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K+ Channels in Cardiomyocytes of the Pulmonate Snail Helix

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Abstract

We used the patch-clamp technique to identify and characterize the electrophysiological, biophysical, and pharmacological properties of K+ channels in enzymatically dissociated ventricular cells of the land pulmonate snail Helix. The family of outward K+ currents started to activate at −30 mV and the activation was faster at more depolarized potentials (time constants: at 0 mV 17.4 ± 1.2 ms vs. 2.5 ± 0.1 ms at + 60 mV). The current waveforms were similar to those of the A-type family of voltage-dependent K+ currents encoded by Kv4.2 in mammals. Inactivation of the current was relatively fast, i.e., 50.2 ± 1.8% of current was inactivated within 250 ms at + 40 mV. The recovery of K+ channels from inactivation was relatively slow with a mean time constant of 1.7 ± 0.2 s. Closer examination of steady-state inactivation kinetics revealed that the voltage dependency of inactivation was U-shaped, exhibiting less inactivation at more depolarized membrane potentials. On the basis of this phenomenon, we suggest that a channel encoded by Kv2.1 similar to that in mammals does exist in land pulmonates of the Helix genus. Outward currents were sensitive to 4-aminopyridine and tetraethylammonium chloride. The last compound was most effective, with an IC 50 of 336 ± 142 µmol l−1. Thus, using distinct pharmacological and biophysical tools we identified different types of voltage-gated K+ channels.

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References

  1. S.I. Alekseev M.C. Ziskin (1995) ArticleTitleTwo types of A-channels in Lymnaea neurons. J. Membrane Biol. 146 327–341 Occurrence Handle1:CAS:528:DyaK2MXnslCnsbg%3D

    CAS  Google Scholar 

  2. R. Bahring L.M. Boland A. Varghese M. Gebauer O. Pongs (2001) ArticleTitleKinetic analysis of open- and closed-state inactivation transitions in human Kv4.2 A-type potassium channels. J. Physiol 535 65–81 Occurrence Handle1:CAS:528:DC%2BD3MXms12lt7g%3D Occurrence Handle11507158

    CAS  PubMed  Google Scholar 

  3. R. Bal M. Janahmadi G.G. Green D.J. Sanders (2001) ArticleTitleTwo kinds of transient outward currents, I A and I Adepol, in F76 and D1 soma membranes of the subesophageal ganglia of Helix aspersa. J. Membrane Biol. 179 71–78 Occurrence Handle10.1007/s002320010038 Occurrence Handle1:CAS:528:DC%2BD3MXitlWjsbY%3D

    Article  CAS  Google Scholar 

  4. B.L. Brezden P.R. Benjamin D.R. Gardner (1991) ArticleTitleThe peptide FMRFamide activates a divalent cation-conducting channel in heart muscle cells of the snail Lymnaea stagnalis. J. Physiol. 443 727–738 Occurrence Handle1:STN:280:By2A2cbivVM%3D Occurrence Handle1688028

    CAS  PubMed  Google Scholar 

  5. B.L. Brezden D.R. Gardner C.E. Morris (1986) ArticleTitleA potassium-selective channel in isolated Lymnaea stagnalis heart muscle cells. J. Exp. Biol. 123 175–189

    Google Scholar 

  6. B.L. Brezden M.S. Yeoman D.R. Gardner P.R. Benjamin (1999) ArticleTitleFMRFamide-activated Ca2+ channels in Lymnaea heart cells are modulated by “SEEPLY,” a neuropeptide encoded on the same gene. J. Neurophysiol. 81 1818–1826 Occurrence Handle1:CAS:528:DyaK1MXivV2jsro%3D Occurrence Handle10200216

    CAS  PubMed  Google Scholar 

  7. K.J. Buckett G.J. Dockray N.N. Osborne P.R. Benjamin (1990) ArticleTitlePharmacology of the myogenic heart of the pond snail Lymnaea stagnalis. J. Neurophysiol. 63 1413–1425 Occurrence Handle1:STN:280:By%2BB1MzovVc%3D Occurrence Handle1694238

    CAS  PubMed  Google Scholar 

  8. J.A. Connor C.F. Stevens (1971a) ArticleTitleInward and delayed outward membrane currents in isolated neural somata under voltage clamp. J. Physiol. 213 1–19 Occurrence Handle1:CAS:528:DyaE3MXhtV2htbY%3D

    CAS  Google Scholar 

  9. J.A. Connor C.F. Stevens (1971b) ArticleTitleVoltage clamp studies of a transient outward membrane current in gastropod neural somata. J. Physiol. 213 21–30 Occurrence Handle1:CAS:528:DyaE3MXhtV2htbc%3D

    CAS  Google Scholar 

  10. T.M. Curtis M.H. Depledge R. Williamson (1999) ArticleTitleVoltage-activated currents in cardiac myocytes of the blue mussel, Mytilus edulis. Comp. Biochem. Physiol A 124 231–241 Occurrence Handle10.1016/S1095-6433(99)00118-X

    Article  Google Scholar 

  11. J.S. Denton J.C. Leiter (2002) ArticleTitleAnomalous effects of external TEA on permeation and gating of the A-type potassium current in H. aspersa neuronal somata. J. Membrane Biol. 190 17–28 Occurrence Handle10.1007/s00232-002-1021-9 Occurrence Handle1:CAS:528:DC%2BD38Xos1amu74%3D

    Article  CAS  Google Scholar 

  12. Y. Furukawa E.R. Kandel P. Pfaffinger (1992) ArticleTitleThree types of early transient potassium currents in Aplysia neurons. J. Neurosci. 12 989–1000 Occurrence Handle1:CAS:528:DyaK38XitFWnsbc%3D Occurrence Handle1545247

    CAS  PubMed  Google Scholar 

  13. O.P. Hamill A. Marty E. Neher B. Sakmann F.J. Sigworth (1981) ArticleTitleImproved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pfluegers Arch. 391 85–100 Occurrence Handle1:STN:280:Bi2D3sjhvVw%3D

    CAS  Google Scholar 

  14. A.L. Hodgkin A.F. Huxley (1952) ArticleTitleCurrents carried by sodium and potassium ions through the membrane of the giant axon of Loligo. J. Physiol. 116 449–472 Occurrence Handle1:STN:280:Cy2D2snot1c%3D Occurrence Handle14946713

    CAS  PubMed  Google Scholar 

  15. H. Huddart R.B. Hill (1996) ArticleTitleModulatory mechanisms in the isolated internally perfused ventricle of the whelk Busycon canaliculatum. Gen. Pharmacol 27 809–818 Occurrence Handle10.1016/0306-3623(95)02111-6 Occurrence Handle1:CAS:528:DyaK28XltFGkt7k%3D Occurrence Handle8842683

    Article  CAS  PubMed  Google Scholar 

  16. G. Isenberg U. Klockner (1982) ArticleTitleCalcium tolerant ventricular myocytes prepared by preincubation in a “KB medium”. Pfluegers Arch. 395 6–18 Occurrence Handle1:STN:280:BiyD1M%2Fisl0%3D

    CAS  Google Scholar 

  17. K.G. Klemic C.C. Shieh G.E. Kirsch S.W. Jones (1998) ArticleTitleInactivation of Kv2.1 potassium channels. Biophys. J. 74 1779–1789 Occurrence Handle1:CAS:528:DyaK1cXislSktb4%3D Occurrence Handle9545040

    CAS  PubMed  Google Scholar 

  18. Kodirov, S., Zhuravlev, V., Kreye, V. 1995. The membrane conductance of cardiac single cells obtained from the edible snail, Helix pomatia, is carried mainly by K+ ions. In: The 8th Symposium on Invertebrate Neurobiology, Tihany, Hungary

  19. K Kuwasawa R. Hill (1997) ArticleTitleEvidence for cholinergic inhibitory and serotonergic excitatory neuromuscular transmission in the heart of the bivalve Mercenaria mercenaria. J. Exp. Biol 200 2123–2135 Occurrence Handle1:CAS:528:DyaK2sXls1Whsr4%3D Occurrence Handle9320037

    CAS  PubMed  Google Scholar 

  20. I. Maruyama C. Yoshida M. Kobayashi H. Oyamada K. Momose (1987) ArticleTitlePreparation of single smooth muscle cells from guinea pig taenia coli by combinations of purified collagenase and papain. J. Pharmacol Methods 18 151–161 Occurrence Handle10.1016/0160-5402(87)90008-8 Occurrence Handle1:CAS:528:DyaL2sXlslWqsb0%3D Occurrence Handle3041121

    Article  CAS  PubMed  Google Scholar 

  21. M.S. Nadal Y. Amarillo E Vega-Saenz de Miera B. Rudy (2001) ArticleTitleEvidence for the presence of a novel Kv4-mediated A-type K+ channel-modifying factor. J. Physiol. 537 801–809 Occurrence Handle10.1113/jphysiol.2001.013316 Occurrence Handle1:CAS:528:DC%2BD38XntVGltg%3D%3D Occurrence Handle11744756

    Article  CAS  PubMed  Google Scholar 

  22. E. Neher (1971) ArticleTitleTwo fast transient current components during voltage clamp on snail neurons. J. Gen. Physiol 58 36–53 Occurrence Handle1:STN:280:CS6B28jjtVw%3D Occurrence Handle5564761

    CAS  PubMed  Google Scholar 

  23. D. Pfrunder V.A. Kreye (1991) ArticleTitleTedisamil blocks single large-conductance Ca2+-activated K+ channels in membrane patches from smooth muscle cells of the guinea-pig portal vein. Pfluegers Arch. 418 308–312 Occurrence Handle1:STN:280:By6A2czjvVE%3D

    CAS  Google Scholar 

  24. B. Rudy K. Sen E Vega-Saenz de Miera D. Lau T. Ried D.C. Ward (1991) ArticleTitleCloning of a human cDNA expressing a high voltage-activating, TEA-sensitive, type-A K+ channel, which maps to chromosome 1 band p21. J. Neurosci. Res. 29 401–412 Occurrence Handle1:CAS:528:DyaK38XlsVCmtrw%3D Occurrence Handle1920536

    CAS  PubMed  Google Scholar 

  25. S.H. Thompson (1977) ArticleTitleThree pharmacologically distinct potassium channels in molluscan neurones. J. Physiol 265 465–488 Occurrence Handle1:CAS:528:DyaE2sXktVSltL8%3D Occurrence Handle850203

    CAS  PubMed  Google Scholar 

  26. J.S. Trimmer (1998) ArticleTitleRegulation of ion channel expression by cytoplasmic subunits. Curr. Opin. Neurobiol 8 370–374 Occurrence Handle10.1016/S0959-4388(98)80063-9 Occurrence Handle1:CAS:528:DyaK1cXktlCju7c%3D Occurrence Handle9687351

    Article  CAS  PubMed  Google Scholar 

  27. M.S. Yeoman P.R. Benjamin (1999) ArticleTitleTwo types of voltage-gated K+ currents in dissociated heart ventricular muscle cells of the snail Lymnaea stagnalis. J. Neurophysiol 82 2415–2427 Occurrence Handle1:CAS:528:DyaK1MXotVCjtbs%3D Occurrence Handle10561415

    CAS  PubMed  Google Scholar 

  28. M.S. Yeoman B.L. Brezden P.R. Benjamin (1999) ArticleTitleLVA and HVA Ca2+ currents in ventricular muscle cells of the Lymnaea heart. J. Neurophysiol 82 2428–2440 Occurrence Handle1:CAS:528:DyaK1MXotVCjtbg%3D Occurrence Handle10561416

    CAS  PubMed  Google Scholar 

  29. V. Zhuravlev V. Bugaj S. Kodirov T. Safonova A. Staruschenko (2001) ArticleTitleGiant multimodal heart motoneurons of Achatina fulica: a new cardioregulatory input in pulmonates. Comp. Biochem. Physiol A 130 183–196 Occurrence Handle10.1016/S1095-6433(01)00384-1 Occurrence Handle1:STN:280:DC%2BD3MrmsFGkuw%3D%3D

    Article  CAS  Google Scholar 

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Acknowledgements

The support of the Deutsche Forschungsgemeinschaft within SFB320 “Herzfunktion und ihre Regulation” is gratefully acknowledged. The authors greatly appreciate the excellent technical support of Isolde Villhauer and Klara Güth.

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Authors and Affiliations

  1. Department of Cardiology, Medical University Hospital Heidelberg, 69120 Heidelberg, Germany

    S. A. Kodirov & J. Brachmann

  2. Department of General Physiology, Saint Petersburg University, 199034 Saint Petersburg, Russia

    S. A. Kodirov, V. L. Zhuravlev & T. A. Safonova

  3. Department of Biophysics, Saint Petersburg University, 199034 Saint Petersburg, Russia

    S. A. Kodirov & V. K. Pavlenko

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  1. S. A. Kodirov
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  2. V. L. Zhuravlev
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  3. V. K. Pavlenko
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  4. T. A. Safonova
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  5. J. Brachmann
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Correspondence to S. A. Kodirov.

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Kodirov, S., Zhuravlev, V., Pavlenko, V. et al. K+ Channels in Cardiomyocytes of the Pulmonate Snail Helix . J. Membrane Biol. 197, 145–154 (2004). https://doi.org/10.1007/s00232-004-0649-z

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