Lipopolysaccharide is inserted into the outer membrane through an intramembrane hole, a lumen gate, and the lateral opening of lptd

Structure

Volumn 23, Issue 3, 2015, Pages 496-504

  Gu, Yinghong ^a   Stansfeld, Phillip J ^b   Zeng, Yi ^a   Dong, Haohao ^c   Wang, Wenjian ^d   Dong, Changjiang ^a  

^a UNIVERSITY OF EAST ANGLIA   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d SUN YAT SEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN D; LIPOPOLYSACCHARIDE TRANSPORT PROTEIN E; O ANTIGEN; OLIGOSACCHARIDE; UNCLASSIFIED DRUG; OUTER MEMBRANE PROTEIN; PROTEIN BINDING;

ARTICLE; ASSAY; ESCHERICHIA COLI; HYDROPHOBICITY; MOLECULAR DYNAMICS; MUTAGENESIS; MUTATION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; BINDING SITE; CHEMICAL PHENOMENA; CHEMICAL STRUCTURE; CHEMISTRY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; TRANSPORT AT THE CELLULAR LEVEL;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

BACTERIAL OUTER MEMBRANE PROTEINS; BINDING SITES; BIOLOGICAL TRANSPORT; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPOPOLYSACCHARIDES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SALMONELLA TYPHIMURIUM;

EID: 84923880501     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.01.001     Document Type: Article

References (42)

1. R.E. Bishop Structural biology: lipopolysaccharide rolls out the barrel Nature 511 2014 37 38
2. R.E. Bishop Emerging roles for anionic non-bilayer phospholipids in fortifying the outer membrane permeability barrier J. Bacteriol. 196 2014 3209 3213
3. M.P. Bos, and J. Tommassen The LptD chaperone LptE is not directly involved in lipopolysaccharide transport in Neisseria meningitidis J. Biol. Chem. 286 2011 28688 28696
4. G. Chimalakonda, N. Ruiz, S.S. Chng, R.A. Garner, D. Kahne, and T.J. Silhavy Lipoprotein LptE is required for the assembly of LptD by the beta-barrel assembly machine in the outer membrane of Escherichia coli Proc. Natl. Acad. Sci. USA 108 2011 2492 2497
5. S.S. Chng, N. Ruiz, G. Chimalakonda, T.J. Silhavy, and D. Kahne Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane Proc. Natl. Acad. Sci. USA 107 2010 5363 5368
6. S.S. Chng, M. Xue, R.A. Garner, H. Kadokura, D. Boyd, J. Beckwith, and D. Kahne Disulfide rearrangement triggered by translocon assembly controls lipopolysaccharide export Science 337 2012 1665 1668
7. D.H. de Jong, G. Singh, W.F.D. Bennett, C. Arnarez, T.A. Wassenaar, L.V. Schafer, X. Periole, D.P. Tieleman, and S.J. Marrink Improved parameters for the martini coarse-grained protein force field J. Chem. Theory Comput. 9 2013 687 697
8. C. Dong, K. Beis, J. Nesper, A.L. Brunkan-Lamontagne, B.R. Clarke, C. Whitfield, and J.H. Naismith Wza the translocon for E. coli capsular polysaccharides defines a new class of membrane protein Nature 444 2006 226 229
9. H. Dong, Q. Xiang, Y. Gu, Z. Wang, N.G. Paterson, P.J. Stansfeld, C. He, Y. Zhang, W. Wang, and C. Dong Structural basis for outer membrane lipopolysaccharide insertion Nature 511 2014 52 56
10. E. Freinkman, S.S. Chng, and D. Kahne The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel Proc. Natl. Acad. Sci. USA 108 2011 2486 2491
11. E. Freinkman, S. Okuda, N. Ruiz, and D. Kahne Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export Biochemistry 51 2012 4800 4806
12. M. Grabowicz, J. Yeh, and T.J. Silhavy Dominant negative lptE mutation that supports a role for LptE as a plug in the LptD barrel J. Bacteriol. 195 2013 1327 1334
13. E.M. Hearn, D.R. Patel, B.W. Lepore, M. Indic, and B. van den Berg Transmembrane passage of hydrophobic compounds through a protein channel wall Nature 458 2009 367 370
14. H. Hong, D.R. Patel, L.K. Tamm, and B. van den Berg The outer membrane protein OmpW forms an eight-stranded beta-barrel with a hydrophobic channel J. Biol. Chem. 281 2006 7568 7577
15. M.A. Khan, and R.E. Bishop Molecular mechanism for lateral lipid diffusion between the outer membrane external leaflet and a beta-barrel hydrocarbon ruler Biochemistry 48 2009 9745 9756
16. H. Liu, and J.H. Naismith An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol BMC Biotechnol. 8 2008 91
17. G. Malojcic, D. Andres, M. Grabowicz, A.H. George, N. Ruiz, T.J. Silhavy, and D. Kahne LptE binds to and alters the physical state of LPS to catalyze its assembly at the cell surface Proc. Natl. Acad. Sci. USA 111 2014 9467 9472
18. V.R. Matias, A. Al-Amoudi, J. Dubochet, and T.J. Beveridge Cryo-transmission electron microscopy of frozen-hydrated sections of Escherichia coli and Pseudomonas aeruginosa J. Bacteriol. 185 2003 6112 6118
19. S. Okuda, E. Freinkman, and D. Kahne Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli Science 338 2012 1214 1217
20. C. Oostenbrink, A. Villa, A.E. Mark, and W.F. van Gunsteren A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6 J. Comput. Chem. 25 2004 1656 1676
21. S. Pronk, S. Pall, R. Schulz, P. Larsson, P. Bjelkmar, R. Apostolov, M.R. Shirts, J.C. Smith, P.M. Kasson, and D. van der Spoel GROMACS 4.5: a high-throughput and highly parallel open source molecular simulation toolkit Bioinformatics 29 2013 845 854
22. S. Qiao, Q. Luo, Y. Zhao, X.C. Zhang, and Y. Huang Structural basis for lipopolysaccharide insertion in the bacterial outer membrane Nature 511 2014 108 111
23. N. Ruiz, D. Kahne, and T.J. Silhavy Transport of lipopolysaccharide across the cell envelope: the long road of discovery Nat. Rev. Microbiol. 7 2009 677 683
24. N. Ruiz, S.S. Chng, A. Hiniker, D. Kahne, and T.J. Silhavy Nonconsecutive disulfide bond formation in an essential integral outer membrane protein Proc. Natl. Acad. Sci. USA 107 2010 12245 12250
25. A. Sali, and T.L. Blundell Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
26. D.J. Sherman, S. Okuda, W.A. Denny, and D. Kahne Validation of inhibitors of an ABC transporter required to transport lipopolysaccharide to the cell surface in Escherichia coli Bioorg. Med. Chem. 21 2013 4846 4851
27. D.J. Sherman, M.B. Lazarus, L. Murphy, C. Liu, S. Walker, N. Ruiz, and D. Kahne Decoupling catalytic activity from biological function of the ATPase that powers lipopolysaccharide transport Proc. Natl. Acad. Sci. USA 111 2014 4982 4987
28. P. Sperandeo, F.K. Lau, A. Carpentieri, C. De Castro, A. Molinaro, G. Dehò, T.J. Silhavy, and A. Polissi Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli J. Bacteriol. 190 2008 4460 4469
29. N. Srinivas, P. Jetter, B.J. Ueberbacher, M. Werneburg, K. Zerbe, J. Steinmann, B. Van der Meijden, F. Bernardini, A. Lederer, and R.L. Dias Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa Science 327 2010 1010 1013
30. P.J. Stansfeld, and M.S.P. Sansom From coarse grained to atomistic: a serial multiscale approach to membrane protein simulations J. Chem. Theory Comput. 7 2011 1157 1166
31. P.J. Stansfeld, E.E. Jefferys, and M.S. Sansom Multiscale simulations reveal conserved patterns of lipid interactions with aquaporins Structure 21 2013 810 819
32. M.D. Suits, P. Sperandeo, G. Deho, A. Polissi, and Z. Jia Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis J. Mol. Biol. 380 2008 476 488
33. D.S. Touw, D.R. Patel, and B. van den Berg The crystal structure of OprG from Pseudomonas aeruginosa, a potential channel for transport of hydrophobic molecules across the outer membrane PLoS One 5 2010 e15016
34. A.X. Tran, M.S. Trent, and C. Whitfield The LptA protein of Escherichia coli is a periplasmic lipid A-binding protein involved in the lipopolysaccharide export pathway J. Biol. Chem. 283 2008 20342 20349
35. A.X. Tran, C. Dong, and C. Whitfield Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli J. Biol. Chem. 285 2010 33529 33539
36. B. van den Berg, P.N. Black, W.M. Clemons Jr., and T.A. Rapoport Crystal structure of the long-chain fatty acid transporter FadL Science 304 2004 1506 1509
37. R. Villa, A.M. Martorana, S. Okuda, L.J. Gourlay, M. Nardini, P. Sperandeo, G. Deho, M. Bolognesi, D. Kahne, and A. Polissi The Escherichia coli Lpt transenvelope protein complex for lipopolysaccharide export is assembled via conserved structurally homologous domains J. Bacteriol. 195 2013 1100 1108
38. Z. Wang, Q. Xiang, X. Zhu, H. Dong, C. He, H. Wang, Y. Zhang, W. Wang, and C. Dong Structural and functional studies of conserved nucleotide-binding protein LptB in lipopolysaccharide transport Biochem. Biophys. Res. Commun. 452 2014 443 449
39. C. Whitfield, and M.S. Trent Biosynthesis and export of bacterial lipopolysaccharides Annu. Rev. Biochem. 83 2014 99 128
40. J.C. Whitney, I.D. Hay, C. Li, P.D. Eckford, H. Robinson, M.F. Amaya, L.F. Wood, D.E. Ohman, C.E. Bear, B.H. Rehm, and P.L. Howell Structural basis for alginate secretion across the bacterial outer membrane Proc. Natl. Acad. Sci. USA 108 2011 13083 13088
41. Q.J. Xiang, H.Y. Wang, Z.S. Wang, Y.Z. Zhang, and C.J. Dong Characterization of lipopolysaccharide transport protein complex Cent. Eur. J. Biol. 9 2014 131 138
42. G. Zhang, T.C. Meredith, and D. Kahne On the essentiality of lipopolysaccharide to Gram-negative bacteria Curr. Opin. Microbiol. 16 2013 779 785