β-barrel proteins from bacterial outer membranes: Structure, function and refolding

Current Opinion in Structural Biology

Volumn 9, Issue 4, 1999, Pages 455-461

  Buchanan, Susan K ^a  

^a UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

OUTER MEMBRANE PROTEIN; PHOSPHOLIPASE A;

BACTERIAL OUTER MEMBRANE; BETA CHAIN; CRYSTAL STRUCTURE; CYTOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; REVIEW; STRUCTURE ACTIVITY RELATION;

BACTERIA (MICROORGANISMS);

EID: 0033178531     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(99)80064-5     Document Type: Article

References (61)

1. Weiss MS, Wacker T, Weckesser J, Welte W, Schulz GE: The three dimensional structure of porin from Rhodobacter capsulatus at 3 Å resolution. FEBS Lett 1990, 267:268-272.
2. Cowan SW, Schirmer T, Rummel G, Steiert M, Ghosh R, Pauptit RA, Jansonius JN, Rosenbusch JP: Crystal structures explain functional properties of two E. coli porins. Nature 1992, 358:727-733.
3. Schirmer T, Keller TA, Wang Y-F, Rosenbusch JP: Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science 1995, 267:512-514.
4. 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 1998, 5:37-45.
5. Schirmer T: General and specific porins from bacterial outer membranes. J Struct Biol 1998, 121:101-109.
6. Song L, Hobaugh MR, Shustak C, Cheley S, Bayley H, Gouaux JE: Structure of Staphylococcal α-hemolysin, a heptameric transmembrane pore. Science 1996, 274:1859-1866.
7. Schmid B, Krömer M, Schulz GE: Expression of porin from Rhodopseudomonas blastica in Escherichia coli inclusion bodies and folding into exact native structure. FEBS Lett 1996, 381:111-114.
8. Surrey T, Jähnig F: Kinetics of folding and membrane insertion of a β-barrel membrane protein. J Biol Chem 1995, 24:28199-28203.
9. Kleinschmidt JH, Tamm LK: Folding intermediates of a β-barrel membrane protein. Kinetic evidence for a multistep membrane insertion mechanism. Biochemistry 1996, 35:12993-13000.
10. Koebnik R: Proposal for a peptidoglycan associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol Microbiol 1995, 16:1269-1270.
11. Ried G, Henning U: A unique amino acid substitution in the outer membrane protein OmpA causes conjugation deficiency in Escherichia coli K-12. FEBS Lett 1987, 223:387-390.
12. Foulds J, Barrett C: Characterization of Escherichia coli mutants tolerant to bacterocin JF246: Two new classes of tolerant mutants. J Bacteriol 1973, 116:885-892.
13. Morona R, Krämer C, Henning U: Bacteriophage receptor area of outer membrane protein OmpA of Escherichia coli K-12. J Bacteriol 1985, 164:539-543.
14. Pautsch A, Schulz GE: Structure of the outer membrane protein A transmembrane domain. Nat Struct Biol 1998, 5:1013-1017. This paper provides a structural description of the OmpA transmembrane domain at 2.5 Å resolution, the smallest β-barrel structure so far determined.
15. Pautsch A, Vogt J, Model K, Siebold C, Schulz GE: Strategy for membrane protein crystallization exemplified with OmpA and OmpX. Proteins 1999, 34:167-172. A strategy for producing a protein that is suitable for structural analysis, improving both quantity and quality, is described. Site-directed mutagenesis was used to remove charged residues in (predicted) loop L3, resulting in better quality crystals. Refolding from guanidine-solubilised inclusion bodies by dilution into detergent and polar additive yielded up to 150 mg of refolded protein per litre of cell culture.
16. Sugawara E, Nikaido H: Pore-forming activity of OmpA protein of Escherichia coli. J Biol Chem 1992, 267:2507-2511.
17. Saint N, De E, Julien S, Orange N, Molle G: Ionophore properties of OmpA of Escherichia coli. Biochim Biophys Acta 1993, 1145:119-123.
18. Nishijima M, Nakaike S, Tamori Y, Nojima S: Detergent-resistant phopholipase of Escherichia coli K12. Eur J Biochem 1977, 73:115-124.
19. Tamori Y, Nishijima M, Nojima S: Properties of purified detergent-resistant phospholipase A of Escherichia coli K12. Inactivation and protection with detergents and phospholipids. J Biochem (Tokyo) 1979, 86:1129-1138.
20. Horrevoets AJG, Hackeng TM, Verheij HM, Dijkman R, De Haas G: Kinetic characterization of Escherichia coli outer membrane phopholipase A using mixed detergent-lipid micelles. Biochemistry 1989, 28:1139-1147.
21. Grant KA, Ubarretxena-Belandia I, Dekker N, Richardson PT, Park SF: Molecular characterization of pldA, the structural gene for a phopholipase A from Campylobacter coli, and its contribution to cell-associated hemolysis. Infect Immun 1997, 65:1172-1180.
22. Bukholm G: Colony variation of Heliobacter pylori: Pathogenic potential is correlated to cell wall lipid composition. Scand J Gastroenterol 1997, 32:445-454.
23. Dekker N, Tommassen J, Lustig A, Rosenbusch JP, Verheij HM: Dimerization regulates the enzymatic activity of Escherichia coli outer membrane phospholipase A. J Biol Chem 1997, 272:3179-3184.
24. Snijder HJ, Dekker N, Ubarretxena I, Blaauw M, Kalk KH, Verheij HM, Dijkstra BW: The crystal structure of outer membrane phospholipase, an integral membrane enzyme. Bull Czech Slovak Cryst Assoc 1998, 5A:95.
25. Dekker N, Merck K, Tommassen J, Verheij HM: In vitro folding of Escherichia coli outer-membrane phospholipase A. Eur J Biochem 1995, 232:214-219.
26. Blaauw M, Dekker N, Verheij HM, Kalk KH, Dijkstra BW: Crystallization and preliminary X-ray analysis of outer membrane phospholipase A from Escherichia coli. FEBS Lett 1995, 373:10-12.
27. 12 transport field.
28. Locher KP, Rees B, Koebnik R, Mitschler A, Moulinier L, Rosenbusch JP, Moras D: Transmembrane signaling across the ligand-gated FhuA receptor: Crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 1998, 95:771-778. The structure of the ferrichrome receptor, with and without bound ferrichrome, at 2.7 Å resolution is described. A good discussion of possible transport mechanisms for ferrichrome, phages and colicins follows.
29. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W: Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science 1998, 282:2215-2220. The structure of the ferrichrome receptor, with and without bound ligand, at 2.7 Å resolution is described. This structure contains an ordered lipopolysaccharide (LPS) molecule that was essential to successful crystallisation. A potential transport channel is described that could be created by a conformational change in the N-terminal domain upon binding the TonB protein.
30. Buchanan SK, Smith BS, 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 1999, 6:56-63. The structure of the ferric enterobactin receptor was determined at 2.4 Å resolution. The iron-binding site is partially occupied in this structure at two (mutually exclusive) sites. The TonB box, a seven-residue motif shown to interact with TonB, extends into the periplasm. This structure and the two FhuA structures [28••,29••] represent the largest β-barrel structures so far observed.
31. Buchanan S, Smith B, Venkatramani L, van der Helm D, Deisenhofer J: Overexpression, refolding, and crystallization of an 80 kD outer membrane protein. Acta Crystallogr A 1996, 52:C141.
32. Booth PJ, Curran AR: Membrane protein folding. Curr Opin Struct Biol 1999, 9:115-121. A comprehensive review on membrane protein folding, with emphasis on α-helical membrane proteins. A large number of experiments have used bacteriorhodopsin, light harvesting complexes and model peptides to study the folding process, resulting in a better understanding of protein folding in the inner membrane.
33. Bayer MH, Costello GP, Bayer ME: Isolation and partial characterization of membrane vesicles carrying markers of the membrane adhesion sites. J Bacteriol 1982, 149:758-767.
34. Sen K, Nikaido H: In vitro trimerization of OmpF porin secreted by spheroplasts of Escherichia coli. Proc Natl Acad Sci USA 1990, 87:743-747.
35. Eppens EF, Nouwen N, Tommassen J: Folding of a bacterial outer membrane protein during passage through the periplasm. EMBO J 1997, 16:4295-4301.
36. de Cock H, Tommassen J: Lipopolysaccharides and divalent cations are involved in the formation of an assembly-competent intermediate of outer-membrane protein PhoE of E. coli. EMBO J 1996, 15:5567-5573.
37. Bolla J-M, Lazdunski C, Pagès J-M: The assembly of the major outer membrane protein OmpF of Escherichia coli depends on lipid synthesis. EMBO J 1988, 7:3595-3599.
38. Bardwell JCA, McGovern K, Beckwith J: Identification of a protein required for disulfide bond formation in vivo. Cell 1991, 67:581-589.
39. Lazar SW, Kolter R: SurA assists the folding of Escherichia coli outer membrane proteins. J Bacteriol 1996, 178:1770-1773.
40. Chen R, Henning U: A periplasmic protein (Skp) of Escherichia coli selectively binds a class of outer membrane proteins. Mol Microbiol 1996, 19:1287-1294.
41. de Cock H, Schäfer U, Potgeter M, Demel R, Müller M, Tommassen J: Affinity of the periplasmic chaperone Skp of Escherichia coli for phospholipids, lipopolysaccharides and non-native outer membrane proteins. Role of Skp in the biogenesis of outer membrane protein. Eur J Biochem 1999, 259:96-103.
42. Eisele J-L, Rosenbusch JP: In vitro folding and oligomerization of a membrane protein. J Biol Chem 1990, 265:10217-10220.
43. Studier FW, Rosenberg AH, Dunn JJ, Dubendorff JW: Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol 1990, 185:60-89.
44. Pullen JK, Liang S-M, Blake MS, Mates S, Tai JY: Production of Haemophilus influenzae type-b porin in Escherichia coli and its folding into the trimeric form. Gene 1995, 152:85-88.
45. Qi HL, Tai JY, Blake MS: Expression of large amounts of Neisserial porin proteins in Escherichia coli and refolding of the proteins into native trimers. Infect Immun 1994, 62:2432-2439.
46. Koppel DA, Kinnally KW, Masters P, Forte M, Blachly-Dyson E, Mannella CA: Bacterial expression and characterization of the mitochondrial outer membrane channel: Effects of N-terminal modifications. J Biol Chem 1998, 273:13794-13800. The voltage-dependent anion-selective channel is the most abundant protein in the mitochondrial outer membrane and is predicted to be a 16-stranded β-barrel. Mitochondrial VDAC was overexpressed in E. coli and refolded by solubilising inclusion bodies in guanidine, adding detergent and removing denaturant by dialysis.
47. Hill K, Model K, Ryan MT, Dietmeier K, Martin F, Wagner R, Pfanner N: Tom40 forms the hydrophilic channel of the mitochondrial import pore for preproteins. Nature 1998, 395:516-521. The authors describe the refolding and functional characterisation of a 40 kDa mitochondrial outer membrane protein that forms the hydrophilic channel for the mitochondrial import machinery. Tom40 is predicted to span the membrane using β-strands and has an estimated pore diameter of 22 Å. Inclusion bodies were solubilised in urea and diluted 10-fold into detergent.
48. Rogl H, Kosemund K, Kühlbrandt W, Collinson I: Refolding of Escherichia coli produced membrane protein inclusion bodies immobilised by nickel chelating chromatography. FEBS Lett 1998, 432:21-26. Toc75 is the chloroplast equivalent to mitochondrial Tom40 and forms the putative channel of the chloroplast protein import machinery. Toc75 has been refolded by solubilising inclusion bodies in urea and detergent, with the removal of denaturant and detergent exchange on a Ni-chelate affinity column. The advantage of this method is that refolding on a column may prevent aggregation.
49. Popp B, Gebauer S, Fischer K, Flügge UI, Benz R: Study of structure and function of recombinant pea root plastid porin by biophysical methods. Biochemistry 1997, 36:2844-2852.
50. Surrey T, Schmid A, Jähnig F: Folding and membrane insertion of the trimeric β-barrel protein OmpF. Biochemistry 1996, 35:2283-2288.
51. Dornmair K, Kiefer H, Jähnig F: Refolding of an integral membrane protein. J Biol Chem 1990, 265:18907-18911.
52. de Cock H, Tommassen J: Lipopolysaccharides and divalent cations are involved in the formation of an assembly-competent intermediate of outer-membrane protein PhoE of E. coli. EMBO J 1996, 15:5567-5573.
53. de Cock H, Brandenburg K, Wiese A, Holst O, Seydel U: Non lamellar structure and negative charges of lipopolysaccharides required for efficient folding of outer membrane protein PhoE of Escherichia coli. J Biol Chem 1999, 274:5114-5117. The in vitro folding of phosphoporin is most efficient when it is supplemented with low concentrations of Triton X-100 and lipopolysaccharides (LPS). This work investigates the properties of LPS that are conducive to folding - negative charges in the inner core and lipid A preferring a nonlamellar structure - suggesting extensive interactions between LPS and PhoE in the early stages of folding in vivo.
54. Booth PJ, Riley ML, Flitsch SL, Templer RH, Farooq A, Curran AR, Chadborn N, Wright P: Evidence that bilayer rigidity affects membrane protein folding. Biochemistry 1997, 36:197-203.
55. van Gelder P, de Cock H, Tommassen J: Detergent-induced folding of the outer-membrane protein PhoE, a pore protein induced by phosphate limitation. Eur J Biochem 1994, 226:783-787.
56. Dahan D, Srikumar R, Laprade R, Coulton JW: Purification and refolding of recombinant Haemophilus influenzae type b porin produced in Bacillus subtilis. FEBS Lett 1996, 392:304-308.
57. Reynolds JA, Tannford C: The gross conformation of protein-sodium dodecyl sulfate complexes. J Biol Chem 1970, 245:5161-5165.
58. Chen G-Q, Gouaux E: Overexpression of a glutamate receptor (GluR2) ligand binding domain in Escherichia coli: Application of a novel protein folding screen. Proc Natl Acad Sci USA 1997, 94:13431-13436.
59. Evans SV: SETOR: Hardware-lighted three-dimensional solid model representations of macromolecules. J Mol Graph 1993, 11:134-138.
60. DINO - a molecular graphics program publicly available on World Wide Web URL: http://www.biozentrum.unibas.ch/̃xray/dino/
61. Surrey T. Jähnig F: Refolding and oriented insertion of a membrane protein into a lipid bilayer. Proc Natl Acad Sci USA 1992, 89:7457-7461.