The structure of bacterial outer membrane proteins

Biochimica et Biophysica Acta - Biomembranes

Volumn 1565, Issue 2, 2002, Pages 308-317

  Schulz, Georg E ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Barrel; Helix; Twist; Chainfold topology; Channel engineering; Shear number

Indexed keywords

FERROUS ION; GRAMICIDIN A; HEMOLYSIN; ISOPROTEIN; MALTOPROTEIN; OUTER MEMBRANE PROTEIN; POLYPEPTIDE; PORIN; UNCLASSIFIED DRUG;

ALPHA HELIX; CALCULATION; CELL INCLUSION; CRYSTAL STRUCTURE; CYTOPLASM; HYDROGEN BOND; MACROMOLECULE; MICELLE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN STRUCTURE; REVIEW; X RAY DIFFRACTION;

BACTERIAL OUTER MEMBRANE PROTEINS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; MODELS, MOLECULAR; PORINS; PROTEIN ENGINEERING; SOLUBILITY;

BACTERIA (MICROORGANISMS);

EID: 0037064291     PISSN: 00052736     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0005-2736(02)00577-1     Document Type: Review

References (75)

1. Liu J., Rost B. Comparing function and structure between entire proteomes. Protein Sci. 10:2001;1970-1979.
2. Sipos L., von Heijne G. Predicting the topology of eukaryotic membrane proteins. Eur. J. Biochem. 213:1993;1333-1340.
3. Schulz G.E. Protein differentiation: emergence of novel proteins during evolution. Angew. Chem., Int. Ed. Engl. 20:1981;143-151.
4. Brenner S.E., Levitt M. Expectations from structural genomics. Protein Sci. 9:2000;197-200.
5. Schulz G.E., Schirmer R.H. Principles of Protein Structure. 1979;84-87 Springer, New York.
6. Bowie J.U. Helix-bundle membrane protein fold templates. Protein Sci. 8:1999;2711-2719.
7. Schmid B., Krömer M., Schulz G.E. Expression of porin from Rhodopseudomonas blastica in Escherichia coli inclusion bodies and folding into exact native structure. FEBS Lett. 381:1996;111-114.
8. Pautsch A., Schulz G.E. High resolution structure of the OmpA membrane domain. J. Mol. Biol. 298:2000;273-282.
9. Birktoft J.J., Blow D.M. Structure of crystalline α-chymotrypsin. J. Mol. Biol. 68:1972;187-240.
10. Banner D.W., Bloomer A.C., Petsko G.A., Phillips D.C., Pogson C.I., Wilson I.A., Corran P.H., Furth A.J., Milman J.D., Offord R.E., Priddle J.D., Waley S.G. Structure of chicken muscle triose phosphate isomerase determined crystallographically at 2.5 Å resolution using amino acid sequence data. Nature. 255:1975;609-614.
11. Hendrickson W.A., Pähler A., Smith J.L., Satow Y., Merritt E.A., Phizackerley R.P. Crystal structure of core streptavidin determined from multi-wavelength anomalous diffraction of synchrotron radiation. Proc. Natl. Acad. Sci. U. S. A. 86:1989;2190-2194.
12. Newcomer M.E., Jones T.A., Åqvist J., Sundelin J., Eriksson U., Rask L., Peterson P.A. The three-dimensional structure of retinol-binding protein. EMBO J. 3:1984;1451-1454.
13. Yoder M.D., Keen N.T., Jurnak F. New domain motif: the structure of pectate lyase C, a secreted plant virulence factor. Science. 260:1993;1503-1507.
14. Baumann U., Wu S., Flaherty K.M., McKay D.B. Three-dimensional structure of the alkaline protease of Pseudomonas aeruginosa: a two-domain protein with a calcium binding parallel beta roll motif. EMBO J. 12:1993;3357-3364.
15. Raetz C.R.H., Roderick S.L. A left-handed parallel β-helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science. 270:1995;997-1000.
16. Ketchem R.R., Hu W., Cross T.A. High-resolution conformation of gramicidin A in a lipid bilayer by solid-state NMR. Science. 261:1993;1457-1460.
17. Ghadiri M.R., Granja J.R., Buehler L.K. Artificial transmembrane ion channels from self-assembling peptide nanotubes. Nature. 369:1994;301-304.
18. Vogt J., Schulz G.E. The structure of the outer membrane protein OmpX from Escherichia coli reveals possible mechanisms of virulence. Structure. 7:1999;1301-1309.
19. Pautsch A., Schulz G.E. Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol. 5:1998;1013-1017.
20. Vandeputte-Rutten L., Kramer R.A., Kroon J., Dekker N., Egmond M.R., Gros P. Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J. 20:2001;5033-5039.
21. Snijder H.J., Ubarretxena-Belandia I., Blaauw M., Kalk K.H., Verhij H.M., Egmond M.R., Dekker N., Dijkstra B.W. Structural evidence for dimerization-regulated activation of an integral membrane phospholipase. Nature. 401:1999;717-721.
22. Koronakis V., Scharff A., Koronakis E., Luisi B., Hughes C. Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature. 405:2000;914-919.
23. Song L., Hobaugh M.R., Shustak C., Cheley S., Bayley H., Gouaux J.E. Structure of staphylococcal α-hemolysin, a heptameric transmembrane pore. Science. 274:1996;1859-1865.
24. Olson R., Nariya H., Yokota K., Kamio Y., Gouaux E. Crystal structure of Staphylococcal LukF delineates conformational changes accompanying formation of a transmembrane channel. Nat. Struct. Biol. 6:1999;134-140.
25. Deisenhofer J., Epp O., Miki K., Huber R., Michel H. Structure of the protein subunits in the photosynthetic reaction centre of Rhodopseudomonas viridis at 3 Å resolution. Nature. 318:1985;618-624.
26. Weiss M.S., Wacker T., Weckesser J., Welte W., Schulz G.E. The three-dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett. 267:1990;268-272.
27. Weiss M.S., Schulz G.E. Structure of porin refined at 1.8 Å resolution. J. Mol. Biol. 227:1992;493-509.
28. Schulz G.E. Structure-function relationships in the membrane channel porin as based on a 1.8 Å resolution crystal structure. Pullman A., Jortner J., Pullman B. Membrane Proteins: Structures, Interactions and Models. 1992;403-412 Kluwer, Dordrecht.
29. Schulz G.E. Structure-function relationships in porins as derived from a 1.8 Å resolution crystal structure. Ghuysen J.M., Hakenbeck R. New Comprehensive Biochemistry. Bacterial Cell Wall. vol. 27:1994;343-352 Elsevier, Amsterdam.
30. Schirmer T., Keller T.A., Wang Y.F., Rosenbusch J.P. Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science. 267:1995;512-514.
31. Meyer J.E.W., Hofnung M., Schulz G.E. Structure of maltoporin from Salmonella typhimurium ligated with a nitrophenyl-maltrotrioside. J. Mol. Biol. 266:1997;761-775.
32. Forst D., Welte W., Wacker T., Diederichs K. Structure of the sucrose-specific porin ScrY from Salmonella typhimurium and its complex with sucrose. Nat. Struct. Biol. 5:1998;37-46.
33. Locher K.P., Rees B., Koebnik R., Mitschler A., Moulinier L., Rosenbusch J.P., Moras D. Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell. 95:1998;771-778.
34. Ferguson A.D., Hofmann E., Coulton J.W., Diederichs K., Welte W. Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science. 282:1998;2215-2220.
35. Buchanan S.K., Smith B.S., Venkatramani L., Xia D., Esser L., Palnitkar M., Chakraborty R., van der Helm D., Deisenhofer J. Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat. Struct. Biol. 6:1999;56-63.
36. Wimley W.C., White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat. Struct. Biol. 3:1996;842-848.
37. Yau W.M., Wimley W.C., Gawrisch K., White S.H. The preference of tryptophan for membrane interfaces. Biochemistry. 37:1998;14713-14718.
38. Pautsch A., Vogt J., Model K., Siebold C., Schulz G.E. Strategy for membrane protein crystallization exemplified with OmpA and OmpX. Proteins: Struct. Funct. Genet. 34:1999;167-172.
39. Welte W., Weiss M.S., Nestel U., Weckesser J., Schiltz E., Schulz G.E. Prediction of the general structure of OmpF and PhoE from the sequence and structure of porin from Rhodobacter capsulatus. Orientation of porin in the membrane. Biochim. Biophys. Acta. 1080:1991;271-274.
40. Schirmer T., Cowan S.W. Prediction of membrane-spanning β-strands and its application to maltoporin. Protein Sci. 2:1993;1361-1363.
41. Gromiha M.M., Majumdar R., Ponnuswamy P.K. Identification of membrane spanning β-strands in bacterial porins. Protein Eng. 10:1997;497-500.
42. Seshadri K., Garemyr R., Wallin E., von Heijne G., Elofsson A. Architecture of β-barrel membrane proteins: analysis of trimeric porins. Protein Sci. 7:1998;2026-2032.
43. Diederichs K., Freigang J., Umhau S., Zeth K., Breed J. Prediction by a neural network of outer membrane β-strand protein topology. Protein Sci. 7:1998;2413-2420.
44. Jacoboni I., Martelli P.L., Fariselli P., de Pinto V., Casadio R. Prediction of the transmembrane regions of β-barrel membrane proteins with a neural network-based predictor. Protein Sci. 10:2001;779-787.
45. Morona R., Klose M., Henning U. Escherichia coli K-12 outer membrane protein (OmpA) as a bacteriophage receptor: analysis of mutant genes expressing altered proteins. J. Bacteriol. 159:1984;570-578.
46. Nikaido H. Prevention of drug access to bacterial targets: permeability barriers and active efflux. Science. 264:1994;382-388.
47. Garavito R.M., Rosenbusch J.P. Three-dimensional crystals of an integral membrane protein: an initial X-ray analysis. J. Cell Biol. 86:1980;327-329.
48. Cowan S.W., Schirmer T., Rummel G., Steiert M., Ghosh R., Pauptit R.A., Jansonius J.N., Rosenbusch J.P. Crystal structures explain functional properties of two E. coli porins. Nature. 358:1992;727-733.
49. Dutzler R., Rummel G., Alberti S., Hernández-Allés S., Phale P.S., Rosenbusch J.P., Benedi V.J., Schirmer T. Crystal structure and functional characterization of OmpK36, the osmoporin of Klebsiella pneumoniae. Structure. 7:1999;425-434.
50. Hirsch A., Breed J., Saxena K., Richter O.M.H., Ludwig B., Diederichs K., Welte W. The structure of porin from Paracoccus denitrificans at 3.1 Å resolution. FEBS Lett. 404:1997;208-210.
51. Zeth K., Diederichs K., Welte W., Engelhardt H. Crystal structure of Omp32, the anion-selective porin from Comamonas acidovorans, in complex with a periplasmic peptide at 2.1 Å resolution. Structure. 8:2000;981-992.
52. Conlan S., Zhang Y., Cheley S., Bayley H. Biochemical and biophysical characterization of OmpG: a monomeric porin. Biochemistry. 39:2000;11845-11854.
53. Meyer J.E.W., Schulz G.E. Energy profile of maltooligosaccharide permeation through maltoporin as derived from the structure and from a statistical analysis of saccharide-protein interactions. Protein Sci. 6:1997;1084-1091.
54. Schirmer T., Phale P.S. Brownian dynamics simulation of ion flow through porin channels. J. Mol. Biol. 294:1999;1159-1167.
55. Dumas F., Koebnik R., Winterhalter M., Van Gelder P. Sugar transport through maltoporin of Escherichia coli. J. Biol. Chem. 275:2000;19747-19751.
56. Rutz J.M., Liu J., Lyons A.J., Goranson J., Armstrong S.K., McIntosh M.A., Feix J.B., Klebba P.E. Formation of a gated channel by a ligand-specific transport protein in the bacterial outer membrane. Science. 258:1992;471-475.
57. Larsen R.A., Thomas M.G., Postle K. Protonmotive force, ExbB and ligand-bound FepA drive conformational changes in TonB. Mol. Microbiol. 31:1999;1809-1824.
58. Reumann S., Davila-Aponte J., Keegstra K. The evolutionary origin of the protein-translocating channel of chloroplastic envelope membranes: identification of a cyanobacterial homolog. Proc. Natl. Acad. Sci. U. S. A. 96:1999;784-789.
59. Mannella C.A. On the structure and gating mechanism of the mitochondrial channel, VDAC. J. Bioenerg. Biomembranes. 29:1997;525-531.
60. Hill K., Model K., Ryan M.T., Dietmeier K., Martin F., Wagner R., Pfanner N. Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature. 395:1998;516-521.
61. Koebnik R. Structural and functional roles of the surface-exposed loops of the β-barrel membrane protein OmpA from Escherichia coli. J. Bacteriol. 181:1999;3688-3694.
62. Cheley S., Braha O., Lu X., Conlan S., Bayley H. A functional protein pore with a "retro" transmembrane domain. Protein Sci. 8:1999;1257-1267.
63. Sugawara E., Nikaido H. OmpA protein of Escherichia coli outer membrane occurs in open and closed channel forms. J. Biol. Chem. 269:1994;17981-17987.
64. Arora A., Rinehart D., Szabo G., Tamm L.K. Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers. J. Biol. Chem. 275:2000;1594-1600.
65. Liu N., Delcour A.H. The spontaneous gating activity of OmpC porin is affected by mutations of a putative hydrogen bond network or of a salt bridge between the L3 loop and the barrel. Protein Eng. 11:1998;797-802.
66. Saxena K., Drosou V., Maier E., Benz R., Ludwig B. Ion selectivity reversal and induction of voltage-gating by site-directed mutations in the Paracoccus denitrificans porin. Biochemistry. 38:1999;2206-2212.
67. Mannella C.A. Conformational changes in the mitochondrial channel protein, VDAC, and their functional implications. J. Struct. Biol. 121:1998;207-218.
68. Schmid B., Maveyraud L., Krömer M., Schulz G.E. Porin mutants with new channel properties. Protein Sci. 7:1998;1603-1611.
69. VanGelder P., Saint N., van Boxtel R., Rosenbusch J.P., Tommassen J. Pore functioning of outer membrane protein PhoE of Escherichia coli: mutagenesis of the constriction loop L3. Protein Eng. 10:1997;699-706.
70. Ulmke D., Kreth J., Lengeler J.W., Welte W., Schmid T. Site-directed mutagenesis of loop L3 of sucrose porin ScrY leads to changes in substrate selectivity. J. Bacteriol. 181:1999;1920-1923.
71. Gu L.Q., Braha O., Conlan S., Cheley S., Bayley H. Stochastic sensing of organic analytes by a pore-forming protein containing a molecular adapter. Nature. 398:1999;686-690.
72. Kreusch A., Schulz G.E. Refined structure of the porin from Rhodopseudomonas blastica: comparison with the porin from Rhodobacter capsulatus. J. Mol. Biol. 243:1994;891-905.
73. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of β-sheet barrels in proteins: I. A theoretical analysis. J. Mol. Biol. 236:1994;1369-1381.
74. Murzin A.G., Lesk A.M., Chothia C. Principles determining the structure of β-sheet barrels in proteins: II. The observed structures. J. Mol. Biol. 236:1994;1382-1400.
75. Liu W.M. Shear numbers of protein β-barrels: definition, refinements and statistics. J. Mol. Biol. 275:1998;541-545.