Advertisement

Ion Channels of Unicellular Microbes

  • Ching Kung
Chapter
Part of the NATO ASI Series book series (NSSA, volume 188)

Abstract

Before the first “nervous system,” there must have been “nervous molecules”. The quintessential nervous molecules are the ion channels. These integral membrane proteins enclose the hydrophilic pathways across the hydrophobic membrane that would be otherwise impenetrable for charged or polar molecules. Since a room without a door is but a tomb, one could argue on first principles that channels probably evolved soon after cell membranes. Arguments and speculations aside, we have now shown that protozoa, yeast, and even bacteria all have ion channels. It appears that all cellular forms of life have ion channels. We are also forced to conclude that they must have evolved very early.

Keywords

Unit Conductance Mechanosensitive Channel Thin Lipid Membrane Transmembrane Alpha Helix Pipette Voltage 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Britten, R. J., and McClure, F. T., 1962, The amino acid pool of Escherichia coli, Bact. Rev. 26:292–335.PubMedGoogle Scholar
  2. Christensen, O., 1987, Mediation of cell volume regulation by Ca2+ influx through stretch-activated channels, Nature 330:66–68.PubMedCrossRefGoogle Scholar
  3. Criado, M., and Keller, B. U., 1987, A membrane fusion strategy for single-channel recordings of membranes usually non-accessible to patch-clamp pipette electrodes, FEBS Letters 224:172–176.PubMedCrossRefGoogle Scholar
  4. Delcour, A. H., Martinac, B., Adler, J., and Kung, C., 1989, A modified reconstitution method used in patch-clamp studies of Escherichia coli ion channels, Biophysical J. 56:631–636.CrossRefGoogle Scholar
  5. Eckert, R., 1972, Bioelectrical control of ciliary activity, Science 176:473–381.PubMedCrossRefGoogle Scholar
  6. Eckert, R., Naitoh, Y., and Friedman, K., 1972, Sensory mechanisms in Paramecium. I. Two components of the electric response to mechanical stimulation of the anterior surface, J. exp. Biol. 56:683–694.PubMedGoogle Scholar
  7. Epstein, W., and Schultz, S. G., 1965, Cation transport in Escherichia coli. V. Regulation of cation content, J. Gen. Physiol. 49:221–234.PubMedCrossRefGoogle Scholar
  8. Falke, L. C., and Misler, S., 1989, Activity of ion channels during volume regulation by clonal N1E115 neuroblastoma cells, Proc. Natl. Acad. Sci. 86:3919–3923.PubMedCrossRefGoogle Scholar
  9. Finkelstein, A., and Cass, A., 1968, Permeability and electrical properties of thin lipid membranes, J. Gen. Physiol. 52:145s–172s.CrossRefGoogle Scholar
  10. Forte, M., Guy, H. R., and Mannella, C. A., 1987, Molecular genetics of the VDAC ion channel: structural model and sequence analysis, J. Bioenergetics Biomembranes 19:341–349.CrossRefGoogle Scholar
  11. Guharay, F., and Sachs, F., 1985, Mechanotransduction ion channels in chick skeletal muscle: The effects of external pH, J. Physiol. (Lond.) 363:119–134.Google Scholar
  12. Gustin, M. C., Martinac, B., Saimi, Y., Culbertson, M. R., and Kung, C., 1986, Ion channels in yeast, Science 233:1195–1197.PubMedCrossRefGoogle Scholar
  13. Gustin, M. C., Zhou, X.-L., Martinac, B., and Kung, C., 1988, A mechanosensitive ion channel in the yeast plasma membrane, Science 242:762–765.PubMedCrossRefGoogle Scholar
  14. Hall, M. N., and Silhavy, T. J., 1981, Genetic analysis of the major membrane proteins in Escherichia coli, Ann. Rev. Genetics. 15:91–142.CrossRefGoogle Scholar
  15. Hamili O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J., 1981, Improved patch-clamp technique for high-resolution current recording from cell and cell-free membrane patches, Plugers Arch. 391:83–100.Google Scholar
  16. Hennessey, T. M., 1987, A novel calcium current is activated by hyperpolarization of Paramecium tetraurelia, Soc. Neurosci. Abs. 13:108.Google Scholar
  17. Hille, B., 1984, Ion Channels of Excitable Membranes, Sinauer Assoc. Inc., Sunderland, MA.Google Scholar
  18. Hinrichsen, R. D., and Schultz, E. J., 1988, Paramecium: a model system for the study of excitable cells, Trends in Neurosciences 11:27–32.PubMedCrossRefGoogle Scholar
  19. Kennedy, E. P., 1982, Osmotic regulation and the biosynthesis of membrane-derived oligosaccharides in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 79:1092–1095.PubMedCrossRefGoogle Scholar
  20. Kim, D., and Gapham, D. E., 1989, Potassium channels in cardiac cells activated by arachidonic acid and phospholipids, Science 242:1174–1176.CrossRefGoogle Scholar
  21. Kim, D., Lewis, D. L., Graziadei, L., Neer, E. J., Bar-Sagi, D., and Clapham, D. E., 1989, G-protein beta gamma-subunits activate three cardiac muscarinic K+-channel via phospholipase A2, Nature 337:557–560.PubMedCrossRefGoogle Scholar
  22. Kubalski, A., Martinac, B., and Saimi, Y., 1989, Proteolytic activation of a hyperpolarization-and Ca2+-activated K channel in Paramecium,J. Membrane Biol., in press.Google Scholar
  23. Laimins, L. A., Rhoads, D. B., and Epstein, W., 1981, Osmotic control of kpd Operon expression in Escherichia coli, Proc. Nail. Acad. Sci. U.S.A. 78:464–468.CrossRefGoogle Scholar
  24. le Rudulier, D., Strom, A. R., Dandekar, A. M., Smith, L. T., and Valentine, R. C., 1984, Molecular biology of osmoregulation, Science 224:1064–1068.PubMedCrossRefGoogle Scholar
  25. Li, C-Y., Boileau, A. J., Kung, C., and Adler, J., 1988, Osmotaxis in Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 85:9451–9455.PubMedCrossRefGoogle Scholar
  26. Machemer, H., 1988, in: Paramecium, pp. 186–215 (H.D. Gortz, ed.), Springer-Verlag, Heidelberg.Google Scholar
  27. Machemer, H., Ogura, A., 1979, Ionic conductances of membranes in ciliated and deciliated Paramecium, J. Physiol. (Lond.) 296:49–60.Google Scholar
  28. Martinac, B., Buechner, M., Delcour, A. H., Adler, J., and Kung, C., 1987, Pressure-sensitive ion channel in Escherichia coli, Proc. Nail. Acad. Sci. USA. 84:2297–2301.CrossRefGoogle Scholar
  29. Martinac, B., Saimi, Y., Gustin, M. C., Culbertson, M. R., Adler, J., and Kung, C., 1988, Ion channels in microbes, Periodicum Biologorum 90:375–384.Google Scholar
  30. Massart, J., 1891, Recherches sur les organismes inferieurs, Acad. Roy. de Med. de Belgique 22:148–163.Google Scholar
  31. Minorsky, P. V., Zhou, X.-L., Culbertson, M. R., and Kung, C., 1989, A patch damp analysis of a cation-current in the vacuolar membrane of the yeast Saccharomyces, Plant Physiology 89:S–882.Google Scholar
  32. Naitoh, Y., and Eckert, R., 1973, Sensory mechanism in Paramecium. II. Ionic basis of the hyperpolarizing mechanoreceptor potential, J. exp. Biol. 59:53–65.Google Scholar
  33. Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Furutani, Y., Hirose, T., Asai, M., Inayama, S., Miyata, T., and Numa, S., 1982, Primary structure of alpha-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence, Nature 299:793–797.PubMedCrossRefGoogle Scholar
  34. Noda, M., Shimizu, S., Tanabe, T., Takai, T., Kayano, T., Ikeda, T., Takahashi, H., Nakayama, H., Kanaoka, Y., Minamino, N., Kangawa, K., Matsuo, H., Raferty, M. A., Hirose, T., Inayama, S., Hayashida, H., Miyata, T., and Numa, S., 1984, Primary structure of Electrophorus electricus sodium channel deduced from cDNA sequence, Nature 312:121–127.PubMedCrossRefGoogle Scholar
  35. Oertel, D., Schein, S. J., and Kung, C., 1977, Separation of membrane currents using a Paramecium mutant, Nature 268:120–124.PubMedCrossRefGoogle Scholar
  36. Oertel, D., Schein, S. J., and Kung, C., 1978, A potassium channel activated by hyperpolarization in Paramecium, J. Membrane Biol. 43:169–185.CrossRefGoogle Scholar
  37. Ogura, A., and Machemer, H., 1980, Distribution of mechanoreceptor channels in the Paramecium surface membrane, J. Comp. Physiol. 135(A):233–242.CrossRefGoogle Scholar
  38. Ordway, R. W., Walsh, J. V. Jr., and Singer, J. S., 1989, Arachidonic acid and other fatty acids directly activate potassium channels in smooth muscle cells, Science 244:1176–1179.PubMedCrossRefGoogle Scholar
  39. Osborn, M. J., Gander, J. E., Parisi, E., and Carson, J., 1972, Mechanism of assembly of the outer membrane of Salmonella typhimurium, J. Biol. Chem. 247:3962–3972.PubMedGoogle Scholar
  40. Papazian, D. M., Schwarz, D. L., Tempel, B. L., Jan, Y. N., and Jan, L. Y., 1987, Sequence of a probable potassium channel component encoded a Shaker locus of Drosophilia, Science 237:749–753.PubMedCrossRefGoogle Scholar
  41. Paul, C., and Rosenbusch, J. P., 1985, Folding patterns of porin and bacteriorhodopsin, EMBO J. 4:1593–1597.PubMedGoogle Scholar
  42. Preston, R. R., and Saimi, Y., 1989, Calcium ions and the regulation of motility in Paramecium, in: The Structure and Function of Cilary and Flagellar Surfaces (R. Bloodgood, ed.), Plenum Press, in press.Google Scholar
  43. Ramanathan, R., Saimi, Y., Hinrichsen, R., Burgess-Cassler, A., and Kung, C., 1988, A genetic dissection of ion-channel functions in Paramecium, in: Paramecium, pp. 236–253 (H. D. Gortz, ed.), Springer-Verlag, Heidelberg.Google Scholar
  44. Rhoads, D. B., Waters, F. B., and Epstein, W., 1976, Cation transport in Escherichia coli. Vm. Potassium transport mutants, J. Gen. Physiol. 67:325–341.PubMedCrossRefGoogle Scholar
  45. Rosenbusch, J. P., 1986, Three-dimensional structure of membrane proteins, in: Bacterial Outer Membranes as Model Systems, pp. 141–162 (M. Inouye, ed.), Wiley, N.Y.Google Scholar
  46. Sachs, F., 1988, Mechanical transduction in biological systems, CRC Critical Review Biomedical Engineering 16:141–169.Google Scholar
  47. Saimi, Y., 1986, Calcium-dependent sodium currents in Paramecium: mutational manipulations and effects of hyperdepolarization, J. Membrane. Biol. 92:227–236.CrossRefGoogle Scholar
  48. Saimi Y., and Kung, C., 1980, A Ca-induced Na-current in Paramecium, J. exp. Biol. 88:305–325.PubMedGoogle Scholar
  49. Saimi Y., and Kung, C., 1987, Behavioral genetics of Paramecium, Ann. Rev. Genetics 21:47–65.CrossRefGoogle Scholar
  50. Saimi Y., and Martinac, B., 1989, A calcium-dependent potassium channel in Paramecium studied under patch-clamp, J. Membrane Biol., in press.Google Scholar
  51. Saimi, Y., Hinrichsen, R. D., Forte, M., and Kung, C., 1983, Mutant analysis shows that the Ca2+-induced K+ current shuts off one type of excitation in Paramecium, Proc. Natl. Acad. Sci. USA 80:5112–5116.PubMedCrossRefGoogle Scholar
  52. Saimi Y., Martinac, B., Gustin, M. C., Culbertson, M. R., Adler, J., and Kung, C., 1988a, Ion channels in Paramecium, yeast, and Eschrichia coli, Trends in Biochemical Sciences 13:304–309.PubMedCrossRefGoogle Scholar
  53. Saimi Y., Martinac, B., Gustin, M. C., Culbertson, M. J., Adler, J., and Kung, C., 1988b, Ion channels in Paramecium, yeast, and Escherichia coli, Cold Spring Harbor Symposia on Quantitative Biology 53:667–673.PubMedCrossRefGoogle Scholar
  54. Satow Y., and Kung, C., 1974, Genetic dissection of active electrogenesis in Paramecium aurellla, Nature 247:69–71.PubMedCrossRefGoogle Scholar
  55. Satow Y., and Kung, C., 1980a, Membrane currents of pawn mutants of the pwA group in Paramecium tetraurelia, J. exp. Biol. 84:57–71.PubMedGoogle Scholar
  56. Satow Y., and Kung, C., 1980b, Ca-induced K+-outward current in Paramecium tetraurelia, J. exp. Biol. 88:293–303.PubMedGoogle Scholar
  57. Schwarz, T. L., Tempel, B. L., Papazian, D. M., Jan, Y. N., and Jan, L. Y., 1988, Multiple potassium-channel components are produced by alternative splicing at the Shaker locus in Drosophilia, Nature 331:137–142.PubMedCrossRefGoogle Scholar
  58. Stock, J. B., Rauch, B., and Roseman, S., 1977, Periplasmic space in Salmonella typhimurium and Escherichia coli, J. Bacterial. 262:7850–7861.Google Scholar
  59. Tanabe T., Takashima, H., Mikami, A., Flockerzi, V., Takahashi, H., Kangawa, K., Kojima, M., Matsuo, H., Hirose, T., and Numa, S., 1987, Primary structure of the receptor for calcium channel blockers from skeletal muscle, Nature 328:313–318.PubMedCrossRefGoogle Scholar
  60. Yatani, A., Mattera, R., Codina, J., Graf, R., Okabe, K., Padrell, E., Iyengar, R., Brown, A. M., and Birnbaumer, L., 1988, The G protein-gated atrial K+ channel is stimulated by three distince Gi alpha-subunits, Nature 336:680–682.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1989

Authors and Affiliations

  • Ching Kung
    • 1
  1. 1.Laboratory of Molecular Biology and Department of GeneticsUniversity of WisconsinMadisonUSA

Personalised recommendations