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. 1983 Jun 1;81(6):805–827. doi: 10.1085/jgp.81.6.805

Mn ions pass through calcium channels. A possible explanation

PMCID: PMC2215560  PMID: 6308126

Abstract

The divalent transition-metal cations Fe, Co, and Ni were used to test the hypothesis that Mn ions pass through calcium channels because Mn ions have a relatively low energy of hydration. The test ions were applied to the bath and comparisons were made of their effects on Ca or Mn spikes elicited from myoepithelial cells of the proventriculus of the polychaete worm Syllis spongiphila. Control experiments showed that (a) results obtained using deoxygenated solutions (required to stabilize Fe2+ ions) could be compared with those using solutions containing oxygen, and (b) the test cations did not measurably affect the electrical coupling between cells. Ca spikes were reversibly abolished by the test cations in the order of effectiveness: Fe (16.1 mM +/- 1.0, SE; n = 15) = Co (14.6 mM +/- 0.8; n = 27) less than Ni (8.3 mM +/- 0.7; n = 16). The test cations diminished Mn spikes by decreasing maximum rates of rise (Fe = Co less than Ni) and overshoot amplitudes (Fe less than Co less than Ni). The test cations also increased the current intensity required for Ca (Fe = Co less than Ni) or Mn spike initiation (Fe less than Co less than Ni). Since the energies of hydration of Fe, Co, and Ni increase stepwise from that of Mn, and the effectiveness of these ions in diminishing Ca and Mn spikes increased in the order Fe less than or equal to Co less than Ni, these data support the hypothesis that Mn ions pass through Ca channels because they shed waters of hydration relatively easily. An additional observation was that, at below-blocking concentrations, the test cations caused decreased duration of Mn spikes and increased duration of Ca spikes.

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Selected References

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  1. Adams D. J., Dwyer T. M., Hille B. The permeability of endplate channels to monovalent and divalent metal cations. J Gen Physiol. 1980 May;75(5):493–510. doi: 10.1085/jgp.75.5.493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Anderson M. Mn2+ ions pass through Ca2+ channels in myoepithelial cells. J Exp Biol. 1979 Oct;82:227–238. doi: 10.1242/jeb.82.1.227. [DOI] [PubMed] [Google Scholar]
  3. Anderson M., del Castillo J. Electrical activity of the proventriculus of the polychaete worm Syllis spongiphila. J Exp Biol. 1976 Jun;64(3):691–710. doi: 10.1242/jeb.64.3.691. [DOI] [PubMed] [Google Scholar]
  4. Bennett M. V. Physiology of electrotonic junctions. Ann N Y Acad Sci. 1966 Jul 14;137(2):509–539. doi: 10.1111/j.1749-6632.1966.tb50178.x. [DOI] [PubMed] [Google Scholar]
  5. Brehm P., Eckert R. Calcium entry leads to inactivation of calcium channel in Paramecium. Science. 1978 Dec 15;202(4373):1203–1206. doi: 10.1126/science.103199. [DOI] [PubMed] [Google Scholar]
  6. EISENMAN G. Cation selective glass electrodes and their mode of operation. Biophys J. 1962 Mar;2(2 Pt 2):259–323. doi: 10.1016/s0006-3495(62)86959-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Eaton D. C., Brodwick M. S. Effects of barium on the potassium conductance of squid axon. J Gen Physiol. 1980 Jun;75(6):727–750. doi: 10.1085/jgp.75.6.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Edwards C. The selectivity of ion channels in nerve and muscle. Neuroscience. 1982 Jun;7(6):1335–1366. doi: 10.1016/0306-4522(82)90249-4. [DOI] [PubMed] [Google Scholar]
  9. FRANKENHAEUSER B., HODGKIN A. L. The action of calcium on the electrical properties of squid axons. J Physiol. 1957 Jul 11;137(2):218–244. doi: 10.1113/jphysiol.1957.sp005808. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Fukuda J., Kawa K. Permeation of manganese, cadmium, zinc, and beryllium through calcium channels of an insect muscle membrane. Science. 1977 Apr 15;196(4287):309–311. doi: 10.1126/science.847472. [DOI] [PubMed] [Google Scholar]
  11. Gorman A. L., Hermann A. Internal effects of divalent cations on potassium permeability in molluscan neurones. J Physiol. 1979 Nov;296:393–410. doi: 10.1113/jphysiol.1979.sp013012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hagiwara S., Byerly L. Calcium channel. Annu Rev Neurosci. 1981;4:69–125. doi: 10.1146/annurev.ne.04.030181.000441. [DOI] [PubMed] [Google Scholar]
  13. Hagiwara S. Ca spike. Adv Biophys. 1973;4:71–102. [PubMed] [Google Scholar]
  14. Hagiwara S. Ca-dependent action potential. Membranes. 1975;3:359–381. [PubMed] [Google Scholar]
  15. Hagiwara S., Fukuda J., Eaton D. C. Membrane currents carried by Ca, Sr, and Ba in barnacle muscle fiber during voltage clamp. J Gen Physiol. 1974 May;63(5):564–578. doi: 10.1085/jgp.63.5.564. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hagiwara S., Miyazaki S. Ca and Na spikes in egg cell membrane. Prog Clin Biol Res. 1977;15:147–158. [PubMed] [Google Scholar]
  17. Hagiwara S., Takahashi K. Surface density of calcium ions and calcium spikes in the barnacle muscle fiber membrane. J Gen Physiol. 1967 Jan;50(3):583–601. doi: 10.1085/jgp.50.3.583. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Hermann A., Gorman A. L. Blockade of voltage-dependent and Ca2+-dependent K+ current components by internal Ba2+ in molluscan pacemaker neurons. Experientia. 1979 Feb 15;35(2):229–231. doi: 10.1007/BF01920633. [DOI] [PubMed] [Google Scholar]
  19. Hille B. An essential ionized acid group in sodium channels. Fed Proc. 1975 Apr;34(5):1318–1321. [PubMed] [Google Scholar]
  20. Hille B. Ionic selectivity of Na and K channels of nerve membranes. Membranes. 1975;3:255–323. [PubMed] [Google Scholar]
  21. Hille B. Ionic selectivity, saturation, and block in sodium channels. A four-barrier model. J Gen Physiol. 1975 Nov;66(5):535–560. doi: 10.1085/jgp.66.5.535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hille B. The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol. 1972 Jun;59(6):637–658. doi: 10.1085/jgp.59.6.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Hille B., Woodhull A. M., Shapiro B. I. Negative surface charge near sodium channels of nerve: divalent ions, monovalent ions, and pH. Philos Trans R Soc Lond B Biol Sci. 1975 Jun 10;270(908):301–318. doi: 10.1098/rstb.1975.0011. [DOI] [PubMed] [Google Scholar]
  24. Keatinge W. R. Mechanism of slow discharges of sheep carotid artery. J Physiol. 1978 Jun;279:275–289. doi: 10.1113/jphysiol.1978.sp012344. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mangum D. C. Sea anemone neuromuscular responses in anaerobic conditions. Science. 1980 Jun 6;208(4448):1177–1178. doi: 10.1126/science.6103580. [DOI] [PubMed] [Google Scholar]
  26. Meech R. W. Calcium-dependent potassium activation in nervous tissues. Annu Rev Biophys Bioeng. 1978;7:1–18. doi: 10.1146/annurev.bb.07.060178.000245. [DOI] [PubMed] [Google Scholar]
  27. Ochi R. Manganese action potentials in mammalian cardiac muscle. Experientia. 1975 Sep 15;31(9):1048–1049. doi: 10.1007/BF02326952. [DOI] [PubMed] [Google Scholar]
  28. Ochi R. The slow inward current and the action of manganese ions in guinea-pig's myocardium. Pflugers Arch. 1970;316(1):81–94. doi: 10.1007/BF00587898. [DOI] [PubMed] [Google Scholar]
  29. Reuter H. Divalent cations as charge carriers in excitable membranes. Prog Biophys Mol Biol. 1973;26:1–43. doi: 10.1016/0079-6107(73)90016-3. [DOI] [PubMed] [Google Scholar]
  30. Smith D. S., Del Castillo J., Anderson M. Fine structure and innervation of an annelid muscle with the longest recorded sarcomere. Tissue Cell. 1973;5(2):281–302. doi: 10.1016/s0040-8166(73)80023-0. [DOI] [PubMed] [Google Scholar]
  31. Sperelakis N., Schneider M. F., Harris E. J. Decreased K+ conductance produced by Ba++ in frog sartorius fibers. J Gen Physiol. 1967 Jul;50(6):1565–1583. doi: 10.1085/jgp.50.6.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Standen N. B., Stanfield P. R. A potential- and time-dependent blockade of inward rectification in frog skeletal muscle fibres by barium and strontium ions. J Physiol. 1978 Jul;280:169–191. doi: 10.1113/jphysiol.1978.sp012379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. WERMAN R., GRUNDFEST H. Graded and all-or-none electrogenesis in arthropod muscle. II. The effects of alkali-earth and onium ions on lobster muscle fibers. J Gen Physiol. 1961 May;44:997–1027. doi: 10.1085/jgp.44.5.997. [DOI] [PMC free article] [PubMed] [Google Scholar]

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