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PMID: 25271166 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

SLO3 K+ channels control calcium entry through CATSPER channels in sperm.

The Journal of biological chemistry ·Vol. 289 ·No. 46 ·2014-11-14 ·Pages 32266-32275

Chávez JC, Ferreira JJ, Butler A, De La Vega Beltrán JL, Treviño CL, Darszon A, Salkoff L, Santi CM

Abstract

Here we show how a sperm-specific potassium channel (SLO3) controls Ca(2+) entry into sperm through a sperm-specific Ca(2+) channel, CATSPER, in a totally unanticipated manner. The genetic deletion of either of those channels confers male infertility in mice. During sperm capacitation SLO3 hyperpolarizes the sperm, whereas CATSPER allows Ca(2+) entry. These two channels may be functionally connected, but it had not been demonstrated that SLO3-dependent hyperpolarization is required for Ca(2+) entry through CATSPER channels, nor has a functional mechanism linking the two channels been shown. In this study we show that Ca(2+) entry through CATSPER channels is deficient in Slo3 mutant sperm lacking hyperpolarization; we also present evidence supporting the hypothesis that SLO3 channels activate CATSPER channels indirectly by promoting a rise in intracellular pH through a voltage-dependent mechanism. This mechanism may work through a Na(+)/H(+) exchanger (sNHE) and/or a bicarbonate transporter, which utilizes the inward driving force of the Na(+) gradient, rendering it intrinsically voltage-dependent. In addition, the sperm-specific Na(+)/H(+) exchanger (sNHE) possess a putative voltage sensor that might be activated by membrane hyperpolarization, thus increasing the voltage sensitivity of internal alkalization.

Keywords
Calcium Calcium Channel Potassium Channel Sperm Spermatozoa pH Regulation
MeSH Terms
Animals Bicarbonates/chemistry Biological Transport Calcium/chemistry Calcium Channels/metabolism Fertility Gene Expression Regulation Hydrogen-Ion Concentration Ionomycin/chemistry Large-Conductance Calcium-Activated Potassium Channels/metabolism Male Mice Mice, Inbred C57BL Protons Sodium/chemistry Spermatozoa/metabolism Valinomycin/chemistry
Chemicals
Bicarbonates Calcium Channels Catsper1 protein, mouse Kcnu1 protein, mouse Large-Conductance Calcium-Activated Potassium Channels Protons Valinomycin Ionomycin Sodium Calcium
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Chávez Julio César
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 and; Instituto de Biotecnología, Universidad Nacional Autónoma de México (UNAM), 62210 Cuernavaca, México.
Ferreira Juan José
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 and.
Butler Alice
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 and.
De La Vega Beltrán José Luis
Instituto de Biotecnología, Universidad Nacional Autónoma de México (UNAM), 62210 Cuernavaca, México.
Treviño Claudia L
Instituto de Biotecnología, Universidad Nacional Autónoma de México (UNAM), 62210 Cuernavaca, México.
Darszon Alberto
Instituto de Biotecnología, Universidad Nacional Autónoma de México (UNAM), 62210 Cuernavaca, México.
Salkoff Lawrence
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 and.
Santi Celia M
Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri 63110 and.
References (58)
58 references, click to expand
  1. A new sperm-specific Na+/H+ exchanger required for sperm motility and fertility.
    Nat Cell Biol. 2003 Dec;5(12):1117-22 PMID: 14634667
  2. Intracellular pH regulates bovine sperm motility and protein phosphorylation.
    Biol Reprod. 1989 Nov;41(5):907-20 PMID: 2624855
  3. Slo3, a novel pH-sensitive K+ channel from mammalian spermatocytes.
    J Biol Chem. 1998 Feb 6;273(6):3509-16 PMID: 9452476
  4. 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
  5. Role of the ionic environment and internal pH on sperm activity.
    Hum Reprod. 1998 Dec;13 Suppl 4:20-30 PMID: 10091055
  6. Egg coat proteins activate calcium entry into mouse sperm via CATSPER channels.
    Biol Reprod. 2009 Jun;80(6):1092-8 PMID: 19211808
  7. K+ and Cl- channels and transporters in sperm function.
    Curr Top Dev Biol. 2013;102:385-421 PMID: 23287041
  8. Ion permeabilities in mouse sperm reveal an external trigger for SLO3-dependent hyperpolarization.
    PLoS One. 2013;8(4):e60578 PMID: 23577126
  9. Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa.
    J Androl. 1991 Sep-Oct;12(5):323-30 PMID: 1765568
  10. Solubilization and partial purification from mouse sperm membranes of the specific binding activity for 3-quinuclidinyl benzilate, a potent inhibitor of the zona pellucida-induced acrosome reaction.
    Mol Reprod Dev. 1994 Dec;39(4):423-32 PMID: 7893491
  11. A fast transient hyperpolarization occurs during the sea urchin sperm acrosome reaction induced by egg jelly.
    FEBS Lett. 1987 Jun 29;218(2):247-50 PMID: 3595869
  12. 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
  13. The SLO3 sperm-specific potassium channel plays a vital role in male fertility.
    FEBS Lett. 2010 Mar 5;584(5):1041-6 PMID: 20138882
  14. Observations on the penetration of the sperm in the mammalian egg.
    Aust J Sci Res B. 1951 Nov;4(4):581-96 PMID: 14895481
  15. The role of Hv1 and CatSper channels in sperm activation.
    J Physiol. 2010 Dec 1;588(Pt 23):4667-72 PMID: 20679352
  16. Membrane hyperpolarization during human sperm capacitation.
    Mol Hum Reprod. 2014 Jul;20(7):619-29 PMID: 24737063
  17. A depolarization can trigger Ca2+ uptake and the acrosome reaction when preceded by a hyperpolarization in L. pictus sea urchin sperm.
    Dev Biol. 1992 Mar;150(1):193-202 PMID: 1371478
  18. Determination of the time course of capacitation in mouse spermatozoa using a chlortetracycline fluorescence assay.
    Dev Biol. 1984 Aug;104(2):287-96 PMID: 6745485
  19. 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
  20. 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
  21. Heartburn: cardiac potassium channels involved in parietal cell acid secretion.
    Pflugers Arch. 2003 May;446(2):143-7 PMID: 12684798
  22. 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
  23. ZP3-dependent activation of sperm cation channels regulates acrosomal secretion during mammalian fertilization.
    J Cell Biol. 1996 Aug;134(3):637-45 PMID: 8707844
  24. Effects of pH on the reactivation of human spermatozoa demembranated with Triton X-100.
    Mol Reprod Dev. 1991 Jun;29(2):157-62 PMID: 1878224
  25. Internal pH can regulate Ca2+ uptake and the acrosome reaction in sea urchin sperm.
    Dev Biol. 1987 Mar;120(1):112-20 PMID: 3817283
  26. Intracellular calcium increases with hyperactivation in intact, moving hamster sperm and oscillates with the flagellar beat cycle.
    Proc Natl Acad Sci U S A. 1993 May 15;90(10):4660-4 PMID: 8506314
  27. Potassium-dependent increases in cytosolic pH stimulate metabolism and motility of mammalian sperm.
    Proc Natl Acad Sci U S A. 1983 Mar;80(5):1327-31 PMID: 6572391
  28. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel.
    Nature. 2006 Feb 9;439(7077):737-40 PMID: 16467839
  29. Simultaneous knockout of Slo3 and CatSper1 abolishes all alkalization- and voltage-activated current in mouse spermatozoa.
    J Gen Physiol. 2013 Sep;142(3):305-13 PMID: 23980198
  30. Fertilizing capacity of spermatozoa deposited into the fallopian tubes.
    Nature. 1951 Oct 20;168(4277):697-8 PMID: 14882325
  31. 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
  32. Modulation of the voltage-sensitive Na+/H+ exchange in sea urchin spermatozoa through membrane potential changes induced by the egg peptide speract.
    J Biol Chem. 1986 Dec 5;261(34):16026-32 PMID: 2430965
  33. Inhibition of bovine spermatozoa by caudal epididymal fluid: II. Interaction of pH and a quiescence factor.
    Biol Reprod. 1984 May;30(4):926-35 PMID: 6329337
  34. Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation.
    J Biol Chem. 2003 Feb 28;278(9):7001-9 PMID: 12496293
  35. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP.
    Dev Biol. 2002 Oct 1;250(1):208-17 PMID: 12297107
  36. External ionic conditions, internal pH and motility of ram and boar spermatozoa.
    J Reprod Fertil. 1993 Jul;98(2):439-49 PMID: 8410809
  37. 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
  38. Regulation of intracellular pH in capacitated human spermatozoa by a Na+/H+ exchanger.
    Mol Reprod Dev. 1999 Feb;52(2):189-95 PMID: 9890750
  39. CATSPER channel-mediated Ca2+ entry into mouse sperm triggers a tail-to-head propagation.
    Biol Reprod. 2007 Sep;77(3):551-9 PMID: 17554080
  40. 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
  41. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel.
    Cell. 2010 Feb 5;140(3):327-37 PMID: 20144758
  42. The Ca2+-activated K+ current of human sperm is mediated by Slo3.
    Elife. 2014 Mar 26;3:e01438 PMID: 24670955
  43. Bovine sperm hyperactivation is promoted by alkaline-stimulated Ca2+ influx.
    Biol Reprod. 2007 Apr;76(4):660-5 PMID: 17182893
  44. Slo1 is the principal potassium channel of human spermatozoa.
    Elife. 2013 Oct 08;2:e01009 PMID: 24137539
  45. Signaling pathways in sperm capacitation and acrosome reaction.
    Cell Mol Biol (Noisy-le-grand). 2003 May;49(3):321-7 PMID: 12887084
  46. A sperm ion channel required for sperm motility and male fertility.
    Nature. 2001 Oct 11;413(6856):603-9 PMID: 11595941
  47. Intracellular pH in sperm physiology.
    Biochem Biophys Res Commun. 2014 Aug 1;450(3):1149-58 PMID: 24887564
  48. 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
  49. 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
  50. Sperm membrane potential: hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion.
    Dev Biol. 1995 Oct;171(2):554-63 PMID: 7556936
  51. A novel testis-specific Na+/H+ exchanger is involved in sperm motility and fertility.
    Front Biosci (Elite Ed). 2010 Jan 01;2:566-81 PMID: 20036903
  52. Intracellular pH of bovine sperm increases during capacitation.
    Mol Reprod Dev. 1995 Apr;40(4):490-502 PMID: 7598914
  53. Stroboscopic illumination using light-emitting diodes reduces phototoxicity in fluorescence cell imaging.
    Biotechniques. 2006 Aug;41(2):191-7 PMID: 16925021
  54. 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
  55. SLC9/NHE gene family, a plasma membrane and organellar family of Na⁺/H⁺ exchangers.
    Mol Aspects Med. 2013 Apr-Jun;34(2-3):236-51 PMID: 23506868
  56. Control of hyperactivation in sperm.
    Hum Reprod Update. 2008 Nov-Dec;14(6):647-57 PMID: 18653675
  57. 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
  58. 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
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2014-11-14
Epub
2014-00-30
Pages
32266-32275
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC4231700
Subset
IM
Grants
NICHD NIH HHS · R01 HD038082 · United States
NICHD NIH HHS · R01 HD069631 · United States
NICHD NIH HHS · R01HD038082 · United States
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