Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane

Proceedings of the National Academy of Sciences of the United States of America

Volumn 107, Issue 12, 2010, Pages 5363-5368

  Chng, Shu Sin ^a   Ruiz, Natividad ^b   Chimalakonda, Gitanjali ^b   Silhavy, Thomas J ^b   Kahne, Daniel ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

Gram negative bacteria; Lipopolysaccharide binding; Outer membrane protein complex

Indexed keywords

BACTERIAL PROTEIN; CARBON; LIPOPOLYSACCHARIDE; NITROGEN;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; CELL SURFACE; CHEMICAL ANALYSIS; ENZYME SUBSTRATE; ESCHERICHIA COLI; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PURIFICATION; STOICHIOMETRY;

CELL MEMBRANE; ESCHERICHIA COLI K12; ESCHERICHIA COLI PROTEINS; LIPOPOLYSACCHARIDES; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TRYPSIN;

ESCHERICHIA COLI; NEGIBACTERIA;

EID: 77950438894     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0912872107     Document Type: Article

References (48)

1. Mühlradt PF, Golecki JR (1975) Asymmetrical distribution and artifactual reorientation of lipopolysaccharide in the outer membrane bilayer of Salmonella typhimurium. Eur J Biochem 51:343-352.
2. Kamio Y, Nikaido H (1976) Outer membrane of Salmonella typhimurium: Accessibility of phospholipid head groups to phospholipase C and cyanogen bromide activated dextran in the external medium. Biochemistry 15:2561-2570.
3. Bos MP, Robert V, Tommassen J (2007) Biogenesis of the Gram-negative bacterial outer membrane. Annu Rev Microbiol 61:191-214. (Pubitemid 350058206)
4. Tokuda H (2009) Biogenesis of outer membranes in Gram-negative bacteria. Biosci Biotechnol Biochem 73:80778 1-9.
5. Ruiz N, Kahne D, Silhavy TJ (2009) Transport of lipopolysaccharide across the cell envelope: The long road of discovery. Nat Rev Microbiol 7:677-683
6. Sperandeo P, Dehò G, Polissi A (2009) The lipopolysaccharide transport system of Gram-negative bacteria. Biochim Biophys Acta 1791:594-602.
7. Nikaido H (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol R 67:593-656.
8. Raetz CRH, Whitfield C (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71:635-700.
9. Sperandeo P, et al. (2007) Characterization of lptA and lptB, two essential genes implicated in lipopolysaccharide transport to the outer membrane of Escherichia coli. J Bacteriol 189:244-253. (Pubitemid 46036240)
10. Sperandeo P, et al. (2008) Functional analysis of protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190:4460-4469.
11. Ruiz N, Gronenberg L, Kahne D, Silhavy TJ (2008) Identification of two inner-membrane proteins required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 105:5537-5542.
12. Narita S, Tokuda H (2009) Biochemical characterization of an ABC transporter LptBFGC complex required for the outer membrane sorting of lipopolysaccharides. FEBS Lett 583:2160-2164.
13. Ma B, Reynolds CM, Raetz CR (2008) Periplasmic orientation of nascent lipid A in the inner membrane of an Escherichia coli LptA mutant. Proc Natl Acad Sci USA 105:13823-13828.
14. Suits MD, Sperandeo P, Dehò G, Polissi A, Jia Z (2008) Novel structure of conversed Gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J Mol Biol 380:476-488.
15. Tran AX, Trent MS, Whitfield C (2008) The LptA protein of Escherichia coli is a periplasmic lipid A-binding protein involved in the lipopolysaccharide export pathway. J Biol Chem 283:20342-20349.
16. Wu T, et al. (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103:11754-11759. (Pubitemid 44182523)
17. Sampson BA, Misra R, Benson SA (1989) Identification and characterization of a new gene of Escherichia coli K-12 involved in outer membrane permeability. Genetics 122:491-501.
18. Braun M, Silhavy TJ (2002) Imp/OstA is required for cell envelope biogenesis in Escherichia coli. Mol Microbiol 45:1289-1302.
19. Ruiz N, Falcone B, Kahne D, Silhavy TJ (2005) Chemical conditionality: a genetic strategy to probe organelle assesmbly. Cell 121:307-317. (Pubitemid 40546397)
20. Wu T, et al. (2005) Identification of a multi-component complex required for outer membrane biogenesis in Escherichia coli. Cell 121:235-245. (Pubitemid 40546391)
21. Ruiz N, Wu T, Kahne D, Silhavy TJ (2006) Probing the barrier function of the outer membrane with chemical conditionality. ACS Chem Biol 1:385-395.
22. Sklar JG, et al. (2007) Lipoprotein SmpA is a component of the YaeT complex that assembles outer membrane proteins in Escherichia coli. Proc Natl Acad Sci USA 104:6400-6405.
23. Vertommen D, Ruiz N, Leverrier P, Silhavy TJ, Collet JF (2009) Characterization of the role of the Escherchia coliperiplasmic chaperone SurA using differential proteomics. Proteomics 9:2432-2443
24. Bos MP, Tefsen B, Geurtsen J, Tommassen J (2004) Identification of an outer membrane protein required for the transport of lipopolysaccharide to the bacterial cell surface. Proc Natl Acad Sci USA 101:9417-9422. (Pubitemid 38812889)
25. Steeghs L, et al. (1998) Meningitis bacterium is viable without endotoxin. Nature 392:449-450. (Pubitemid 28168969)
26. Link AJ, Robison K, Church GM (1997) Comparing the predicted and observed properties of proteins encoded in the genome of Escherichia coli K-12. Electrophoresis 18:1259-1313. (Pubitemid 27371433)
27. Takase I, et al. (1987) Genes encoding two lipoproteins in the leuS-dacA region of the Escherichia colichromosome. J Bacteriol 169:5692-5699.
28. Inouye M, Yee ML (1973) Homogeneity of envelope proteins of Escherichia coli separated by gel electrophoresis in sodium dodecyl sulfate. J Bacteriol 113:304-312.
29. Nakamura K, Mizushima S (1976) 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.
30. Marlovits TC, et al. (2004) Structural insights into the assembly of the Type III secretion needle complex. Science 306:1040-1042. (Pubitemid 39482908)
31. Finn RD, et al. (2008) The Pfam protein families database. Nucleic Acids Res 36:D281-288.
32. Hu KY, Saier MH Jr (2006) Bioinformatics analyses of Gram-negative bacterial OstA outer membrane assembly homologues. Curr Genomics 7:447-461.
33. Vorobiev SM, et al. (2007) Crystal structure of the A1KSW9-NEIMF protein from Neisseria meningitidis. PDB ID: 3BF2 (DOI: 10.2210/pdb3bf2/pdb).
34. Forouhar F, et al. (2007) Crystal structure of the rare lipoprotein B (SO-1173) from Shewanella oneidensis. PDB ID: 2R76 (DOI: 10.2210/pdb2r76/pdb).
35. Rossi P, Xiao R, Acton TB, Montelione GT (2007) Solution NMR structure of uncharacterized lipoprotein B from Nitrosomonas europaea. PDB ID: 2JXP (DOI: 10.2210/pdb2jxp/pdb).
36. Tsukahara J, Mukaiyama K, Okuda S, Narita S, Tokuda H (2009) Dissection of LolB function - lipoprotein binding, membrane targeting and incorporation of lipoproteins into lipid bilayers. FEBS J 276:4496-4504.
37. Matsuyama S, Yokota N, Tokuda H (1997) A novel outer membrane lipoprotein, LolB (HemM), involved in the LolA (p20)-dependent localization of lipoproteins to the outer membrane of Escherichia coli. EMBO J 16:6947-6955.
38. Ferguson AD, Hofmann E, Coulton JW, Diederichs K, Welte W (1998) Siderophore-mediated iron transport: Crystal structure of FhuA with bound lipopolysaccharide. Science 282:2215-2220. (Pubitemid 29004062)
39. Remaut H, et al. (2008) Fiber formation across the bacterial outer membrane by the chaperone/usher pathway. Cell 133:640-652.
40. Huang Y, Smith BS, Chen LX, Baxter RHG, Deisenhofer J (2009) Insights into pilus assembly and secretion from the structure and functional characterization of usher PapC. Proc Natl Acad Sci USA 106:7403-7407.
41. Braun M, Endriss F, Killmann H, Braun V (2003) In vivo reconstitution of the FhuA transport protein of Escherichia coli K-12. J Bacteriol 185:5508-5518.
42. Locher KP, et al. (1998) Transmembrane signaling across the ligand-gated FhuA receptor: crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell 95:771-778.
43. Buchanan SK, et al. (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nat Struct Biol 6:56-63. (Pubitemid 29232425)
44. Ferguson AD, et al. (2002) Structural basis of gating by the outer membrane transporter FecA. Science 295:1715-1719.
45. Yue WW, Grizot S, Buchanan SK (2003) Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA. J Mol Biol 332:353-368. (Pubitemid 37013505)
46. Usher KC, Ōzkan E, Gardner KH, Deisenhofer J (2001) The plug domain of FepA, a TonB-dependent transport protein from Escherichia coli, binds its siderophore in the absence of the transmembrane barrel domain. Proc Natl Acad Sci USA 98:10676-10681. (Pubitemid 32878680)
47. Tsai C-M, Frasch CE (1982) A sensitive silver stain for detecting lipopolysaccharide in polyacrylamide gels. Anal Biochem 119:115-119.
48. Pitre A, Pan Y, Pruett S, Skalli O (2007) On the use of ratio standard curves to accurately quantite relative changes in protein levels by western blot. Anal Biochem 361:305-307. (Pubitemid 46164761)