Lipid A 3'-O-deacylation by Salmonella outer membrane enzyme LpxR modulates the ability of lipid A to stimulate Toll-like receptor 4

Biochemical and Biophysical Research Communications

Volumn 428, Issue 3, 2012, Pages 343-347

  Kawasaki, Kiyoshi ^a   Teramoto, Mai ^a   Tatsui, Rie ^a   Amamoto, Shoko ^a  

^a DOSHISHA WOMEN'S COLLEGE OF LIBERAL ARTS   (Japan)

Author keywords

Bacterial pathogenesis; Innate immunity; Lipopolysaccharide; Modification; Molecular recognition

Indexed keywords

BACTERIAL ENZYME; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPID A; LPXR PROTEIN; MYRISTIC ACID; PROTEIN MD 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; DEACYLATION; DRUG ACTIVITY; ESCHERICHIA COLI; IMMUNOSURVEILLANCE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURIFICATION; SALMONELLA; SIGNAL TRANSDUCTION; THIN LAYER CHROMATOGRAPHY;

CARBOXYLIC ESTER HYDROLASES; CELL LINE; HUMANS; LIPID A; LYMPHOCYTE ANTIGEN 96; TOLL-LIKE RECEPTOR 4;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; SALMONELLA;

EID: 84869863296     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.10.054     Document Type: Article

References (28)

1. Raetz C.R., Reynolds C.M., Trent M.S., Bishop R.E. Lipid A modification systems in gram-negative bacteria. Annu. Rev. Biochem. 2007, 76:295-329.
2. Raetz C.R., Whitfield C. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 2002, 71:635-700.
3. Park B.S., Song D.H., Kim H.M., Choi B.S., Lee H., Lee J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 2009, 458:1191-1195.
4. Kobayashi M., Saitoh S., Tanimura N., Takahashi K., Kawasaki K., Nishijima M., Fujimoto Y., Fukase K., Akashi-Takamura S., Miyake K. Regulatory roles for MD-2 and TLR4 in ligand-induced receptor clustering. J. Immunol. 2006, 176:6211-6218.
5. Angus D.C., Linde-Zwirble W.T., Lidicker J., Clermont G., Carcillo J., Pinsky M.R. Epidemiology of severe sepsis in the United States: analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 2001, 29:1303-1310.
6. Matsuura M., Kawasaki K., Kawahara K., Mitsuyama M. Evasion of human innate immunity without antagonizing TLR4 by mutant Salmonella enterica serovar Typhimurium having penta-acylated lipid A. Innate Immun. 2012, 18:764-773.
7. Somerville J.E., Cassiano L., Bainbridge B., Cunningham M.D., Darveau R.P. A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J. Clin. Invest. 1996, 97:359-365.
8. Okemoto K., Kawasaki K., Hanada K., Miura M., Nishijima M. A potent adjuvant monophosphoryl lipid A triggers various immune responses, but not secretion of IL-1beta or activation of caspase-1. J. Immunol. 2006, 176:1203-1208.
9. Mata-Haro V., Cekic C., Martin M., Chilton P.M., Casella C.R., Mitchell T.C. The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007, 316:1628-1632.
10. Giannini S.L., Hanon E., Moris P., Van Mechelen M., Morel S., Dessy F., Fourneau M.A., Colau B., Suzich J., Losonksy G., Martin M.T., Dubin G., Wettendorff M.A. Enhanced humoral and memory B cellular immunity using HPV16/18 L1 VLP vaccine formulated with the MPL/aluminium salt combination (AS04) compared to aluminium salt only. Vaccine 2006, 24:5937-5949.
11. Miller S.I., Ernst R.K., Bader M.W. LPS, TLR4 and infectious disease diversity. Nat. Rev. Microbiol. 2005, 3:36-46.
12. Bishop R.E., Gibbons H.S., Guina T., Trent M.S., Miller S.I., Raetz C.R. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 2000, 19:5071-5080.
13. Trent M.S., Pabich W., Raetz C.R., Miller S.I. A PhoP/PhoQ-induced Lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J. Biol. Chem. 2001, 276:9083-9092.
14. Reynolds C.M., Ribeiro A.A., McGrath S.C., Cotter R.J., Raetz C.R., Trent M.S. An outer membrane enzyme encoded by Salmonella typhimurium lpxR that removes the 3'-acyloxyacyl moiety of lipid A. J. Biol. Chem. 2006, 281:21974-21987.
15. Rutten L., Mannie J.P., Stead C.M., Raetz C.R., Reynolds C.M., Bonvin A.M., Tommassen J.P., Egmond M.R., Trent M.S., Gros P. Active-site architecture and catalytic mechanism of the lipid A deacylase LpxR of Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 2009, 106:1960-1964.
16. Kawasaki K., Ernst R.K., Miller S.I. 3-O-deacylation of lipid A by PagL, a PhoP/PhoQ-regulated deacylase of Salmonella typhimurium, modulates signaling through Toll-like receptor 4. J. Biol. Chem. 2004, 279:20044-20048.
17. Kawano M., Manabe T., Kawasaki K. Salmonella enterica serovar Typhimurium lipopolysaccharide deacylation enhances its intracellular growth within macrophages. FEBS Lett. 2010, 584:207-212.
18. Jarvik T., Smillie C., Groisman E.A., Ochman H. Short-term signatures of evolutionary change in the Salmonella enterica serovar typhimurium 14028 genome. J. Bacteriol. 2010, 192:560-567.
19. Guzman L.M., Belin D., Carson M.J., Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 1995, 177:4121-4130.
20. Zhou Z., Lin S., Cotter R.J., Raetz C.R. Lipid A modifications characteristic of Salmonella typhimurium are induced by NH4VO3 in Escherichia coli K12. Detection of 4-amino-4-deoxy-l-arabinose, phosphoethanolamine and palmitate. J. Biol. Chem. 1999, 274:18503-18514.
21. Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., Datsenko K.A., Tomita M., Wanner B.L., Mori H. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol. Syst. Biol. 2006, 2:0008.
22. Kawasaki K., Akashi S., Shimazu R., Yoshida T., Miyake K., Nishijima M. Mouse toll-like receptor 4.MD-2 complex mediates lipopolysaccharide-mimetic signal transduction by Taxol. J. Biol. Chem. 2000, 275:2251-2254.
23. Jia W., El Zoeiby A., Petruzziello T.N., Jayabalasingham B., Seyedirashti S., Bishop R.E. Lipid trafficking controls endotoxin acylation in outer membranes of Escherichia coli. J. Biol. Chem. 2004, 279:44966-44975.
24. Shimazu R., Akashi S., Ogata H., Nagai Y., Fukudome K., Miyake K., Kimoto M. MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J. Exp. Med. 1999, 189:1777-1782.
25. Tanamoto K., Azumi S. Salmonella-type heptaacylated lipid A is inactive and acts as an antagonist of lipopolysaccharide action on human line cells. J. Immunol. 2000, 164:3149-3156.
26. Ohto U., Fukase K., Miyake K., Shimizu T. Structural basis of species-specific endotoxin sensing by innate immune receptor TLR4/MD-2. Proc. Natl. Acad. Sci. USA 2012, 109:7421-7426.
27. Kawasaki K. Alternative procedures for analysis of lipid A modification with phosphoethanolamine or aminoarabinose. J. Microbiol. Methods 2009, 76:313-315.
28. Yi E.C., Hackett M. Rapid isolation method for lipopolysaccharide and lipid A from gram-negative bacteria. Analyst 2000, 125:651-656.