online ISSN 2415-3176
print ISSN 1609-6371
logoExperimental and Clinical Physiology and Biochemistry
  • 3 of 16
Up
ECPB 2015, 71(3): 20–26
https://doi.org/10.25040/ecpb2015.03.020
Experimental physiology and biochemistry

Рassive ion-transporting systems of sodium and calcium ions in mammalian spermatozoa

MAKAR N.
Abstract

The article summarizes and analyzes published material related to the functioning and properties of passive ion-transporting systems in mammalian, in particular human spermatozoa. Transporting systems of Ca2+ and Na+ and their impact on sperm functional status and mammals fertility were described. Close attention was given to ion-transporting systems, the presence of which is proved in human spermatozoa.

Ion channels regulate the membrane potential and intracellular ionic concentration and thus serve a central role in various cellular processes. Several ion channels have been identified in the sperm plasma membrane, emphasizing their importance in male fertility and reproduction. They are essential for sperm motility, sperm activation, the acrosome reaction, and the journey toward the egg for fertilization.

The novel class of Ca2+ channels Catsper has been identified in human sperm and shown to be essential for mammalian hyperactivated sperm motility, sperm detachment from the female reproductive tract and egg coat penetration and fertility. Recent works suggest that CatSper may contribute to the [Ca2+]i increase that accompanies the acrosome reaction.

CatSper channels are constitutively active, weakly voltage-dependent, Ca-selective and strongly potentiated by intracellular alkalinization.

CatSper’s pore is formed by four α subunits Catsper1, Catsper2, Catsper3, Catsper4 and three auxiliary subunits – CatSperβ, CatSperγ, and CatSperδ. All four CatSper subunits (1–4) are needed for functional expression in mouse sperm, as knockout of any one of them results in absence of the other subunits in mature sperm with the consequent observation of male infertility and the lack of the CatSper associated currents. The absence of a single subunit may lead to degradation of remaining CatSper proteins.

Humans with mutations or deletions in CatSper1 and CatSper2 are infertile. It is suspected that loss-of-function mutations in any of the seven known CatSper subunits result in male infertility. CatSper1-/- male mice also display defects in cAMP and depolarization-induced calcium entry.

Other transporters appear as main candidates responsible for Ca2+ influx are voltagegated calcium channels CaVs. They convert changes of membrane potential into calcium signals. Though transcripts and proteins for both high voltage-activated and low voltage-activated types of CaV have been detected in mammalian sperm, electrophysiological evidence has mainly revealed the functional presence of CaV3 channels in mouse and human spermatogenic cells. It was proposed that they participate in acrosome reaction.

The presence of voltage-dependent Na+ channels NaV in human sperm was reported and supports a role for these channels in the regulation of mature sperm function. NaV channels could play a crucial role in noncapacitated sperm and in the initial capacitation steps.

ENaCs are present in mouse and human sperm. These channels may be regulated by рН, Са2+, Na+, Cl– and phosphorylation, parameters that change during capacitation. These channels are Na-selective, amiloride-sensitive and contribute to the resting membrane potential in cells by displacing it towards the Na+ equilibrium potential.

Mentioned ion channels control the sperm ability to fertilize the egg by regulating sperm maturation in the female reproductive tract and by triggering key sperm physiological responses required for successful fertilization such as hyperactivated motility, acrosome reaction.

Keywords: spermatozoa, ion transport, ion channels, calcium, sodium

Full text: PDF (Ukr) 1.14M

References
  1. 1. Avdonin P, Tkachuk V. Receptors and intracellular calcium. Moscow: Nauka; 1994. 288.
  2. 2. Vyslobokov A, Kopylov А, Bovtyushko V. Calcium channels of cellular membranes. Uspehi physiol. nauk. 1995;26(1):93 109.
  3. 3. Vorobets Z, Chupashko О, Terletska О. The level of lipid peroxidation and activity of Са2+, Мg2+ ATPase in normal and tumor cells under the influence of polypeptide growth factors. Visn. probl. boil. i med. 1998;4:21 27.
  4. 4. Zvarich Y. Са2+-АТРase of plasma membranes. Structure and functions. Biol. membrany. 1991;8(6):565 585.
  5. 5. Kosterin S. Kinetic and energy aspects of influence of the dielectric permeability of incubation medium on the catalytic and transport activity of Мg2+, АТР -dependent calcium pump of the plasma membrane. Ukr. biohim. zhurnal. 2000;72(4 5):44 59).
  6. 6. Kostyuk P. Calcium and cellular excitability. Moscow: Nauka; 1986. 254.
  7. 7. Kurskii M, Vorobets Z. A mechanism of passive transport of calcium in muscle sarcoplasmic reticulum. Ukr. biohim. zhurnal. 1989;61(6):З 13.
  8. 8. Kurskii M, Vorobets Z, Kosterin S. Regulation of intracellular calcium сoncentration in muscles. Кyiv: Naukova dumka; 1987. 144.
  9. 9. Tkachuk V. Membrane receptors and intracellular calcium. Biol. membr. 1999;16(2):212 229.
  10. 10. Tkachuk V. Phosphoinositide metabolism and Са2+ oscillation. Biochemistry. 1998; 63(1):47 56.
  11. 11. Arnoult C, Cardullo R, Lemos J, Florman H. Activation of mouse sperm T-type Ca2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci, USA. 1996;93:13004-13009. doi.org/10.1073/pnas.93.23.13004
  12. 12. Arnoult C, Kazam I, Visconti P, Kopf G, Villaz M, Florman H. Control of the low voltageactivated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci, USA. 1999;96:6757-6762. doi.org/10.1073/pnas.96.12.6757
  13. 13. Avenarius M, Hildebrand M, Zhang Y, Meyer N, Smith L, Kahrizi K et al. Human male infertility caused by mutations in the CATSPER1 channel protein. Am. J. Hum. Genet. 2009;84:505-510.
  14. 14. Avidan N, Tamary H, Dgany O, Cattan D, Pariente A, Thulliez M et al. CATSPER2, a human autosomal nonsyndromic male infertility gene. Eur. J. Hum. Genet. 2003;11:497-502.
  15. 15. Awayda M. Regulation of the epithelial Na+ channel by intracellular Na+. Am J Physiol. 1999;277:216-224.
  16. 16. Beuckmann C, Sinton C, Miyamoto N. N-type calcium channel α1B subunit (CaV2.2) knock-out mice display hyperactivity and vigilance state differences. J. Neurosci. 2003;23:6793-6797.
  17. 17. Carlson A, Quill T, Westenbroek R, Schuh S, Hille B, Babcock D. Identical phenotypes of CatSper1 and CatSper2 null sperm. J. Biol. Chem. 2005;280:32238-32244.
  18. 18. Carlson A, Westenbroek R, Quill T, Ren D, Clapham D, Hille B et al.CatSper1 required for evoked Ca2+ entry and control of flagellar function in sperm. Proc Natl Acad Sci, USA. 2003;100:14864-14868. doi.org/10.1073/pnas.2536658100
  19. 19. Chung J, Navarro B, Krapivinsky G, Krapivinsky L • Clapham D. A novel gene required for male fertility and functional CATSPER channel formation in spermatozoa. Nat. Commun. 2011;2:153.
  20. 20. Clapham D. Calcium signaling. Cell. 2007;131:1047-1058. doi.org/10.1016/j.cell.2007.11.028
  21. 21. Darszon A, Acevedo J, Galindo B, Beltran C. Sperm channel diversity and functional multiplicity. Reproduction. 2006;131:977-988. doi.org/10.1530/rep.1.00612
  22. 22. Florman H, Arnoult C, Kazam I, Li C, O'Toole C. A perspective on the control of mammalian fertilization by egg-activated ion channels in sperm: a tale of two channels. Biol. Reprod. 1998;59:12-16. doi.org/10.1095/biolreprod59.1.12
  23. 23. Foresta C, Rossato M, Chiozzi P, Di Virgilio F. Mechanism of human sperm activation by extracellular ATP. Am. J. Physiol. Cell Physiol. 1996;270:1709-1714.
  24. 24. Harper C, Barratt C, Publicover S. Stimulation of human spermatozoa with progesterone gradients to simulate approach to the oocyte. J. Biol. Chem. 2004;279:46315-46325.
  25. 25. Hernández-González E, Sosnik J, Edwards J, Acevedo J, Mendoza-Lujambio I, López-González I et al. Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm. J. Biol. Chem. 2006;281:5623-5633.
  26. 26. Hildebrand M, Avenarius M, Fellous M, Zhang Y, Meyer N, Auer J et al.Genetic male infertility and mutation of CATSPER ion channels. Eur. J.Hum.Genet. 2010;18:1178-1184.
  27. 27. Ho H, Suarez S. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol. Reprod. 2003;68:1590-1596. doi.org/10.1095/biolreprod.102.011320
  28. 28. Ho K, Wolff C, Suarez S. CatSper-null mutant spermatozoa are unable to ascend beyond the oviductal reservoir. Reprod. Fertil. Dev. 2009;21:345-350.
  29. 29. Jose O, Hernandez-Hernandez O, Chirinos M, Gonzalez-Gonzalez M, Larrea F, Almanza A et al. 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;395:530-534.
  30. 30. Jun K, Piedras-Rentería E, Smith S, Wheeler D, Lee S, Lee T et al. Ablation of P/Q-type Ca2+ channel currents, altered synaptic transmission, and progressive ataxia in mice lacking the α1A-subunit. Proc. Natl. Acad. Sci. USA. 1999;96:15245-15250. doi.org/10.1073/pnas.96.26.15245
  31. 31. Kellenberger S, Schild L. Epithelial sodium channel/degenerin family of ion channels: a variety of functions for a shared structure. Physiol. Rev. 2002;82:735-767.
  32. 32. Kim D, Song I, Keum S, Lee T, Jeong M, Kim S et al.Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking α1G T-type Ca2+ channels. Neuron. 2001;31:35-45. doi.org/10.1016/S0896-6273(01)00343-9
  33. 33. Kirichok Y, Navarro B, Clapham D. Whole-cell patch-clamp measurements of spermatozoa reveal an alkaline-activated Ca2+ channel. Nature. 2006;439:737 740. doi.org/10.1038/nature04417
  34. 34. Lievano A, Santi C, Serrano C, Darszon A. T-type Ca2+ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett. 1996;388:150-154. doi.org/10.1016/0014-5793(96)00515-7
  35. 35. Lishko P, Botchkina I, Fedorenko A, Kirichok Y. Acid extrusion from human spermatozoa is mediated by flagellar voltage-gated proton channel. Cell. 2010;140:327 337. doi.org/10.1016/j.cell.2009.12.053
  36. 36. Lishko P, Botchkina I, Kirichok Y. Progesterone activates the principal Ca2+ channel of human sperm. Nature. 2011;471:387-391. doi.org/10.1038/nature09767
  37. 37. Lishko P, Kirichok Y. The role of Hv1 and CatSper channels in sperm activation. J. Physiol. 2010;588:4667-4672. doi.org/10.1113/jphysiol.2010.194142
  38. 38. Liu J, Xia J, Cho K, Clapham D, Ren D. CatSperв, a novel transmembrane protein in the CatSper channel complex. J. Biol. Chem. 2007;282:18945-18952.
  39. 39. Lobley A, Pierron V, Reynolds L, Allen L, Michalovich D. Identification of human and mouse CatSper3 and CatSper4 genes: characterisation of a common interaction domain and evidence for expression in testis. Reprod. Biol. Endocrinol. 2003;1:53.
  40. 40. Marquez B, Suarez S. Bovine sperm hyperactivation is promoted by alkaline-stimulated Ca2+ influx. Biol. Reprod. 2007;76:660 665. doi.org/10.1095/biolreprod.106.055038
  41. 41. Martinez-Lopez P, Trevino C, De La Vegabeltran J, De Blas G. TRPM8 in mouse sperm detects temperature changes and may influence the acrosome reaction. J. Cell. Physiol. e-pub ahead of print 10 November 2010; doi: 10.1002/ jcp.22493.
  42. 42. Navarro B, Kirichok Y, Chung J , Clapham D. Ion channels that control fertility in mammalian spermatozoa. Int. J. Dev. Biol. 2008;52:607-613.
  43. 43. Nicholls D, Chalmers S. The integration of mitochondrial calcium transport and storage. J. Bioenerg. Biomembr. 2004;36:1573-6881.
  44. 44. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol. Rev. 2003;83:117-161.
  45. 45. Pinto F, Ravina C, Fernández-Sánchez М, Gallardo-Castro M, Cejudo-Román A, Candenas L. Molecular and functional characterization of voltage-gated sodium channels in human sperm. Reprod. Biol. Endocrinol. 2009;7:71.
  46. 46. Publicover S, Barratt C. Voltage-operated Ca2+ channels and the acrosome reaction: which channels are present and what do they do? Hum. Reprod. 1999;14:873-879. doi.org/10.1093/humrep/14.4.873
  47. 47. Qi H, Moran M, Navarro B, Chong J, Krapivinsky G, Krapivinsky L et al. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc. Natl. Acad. Sci. USA. 2007;104:1219-1223. doi.org/10.1073/pnas.0610286104
  48. 48. Quill T, Sugden S, Rossi K, Doolittle L, Hammer R, Garbers D. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc. Natl. Acad. Sci. USA. 2003;100:14869-14874. doi.org/10.1073/pnas.2136654100
  49. 49. Ren D, Navarro B, Perez G, Jackson A, Hsu S, Shi Q et al. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413:603-609. doi.org/10.1038/35098027
  50. 50. Ren D, Xia J. Calcium signaling through CatSper channels in mammalian fertilization. Physiology (Bethesda). 2010;25:165-175. doi.org/10.1152/physiol.00049.2009
  51. 51. Saegusa H, Kurihara T, Zong S, Minowa O, Kazuno A, Han W et al. Altered pain responses in mice lacking α1E subunit of the voltage-dependent Ca2+ channel. Proc. Natl. Acad. Sci. USA. 2000;97:132-137.
  52. 52. Santi C, Darszon A, Hernandez-Cruz A. A dihydropyridine-sensitive T-type Ca2+ current is the main Ca2+ current carrier in mouse primary spermatocytes. Am. J. Physiol. 1996;271:1583-1593.
  53. 53. Seisenberger C, Specht V, Welling A et al. Functional embryonic cardiomyocytes after disruption of the L-type α1C (Cav1.2) calcium channel gene in the mouse. J. Biol. Chem. 2000;275:39193-–39199.
  54. 54. Wang D, Hu J, Bobulescu I et al. 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. USA. 2007;104:9325-9330. doi.org/10.1073/pnas.0611296104
  55. 55. Wang H, Liu J, Cho K et al. Anovel, single, transmembrane protein CATSPERG is associated with CATSPER1 channel protein. Biol. Reprod. 2009;81:539-544. doi.org/10.1095/biolreprod.109.077107
  56. 56. Wertheimer E, Salicioni A, Liu W et al. Chloride Is essential for capacitation and for the capacitation-associated increase in tyrosine phosphorylation. J. Biol. Chem. 2008;283:35539-355550.
  57. 57. Wiesner B, Weiner J, Middendorff R et al. Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J.Cell Biol. 1998;142:473-484. doi.org/10.1083/jcb.142.2.473
  58. 58. Zhang Y, Malekpour M, Al-Madani N et al. Sensorineural deafness and male infertility: a contiguous gene deletion syndrome. J. Med. Genet. 2007; 44: 233-240.


Програмування - Roman.im