Crystal structure of LptH, the periplasmic component of the lipopolysaccharide transport machinery from Pseudomonas aeruginosa

FEBS Journal

Volumn 282, Issue 10, 2015, Pages 1980-1997

  Bollati, Michela ^a   Villa, Riccardo ^a   Gourlay, Louise J ^a   Benedet, Mattia ^a   Dehò, Gianni ^a   Polissi, Alessandra ^b   Barbiroli, Alberto ^a   Martorana, Alessandra M ^b   Sperandeo, Paola ^b   Bolognesi, Martino ^a   Nardini, Marco ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF MILANO BICOCCA   (Italy)

Author keywords

crystal structure; lipopolysaccharide; LptA; LptH; Pseudomonas aeruginosa

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; GLYCINE; PSEUDOMONAS AERUGINOSA LIPOPOLYSACCHARIDE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; LIPOPOLYSACCHARIDE;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL OUTER MEMBRANE; CARBOHYDRATE ANALYSIS; CARBOHYDRATE TRANSPORT; CONTROLLED STUDY; CRYSTAL STRUCTURE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SHIGELLA FLEXNERI; CYTOPLASM; METABOLISM;

ESCHERICHIA COLI; NEGIBACTERIA; PSEUDOMONAS AERUGINOSA; SHIGELLA FLEXNERI;

BACTERIAL PROTEINS; LIPOPOLYSACCHARIDES; PERIPLASM; PSEUDOMONAS AERUGINOSA;

EID: 84929573471     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13254     Document Type: Article

References (52)

1. Pier GB, (2007) Pseudomonas aeruginosa lipopolysaccharide: a major virulence factor, initiator of inflammation and target for effective immunity. Int J Med Microbiol 297, 277-295.
2. Schroeder TH, Reiniger N, Meluleni G, Grout M, Coleman FT, &, Pier GB, (2001) Transgenic cystic fibrosis mice exhibit reduced early clearance of Pseudomonas aeruginosa from the respiratory tract. J Immunol 166, 7410-7418.
3. Augustin DK, Song Y, Baek MS, Sawa Y, Singh G, Taylor B, Rubio-Mills A, Flanagan JL, Wiener-Kronish JP, &, Lynch V, (2007) Presence or absence of lipopolysaccharide O antigens affects type III secretion by Pseudomonas aeruginosa. J Bacteriol 189, 2203-2209.
4. Lau PCY, Lindhout T, Beveridge TJ, Dutcher JR, &, Lam JS, (2009) Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms. J Bacteriol 191, 6618-6631.
5. Raetz CR, Guan Z, Ingram BO, Six DA, Song F, Wang X, &, Zhao J, (2009) Discovery of new biosynthetic pathways: the lipid A story. J Lipid Res 50 (Suppl), S103-S108.
6. Silhavy TJ, Kahne D, &, Walker S, (2010) The bacterial cell envelope. Cold Spring Harb Perspect Biol 2, a000414.
7. Polissi A, &, Sperandeo P, (2014) The lipopolysaccharide export pathway in Escherichia coli: structure, organization and regulated assembly of the Lpt machinery. Mar Drugs 12, 1023-1042.
8. Chng SS, Gronemberg LS, &, Kahne D, (2010) Proteins required for lipopolysaccharide assembly in Escherichia coli form a transenvelope complex. Biochemistry 49, 4565-4567.
9. Chng SS, Ruiz N, Chimalakonda G, Silhavy TJ, &, Kahne D, (2010) Characterization of the two-protein complex in Escherichia coli responsible for lipopolysaccharide assembly at the outer membrane. Proc Natl Acad Sci USA 107, 5363-5368.
10. Sperandeo P, Lau FK, Carpentieri A, De Castro C, Molinaro A, Dehò G, Silhavy TJ, &, Polissi A, (2008) Functional analysis of the protein machinery required for transport of lipopolysaccharide to the outer membrane of Escherichia coli. J Bacteriol 190, 4460-4469.
11. Villa R, Martorana AM, Okuda S, Gourlay LJ, Nardini M, Sperandeo P, Dehò G, Bolognesi M, Kahne D, &, Polissi A, (2013) The Escherichia coli Lpt transenvelope protein complex for lipopolysaccharide export is assembled via conserved structurally homologous domains. J Bacteriol 195, 1100-1108.
12. Freinkman E, Chng SS, &, Kahne D, (2011) The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc Natl Acad Sci USA 108, 2486-2491.
13. Serina S, Nozza F, Nicastro G, Faggioni F, Mottl H, Dehò G, &, Polissi A, (2004) Scanning the Escherichia coli chromosome by random transposon mutagenesis and multiple phenotypic screening. Res Microbiol 155, 692-701.
14. Sperandeo P, Pozzi C, Dehò G, &, Polissi A, (2006) Non-essential KDO biosynthesis and new essential cell envelope biogenesis genes in the Escherichia coli yrbG-yhbG locus. Res Microbiol 157, 547-558.
15. Sperandeo P, Cescutti R, Villa R, Di Benedetto C, Candia D, Dehò G, &, Polissi A, (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.
16. Okuda S, Freinkman E, &, Kahne D, (2012) Cytoplasmic ATP hydrolysis powers transport of lipopolysaccharide across the periplasm in E. coli. Science 338, 1214-1217.
17. Freinkman E, Okuda S, Ruiz N, &, Kahne D, (2012) Regulated assembly of the transenvelope protein complex required for lipopolysaccharide export. Biochemistry 51, 4800-4806.
18. Suits MD, Sperandeo P, Dehò G, Polissi A, &, Jia Z, (2008) Novel structure of the conserved gram-negative lipopolysaccharide transport protein A and mutagenesis analysis. J Mol Biol 380, 476-488.
19. Tran AX, Dong C, &, Whitfield C, (2010) Structure and functional analysis of LptC, a conserved membrane protein involved in the lipopolysaccharide export pathway in Escherichia coli. J Biol Chem 285, 33529-33539.
20. Merten JA, Schultz KM, &, Klug CS, (2012) Concentration-dependent oligomerization and oligomeric arrangement of LptA. Protein Sci 21, 211-218.
21. Santambrogio C, Sperandeo P, Villa R, Sobott F, Polissi A, &, Grandori R, (2013) LptA assembles into rod-like oligomers involving disorder-to-order transitions. J Am Soc Mass Spectrom 24, 1593-1602.
22. Schultz KM, Feix JB, &, Klug CS, (2013) Disruption of LptA oligomerization and affinity of the LptA-LptC interaction. Protein Sci 22, 1639-1645.
23. Sperandeo P, Villa R, Martorana AM, Samalikova M, Grandori R, Dehò G, &, Polissi A, (2011) New insights into the Lpt machinery for lipopolysaccharide transport to the cell surface: LptA-LptC interaction and LptA stability as sensors of a properly assembled transenvelope complex. J Bacteriol 193, 1042-1053.
24. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al,. (2014) The Pfam protein families database. Nucleic Acids Res (Database Issue) 42, D222-D230.
25. Qiao S, Luo Q, Zhao Y, Zhang X-C, &, Huang Y, (2014) Structural basis for lipopolysaccharide insertion in the bacterial outer membrane. Nature 511, 108-111.
26. Dong H, Xiang Q, Gu Y, Wang Z, Paterson NG, Stansfeld PJ, He C, Zhang Y, Wang W, &, Dong C, (2014) Structural basis for outer membrane lipopolysaccharide insertion. Nature 511, 52-56.
27. Winsor GL, Lam DK, Fleming L, Lo R, Whiteside MD, Yu NY, Hancock RE, &, Brinkman FS, (2011) Pseudomonas Genome Database: improved comparative analysis and population genomics capability for Pseudomonas genomes. Nucleic Acids Res (Database issue) 39, D596-D600.
28. Chimalakonda G, Ruiz N, Chng SS, Garner RA, Kahne D, &, Silhavy TJ, (2011) 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, 2492-2497.
29. 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.
30. Srinivas N, Jetter P, Ueberbacher BJ, Werneburg M, Zerbe K, Steinmann J, Van der Meijden B, Bernardini F, Lederer A, Dias RL, et al,. (2010) Peptidomimetic antibiotics target outer-membrane biogenesis in Pseudomonas aeruginosa. Science 327, 1010-1013.
31. Schmidt J, Patora-Komisarska K, Moehle K, Obrecht D, &, Robinson JA, (2013) Structural studies of β-hairpin peptidomimetic antibiotics that target LptD in Pseudomonas sp. Bioorg Med Chem 21, 5806-5810.
32. Wu T, McCandlish AC, Gronenberg LS, Chng SS, Silhavy TJ, &, Kahne D, (2006) Identification of a protein complex that assembles lipopolysaccharide in the outer membrane of Escherichia coli. Proc Natl Acad Sci USA 103, 11754-11759.
33. Grant SGN, Jessee J, Bloom FR, &, Hanahan D, (1990) Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc Natl Acad Sci USA 87, 4645-4649.
34. Hanahan J, (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557-580.
35. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FSL, Hufnagle WO, Kowalik DJ, Lagrou M, et al,. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959-964.
36. Datsenko KA, &, Wanner BL, (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97, 6640-6645.
37. Martorana AM, Sperandeo P, Polissi A, &, Dehò G, (2011) Complex transcriptional organization regulates an Escherichia coli locus implicated in lipopolysaccharide biogenesis. Res Microbiol 162, 470-482.
38. Bertani G, (1951) Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 62, 293-300.
39. Ghisotti D, Chiaramonte R, Forti F, Zangrossi S, Sironi G, &, Dehò G, (1992) Genetic analysis of the immunity region of phage-plasmid P4. Mol Microbiol 6, 3405-3413.
40. Sambrook J, Fritsch EF, &, Maniatis T, (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
41. Kabsch W, (2010) XDS. Acta Crystallogr D Biol Crystallogr 66, 125-132.
42. Evans P, (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62, 72-82.
43. Storoni LC, McCoy AJ, &, Read RJ, (2004) Likelihood-enhanced fast rotation functions. Acta Crystallogr D Biol Crystallogr 60, 432-438.
44. Adams PD, Afonine PV, Bunkõczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung L-W, Kapral GJ, Grosse-Kunstleve RW, et al,. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66, 213-221.
45. Emsley P, &, Cowtan K, (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
46. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, Paciorek W, Roversi P, Sharff A, Smart OS, Vonrhein C, et al,. (2010) BUSTER Version 2.9. Global Phasing Ltd, Cambridge, UK.
47. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, &, Richardson DC, (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66, 12-21.
48. Laskowski RA, Watson JD, &, Thornton JM, (2005) ProFunc: a server for predicting protein function from 3D structure. Nucleic Acids Res 33, W89-W93.
49. Thompson JD, Higgins DG, &, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673-4680.
50. Sali A, &, Blundell TL, (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234, 779-815.
51. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, &, Ferrin TE, (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25, 1605-1612.
52. Shen MY, &, Sali A, (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15, 2507-2524.