Analysis and Chemical Modification of Bacterial Porins

  • Roland Benz

Abstract

The cell envelope of gram-negative bacteria such as Escherichia coli, Salmonella typhimurium, and Pseudomonas aeruginosa consists of three different layers, the outer membrane, the peptidoglycan (murein) layer, and the inner membrane (Nikaido, 1979a; Beveridge, 1981). The inner membrane acts as a real diffusion barrier and contains, in addition to the respiration chain and the H+ -ATPase, a large number of different transport systems for substrates. The peptidoglycan or murein layer consists of repeating N-acetylglucosaminyl-N-acetylmuramyl dimers, which form a macromolecule surrounding the cell (Beveridge, 1981). This layer protects the cells from lysis. The outer membrane is a molecular filter with defined exclusion limits for hydrophilic substrates (Nikaido and Nakae, 1979). In enteric bacteria, the outer membrane acts also as a barrier for hydrophobic compounds such as detergents (Nikaido, 1979b). The active substrates of the molecular sieving properties for hydrophilic substances are a major class of proteins called matrix proteins (Rosenbusch, 1974) or porins (Nakae, 1976).

Keywords

Outer Membrane Outer Membrane Protein Lipid Bilayer Membrane Selectivity Filter General Diffusion 
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. Angus, B. L., Carey, A. M., Caron, D. A., Kropinski, A. M. B., and Hancock, R. E. W., 1981 Outer membrane permeability in Pseudomonas aeruginosa: Comparison of a wild-type with an antibiotic-supersusceptible mutant, Antimicrob. Agents Chemother. 21:299–309.CrossRefGoogle Scholar
  2. Benz, R., 1984, Structure and selectivity of porin channels, in: Current Topics in Membranes and Transport, Vol. 21 (E. D. Stein, ed.), pp. 199–219, Academic Press, San Diego.Google Scholar
  3. Benz, R., 1985, Porin from bacterial and mitochondrial outer membranes, CRC Crit. Rev. Biochem. 19:145–190.PubMedCrossRefGoogle Scholar
  4. Benz, R., and Böhme, H., 1985, Pore formation by an outer membrane protein of the cyanobacterium Anabaena variabilis, Biochim. Biophys. Acta 812:286–292.CrossRefGoogle Scholar
  5. Benz, R., and Hancock, R. E. W., 1981, Properties of the large ion permeable pores formed from protein F of Pseudomonas aeruginosa in lipid bilayer membranes, Biochim. Biophys. Acta 646:298–308.PubMedCrossRefGoogle Scholar
  6. Benz, R., Boehler-Kohler, B. A., Dieterle, R., and Boos, W., 1978a, Porin activity in the osmotic shock fluid of Escherichia coli, J. Bacteriol. 135:1080–1090.Google Scholar
  7. Benz, R., Janko, K., Boos, W., and Läuger, P., 1978b, Formation of large ion-permeable membrane channels by the matrix protein (porin) of Escherichia coli, Biochim. Biophys. Acta 511:305–319.CrossRefGoogle Scholar
  8. Benz, R., Janko, K., and Läuger, P., 1979, Ionic selectivty of pores formed by the matrix protein (porin) of Escherichia coli, Biochim. Biophys. Acta 551:238–247.CrossRefGoogle Scholar
  9. Benz, R., Ishii, J., and Nakae, T., 1980, Determination of ion permeability through the channels made of porins from the outer membrane of Salmonella typhimurium in lipid bilayer membranes, J. Memb. Biol. 56:19–29.CrossRefGoogle Scholar
  10. Benz, R., Gimple, M., Poole, K., and Hancock, R. E. W., 1983, An anion selective channel from the Pseudomonas aeruginosa outer membrane, Biochim. Biophys. Acta 730:387–390.CrossRefGoogle Scholar
  11. Benz, R., Darveau, R. P., and Hancock, R. E. W., 1984a, Outer membrane protein PhoE from Escherichia coli forms anion-selective pores in lipid bilayer membranes, Eur. J. Biochem. 140:319–324.PubMedCrossRefGoogle Scholar
  12. Benz, R., Poole, K., and Hancock, R. E. W., 1984b, Characterization and chemical modification of small anion specific channels formed in lipid bilayer membranes by outer membrane protein of Pseudomonas aeruginosa, Biophys. J. 45:81–82.CrossRefGoogle Scholar
  13. Benz, R., Tokunaga, H., and Nakae, T., 1984c, Properties of chemically modified porin from Escherichia coli in lipid bilayer membranes, Biochim. Biophys. Acta 769:348–356.PubMedCrossRefGoogle Scholar
  14. Benz, R., Schmid, A., and Hancock, R. E. W., 1985, Ion selectivity of gramnegative bacterial porins, J. Bacteriol. 162:722–727.PubMedGoogle Scholar
  15. Benz, R., Poole, K., and Hancock, R. E. W., 1986a, Mechanism of ion translocation through the anion selective channel of Pseudomonas aeruginosa outer membrane, J. Gen. Physiol. (in press).Google Scholar
  16. Benz, R., Schmid, A., Nakae, T., and Vos-Scheperkeuter, G., 1986b, Pore formation by LamB preparations of E. coli in lipid bilayer membranes, J. Bacteriol. (in press).Google Scholar
  17. Beveridge, T. J., 1981, Ultrastructure, chemistry and function of the bacterial wall, Int. Rev. Cytol. 72:229–317.PubMedCrossRefGoogle Scholar
  18. Castellan, G. W., 1983, Physical Chemistry. The Electrical Current in Ionic Solutions, pp. 769–780, Addison-Wesley, Reading.Google Scholar
  19. Chen, R., Kramer, C., Schmidmayer, W., and Henning, U., 1979, Primary structure of major outer membrane protein I of Escherichia coli B, Proc. Natl. Acad. Sci. U.S.A. 76:5014–5017.PubMedCrossRefGoogle Scholar
  20. Clément, J. M., and Hofnung, M., 1981, Gene sequence of the λ receptor, an outer membrane protein of Escherichia coli K12, Cell 27:507–514.PubMedCrossRefGoogle Scholar
  21. Cohen, F. S., Akabas, M. H., and Finkelstein, A., 1982, Osmotic swelling of phospholipid vesicles causes them to fuse with a planar phospholipid bilayer membrane, Science 217:458–460.PubMedCrossRefGoogle Scholar
  22. Darveau, R. P., Hancock, R. E. W., and Benz, R., 1984, Chemical modification of the anion selectivity of the PhoE porin from the Escherichia coli outer membrane, Biochim. Biophys. Acta 774:67–74.PubMedCrossRefGoogle Scholar
  23. Di Rienzo, J. M., Nakamura, K., and Inouye, M., 1978, The outer membrane of gram-negative bacteria: Biosynthesis, assembly and function, Annu. Rev. Biochem. 47:481–532.CrossRefGoogle Scholar
  24. Dorset, D. L., Engel, A., Häner, M., Massalski, A., and Rosenbusch, J. P., 1983, Two-dimensional crystal packing of matrix porin. A channel forming protein in Escherichia coli outer membrane, J. Mol. Biol. 165:701–710.PubMedCrossRefGoogle Scholar
  25. Dorset, D. L., Engel, A., Massalski, A., and Rosenbusch, J. P., 1984, Three dimensional structure of a membrane pore. Electron microscopical analysis of Escherichia coli outer membrane matrix porin, Biophys. J. 45:128–129.PubMedCrossRefGoogle Scholar
  26. Eisenman, G., 1965, Some elementary factors involved in specific ion permeation. Excerpta Medica Int. Cong. Ser. 87:489–506.Google Scholar
  27. Ferenci, T., Schwentorat, M., Ullrich, S., and Vilmart, J., 1980, Lambda receptor in the outer membrane of Escherichia coli as a binding protein for maltodextrins and starch polysaccharides, J. Bacteriol. 142:521–526.PubMedGoogle Scholar
  28. Garavito, R. M., Jenkins, J. A., Jansonius, J. N., Karlsson, R., and Rosenbusch, J. P., 1983, X-ray diffraction analysis of matrix porin, an integral membrane protein A from Escherichia coli outer membranes, J. Mol. Biol. 164:313–327.PubMedCrossRefGoogle Scholar
  29. Hancock, R. E. W., and Nikaido, H., 1978, Outer membranes of gram-negative bacteria XIX. Isolation from Pseudomonas aeruginosa PA 01 and use in reconstitution and definition of permeability barrier, J. Bacteriol. 136:381–390.PubMedGoogle Scholar
  30. Hancock, R. E. W., Decad, G. M., and Nikaido, H., 1979, Identification of the protein producing transmembrane diffusion pores in the outer membrane of Pseudomonas aeruginosa PA 01, Biochim. Biophys. Acta 554:323–331.PubMedCrossRefGoogle Scholar
  31. Hancock, R. E. W., Poole, R. K., and Benz, R., 1982, Outer membrane protein P of Pseudomonas aeruginosa regulation by phosphate deficiency and formation of small anion-specific channels in lipid bilayer membranes, J. Bacteriol. 150:730–738.PubMedGoogle Scholar
  32. Hancock, R. E. W., Poole, R. K., Gimple, M., and Benz, R., 1983, Modification of the conductance, selectivity, and concentration-dependent saturation of Pseudomonas aeruginosa protein P channels by chemical acetylation, Biochim. Biophys. Acta 735:137–144.PubMedCrossRefGoogle Scholar
  33. Inokuchi, K., Muthoh, N., Matsuyama, S., and Mizushima, S., 1982, Primary structure of the OmpF gene that codes for a major outer membrane protein of Escherichia coli K12, Nucleic Acids Res. 10:6957–6968.PubMedCrossRefGoogle Scholar
  34. Läuger, P., 1973, Ion transport through pores: A rate-theory analysis Biochim. Biophys. Acta 311:423–441.CrossRefGoogle Scholar
  35. Luckey, M., and Nikaido, H., 1980a, Diffusion of solutes through channels produced by phage lambda receptor protein of Escherichia coli: Inhibition by higher oligosaccharides of maltose series, Biochem. Biophys. Res. Commun. 93:166–171.PubMedCrossRefGoogle Scholar
  36. Luckey, M., and Nikaido, H., 1980b, Specificity of diffusion channels produced by X phage receptor protein of Escherichia coli, Proc. Natl. Acad. Sci. U.S.A. 77:167–171.CrossRefGoogle Scholar
  37. Lugtenberg, B., and van Alphen, L., 1983, Molecular architecture and functioning of the outer membrane of Escherichia coli and other gram-negative bacteria, Biochim. Biophys. Acta 737:51–115.PubMedCrossRefGoogle Scholar
  38. Mizuno, T., Chou, M.-Y., and Inouye, M., 1983, A comparative study on the genes for three porins of the Escherichia coli outer membrane: DNA sequence of the osmoregulated ompC gene, J. Biol. Chem. 258:6932–6940.PubMedGoogle Scholar
  39. Nakae, T., 1975, Outer membrane of Salmonella typhimurium: Reconstitution of sucrose-permeable membrane vesicles, Biochem. Biophys. Res. Commun. 64:1224–1230.PubMedCrossRefGoogle Scholar
  40. Nakae, T., 1976, Identification of the outer membrane protein of Escherichia coli that produces transmembrane channels in reconstituted vesicle membranes, Biochem. Biophys. Res. Commun. 71:877-889.Google Scholar
  41. Nakae, T., Ishii, J., and Tokunaga, M., 1979, Subunit structure of functional porin oligomers that form permeability channels in the outer membrane of Escherichia coli, J. Biol. Chem. 254:1457–1461.Google Scholar
  42. Nakamura, K., and Mizushima, S., 1976, Effects of heating in dodecyl sulfate solution on the conformation and electrophoretic mobility of isolated major outer membrane proteins from Escherichia coli K12, J. Biochem. 80:1411–1422.PubMedGoogle Scholar
  43. Nikaido, H., 1979a, Permeability of the outer membrane of bacteria, Angew. Chem. 18:337–350.CrossRefGoogle Scholar
  44. Nikaido, H., 1979b, Nonspecific transport through the outer membrane, in: Bacterial Outer Membranes (M. Inouye, ed.), pp. 367-407, Wiley-Interscience, New York.Google Scholar
  45. Nikaido, H., 1983, Proteins forming large channels from bacterial and mitochondrial outer membranes: Porins and phage lambda receptor protein, Methods. Enzymol. 97:85–100.PubMedCrossRefGoogle Scholar
  46. Nikaido, H., and Nakae, T., 1979, The outer membrane of gram-negative bacteria, Adv. Microb. Physiol. 20:163–250.PubMedCrossRefGoogle Scholar
  47. Nikaido, H., and Rosenberg, E. Y., 1981, Effect of solute size on diffusion rates through the transmembrane pores of the outer membrane of Eseherichia coli, J. Gen. Physiol. 77:121–135.CrossRefGoogle Scholar
  48. Nikaido, H., and Rosenberg, E. Y., 1983, Porin channels in Escherichia coli: Studies with liposomes reconstituted from purified proteins, J. Bacteriol. 153:241–252.PubMedGoogle Scholar
  49. Nikaido, H., and Vaara, M., 1985, Molecular basis of bacterial outer membrane permeability, Microbiol. Rev. 49:1–32.PubMedGoogle Scholar
  50. Nikaido, H., Rosenberg, E. Y., and Foulds, J., 1983, Porin channels in Escherichia coli: Studies with β-lactams in intact cells, J. Bacteriol. 153:232–240.PubMedGoogle Scholar
  51. Overbeeke, N., Bergmans, H., van Mansfeld, F., and Lugtenberg, B., 1983, Complete nucleotide sequence of phoE, the structural gene for the phosphate limitation inducible outer membrane pore protein of Escherichia coli K12, J. Mol. Biol. 163:513–532.PubMedCrossRefGoogle Scholar
  52. Overbeeke, N., van Scharrenburg, G., and Zugtenberg, B., 1980, Antigenic relationships between pore proteins of Escherichia coli K12, Eur. J. Biochem. 110:247–254.PubMedCrossRefGoogle Scholar
  53. Pauling, L., 1960, The Nature of the Chemical Bond, Cornell University Press, Ithaca.Google Scholar
  54. Rosenbusch, J. P., 1974, Characterization of the major envelope protein from Escherichia coli, J. Biol. Chem. 249:8019–8029.PubMedGoogle Scholar
  55. Schindler, H., and Rosenbusch, J. P., 1978, Matrix protein of Escherichia coli outer membranes forms voltage-controlled channels in lipid bilayers, Proc. Natl. Acad. Sci. U.S.A. 75:3751–3755.PubMedCrossRefGoogle Scholar
  56. Stock, J. B., Rauch, B., and Roseman, S., 1977, Periplasmic space in Salmonella typhimurium and Escherichia coli, J. Biol. Chem. 252:7850–7861.Google Scholar
  57. Szmelcman, S., and Hofnung, M., 1975, Maltose transport in Escherichia coli K12: Involvement of the bacteriophage lambda receptor, J. Bacteriol. 124:112–118.PubMedGoogle Scholar
  58. Tokunaga, M., Tokunaga, H., Okajima, Y., and Nakae, T., 1979, Characterization of porins from the outer membrane of Salmonella typhimurium. 2 Physical properties of the functional oligomeric aggregates, Eur. J. Biochem. 95:441–448.PubMedCrossRefGoogle Scholar
  59. Tokunaga, H., Tokunaga, M., and Nakae, T., 1981, Permeability properties of chemically modified porin trimers from Escherichia coli B, J. Biol. Chem. 256:8024–8029.PubMedGoogle Scholar
  60. Tommassen, J., and Lugtenberg, B., 1980, Outer membrane protein e of Escherichia coli K-12 is coregulated with alkaline phosphatase, J. Bacteriol. 143:151–157.PubMedGoogle Scholar
  61. Tommassen, J., Pugsley, A. P., Korteland, J., Verbakel, J., and Lugtenberg, B., 1984, Gene encoding a hybrid ompF-PhoE pore protein in the outer membrane of Escherichia coli K12, Mol. Gen. Genet. 197:503–508.PubMedCrossRefGoogle Scholar
  62. Tommassen, J., van der Ley, P., van Zeijl, M., and Agterberg, M., 1985, Localization of functional domains in E. coli K-12 outer membrane porins with the aid of hybrid genes obtained by in vivo recombination, EMBO J. 4:1583–1587.PubMedGoogle Scholar
  63. van Alphen, L., and Lugtenberg, B., 1978, Influence of osmolarity of the growth medium on the outer membrane protein pattern of Escherichia coli, J. Bacteriol. 131:623–630.Google Scholar
  64. Yoshimura, F., Zalman, L. S., and Nikaido, H., 1983, Purification and properties of Pseudomonas aeruginosa porin, J. Biol. Chem. 258:2308–2314.PubMedGoogle Scholar
  65. Young, J. D.-E., Blake, M., Mauro, A., and Cohn, Z. A., 1983, Properties of the major outer membrane protein from Neisseria gonorrhoeae incorporated into model lipid membranes, Proc. Natl. Acad. Sci. U.S.A. 80:3831–3835.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1986

Authors and Affiliations

  • Roland Benz
    • 1
  1. 1.Department of BiologyUniversity of KonstanzKonstanzWest Germany

Personalised recommendations