Structure and functional mechanism of porins

Physiological Reviews

Volumn 76, Issue 4, 1996, Pages 1073-1088

  Jap, Bing K ^a   Walian, Peter J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL OUTER MEMBRANE; CELL MEMBRANE POTENTIAL; CELL MEMBRANE TRANSPORT; CELLULAR DISTRIBUTION; CHANNEL GATING; LIPID BILAYER; MEMBRANE STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STRUCTURE ACTIVITY RELATION;

EID: 0029907916     PISSN: 00319333     EISSN: None     Source Type: Journal    
DOI: 10.1152/physrev.1996.76.4.1073     Document Type: Article

References (84)

1. BAUER, K., M. STRUYVÉ, D. BOSCH, R. BENZ, AND J. TOMMASSEN. One single lysine residue is responsible for the special interaction between polyphosphate and the outer membrane porin PhoE of Escherichia coli. J. Biol. Chem. 264: 16393-16398, 1989.
2. BENSON, S. A., J. L. L. OCCI, AND B. A. SAMPSON. Mutations that alter the pore function of the OmpF porin of Escherichia coli K12. J. Mol. Biol. 203: 961-970, 1988.
3. BENZ, R. Permeation of hydrophilic solutes through mitochondrial outer membranes: review on mitochondrial porins. Biochim. Biophys. Acta 1197: 167-196, 1994.
4. BENZ, R., A. SCHMID, AND R. E. W. HANCOCK. Ion selectivity of gram-negative bacterial porins. J. Bacteriol. 162: 722-727, 1985.
5. BERRIER, C., A. COULOMBE, C. HOUSSIN, AND A. GHAZI. Fast and slow kinetics of porin channels from Escherichia coli reconstituted into giant liposomes and studied by patch-clamp. FEBS Lett. 306: 251-256, 1992.
6. BISHOP, N. D., AND E. J. A. LEA. Characterisation of the porin of Rhodobacter capsulatus 37b4 in planar lipid bilayers. FEBS Lett. 349: 69-74, 1994.
7. BJÖRKSTÉN, J., C. M. SOARES, O. NILSSON, AND O. TAPIA. On the stability and plastic properties of the interior L3 loop in R. capsulatus porin. A molecular dynamics study. Protein Eng. 7: 487-493, 1994.
8. BUEHLER, L. K., AND J. P. ROSENBUSCH. Single channel behavior of matrix porin of Escherichia coli. Biochem. Biophys. Res. Commun. 190: 624-629, 1993.
9. COLOMBINI, M. A candidate for the permeability pathway of the outer mitochondrial membrane. Nature Lond. 279: 643-645, 1979.
10. COWAN, S. W., T. SCHIRMER, G. RUMMEL, M. STEIERT, R. GHOSH, R. A. PAUPTIT, J. N. JANSONIUS, AND J. P. ROSENBUSCH. Crystal structures explain functional properties of two E. coli porins. Nature Lond. 358: 727-733, 1992.
11. DARGENT, B., W. HOFMANN, F. PATTUS, AND J. P. ROSENBUSCH. The selectivity filter of voltage-dependent channels formed by phosphoporin (PhoE protein) from E. coli. EMBO J. 5: 773-778, 1986.
12. DARGENT, B., J. ROSENBUSCH, AND F. PATTUS. Selectivity for maltose and maltodextrins of maltoporin, a pore-forming protein of E. coli outer membrane. FEBS Lett. 220: 136-142, 1987.
13. DECAD, G. M., AND H. NIKAIDO. Outer membrane of gram-negative bacteria. XII. Molecular-sieving function of cell wall. J. Bacteriol. 128: 325-336, 1976.
14. DELCOUR, A. H., J. ADLER, AND C. KUNG. A single amino acid substitution alters conductance and gating of OmpC porin of Escherichia coli. J. Membr. Biol. 119: 267-275, 1991.
15. DORSET, D. L., A. ENGEL, M. HANER, A. MASSALSKI, AND J. P. ROSENBUSCH. Two-dimensional crystal packing of matrix porin. A channel forming protein in Escherichia coli outer membranes. J. Mol. Biol. 165: 701-710, 1983.
16. DORSET, D. L., A. ENGEL, A. MASSALSKI, AND J. P. ROSENBUSCH. Three dimensional structure of a membrane pore. Electron microscopical analysis of Escherichia coli outer membrane maxtrix porin. Biophys. J. 45: 128-129, 1984.
17. EARNEST, T. N., P. WALIAN, K. GEHRING, AND B. K. JAP. Phase refinement in the electron crystallographic structure determination of PhoE porin. Trans. Am. Cryst. Assoc. 28: 159-164, 1992.
18. EHRENSTEIN, G., H. LECAR, AND R. NOSSAL. The nature of the negative resistance in bimolecular lipid membranes containing excitability-inducing material. J. Gen. Physiol. 55: 119-133, 1970.
19. EL KOUHEN, R., A. HOENGER, A. ENGEL, AND J. M. PAGES. In vitro approaches to investigation of the early steps of colicin-OmpF interaction. Eur. J. Biochem. 224: 723-728, 1994.
20. ENGEL, A., A. MASSALSKI, H. SCHINDLER, D. L. DORSET, AND J. P. ROSENBUSCH. Porin channel triplets merge into single outlets in Escherichia coli outer membranes. Nature Lond. 317: 643-645, 1985.
21. FISCHER, K., A. WEBER, S. BRINK, B. ARBINGER, D. SCHÜNEMANN, S. BORCHERT, H. W. HELDT, B. POPP, R. BENZ, T. A. LINK, C. ECKERSKORN, AND U.-I. FLÜGGE. Porins from plants. Molecular cloning and functional characterization of two new members of the porin family. J. Biol. Chem. 269: 25754-25760, 1994.
22. GABLER, R. Electrical Interactions in Molecular Biophysics. San Francisco, CA: Academic, 1978.
23. GARAVITO, R. M., J. JENKINS, J. N. JANSONIUS, R. KARLSSON, AND J. P. ROSENBUSCH. X-ray diffraction analysis of matrix porin, an integral membrane protein from Escherichia coli outer membranes. J. Mol. Biol. 164: 313-327, 1983.
24. GARAVITO, R. M., J. A. JENKINS, J. M. NEUHAUS, A. P. PUGSLEY, AND J. P. ROSENBUSCH. Structural investigations of outer membrane proteins from Escherichia coli. Ann. Microbiol. 133: 37-41, 1982.
25. GARAVITO, R. M., AND J. P. ROSENBUSCH. Three-dimensional crystals of an integral membrane protein: an initial X-ray analysis. J. Cell Biol. 86: 327-329, 1980.
26. HEAD-GORDON, T. Is water structure around hydrophobic groups clathrate-like? Proc. Natl. Acad. Sci. USA 92: 8308-8312, 1995.
27. HOENGER, A., H. GROSS, U. AEBI, AND A. ENGEL. Localization of the lipopolysaccharides in metal-shadowed reconstituted lipid-porin membranes. J. Struct. Biol. 103: 185-195, 1990.
28. HOSHI, T., W. N. ZAGOTTA, AND R. W. ALDRICH. Shaker potassium channel gating. I. Transitions near the open state. J. Gen. Physiol. 103: 249-278, 1994.
29. JAP, B. K. High-resolution electron diffraction of reconstituted PhoE porin. J. Mol. Biol. 199: 229-231, 1988.
30. JAP, B. K. Molecular design of PhoE porin and its functional consequences. J. Mol. Biol. 205: 407-419, 1989.
31. JAP, B. K., K. H. DOWNING, AND P. J. WALIAN. Structure of PhoE porin in projection at 3.5 Å resolution. J. Struct. Biol. 103: 57-63, 1990.
32. JAP, B. K., AND P. J. WALIAN. Biophysics of the structure and function of porins. Q. Rev. Biophys. 23: 367-403, 1990.
33. JAP, B. K., P. J. WALIAN, AND K. GEHRING. Structural architecture of an outer membrane channel as determined by electron crystallography. Nature Lond. 350: 167-170, 1991.
34. KARSHIKOFF, A., V. SPASSOV, S. W. COWAN, R. LADENSTEIN, AND T. SCHIRMER. Electrostatic properties of two porin channels from Escherichia coli. J. Mol. Biol. 240: 372-384, 1994.
35. KLEFFEL, B., R. M. GARAVITO, W. BAUMEISTER, AND J. P. ROSENBUSCH. Secondary structure of a channel-forming protein: porin from E. coli outer membranes. EMBO J. 4: 1589-1592, 1985.
36. KORTELAND, J., J. TOMMASSEN, AND B. LUGTENBERG. PhoE protein pore of the outer membrane of Escherichia coli K12 is a particularly efficient channel for organic and inorganic phosphate. Biochim. Biophys. Acta 690: 282-289, 1982.
37. KREUSCH, A., A. NEUBÜSER, E. SCHILTZ, J. WECKESSER, AND G. E. SCHULZ. Structure of the membrane channel porin from Rhodopseudomonas blastica at 2.0 Å resolution. Protein Sci. 3: 58-63, 1994.
38. KREUSCH, A., AND G. E. SCHULZ. Refined structure of the porin from Rhodopseudomonas blastica. Comparison with the porin from Rhodobacter capsulatus. J. Mol. Biol. 243: 891-905, 1994.
39. LAKEY, J. H., AND F. PATTUS. The voltage-dependent activity of Escherichia coli porins in different planar bilayer reconstitutions. Eur. J. Biochem. 186: 303-308, 1989.
40. LEPAULT, J., B. DARGENT, W. TICHELAAR, J. P. ROSENBUSCH, K. LEONARD, AND F. PATTUS. Three-dimensional reconstruction of maltoporin from electron microscopy and image processing. EMBO J. 7: 261-268, 1988.
41. MANNELLA, C. A., X.-W. GUO, AND B. COGNON. Diameter of the mitochondrial outer membrane channel: evidence from electron microscopy of frozen-hydrated membrane crystals. FEBS Lett. 253: 231-234, 1989.
42. 2 treatment of the Neurospora membrane. Biophys. J. 49: 307-318, 1986.
43. MAURO, A., M. BLAKE, AND P. LABARCA. Voltage gating of conductance in lipid bilayers induced by porin from outer membrane of Neisseria gonorrhoeae. Proc. Natl. Acad. Sci. USA 85: 1071-1075, 1988.
44. MISRA, R., AND S. A. BENSON. Genetic identification of the pore domain of the OmpC porin of Escherichia coli K-12. J. Bacteriol. 170: 3611-3617, 1988.
45. NABEDRYK, E., R. M. GARAVITO, AND J. BRETON. The orientation of β-sheets in porin. A polarized Fourier transform infrared spectroscopic investigation. Biophys. J. 53: 671-676, 1988.
46. NAKAE, T. Identification of the outer membrane protein of E. coli that produces transmembrane channels in reconstituted vesicle membranes. Biochem. Biophys. Res. Commun. 71: 877-884, 1976.
47. NAKAE, T. Outer membrane of Salmonella. Isolation of protein complex that produces transmembrane channels. J. Biol. Chem. 251: 2176-2178, 1976.
48. NAKAMURA, K., AND S. MIZUSHIMA. Effects of heating in dodecyl sulfate solution on the conformation and electrophoretic mobility of isolated major outer membrane proteins from Escherichia coli K-12. J. Biochem. 80: 1411-1422, 1976.
49. NAKAMURA, K., D. N. OSTEROVSKY, T. MIYAZAWA, AND S. MIZUSHIMA. Infrared spectra of outer and cytoplasmic membranes of Escherichia coli. Biochim. Biophys. Acta 332: 329-335, 1974.
50. NESTEL, U., T. WACKER, D. WOITZIK, J. WECKESSER, W. KREUTZ, AND W. WELTE. Crystallization and preliminary X-ray analysis of porin from Rhodobacter capsulatus. FEBS Lett. 242: 405-408, 1989.
51. NIKAIDO, H. Porins and specific channels of bacterial outer membranes. Mol. Microbiol. 6: 435-442, 1992.
52. NIKAIDO, H. Transport across the bacterial outer membrane. J. Bioenerg. Biomembr. 25: 581-589, 1993.
53. NIKAIDO, H. Porins and specific diffusion channels in bacterial outer membranes. J. Biol. Chem. 269: 3905-3908, 1994.
54. NIKAIDO, H., K. NIKAIDO, AND S. HARAYAMA. Identification and characterization of porins in Pseudomonas aeruginosa. J. Biol. Chem. 266: 770-779, 1991.
55. NIKAIDO, H., AND E. Y. ROSENBERG. Effect of solute size on diffusion rates through the transmembrane pores of the outer membrane of Escherichia coli. J. Gen. Physiol. 77: 121-135, 1981.
56. NIKAIDO, H., AND E. Y. ROSENBERG. Porin channels in Escherichia coli: studies with liposomes reconstituted from purified proteins. J. Bacteriol. 153: 241-252, 1983.
57. NIKAIDO, H., E. Y. ROSENBERG, AND J. FOULDS. Porin channels in Escherichia coli: studies with β-lactams in intact cells. J. Bacteriol. 153: 232-240, 1983.
58. NIKAIDO, H., AND M. VAARA. Molecular basis of bacterial outer membrane permeability. Microbiol. Rev. 49: 1-32, 1985.
59. PLESIAT, P., AND H. NIKAIDO. Outer membranes of gram-negative bacteria are permeable to steroid probes. Mol. Microbiol. 6: 1323-1333, 1992.
60. REID, J., H. FUNG, K. GEHRING, P. E. KLEBBA, AND H. NIKAIDO. Targeting of porin to the outer membrane of Escherichia coli. Rate of trimer assembly and identification of a dimer intermediate. J. Biol. Chem. 263: 7753-7759, 1988.
61. ROCQUE, W. J., R. T. COUGHLIN, AND E. J. MCGROARTY. Lipopolysaccharide tightly bound to porin monomers and trimers from Escherichia coli K-12. J. Bacteriol. 169: 4003-4010, 1987.
62. ROSENBUSCH, J. P. Characterization of the major envelope protein from Escherichia coli. Regular arrangement on the peptidoglycan and unusual dodecyl sulfate binding. J. Biol. Chem. 249: 8019-8029, 1974.
63. SASS, H. J., G. BÜLDT, E. BECKMANN, F. ZEMLIN, M. VAN HEEL, E. ZEITLER, J. P. ROSENBUSCH, D. L. DORSET, AND A. MASSALSKI. Densely packed β-structure at the protein-lipid interface of porin is revealed by high-resolution cryo-electron microscopy. J. Mol. Biol. 209: 171-175, 1989.
64. SCHEIN, S. J., M. COLOMBINI, AND A. FINKELSTEIN. Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria. J. Membr. Biol. 30: 99-120, 1976.
65. SCHINDLER, H., AND J. P. ROSENBUSCH. Matrix protein in planar membranes: clusters of channels in a native environment and their functional reassembly. Proc. Natl. Acad. Sci. USA 78: 2302-2306, 1981.
66. SCHIRMER, T., T. A. KELLER, Y.-F. WANG, AND J. P. ROSENBUSCH. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science Wash. DC 267: 512-514, 1995.
67. SCHULZ, G. E. Structure and function of the membrane channel porin. In: Biochemistry of Cell Membranes. Basel, Switzerland: Birkhäuser Verlag, 1995, p. 327-338.
68. SEN, K., J. HELLMAN, AND H. NIKAIDO. Porin channels in intact cells of Escherichia coli are not affected by Donnan potentials across the outer membrane. J. Biol. Chem. 263: 1182-1187, 1988.
69. SPURLINO, J. C., G.-Y. LU, AND F. A. QUIOCHO. The 2.3-Å resolution structure of the maltose- or maltodextrin-binding protein, a primary receptor of bacterial active transport and chemotaxis. J. Biol. Chem. 266: 5202-5219, 1991.
70. STEVEN, A. C., B. TEN HEGGELER, R. MÜLLER, J. KISTLER, AND J. P. ROSENBUSCH. Ultrastructure of a periodic protein layer in the outer membrane of Escherichia coli. J. Cell Biol. 72: 292-301, 1977.
71. STILLINGER, F. H. Water revisited. Science Wash. DC 209: 451-457, 1980.
72. SUGAWARA, E., AND H. NIKAIDO. Pore-forming activity of OmpA protein of Escherichia coli. J. Biol. Chem. 267: 2507-2511, 1992.
73. SUGAWARA, E., AND H. NIKAIDO. OmpA protein of Escherichia coli outer membrane occurs in open and closed channel forms. J. Biol. Chem. 269: 17981-17987, 1994.
74. THINNES, F. P. Evidence for extra-mitochondrial localization of the VDAC/porin channel in eukaryotic cells. J. Bioenerg. Biomembr. 24: 71-75, 1992.
75. THINNES, F. P., H. FLÖRKE, H. WINKELBACH, U. STADTMÜLLER, M. HEIDEN, A. KARABINOS, D. HESSE, H. D. KRATZIN, E. FLEER, AND N. HILSCHMANN. Channel active mammalian porin, purified from crude membrane fractions of human B lymphocytes or bovine skeletal muscle, reversibly binds the stilbene-disulfonate group of the chloride channel blocker DIDS. Biol. Chem. Hoppe-Seyler 375: 315-322, 1994.
76. TODT, J. C., W. J. ROCQUE, AND E. J. MCGROARTY. Effects of pH on bacterial porin function. Biochemistry 31: 10471-10478, 1992.
77. TOMMASSEN, J. Biogenesis and membrane topology of outer membrane proteins in Escherichia coli. In: Membrane Biogenesis. Heidelberg, Germany: Springer-Verlag, 1988, p. 351-373.
78. VACATA, V., L. GROSS, AND H. LECAR. Trimeric gating of bacterial porins reconstituted in lipid bilayers. Biophys. J. 57: 478a, 1990.
79. VOGEL, H., AND F. JÄHNIG. Models for the structure of outer-membrane proteins of Escherichia coli derived from raman spectroscopy and prediction methods. J. Mol. Biol. 190: 191-199, 1986.
80. WEISS, M. S., U. ABELE, J. WECKESSER, W. WELTE, E. SCHILTZ, AND G. E. SCHULZ. Molecular architecture and electrostatic properties of a bacterial porin. Science Wash. DC 254: 1627-1630, 1991.
81. WEISS, M. S., AND G. E. SCHULZ. Structure of porin refined at 1.8 Å resolution. J. Mol. Biol. 227: 493-509, 1992.
82. WEISS, M. S., T. WACKER, J. WECKESSER, W. WELTE, AND G. E. SCHULZ. The three-dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett. 267: 268-272, 1990.
83. XU, G. Z., B. SHI, E. J. MCGROARTY, AND H. T. TIEN. Channel-closing activity of porins from Escherichia coli in bilayer lipid membranes. Biochim. Biophys. Acta 862: 57-64, 1986.
84. YAMADA, H., AND S. MIZUSHIMA. Interaction between major outer membrane protein (0-8) and lipopolysaccharide in Escherichia coli K12. Eur. J. Biochem. 103: 209-218, 1980.