Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지

Role of $Ca^{2+}$ and Calmodulin on the Initiation of Sperm Motility in Salmonid Fishes

  • Kho, Kang-Hee (Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo) ;
  • Morisawa, Masaaki (Misaki Marine Biological Station, Graduate School of Science, The University of Tokyo) ;
  • Choi, Kap-Seong (Department of Food Science and Technology, Sunchon National University)
  • Published : 2004.06.01
Download PDF
⟨ Previous Next ⟩

Abstract

$K^+$ efflux through a certain type of $K^+$ channels causes the change of membrane potential and leads to cAMP synthesis in the transmembrane cell signaling for the initiation of sperm motility in the salmonid fishes. The addition of $Ca^{2+}$ conferred motility to the trout sperm that were immobilized by external $K^+$ and other alkaline metals, $Rb^+$ and $Cs^{2+}$, suggesting the participation of external $Ca^{2+}$ in the initiation of sperm motility. L-type $Ca^{2+}$ channel blockers such as nifedipine, nimodipine, and FS-2 inhibited the motility, but N-type $Ca^{2+}$ channel blocker, w-conotoxin MvIIA, did not. On the other hand, the membrane hyperpolarization and cAMP synthesis were suppressed by $Ca^{2+}$ channel blockers, nifedipine, and trifluoroperazine. Furthermore, these suppressions were relieved by the addition of $K^+$ ionophore, valinomycin. Inhibitors of calmodulin, such as W-7, trifluoperazine, and calrnidazol-C1, inhibited the sperm motility, membrane hyperpolarization, and cAMP synthesis. The results suggest that $Ca^{2+}$ influx through $Ca^{2+}$ channels that are sensitive to specific $Ca^{2+}$ channel blockers and calmodulin participate in the changes of membrane potential, leading to synthesis of cAMP in the cell signaling for the initiation of trout sperm motility.

Keywords

References

  1. J. Reprod. Fertil. v.101 Regluation of flagellar motility of fowel spermatozoa: Evidence for the involvement of intracellular $Ca^{2＋}$ and calmodulin Ashizawa,K.;H.Tomonaga;Y.Tsuzuki https://doi.org/10.1530/jrf.0.1010265
  2. J. Reprod. Fertil. v.104 Regulatory mechanisms of fowel sperm motility: Possible role of endogenous myosin light chain kinase-like protein Ashizawa,K.;G.R.Wishart;Y.Tsuzuki https://doi.org/10.1530/jrf.0.1040141
  3. Proc. Natl. Acad. Sci. USA v.89 Early persistent activation of sperm $K^+$ channels by the egg peptide speract Babcock,D.F.;M.Mosma;D.E.Battaglia;A.Darszon https://doi.org/10.1073/pnas.89.13.6001
  4. J. Fish Biol. v.19 Rainbow trout, Salmo gairdneri Richardson, spermatozoa: Effects of cations and pH on motility Baynes,S.M.;A.P.Scott;A.P.Dawson https://doi.org/10.1111/j.1095-8649.1981.tb05830.x
  5. J. Cell Sci. v.98 Membrane hyperpolarization activates trout sperm without an increase in intracellular pH Boitano,S.;C.K.Omoto
  6. Cell Motil. Cytoskel. v.21 Trout sperm swimming patterns and role of intracellilar $Ca^{2＋}$ Boitano,S.;C.K.Omoto https://doi.org/10.1002/cm.970210109
  7. J. Cell Biol. v.111 Purification of sea urchin sperm adenylyl cylase Bookbinder,H.;G.W.Moy;V.D.Vacquier https://doi.org/10.1083/jcb.111.5.1859
  8. Anal. Biochem. v.72 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford,M.M. https://doi.org/10.1016/0003-2697(76)90527-3
  9. Cell Motil. Cytoskel. v.18 Calcium sensors in sea urchin sperm flagella Brokaw,C.J. https://doi.org/10.1002/cm.970180207
  10. J. Cell Biol. v.100 Modulation of the asymmetry of sea urchin sperm flagellar bending by calmodulin Brokaw,C.J.;S.M.Nagayama https://doi.org/10.1083/jcb.100.6.1875
  11. J. Biol. Chem. v.268 Selective modulation by cGMP of the $K^{+}$ channel activated by speract Cook,S.P.;D.F.Babcock
  12. J. Biol. Chem. v.268 Activation of $Ca^{2＋}$ permeability by cAMP is coordinated through the pH increase induced by speract Cook,S.P.;D.F.Babcock
  13. Cell Motil. Cytoskel. v.14 Rise of internal $Ca^{2＋}$ accompanies the initiation of trout sperm motility Cosson,M.P.;R.Billard;L.Letellier https://doi.org/10.1002/cm.970140312
  14. FEBS Lett. v.372 Mouse sperm membrane potential: Changes induced by $Ca^{2＋}$ Espinosa,F.;A.Darszon https://doi.org/10.1016/0014-5793(95)00962-9
  15. Dev. Biol. v.221 Participation of a $K^{＋}$ channel modulation directly by cGMP in the speract-induced signaling cascade of Strongylocentrout purpuratus sea urchin sperm Galindo,B.E.;C.Beltran;E.J.Cragoe;A.Darszon https://doi.org/10.1006/dbio.2000.9678
  16. Annu. Rev. Biochem. v.58 Molecular basis of fertilization Garbers,D.L. https://doi.org/10.1146/annurev.bi.58.070189.003443
  17. FEBS Lett. v.218 A first transient hyperpolarization occurs during the sea urchin sperm acrosome reaction induced by egg jelly Gonzalez-Martinez,M.T.;A.Darszon https://doi.org/10.1016/0014-5793(87)81055-4
  18. J. Biol. Chem. v.256 Sodium-dependent activation of sea urchin spermatozoa by speract and monesin Hansbrough,J.R.;D.L.Garbers
  19. J. Biol. Chem. v.262 Involvement of tyrosine kinase in the initiation of flagellar movement in rainbow trout spermatozoa Hayashi,H.;K.Yamamoto;H.Yonekawa;M.Morisawa
  20. J. Cell Sci. v.111 Proteasomes regulate the motility of salmonid fish sperm through modulation of cAMP-dependent phosphorylation of an outer arm dynein light chain Inaba,K.;S.Morisawa;M.Morisawa
  21. Zool. Sci. v.4 Effects of calmodulin antagoists on motility and acrosome reaction of sea urchin sperm Iwasa,F.;Y.Hasegawa;H.Mohri
  22. Dev. Biol. v.213 Membrane hyperpolarization by sperm activating and attraction factor increase cAMP level and activate sperm motility in the ascidian Ciona intestinalis Izumi,H.;K.Inaba;Y.Oka;M.Morisawa https://doi.org/10.1006/dbio.1999.9367
  23. J. Microbiol. Biotechnol. v.13 Membrane hyperpolarization increases cAMP to induce the initiation of sperm motility in salmonid fishes Koh,K.H.;M.Morisawa;K.S.Chol
  24. FEBS Lett. v.388 T-type $Ca^{2＋}$-channels and expression in spermatogenic cells, and their possibility relevance to the sperm acrosome reaction Lievano,A.;C.M.Santi;A.Darszon https://doi.org/10.1016/0014-5793(96)00515-7
  25. Cell v.13 A camp-induced increase in the mobility of demembraned bull sperm models Lindemann,C.B. https://doi.org/10.1016/0092-8674(78)90133-2
  26. Ann, NY. Acad. Sci. v.383 Regulation of the cytoskelton by $Ca^{2＋}$-calmodulin and cAMP Means,A.R.;J.S.Tash;V.Guerriero https://doi.org/10.1111/j.1749-6632.1982.tb23162.x
  27. Zool. Sci. v.11 Cell signaling mechanisms for sperm mobility Morisawa,M.
  28. Zool. Sci. v.2 Initiation mechanism of sperm motility at spawning in teleosts Morisawa,M.
  29. J. Exp. Zool. v.242 Short-term changes in levels of cyclic AMP, adenylatecyclase, and phosphodiesterase during the initiation of sperm motility in rainbow trout Morisawa,M.;K.Ishida https://doi.org/10.1002/jez.1402420211
  30. Zool. Sci. v.1 Initiation of sperm motility in Ciona intestinalis by calcium and cyclic AMP Morisawa,M.;S.Morisawa;R.D.Santis
  31. Nature v.295 Cyclic AMP induces maturation of trout sperm axoneme to initiate motility Morisawa,M.;M.Okuno https://doi.org/10.1038/295703a0
  32. Science v.210 Osmolarity and potassium ion: Their roles in initiation of sperm motility in teleosts Morisawa,M.;K.Suzuki https://doi.org/10.1126/science.7444445
  33. Biochem. Biophys. Res. Com. v.56 The activation of motility in quiescent hamster sperm from the epididymis by calcium and cyclic nucleotides Morton,B.;J.Hrrigan-Lum;L.Albabli;T.Jooss https://doi.org/10.1016/0006-291X(74)90852-3
  34. Dissertation. Life Science Institute, Graduate School of Science Nomura,M.
  35. Dev. Growth Differ. v.42 Cyclic AMP and calmodulin-dependent phosphorylation of 21 and 26 kDa proteins in axoneme is a prerequisite for SAAF-induced motile activation in ascidian spermatozoa Nomura,M.;K.Inaba;M.Morisawa https://doi.org/10.1046/j.1440-169x.2000.00489.x
  36. J. Biol. Chem. v.260 Sodium bicarbonate in seminal plasma stimulates the mobility of mammalian spermatozoa through direct activation of adenylyl cyclase Okamura,N.;Y.Tajima;Y.Sugita
  37. Cell Motil. Cytoskel. v.14 Effect of calcium on motility of rainbow trout sperm flagella demembraned with Triton X-100 Okuno,M.;M.Morisawa https://doi.org/10.1002/cm.970140206
  38. Am. J. Physiol. v.271 A dihydropyridine-sensitive T-type $Ca^{2＋}$ current is the main $Ca^{2＋}$ current carrier in mouse primary spermatocytes Santi,C.M.;A.Darszon;A.Hernandez https://doi.org/10.1152/ajpcell.1996.271.5.C1583
  39. Zool. Sci. v.12 Structure, function and biosynthesis of sperm-activating peptides and fucose sulfate glycoconjugate in the extracellular coat of sea urchin eggs Suzuki,N. https://doi.org/10.2108/zsj.12.13
  40. Biol. Reprod. v.30 Stimulation of sperm respiration rates by speract and resact at alkaline extracelluar pH Suzuki,N.;D.L.Garbers https://doi.org/10.1095/biolreprod30.5.1167
  41. Mol. Reprod. Dev. v.39 Implication that potassium flux and increase in intracellular calcium are necessary for the initiation of sperm motility in salmonid fishes Tanimoto,S.;Y.Kudo;T.Nakazawa;M.Morisawa https://doi.org/10.1002/mrd.1080390409
  42. Dev. Growth Diff. v.30 Roles of potassium and calcium channels in the initiation of sperm motility in rainbow trout Tanimoto,S.;M.Morisawa https://doi.org/10.1111/j.1440-169X.1988.00117.x
  43. J. Cell Biol. v.106 Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm Tash,J.S.;M.Krinks;R.L.Means;A.R.Means https://doi.org/10.1083/jcb.106.5.1625
  44. Biol. Reprod. v.28 Cyclic adenosine 3',5'-monophosphate, calcium and protein phosphorylation in flagellar motility Tash,J.S.;A.R.Means https://doi.org/10.1095/biolreprod28.1.75
  45. J. Cell Biol. v.101 Chemotaxis of Arbacia punctulata spermatozoa to resact, a peptide from egg jelly layer Ward,C.R.;C.J.Brokaw;D.L.Garbers;V.D.Vacquier https://doi.org/10.1083/jcb.101.6.2324
  46. Dev. Biol. v.158 Molecular events mediating sperm activation Ward,C.R.;G.S.Kopf https://doi.org/10.1006/dbio.1993.1165
  47. Dev. Growth Differ v.36 Calcium and cyclic AMP mediate sperm activation, but calcium alone contributes sperm chemotaxis in the ascidian, Ciona savignyi Yoshida,M.;K.Inaba;K.Ishida;M.Morisawa https://doi.org/10.1111/j.1440-169X.1994.00589.x
  48. Annu. Rev. Neurosci. v.15 Guanylyl cyclase-linked receptors Yuen,P.S.;D.L.Garbers https://doi.org/10.1146/annurev.ne.15.030192.001205