ejaculated spermatozoa.
    J Clin Endocrinol Metab. 2005 Aug;90(8):4753-61 PMID: 15944217
  14. High-conductance potassium channels of the SLO family.
    Nat Rev Neurosci. 2006 Dec;7(12):921-31 PMID: 17115074
  15. A novel aminophospholipid transporter exclusively expressed in spermatozoa is required for membrane lipid asymmetry and normal fertilization.
    Dev Biol. 2004 Mar 1;267(1):203-15 PMID: 14975727
  16. Effect of methyl-beta-cyclodextrin on the acrosomal responsiveness of human sperm.
    Mol Reprod Dev. 1999 May;53(1):92-8 PMID: 10230821
  17. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation.
    Development. 1995 Apr;121(4):1129-37 PMID: 7743926
  18. The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation.
    Mol Reprod Dev. 2010 Mar;77(3):197-208 PMID: 19908247
  19. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization.
    Dev Cell. 2005 Aug;9(2):249-59 PMID: 16054031
  20. Calcium requirements for human sperm function in vitro.
    Fertil Steril. 2003 Jun;79(6):1396-403 PMID: 12798888
  21. Cl- is required for HCO3- entry necessary for sperm capacitation in guinea pig: involvement of a Cl-/HCO3- exchanger (SLC26A3) and CFTR.
    Biol Reprod. 2009 Jan;80(1):115-23 PMID: 18784352
  22. Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation.
    Int J Dev Biol. 2008;52(5-6):463-72 PMID: 18649259
  23. A new sperm-specific Na+/H+ exchanger required for sperm motility and fertility.
    Nat Cell Biol. 2003 Dec;5(12):1117-22 PMID: 14634667
  24. Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation.
    Mol Reprod Dev. 2004 Apr;67(4):487-500 PMID: 14991741
  25. Phorbol esters stimulate cyclic adenosine 3', 5'-monophosphate accumulation in hamster spermatozoa during in vitro capacitation.
    Biol Reprod. 1989 Feb;40(2):223-31 PMID: 2541812
  26. Ion channels in sperm motility and capacitation.
    Soc Reprod Fertil Suppl. 2007;65:229-44 PMID: 17644965
  27. 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
  28. Aminophospholipid asymmetry: A matter of life and death.
    Annu Rev Physiol. 2003;65:701-34 PMID: 12471163
  29. The role of Hv1 and CatSper channels in sperm activation.
    J Physiol. 2010 Dec 1;588(Pt 23):4667-72 PMID: 20679352
  30. Dual regulation of the T-type Ca(2+) current by serum albumin and beta-estradiol in mammalian spermatogenic cells.
    FEBS Lett. 2000 Jun 23;475(3):251-6 PMID: 10869566
  31. Increased activity of the human sperm tyrosine kinase SRC by the cAMP-dependent pathway in the presence of calcium.
    Biol Reprod. 2008 Oct;79(4):657-66 PMID: 18562702
  32. Expression and localization of five members of the testis-specific serine kinase (Tssk) family in mouse and human sperm and testis.
    Mol Hum Reprod. 2011 Jan;17(1):42-56 PMID: 20729278
  33. The role of proteomics in understanding sperm cell biology.
    Int J Androl. 2008 Jun;31(3):295-302 PMID: 18179557
  34. 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
  35. C1 domains exposed: from diacylglycerol binding to protein-protein interactions.
    Biochim Biophys Acta. 2006 Aug;1761(8):827-37 PMID: 16861033
  36. KATP channels in mouse spermatogenic cells and sperm, and their role in capacitation.
    Dev Biol. 2006 Jan 15;289(2):395-405 PMID: 16343479
  37. Biophysical and pharmacological characterization of spermatogenic T-type calcium current in mice lacking the CaV3.1 (alpha1G) calcium channel: CaV3.2 (alpha1H) is the main functional calcium channel in wild-type spermatogenic cells.
    J Cell Physiol. 2004 Jul;200(1):116-24 PMID: 15137064
  38. PKA, germ cells, and fertility.
    Physiology (Bethesda). 2007 Feb;22:40-6 PMID: 17289929
  39. Identification of mouse trp homologs and lipid rafts from spermatogenic cells and sperm.
    FEBS Lett. 2001 Nov 30;509(1):119-25 PMID: 11734218
  40. Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm.
    J Cell Biol. 1998 Jul 27;142(2):473-84 PMID: 9679145
  41. Localization of low-density detergent-resistant membrane proteins in intact and acrosome-reacted mouse sperm.
    Biol Reprod. 2009 May;80(5):897-904 PMID: 19144954
  42. Model systems, lipid rafts, and cell membranes.
    Annu Rev Biophys Biomol Struct. 2004;33:269-95 PMID: 15139814
  43. A role for the human sperm glycine receptor/Cl(-) channel in the acrosome reaction initiated by recombinant ZP3.
    Biol Reprod. 2002 Jan;66(1):91-7 PMID: 11751269
  44. 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
  45. Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose.
    Biol Reprod. 2001 May;64(5):1350-7 PMID: 11319138
  46. Expression of sperm Ca2+-activated K+ channels in Xenopus oocytes and their modulation by extracellular ATP.
    FEBS Lett. 1998 Nov 6;438(3):177-82 PMID: 9827541
  47. Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa.
    J Cell Sci. 2006 Aug 1;119(Pt 15):3182-92 PMID: 16835269
  48. Transmembrane phospholipid distribution in blood cells: control mechanisms and pathophysiological significance.
    Biol Chem. 1998 Aug-Sep;379(8-9):973-86 PMID: 9792430
  49. Use of detergents to study membrane rafts: the good, the bad, and the ugly.
    Biol Chem. 2003 Sep;384(9):1259-63 PMID: 14515986
  50. Inwardly rectifying potassium channels: their structure, function, and physiological roles.
    Physiol Rev. 2010 Jan;90(1):291-366 PMID: 20086079
  51. Cholesterol depletion disrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes.
    Eur J Immunol. 2000 Mar;30(3):954-63 PMID: 10741414
  52. Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation.
    Mol Hum Reprod. 2006 Dec;12(12):781-9 PMID: 17050774
  53. Calcium signaling through CatSper channels in mammalian fertilization.
    Physiology (Bethesda). 2010 Jun;25(3):165-75 PMID: 20551230
  54. The mouse sperm glycine receptor/chloride channel: cellular localization and involvement in the acrosome reaction initiated by glycine.
    J Androl. 2000 Jan-Feb;21(1):99-106 PMID: 10670525
  55. Slo3, a novel pH-sensitive K+ channel from mammalian spermatocytes.
    J Biol Chem. 1998 Feb 6;273(6):3509-16 PMID: 9452476
  56. Immunohistolocalization of the carbonic anhydrase isoenzymes (CA-I, CA-II, and CA-III) in the reproductive tract of male horses.
    Am J Vet Res. 1996 Apr;57(4):439-43 PMID: 8712504
  57. Targeted disruption of the Akap4 gene causes defects in sperm flagellum and motility.
    Dev Biol. 2002 Aug 15;248(2):331-42 PMID: 12167408
  58. Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH.
    Biol Reprod. 1989 Oct;41(4):683-99 PMID: 2620077
  59. 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
  60. Isolation and proteomic analysis of mouse sperm detergent-resistant membrane fractions: evidence for dissociation of lipid rafts during capacitation.
    Biol Reprod. 2005 Oct;73(4):721-9 PMID: 15917346
  61. Signal transduction pathways that regulate sperm capacitation and the acrosome reaction.
    Arch Biochem Biophys. 2009 May 1;485(1):72-81 PMID: 19217882
  62. Expression, localization and functions in acrosome reaction and sperm motility of Ca(V)3.1 and Ca(V)3.2 channels in sperm cells: an evaluation from Ca(V)3.1 and Ca(V)3.2 deficient mice.
    J Cell Physiol. 2007 Sep;212(3):753-63 PMID: 17450521
  63. Voltage-operated Ca2+ channels and the acrosome reaction: which channels are present and what do they do?
    Hum Reprod. 1999 Apr;14(4):873-9 PMID: 10221211
  64. Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa.
    Biol Reprod. 2008 Dec;79(6):1153-9 PMID: 18753612
  65. Protein kinase A and protein kinase C(alpha)/PPP1CC2 play opposing roles in the regulation of phosphatidylinositol 3-kinase activation in bovine sperm.
    Reproduction. 2010 Jul;140(1):43-56 PMID: 20442273
  66. Src activation triggers capacitation and acrosome reaction but not motility in human spermatozoa.
    Hum Reprod. 2008 Dec;23(12):2652-62 PMID: 18753142
  67. Interactions between beta subunits of the KCNMB family and Slo3: beta4 selectively modulates Slo3 expression and function.
    PLoS One. 2009 Jul 03;4(7):e6135 PMID: 19578543
  68. Factors regulating sperm capacitation.
    Syst Biol Reprod Med. 2010 Oct;56(5):334-48 PMID: 20849222
  69. Cholesterol efflux-mediated signal transduction in mammalian sperm. beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation.
    J Biol Chem. 1999 Jan 29;274(5):3235-42 PMID: 9915865
  70. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel.
    Nature. 2006 Feb 9;439(7077):737-40 PMID: 16467839
  71. Insights into sperm cell motility signaling through sNHE and the CatSpers.
    Mol Cell Endocrinol. 2006 May 16;250(1-2):84-92 PMID: 16413670
  72. Mouse sperm patch-clamp recordings reveal single Cl- channels sensitive to niflumic acid, a blocker of the sperm acrosome reaction.
    FEBS Lett. 1998 Apr 10;426(1):47-51 PMID: 9598976
  73. Regulating the acrosome reaction.
    Int J Dev Biol. 2008;52(5-6):503-10 PMID: 18649263
  74. Fertilization of rabbit ova in vitro.
    Nature. 1959 Aug 8;184(Suppl 7):466-7 PMID: 13809155
  75. Cyclodextrin removes cholesterol from mouse sperm and induces capacitation in a protein-free medium.
    Biol Reprod. 1998 Dec;59(6):1328-33 PMID: 9828175
  76. Fertilizing capacity of spermatozoa deposited into the fallopian tubes.
    Nature. 1951 Oct 20;168(4277):697-8 PMID: 14882325
  77. 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
  78. The BSA-induced Ca2+ influx during sperm capacitation is CATSPER channel-dependent.
    Reprod Biol Endocrinol. 2009 Oct 27;7:119 PMID: 19860887
  79. Tracking diffusion of GM1 gangliosides and zona pellucida binding molecules in sperm plasma membranes following cholesterol efflux.
    Dev Biol. 2010 Mar 15;339(2):398-406 PMID: 20060391
  80. Structure and regulation of voltage-gated Ca2+ channels.
    Annu Rev Cell Dev Biol. 2000;16:521-55 PMID: 11031246
  81. 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
  82. Caspase-independent exposure of aminophospholipids and tyrosine phosphorylation in bicarbonate responsive human sperm cells.
    Biol Reprod. 2003 Jun;68(6):2122-34 PMID: 12606386
  83. Identification of Thr29 as a critical phosphorylation site that activates the human proton channel Hvcn1 in leukocytes.
    J Biol Chem. 2010 Feb 19;285(8):5117-21 PMID: 20037153
  84. Phospholipids in animal eukaryotic membranes: transverse asymmetry and movement.
    Biochem J. 1993 Aug 15;294 ( Pt 1):1-14 PMID: 8363559
  85. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization.
    Dev Biol. 2006 Aug 15;296(2):353-62 PMID: 16842770
  86. 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
  87. 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
  88. Phosphatidylinositol 4,5-bisphosphate activates Slo3 currents and its hydrolysis underlies the epidermal growth factor-induced current inhibition.
    J Biol Chem. 2010 Jun 18;285(25):19259-66 PMID: 20392696
  89. CatSperbeta, a novel transmembrane protein in the CatSper channel complex.
    J Biol Chem. 2007 Jun 29;282(26):18945-52 PMID: 17478420
  90. Extracellular signal-regulated kinases modulate capacitation of human spermatozoa.
    Biol Reprod. 1998 Jun;58(6):1476-89 PMID: 9623609
  91. Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains.
    Nat Cell Biol. 1999 Jun;1(2):98-105 PMID: 10559881
  92. Identification of the major tyrosine phosphorylated protein of capacitated hamster spermatozoa as a homologue of mammalian sperm a kinase anchoring protein.
    Mol Reprod Dev. 2002 Feb;61(2):258-70 PMID: 11803562
  93. Biochemical characterization of membrane fractions in murine sperm: identification of three distinct sub-types of membrane rafts.
    J Cell Physiol. 2009 Mar;218(3):537-48 PMID: 19006178
  94. 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
  95. The scaffold role of the fibrous sheath.
    Soc Reprod Fertil Suppl. 2007;65:45-62 PMID: 17644954
  96. Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation.
    J Biol Chem. 2003 Feb 28;278(9):7001-9 PMID: 12496293
  97. The porcine lung as a potential model for cystic fibrosis.
    Am J Physiol Lung Cell Mol Physiol. 2008 Aug;295(2):L240-63 PMID: 18487356
  98. Cholesterol and Kir channels.
    IUBMB Life. 2009 Aug;61(8):781-90 PMID: 19548316
  99. Signalling pathways involved in sperm capacitation.
    Soc Reprod Fertil Suppl. 2007;65:245-59 PMID: 17644966
  100. Calcium as an extracellular signalling molecule: perspectives on the Calcium Sensing Receptor in the brain.
    C R Biol. 2005 Aug;328(8):691-700 PMID: 16125647
  101. Regulation of luminal acidification in the male reproductive tract via cell-cell crosstalk.
    J Exp Biol. 2009 Jun;212(Pt 11):1753-61 PMID: 19448084
  102. KSper, a pH-sensitive K+ current that controls sperm membrane potential.
    Proc Natl Acad Sci U S A. 2007 May 1;104(18):7688-92 PMID: 17460039
  103. A dihydropyridine-sensitive T-type Ca2+ current is the main Ca2+ current carrier in mouse primary spermatocytes.
    Am J Physiol. 1996 Nov;271(5 Pt 1):C1583-93 PMID: 8944642
  104. 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
  105. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility.
    J Biol Chem. 1997 Feb 21;272(8):4747-52 PMID: 9030527
  106. Egg coat proteins activate calcium entry into mouse sperm via CATSPER channels.
    Biol Reprod. 2009 Jun;80(6):1092-8 PMID: 19211808
  107. 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
  108. Assessment of the CFTR and ENaC association.
    Mol Biosyst. 2009 Feb;5(2):123-7 PMID: 19156256
  109. 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
  110. 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
  111. Birth after the reimplantation of a human embryo.
    Lancet. 1978 Aug 12;2(8085):366 PMID: 79723
  112. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel.
    Cell. 2010 Feb 5;140(3):327-37 PMID: 20144758
  113. How cells handle cholesterol.
    Science. 2000 Dec 1;290(5497):1721-6 PMID: 11099405
  114. T-type Ca2+ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction.
    FEBS Lett. 1996 Jun 17;388(2-3):150-4 PMID: 8690075
  115. Protein kinase C and mammalian spermatozoa acrosome reaction.
    Trends Endocrinol Metab. 1997 Nov;8(9):337-42 PMID: 18406822
  116. 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
  117. Genetic male infertility and mutation of CATSPER ion channels.
    Eur J Hum Genet. 2010 Nov;18(11):1178-84 PMID: 20648059
  118. Expression and localization of two-pore domain K(+) channels in bovine germ cells.
    Reproduction. 2009 Feb;137(2):237-44 PMID: 18987255
  119. Expression of a nonmyristylated variant of the catalytic subunit of protein kinase A during male germ-cell development.
    Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6433-8 PMID: 10841548
  120. A requirement of bicarbonate for Ca2+-induced elevations of cyclic AMP in guinea pig spermatozoa.
    J Biol Chem. 1982 Aug 10;257(15):8980-4 PMID: 6284752
  121. Regulation of transbilayer plasma membrane phospholipid asymmetry.
    J Lipid Res. 2003 Feb;44(2):233-42 PMID: 12576505
  122. Regulation of sperm storage and movement in the mammalian oviduct.
    Int J Dev Biol. 2008;52(5-6):455-62 PMID: 18649258
  123. Functions of lipid rafts in biological membranes.
    Annu Rev Cell Dev Biol. 1998;14:111-36 PMID: 9891780
  124. Lipid rafts and little caves. Compartmentalized signalling in membrane microdomains.
    Eur J Biochem. 2002 Feb;269(3):737-52 PMID: 11846775
  125. Phospholipid scramblase: an update.
    FEBS Lett. 2010 Jul 2;584(13):2724-30 PMID: 20302864
  126. Attenuated pain responses in mice lacking Ca(V)3.2 T-type channels.
    Genes Brain Behav. 2007 Jul;6(5):425-31 PMID: 16939637
  127. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect.
    Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):2993-8 PMID: 14976244
  128. Sodium-potassium-chloride cotransport.
    Physiol Rev. 2000 Jan;80(1):211-76 PMID: 10617769
  129. A perspective on the control of mammalian fertilization by egg-activated ion channels in sperm: a tale of two channels.
    Biol Reprod. 1998 Jul;59(1):12-6 PMID: 9674987
  130. Localization and age-dependent expression of the inward rectifier K+ channel subunit Kir 5.1 in a mammalian reproductive system.
    FEBS Lett. 1999 Apr 23;449(2-3):146-52 PMID: 10338121
  131. The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion.
    Mol Hum Reprod. 2002 Feb;8(2):124-35 PMID: 11818515
  132. Identification of distinct K+ channels in mouse spermatogenic cells and sperm.
    Zygote. 2002 May;10(2):183-8 PMID: 12056459
  133. 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
  134. Sensors and regulators of intracellular pH.
    Nat Rev Mol Cell Biol. 2010 Jan;11(1):50-61 PMID: 19997129
  135. Recombinant human ZP3-induced sperm acrosome reaction: evidence for the involvement of T- and L-type voltage-gated calcium channels.
    Biochem Biophys Res Commun. 2010 May 14;395(4):530-4 PMID: 20394732
  136. Sperm membrane potential: hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion.
    Dev Biol. 1995 Oct;171(2):554-63 PMID: 7556936
  137. Regulation of the epithelial Na(+) channel by intracellular Na(+).
    Am J Physiol. 1999 Aug;277(2):C216-24 PMID: 10444397
  138. Selective diffusion barriers separate membrane compartments.
    Biophys J. 2010 Jul 7;99(1):L1-3 PMID: 20655822
  139. 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
  140. CABYR isoforms expressed in late steps of spermiogenesis bind with AKAPs and ropporin in mouse sperm fibrous sheath.
    Reprod Biol Endocrinol. 2010 Aug 23;8:101 PMID: 20731842
  141. External Ca2+ acts upstream of adenylyl cyclase SACY in the bicarbonate signaled activation of sperm motility.
    Dev Biol. 2007 Dec 1;312(1):183-92 PMID: 17950270
  142. Tissue-specific PKA inhibition using a chemical genetic approach and its application to studies on sperm capacitation.
    Proc Natl Acad Sci U S A. 2008 Dec 30;105(52):20740-5 PMID: 19074277
  143. Sperm channel diversity and functional multiplicity.
    Reproduction. 2006 Jun;131(6):977-88 PMID: 16735537
  144. 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
  145. CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir.
    Reprod Fertil Dev. 2009;21(2):345-50 PMID: 19210926
  146. Investigation of the role of SRC in capacitation-associated tyrosine phosphorylation of human spermatozoa.
    Mol Hum Reprod. 2008 Apr;14(4):235-43 PMID: 18245108
  147. Membrane cholesterol, protein phosphorylation, and lipid rafts.
    Sci STKE. 2001 Jan 30;2001(67):pe1 PMID: 11752636
  148. 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
  149. 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
  150. 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
  151. Novel signaling pathways involved in sperm acquisition of fertilizing capacity.
    J Reprod Immunol. 2002 Jan;53(1-2):133-50 PMID: 11730911
  152. Sperm-specific protein kinase A catalytic subunit Calpha2 orchestrates cAMP signaling for male fertility.
    Proc Natl Acad Sci U S A. 2004 Sep 14;101(37):13483-8 PMID: 15340140
  153. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa.
    J Androl. 1991 Sep-Oct;12(5):323-30 PMID: 1765568
  154. Evolutionary genomics reveals lineage-specific gene loss and rapid evolution of a sperm-specific ion channel complex: CatSpers and CatSperbeta.
    PLoS One. 2008;3(10):e3569 PMID: 18974790
  155. Ion channels that control fertility in mammalian spermatozoa.
    Int J Dev Biol. 2008;52(5-6):607-13 PMID: 18649274
  156. Minimum and maximum extracellular Ca2+ requirements during mouse sperm capacitation and fertilization in vitro.
    J Reprod Fertil. 1987 Sep;81(1):77-89 PMID: 3668962
  157. Ca(2+)-related changes in the capacitation state of human spermatozoa assessed by a chlortetracycline fluorescence assay.
    J Reprod Fertil. 1993 Sep;99(1):135-43 PMID: 8283430
  158. Functions of phospholipid flippases.
    J Biochem. 2011 Feb;149(2):131-43 PMID: 21134888
  159. 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
  160. Development of a Mn-2+-sensitive, "soluble" adenylate cyclase in rat testis.
    Proc Natl Acad Sci U S A. 1975 Mar;72(3):1097-101 PMID: 1055368
  161. The capacitation of the mammalian sperm.
    Nature. 1952 Aug 23;170(4321):326 PMID: 12993150
  162. Molecular physiology of low-voltage-activated t-type calcium channels.
    Physiol Rev. 2003 Jan;83(1):117-61 PMID: 12506128
  163. 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
  164. Sperm surface proteomics: from protein lists to biological function.
    Mol Hum Reprod. 2010 Feb;16(2):68-79 PMID: 19717474
  165. Calcium channels in the development, maturation, and function of spermatozoa.
    Physiol Rev. 2011 Oct;91(4):1305-55 PMID: 22013213
  166. Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida.
    Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13004-9 PMID: 8917534
  167. Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation.
    J Biol Chem. 2007 Aug 17;282(33):24397-406 PMID: 17588945
Article Info
Journal
Asian journal of andrology
Abbr.
Asian J Androl
ISSN
1745-7262
Published
2011-05-00
Pages
395-405
Language
English
Region
China
NLM ID
100942132
PMCID
PMC3739340
Subset
IM
Grants
NICHD NIH HHS · R01 HD038082 · United States
NICHD NIH HHS · R01 HD044044 · United States
NICHD NIH HHS · R01 HD44044 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]