Skip to main content
SpringerLink
Log in

Structure and mechanism of bacterial periplasmic transport systems

  • Mini-Review
  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Bacterial periplasmic transport systems are complex, multicomponent permeases, present in Gram-negative bacteria. Many such permeases have been analyzed to various levels of detail. A generalized picture has emerged indicating that their overall structure consists of four proteins, one of which is a soluble periplasmic protein that binds the substrate and the other three are membrane bound. The liganded periplasmic protein interacts with the membrane components, which presumably form a complex, and which by a series of conformational changes allow the formation of an entry pathway for the substrate. The two extreme alternatives for such pathway involve either the formation of a nonspecific hydrophilic pore or the development of a ligand-binding site(s) on the membrane-bound complex. One of the membrane-bound components from each system constitutes a family of highly homologous proteins containing sequence domains characteristic of nucleotide-binding sites. Indeed, in several cases, they have been shown to bind ATP, which is thus postulated to be involved in the energy-coupling mechanism. Interestingly, eukaryotic proteins homologous to this family of proteins have been identified (mammalianmdr genes and Drosophilawhite locus), thus indicating that they perform a universal function, presumably related to energy coupling in membrane-related processes. The mechanism of energy coupling in periplasmic permeases is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ames, G. F.-L. (1972). InBiological Membranes. Proceedings of the 1972 ICN-UCLA Symposium in Molecular Biology, (Fox, C. F., ed.), Academic Press, New York.

    Google Scholar 

  • Ames, G. F.-L. (1985).Curr. Top. Membr. Transport 23, 103–119.

    Google Scholar 

  • Ames, G. F.-L. (1986a).Annu. Rev. Biochem. 55, 397–425.

    Google Scholar 

  • Ames, G. F.-L. (1986b).Cell,47, 323–324.

    Google Scholar 

  • Ames, G. F.-L., and Higgins, C. F. (1983).Trends Biochem. Sci. 8, 97–100.

    Google Scholar 

  • Ames, G. F.-L., and Lever, J. (1970).Proc. Natl. Acad. Sci. USA 66, 1096–1103.

    Google Scholar 

  • Ames, G. F.-L., and Nikaido, K. (1978).Proc. Natl. Acad. Sci. USA 75, 5447–5451.

    Google Scholar 

  • Ames, G. F.-L., and Nikaido, K. (1981).Eur. J. Biochem. 115, 525–531.

    Google Scholar 

  • Ames, G. F.-L., and Spudich, E. N. (1976).Proc. Natl. Acad. Sci. USA 73, 1877–1881.

    Google Scholar 

  • Argos, P., Mahoney, W. C., Hermodson, M. A., and Haney, M. (1981).J. Biol. Chem. 256, 1131–1133.

    Google Scholar 

  • Bavoil, P., and Nikaido, H. (1981).J. Biol. Chem. 256, 11385–11388.

    Google Scholar 

  • Bavoil, P., Hofnung, M., and Nikaido, H. (1980).J. Biol. Chem. 255, 8366–8369.

    Google Scholar 

  • Bell, A. W., Buckel, S. D., Groarke, J. M., Hope, J. N., Kingsley, D. H., and Hermodson, M. A. (1986).J. Biol. Chem. 261, 7652–7658.

    Google Scholar 

  • Berger, E. A. (1973).Proc. Natl. Acad. Sci. USA 70, 1514–1518.

    Google Scholar 

  • Berger, E. A., and Heppel, L. A. (1974).J. Biol. Chem. 249, 7747–7755.

    Google Scholar 

  • Brenner, M., and Ames, B. N. (1971). InMetabolic Regulation (Vogel, H. J., ed.), Metabolic Pathways, Vol 5, Academic Press, New York.

    Google Scholar 

  • Celis, R. T. F. (1984).Eur. J. Biochem. 145, 403–411.

    Google Scholar 

  • Chen, C.-J., Chin, J. E., Ueda, K., Clark, D. P., Pastau, I., Gottesman, M. M., and Roninson, I. (1986)Cell 47, 381–389.

    Google Scholar 

  • Darnwalle, K. R., Paxton, A. T., and Henderson, P. J. F. (1981).Biochem. J. 200, 611–627.

    Google Scholar 

  • Dassa, E., and Hofnung, M. (1985).EMBO J. 4, 2287–2293.

    Google Scholar 

  • Dietzel, I., Kolb, V., and Boos, W. (1978).Arch Microbiol. 118, 207–218.

    Google Scholar 

  • Doolittle, R. F., Johnson, M. S., Husaim, I., Van Houten, B., Thomas, D. S., and Sanca, A. (1986).Nature (London)323, 451–453.

    Google Scholar 

  • Froshauer, S. and Beckwith, J. (1984).J. Biol. Chem. 259, 10896–10903.

    Google Scholar 

  • Furlong, C. E. (1987). InEscherichia coli andSalmonella typhimunium: Cellular and Molecular Biology (Neidhardt, F. C., ed), ASM, Washington, D.C.

    Google Scholar 

  • Gilliland, G. L. and Quiocho, F. A. (1981).J. Mol. Biol. 146, 341–362.

    Google Scholar 

  • Gilson, E., Higgins, C. F., Hofnung, M., Ames, G. F.-L., and Nikaido, H. (1982).J. Biol. Chem. 257, 9915–9918.

    Google Scholar 

  • Groarke, J. M., Narayama, S. V. L., Argos, P., and Hermodson, M. A. (1987), submitted for publication.

  • Gros, P., Croop, J., and Housman, D. (1986).Cell 47, 371–380.

    Google Scholar 

  • Harayama, S., Bollinger, J., Iino, T., and Hazelbauer, G. L. (1983).J. Bacteriol. 153, 408–415.

    Google Scholar 

  • Hengge, R. and Boos, W. (1983).Biochim. Biophys. Acta 737, 443–478.

    Google Scholar 

  • Higgins, C. F., and Ames, G. F.-L. (1981).Proc. Natl. Acad. Sci. USA. 78, 6038–6042.

    Google Scholar 

  • Higgins, C. F., Haag, P. D., Nikaido, K., Ardeshir, F., Garcia, G., and Ames, G. F.-L. (1982).Nature (London)298, 723–727.

    Google Scholar 

  • Higgins, C. F., Hiles, I. D., Whalley, K., and Jamieson, D. K. (1985).EMBO J. 4, 1033–1040.

    Google Scholar 

  • Higgins, C. F., Hiles, I. D., Salmond, G. P. C., Gill, D. R., Downie, J. A., Evans, I. J., Holland, I. B., Gray, L., Buckel, S. D., Bell, A. W., and Hermodson, M. A. (1986).Nature (London)323, 448–450.

    Google Scholar 

  • Hiles, I. D., and Higgins, C. F. (1987), submitted for publication.

  • Hobson, A. C., Weatherwax, R., and Ames, G. F.-L. (1984).Proc. Natl. Acad. Sci. USA 81, 7333–7337.

    Google Scholar 

  • Hong, J.-S. (1986). InMethods Enzymol. 125, 180–186.

    Google Scholar 

  • Hong, J.-S., and Hunt, A. G. (1980).J. Supramol. Struct. 4, 77.

    Google Scholar 

  • Hong, J.-S., Hunt, A. G., Masters, P. S., and Lieberman, M. A. (1979).Proc. Natl. Acad. Sci. USA 76, 1213–1217.

    Google Scholar 

  • Hope, J. N., Bell, A. W., Hermodson, M. A., and Groarke, J. M. (1985).J. Biol. Chem. 261, 7663–7668.

    Google Scholar 

  • Hunt, A. C., and Hong, J.-S. (1981a).J. Biol. Chem. 256, 11988–11990.

    Google Scholar 

  • Hunt, A. G., and Hong, J.-S. (1981b). InMembranes and Transport, Vol. II (Martonosi, A. N., ed.), Plenum Press, New York.

    Google Scholar 

  • Hunt, A. G., and Hong, J.-S. (1983a).Biochemistry 22, 844–850.

    Google Scholar 

  • Hunt, A. G., and Hong, J.-S. (1983b).Biochemistry 22, 851–854.

    Google Scholar 

  • Johann, S., and Hinton, S. M. (1987),169, 1911–1916.

  • Kaback, H. R. (1983).J. Membr. Biol. 76, 95–112.

    Google Scholar 

  • Kustu, S. G., and Ames, G. F.-L. (1973).J. Bacteriol. 116, 107–113.

    Google Scholar 

  • Kustu, S. G., and Ames, G. F.-L. (1974).J. Biol. Chem. 249, 6976–6983.

    Google Scholar 

  • Landick, R., and Oxender, D. L. (1985).J. Biol. Chem. 260, 8257–8261.

    Google Scholar 

  • Landick, R., Oxender, D. L., and Ames, G. F.-L. (1985). InThe Enzymes of Biological Membranes, Vol. 3 (Martonosi, A. N., ed.) Plenum Press, New York.

    Google Scholar 

  • Lever, J. E. (1972).Anal. Biochem. 50, 73–83.

    Google Scholar 

  • Manuck, B. A. and Ho, C. (1979).Biochemistry 18, 566–573.

    Google Scholar 

  • Mao, B., Pear, M. P., McCammon, J. A., and Quiocho, F. A. (1982).J. Biol. Chem. 257, 1131–1133.

    Google Scholar 

  • Miller, D. M., III, Olson, J. S., and Quiocho, F. A. (1980).J. Biol. Chem. 255, 2465–2471.

    Google Scholar 

  • Miller, D. M., III, Olson, J. S., Pflugrath, J. W., and Quiocho, F. A. (1983).J. Biol. Chem. 258, 13665–13672.

    Google Scholar 

  • Mount, S. M. (1987).Nature (London)325, 487.

    Google Scholar 

  • Mowbray, S. L., and Petsko, G. A. (1983).J. Biol. Chem. 258, 7991–7997.

    Google Scholar 

  • Muller, N., Heine, H.-G., and Boos, W. (1985).J. Bacteriol. 163, 37–45.

    Google Scholar 

  • Neu, H. C., and Heppel, L. A. (1965).J. Biol. Chem. 240, 3685–3692.

    Google Scholar 

  • Newcomer, M. E., Lewis, B. A., and Quiocho, F. A. (1981).J. Biol. Chem. 256, 13218–13222.

    Google Scholar 

  • Nikaido, H. and Vaara, M. (1985).Microb. Rev. 49, 1–32.

    Google Scholar 

  • Nohno, T., Saito, T., and Hong, J.-S. (1986).Mol. Gen. Genet. 205, 260–269.

    Google Scholar 

  • Overath, P. and Wright, J. K. (1983).Trends Biochem. Sci. 8, 404–408.

    Google Scholar 

  • Payne, G., Spudich, E. N., and Ames, G. F.-L. (1985).Mol. Gen. Genet. 200, 493–496.

    Google Scholar 

  • Pflugrath, J. W., and Quiocho, F. A. (1985).Nature (London)314, 257–260.

    Google Scholar 

  • Plate, C. A. (1979).J. Bacteriol. 137, 221–225.

    Google Scholar 

  • Richarme, G., and Kepes, A. (1974).Eur. J. Biochem. 45, 127–133.

    Google Scholar 

  • Robbins, A. R., Guzman, R., and Rotman, B. (1976).J. Biol. Chem. 251 3112–3116.

    Google Scholar 

  • Rosenberg, H., Gerdes, R. G., and Chegwidden, K. (1977).J. Bacteriol. 131, 505–511.

    Google Scholar 

  • Rotman, B., and Guzman, R. (1984). InMicrobiology (Leive, L., and Schlessinger, D., eds.), Am. Soc. Microbiol., Washington, D.C., pp. 57–60.

    Google Scholar 

  • Saper, M. A., and Quiocho, F. A. (1983).J. Biol. Chem. 258, 11057–11062.

    Google Scholar 

  • Shen, Q., Simplacenau, V., Cottam, P. F., and Ho, C. (1985).Biophys. J. 47, 88a.

    Google Scholar 

  • Shuman, H. A. (1982).J. Biol. Chem. 252, 5455–5461.

    Google Scholar 

  • Shuman, H. A., and Silhavy, T. J. (1981).J. Biol. Chem. 256, 560–562.

    Google Scholar 

  • Shuman, H. A., and Treptow, N. A. (1985). InThe Enzymes of Biological Membranes, Vol. 3 (Martonois, A. N., ed.), Plenum Press, New York.

    Google Scholar 

  • Shuman, H. A., Silhavy, T. J., and Beckwith, J. (1980).J. Biol. Chem. 255, 168–174.

    Google Scholar 

  • Singh, A. P., and Bragg, P. D. (1976).Biochim. Biophys. Acta 438, 450–461.

    Google Scholar 

  • Singh, A. P., and Bragg, P. D. (1977).J. Supramol. Struct. 6, 389–398.

    Google Scholar 

  • Surin, B. P., Rosenberg, H., and Cox, G. B. (1985).J. Bacteriol. 161, 189–198.

    Google Scholar 

  • Szmelcman, S., Schwartz, M., Silhavy, T. J., and Boos, W. (1976).Eur. J. Biochem. 65, 13–19.

    Google Scholar 

  • Treptow, N. A., and Shuman, H. A. (1985).J. Bacteriol. 163, 654–660.

    Google Scholar 

  • Vyas, N. K., Vyas, M. N., and Quiocho, F. A. (1983).Proc. Natl. Acad. Sci. USA 80, 1792–1796.

    Google Scholar 

  • Walker, J. E., Saraste, M., Runswick, M. J., and Gay, N. J. (1982).EMBO J. 1, 945–951.

    Google Scholar 

  • Wandersman, C., Schwartz, M., and Ferenci, T. (1979).J. Bacteriol. 140, 1–13.

    Google Scholar 

  • Winkler, H. H., and Wilson, T. H. (1966).J. Biol. Chem. 241, 2200–2211.

    Google Scholar 

  • Zukin, R. S., Klos, M. F., and Hirsch, R. E. (1986).Biophys. J. 49, 1229–1235.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, University of California, 94720, Berkeley, California

    Giovanna Ferro-Luzzi Ames

Authors
  1. Giovanna Ferro-Luzzi Ames
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ames, G.FL. Structure and mechanism of bacterial periplasmic transport systems. J Bioenerg Biomembr 20, 1–18 (1988). https://doi.org/10.1007/BF00762135

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00762135

Key Words

Search

Navigation