Abstract
Diffusion of small molecules across the outer membrane of gram-negative bacteria may occur through protein channels and through lipid bilayer domains. Among protein channels, many examples of trimeric porins, which produce water-filled diffusion channels, are known. Although the channels are nonspecific, the diffusion rates of solutes are often drastically affected by their gross physicochemical properties, such as size, charge, or lipophilicity, because the channel has a dimension not too different from that of the diffusing solutes. In the last few years, the structures of three such porins have been solved by X-ray crystallography. It is now known that a monomer unit traverses the membrane 16 times as β-strands, and one of the external loop folds back into the channel to produce a narrow constriction. Most of the static properties of the channel, such as the pore size and the position of the amino acids that produce the constriction, can now be explained by the three-dimensional structure. Controversy, however, still surrounds the issue of whether there are dynamic modulation of the channel properties in response to pH, ionic strength, or membrane potential, and of whether such responses are physiological. More recently, two examples of monomeric porins have been identified. These porins allow a very slow diffusion of solutes, but the reason for this low permeability is still unclear. Finally, channels with specific binding sites facilitate the diffusion of specific classes of nutrients, often those compounds that are too large to penetrate rapidly through the porin channels. Lipid bilayers in the outer membrane were shown to be perhaps 50- to 100-fold less permeable to uncharged, lipophilic molecules in comparison with the bilayers made of the usual glycerophospholipids. This is caused by the presence of a lipopolysaccharide leaflet in the bilayer, and more specifically, by the presence of a larger number of fatty acids in each lipid molecule, and by the absence of unsaturated fatty acids in the lipopolysaccharide structure.
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Bauer, K., Struyve, M., Bosch, D., Benz, R., and Tommassen, J. (1989).K. Biol. Chem. 264 16393–16398.
Bellido, F., Martin, N. L., Siehnel, R. J., and Hancock, R. E. W. (1992).J. Bacteriol. 174 5196–5203.
Benson, S. A., Occi, J. L. L., and Sampson, B. A. (1988).J. Mol. Biol. 203 961–970.
Benz, R., Janko, K., and Lauger, P. (1979).Biochim. Biophys. Acta 551 238–247.
Benz, R., Darveau, R. P., and Hancock, R. E. W. (1984).Eur. J. Biochem. 140 319–324.
Benz. R., Schmidt, A., and Vos-Scheperkeuter, G. H. (1987).J. Membr. Biol. 100 21–29.
Berrier, C., Coulombe, A., Houssin, C., and Ghazi, A. (1989).FEBS Lett. 259 27–32.
Blachly-Dyson, E., Peng, S., Colombini, M., and Forte, M. (1990)Science 247 1233–1236.
Bremer, E., Middendorf, J., Martinussen, J., and Valentin-Hansen, P. (1990).Gene 96 59–65.
Buechner, M., Delcour, A. H., Martinac, B., Adler, J., and Kung, C. (1990).Biochim. Biophys. Acta 1024 111–121.
Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., Jansonius, J. N., and Rosenbusch, J. P. (1992).Nature (London),358 727–733.
Death, A., Notley, L., and Ferenci, T. (1993).J. Bacteriol. 175 1475–1483.
Ferenci, T., and Lee, K.-S. (1982).J. Mol. Biol. 160 431–444.
Ferenci, T., Saurin, W., and Hofnung, M. (1988).J. Mol. Biol. 201 493–496.
Forst, D., Schulein, K., Wacker, T., Diedrichs, K., Kreutz, W., Benz, R., and Welte, W. (1993).J. Mol. Biol. 229 258–262.
Freundlieb, S., Ehmann, U., and Boos, W. (1988).J. Biol. Chem. 263 314–320.
Garavito, R. M., and Rosenbusch, J. P. (1980).J. Cell. Biol. 86 327–329.
Hancock, R. E. W., and Benz, R. (1986).Biochim. Biophys. Acta 860 699–707.
Hancock, R. E. W., and Carey, A. M. (1979).J. Bacteriol. 140 902–910.
Hancock, R. E. W., Poole. K., and Benz, R. (1982).J. Bacteriol. 150 730–738.
Hancock, R. E. W., Egli, C., Benz, R., and Siehnel, R. J. (1992).J. Bacteriol. 174 471–476.
Heine, H.-G., Francis, G., Lee, K.-S., and Ferenci, T. (1988).J. Bacteriol. 170 1730–1738.
Jap, B. K., and Walian, P. J. (1990).Q. Rev. Biophys. 23 367–403.
Jap, B. K., Walian, P. J., and Gehring, K. (1991).Nature (London),350 167–170.
Labischinski, H., Barnickel, G., Bradaczek, H., Naumann, D., Rietschel, E. T., and Giesbrecht, P. (1985).J. Bacteriol. 169 9–20.
Labischinski, H., Naumann, D., Shulz, C., Kusumoto, S., Shiba, T., Rietschel, E. T., and Giesbrecht, P. (1989).Eur. J. Biochem. 179 659–665.
Levy, S. B. (1992).Antimicrob. Agents Chemother. 36 695–703.
Luckey, M., and Nikaido, H. (1980).Proc. Natl. Acad. Sci. USA 77 167–171.
Maier, C., Bremer, E., Schmid, A., and Benz, R. (1988).J. Biol. Chem. 263 2493–2499.
Martinac, B., Buechner, M., Delcour, A. H., Adler, J., and Kung, C. (1987).Proc. Natl. Acad. Sci. USA 84 2297–2301.
Misra, R., and Benson, S. A. (1988).J. Bacteriol. 170 3611–3617.
Nikaido, H. (1990). InMembrane Transport and Information Storage. Advances in Membrane Fluidity, Vol. 4 (Aloia, R. C., Curtain, C. C., and Gordon, L. M., eds.), Alan, R. Liss, New York, pp. 165–190.
Nikaido, H. (1992).Mol. Microbiol. 6 435–442.
Nikaido, H., and Vaara, M. (1985).Microbiol. Rev. 49 1–32.
Nikaido, H., Takeuchi, Y., Ohnishi, S., and Nakae, T. (1977)Biochim. Biophys. Acta 465 152–164.
Nikaido, H., Nikaido, K., and Harayama, S. (1991).J. Biol. Chem. 266 770–779.
Nikaido, H., Kim, S.-H., and Rosenberg, E. Y. (1993).Mol. Microbiol. 8 1025–1030.
Pauptit, R. A., Schirmer, T., Jansonius, J. N., Rosenbusch, J. P., Parker, M. W., Tucker, A. D., Tsernoglou, D., Weiss, M. S., and Schulz, G. E. (1991).J. Struct. Biol. 107 136–145.
Plesiat, P., and Nikaido, H. (1992).Mol. Microbiol. 6 1323–1333.
Quinn, J. P., Dudek, C. A., di Vicenzo, C. A., Lucks, D. A., and Lerner, S. A. (1986).J. Infect. Dis. 154 289–294.
Rachel, R., Engel, A. M., Huber, R., Stetter, K.-O., and Baumeister, W. (1990).FEBS Lett. 262 64–68.
Schiltz, E., Kreusch, A., Nestel, U., and Schulz, G. E. (1991).Eur. J. Biochem. 199 587–594.
Schulein, K., Schmid, A., and Benz, R. (1991).Mol. Microbiol. 5 2233–2241.
Sen, K., and Nikaido, H. (1990).Proc. Natl. Acad. Sci. USA 87 743–747.
Sen, K., and Nikaido, H. (1991).J. Bacteriol. 173 926–928.
Sen, K., Hellman, J., and Nikaido, H. (1988).J. Biol. Chem. 263 1182–1187.
Stein, W. D. (1967).The Movement of Molecules across Cell Membranes. Academic Press, New York.
Struyve, M., Visser, J., Adriaanse, H., Benz, R., and Tommassen, J. (1993).Mol. Microbiol. 7 131–140.
Sugawara, E., and Nikaido, H. (1992).J. Biol. Chem. 267 2507–2511.
Takeuchi, Y., and Nikaido, H. (1981).Biochemistry 20 523–529.
Todt, J. C., Rocque, W. J., and McGroarty, E. J. (1992).Biochemistry 31 10471–10478.
Trias, J., and Nikaido, H. (1990).J. Biol. Chem. 265 15680–15684.
Trias, J., Rosenberg, E. Y., and Nikaido, H. (1988).Biochim. Biophys. Acta 938 493–496.
Trias, J., Dufresne, J., Levesque, R. C., and Nikaido, H. (1989).Antimicrob. Agents Chemother. 33 1201–1206.
Trias, J., Jarlier, V., and Benz, R. (1992).Science 258 1479–1481.
Vaara, M. (1992).Microbiol. Rev. 56 395–411.
Vaara, M. (1993).Antimicrob. Agents Chemother., in press.
Weiss, M. S., and Schulz, G. E. (1992).J. Mol. Biol. 227 493–509.
Weiss, M. S., Abele, U., Weckesser, J., Welte, W., Shiltz, E., and Schulz, G. E. (1991).Science 254 1627–1629.
Yoshimoto, T., Higashi, H., Kanatani, A., Lin, X.-S., Nagai, H., Oyama, H., Kurazono, K., and Tsuru, D. (1991).J. Bacteriol. 173 2173–2179.
Yoshimura, F., and Nikaido, H. (1982).J. Bacteriol. 152 636–642.
Zimmermann, W., and Rosselet, A. (1977).Antimicrob. Agents Chemother. 12 368–372.
Zoratti, M., and Petronilli, V. (1988).FEBS Lett. 240 105–109.
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Nikaido, H. Transport across the bacterial outer membrane. J Bioenerg Biomembr 25, 581–589 (1993). https://doi.org/10.1007/BF00770245
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DOI: https://doi.org/10.1007/BF00770245