Periplasmic phosphorylation of lipid A is linked to the synthesis of undecaprenyl phosphate

Molecular Microbiology

Volumn 67, Issue 2, 2008, Pages 264-277

  Touzé, Thierry ^a   Tran, An X ^b   Hankins, Jessica V ^c   Mengin Lecreulx, Dominique ^a   Trent, M Stephen ^c  

^a INSTITUT D'OPTIQUE GRADUATE SCHOOL   (France)

^b East Tennessee State University   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; BACITRACIN; LIPID A; MEMBRANE ENZYME; MSBA PROTEIN; PEPTIDOGLYCAN; PHOSPHATE; PHOSPHORUS 32; PHOSPHORUS DERIVATIVE; POLYMER; PYROPHOSPHATE;

ARTICLE; BACTERIAL MEMBRANE; CATALYSIS; CYTOPLASM; ENZYME ACTIVE SITE; ESCHERICHIA COLI; LIPID MEMBRANE; LIPID TRANSPORT; LIPOGENESIS; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS;

ANTI-BACTERIAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; BACITRACIN; BACTERIAL PROTEINS; ESCHERICHIA COLI K12; LIPID A; MEMBRANE LIPIDS; MUTATION; PEPTIDYL TRANSFERASES; PERIPLASM; PHOSPHATES; PHOSPHORYLATION; POLYISOPRENYL PHOSPHATES; PYROPHOSPHATASES;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 37349106728     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2007.06044.x     Document Type: Article

References (53)

1. Apfel, C.M., Takacs, B., Fountoulakis, M., Stieger, M. Keck, W. (1999) Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: cloning, expression, and characterization of the essential uppS gene. J Bacteriol 181 : 483 492.
2. Bernard, R., El Ghachi, M., Mengin-Lecreulx, D., Chippaux, M. Denizot, F. (2005) BcrC from Bacillus subtilis acts as an undecaprenyl pyrophosphate phosphatase in bacitracin resistance. J Biol Chem 280 : 28852 28857.
3. Bishop, R.E., Gibbons, H.S., Guina, T., Trent, M.S., Miller, S.I. Raetz, C.R. (2000) Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J 19 : 5071 5080.
4. Boon Hinckley, M., Reynolds, C.M., Ribeiro, A.A., McGrath, S.C., Cotter, R.J., Lauw, F.N., et al. (2005) A Leptospira interrogans enzyme with similarity to yeast Ste14p that methylates the 1-phosphate group of lipid A. J Biol Chem 280 : 30214 30224.
5. Clementz, T., Bednarski, J.J. Raetz, C.R. (1996) Function of the htrB high temperature requirement gene of Escherchia coli in the acylation of lipid A: HtrB catalyzed incorporation of laurate. J Biol Chem 271 : 12095 12102.
6. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
7. Dillon, D.A., Wu, W.I., Riedel, B., Wissing, J.B., Dowhan, W. Carman, G.M. (1996) The Escherichia coli pgpB gene encodes for a diacylglycerol pyrophosphate phosphatase activity. J Biol Chem 271 : 30548 30553.
8. Doerrler, W.T. Raetz, C.R. (2002) ATPase activity of the MsbA lipid flippase of Escherichia coli. J Biol Chem 277 : 36697 36705.
9. Doerrler, W.T., Reedy, M.C. Raetz, C.R. (2001) An Escherichia coli mutant defective in lipid export. J Biol Chem 276 : 11461 11464.
10. El Ghachi, M., Bouhss, A., Blanot, D. Mengin-Lecreulx, D. (2004) The bacA gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. J Biol Chem 279 : 30106 30113.
11. El Ghachi, M., Derbise, A., Bouhss, A. Mengin-Lecreulx, D. (2005) Identification of multiple genes encoding membrane proteins with undecaprenyl pyrophosphate phosphatase (UppP) activity in Escherichia coli. J Biol Chem 280 : 18689 18695.
12. 2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol Microbiol 55 : 425 440.
13. Gunn, J.S. (2001) Bacterial modification of LPS and resistance to antimicrobial peptides. J Endotoxin Res 7 : 57 62.
14. Gunn, J.S., Lim, K.B., Krueger, J., Kim, K., Guo, L., Hackett, M. Miller, S.I. (1998) PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol Microbiol 27 : 1171 1182.
15. Gunn, J.S., Ernst, R.K., McCoy, A.J. Miller, S.I. (2000) Constitutive mutations of the Salmonella enterica serovar Typhimurium transcriptional virulence regulator phoP. Infect Immun 68 : 3758 3762.
16. Guo, L., Lim, K.B., Gunn, J.S., Bainbridge, B., Darveau, R.P., Hackett, M. Miller, S.I. (1997) Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276 : 250 253.
17. van Heijenoort, J. (2001a) Formation of the glycan chains in the synthesis of bacterial peptidoglycan. Glycobiology 11 : 25R 36R.
18. van Heijenoort, J. (2001b) Recent advances in the formation of the bacterial peptidoglycan monomer unit. Nat Prod Rep 18 : 503 519.
19. Icho, T. Raetz, C.R. (1983) Multiple genes for membrane-bound phosphatases in Escherichia coli and their action on phospholipid precursors. J Bacteriol 153 : 722 730.
20. Johnson, J.G. Wilson, D.B. (1977) Role of a sugar-lipid intermediate in colanic acid synthesis by Escherichia coli. J Bacteriol 129 : 225 236.
21. Kanjilal-Kolar, S. Raetz, C.R. (2006) Dodecaprenyl phosphate-galacturonic acid as a donor substrate for lipopolysaccharide core glycosylation in Rhizobium leguminosarum. J Biol Chem 281 : 12879 12887.
22. Kato, J., Fujisaki, S., Nakajima, K., Nishimura, Y., Sato, M. Nakano, A. (1999) The Escherichia coli homologue of yeast RER2, a key enzyme of dolichol synthesis, is essential for carrier lipid formation in bacterial cell wall synthesis. J Bacteriol 181 : 2733 2738.
23. Kim, S.H., Jia, W., Parreira, V.R., Bishop, R.E. Gyles, C.L. (2006) Phosphoethanolamine substitution in the lipid A of Escherichia coli O157: H7 and its association with PmrC. Microbiology 152 : 657 666.
24. Meredith, T.C., Aggarwal, P., Mamat, U., Lindner, B. Woodard, R.W. (2006) Redefining the requisite lipopolysaccharide structure in Escherichia coli. ACS Chem Biol 1 : 33 42.
25. Miller, J.R. (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY : Cold Spring Harbor Laboratory.
26. Nanninga, N. (1998) Morphogenesis of Escherichia coli. Microbiol Mol Biol Rev 62 : 110 129.
27. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67 : 593 656.
28. Raetz, C.R. Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71 : 635 700.
29. Raetz, C.R., Reynolds, C.M., Trent, M.S. Bishop, R.E. (2007) Lipid a modification systems in gram-negative bacteria. Annu Rev Biochem 76 : 295 329.
30. Reynolds, C.M., Ribeiro, A.A., McGrath, S.C., Cotter, R.J., Raetz, C.R. Trent, M.S. (2006) An outer membrane enzyme encoded by Salmonella typhimurium lpxR that removes the 3′-acyloxyacyl moiety of lipid A. J Biol Chem 281 : 21974 21987.
31. Rick, P.D., Hubbard, G.L., Kitaoka, M., Nagaki, H., Kinoshita, T., Dowd, S., et al. (1998) Characterization of the lipid-carrier involved in the synthesis of enterobacterial common antigen (ECA) and identification of a novel phosphoglyceride in a mutant of Salmonella typhimurium defective in ECA synthesis. Glycobiology 8 : 557 567.
32. Scher, M., Lennarz, W.J. Sweeley, C.C. (1968) The biosynthesis of mannosyl-1-phosphoryl-polyisoprenol in Micrococcus lysodeikticus and its role in mannan synthesis. Proc Natl Acad Sci USA 59 : 1313 1320.
33. Schleifer, K.H. Kandler, O. (1972) Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36 : 407 477.
34. Smith, P.K., Krohn, R.I., Hermanson, G.T., Mallia, A.K., Gartner, F.H., Provenzano, M.D., et al. (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150 : 76 85.
35. Sonnhammer, E.L., von Heijne, G. Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6 : 175 182.
36. Storm, D.R. Strominger, J.L. (1973) Complex formation between bacitracin peptides and isoprenyl pyrophosphates. The specificity of lipid-peptide interactions. J Biol Chem 248 : 3940 3945.
37. Stukey, J. Carman, G.M. (1997) Identification of a novel phosphatase sequence motif. Protein Sci 6 : 469 472.
38. Tatar, L.D., Marolda, C.L., Polischuk, A.N., van Leeuwen, D. Valvano, M.A. (2007) An Escherichia coli undecaprenyl-pyrophosphate phosphatase implicated in undecaprenyl phosphate recycling. Microbiology 153 : 2518 2529.
39. Tran, A.X., Karbarz, M.J., Wang, X., Raetz, C.R., McGrath, S.C., Cotter, R.J. Trent, M.S. (2004) Periplasmic cleavage and modification of the 1-phosphate group of Helicobacter pylori lipid A. J Biol Chem 279 : 55780 55791.
40. Trent, M.S., Ribeiro, A.A., Lin, S., Cotter, R.J. Raetz, C.R. (2001a) An inner membrane enzyme in Salmonella and Escherichia coli that transfers 4-amino-4-deoxy-L-arabinose to lipid A: induction on polymyxin-resistant mutants and role of a novel lipid-linked donor. J Biol Chem 276 : 43122 43131.
41. Trent, M.S., Ribeiro, A.A., Doerrler, W.T., Lin, S., Cotter, R.J. Raetz, C.R. (2001b) Accumulation of a polyisoprene-linked amino sugar in polymyxin-resistant Salmonella typhimurium and Escherichia coli: structural characterization and transfer to lipid A in the periplasm. J Biol Chem 276 : 43132 43144.
42. Trent, M.S., Pabich, W., Raetz, C.R. Miller, S.I. (2001c) A PhoP/PhoQ-induced Lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J Biol Chem 276 : 9083 9092.
43. Trent, M.S., Stead, C.M., Tran, A.X. Hankins, J.V. (2006) Diversity of endotoxin and its impact on pathogenesis. J Endotoxin Res 12 : 205 223.
44. van Velkinburgh, J.C. Gunn, J.S. (1999) PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect Immun 67 : 1614 1622.
45. Wang, X., McGrath, S.C., Cotter, R.J. Raetz, C.R. (2006a) Expression cloning and periplasmic orientation of the Francisella novicida lipid A 4′-phosphatase LpxF. J Biol Chem 281 : 9321 9330.
46. Wang, X., Ribeiro, A.A., Guan, Z., McGrath, S.C., Cotter, R.J. Raetz, C.R. (2006b) Structure and biosynthesis of free lipid A molecules that replace lipopolysaccharide in Francisella tularensis subsp. novicida. Biochemistry 45 : 14427 14440.
47. Watkinson, R.J., Hussey, H. Baddiley, J. (1971) Shared lipid phosphate carrier in the biosynthesis of teichoic acid and peptidoglycan. Nat New Biol 229 : 57 59.
48. Wheeler, D.L., Church, D.M., Federhen, S., Lash, A.E., Madden, T.L., Pontius, J.U., et al. (2003) Database resources of the National Center for Biotechnology. Nucleic Acids Res 31 : 28 33.
49. Whitfield, C. (1995) Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol 3 : 178 185.
50. Wright, A., Dankert, M., Fennessey, P. Robbins, P.W. (1967) Characterization of a polyisoprenoid compound functional in O-antigen biosynthesis. Proc Natl Acad Sci USA 57 : 1798 1803.
51. Wu, W.I., Liu, Y., Riedel, B., Wissing, J.B., Fischl, A.S. Carman, G.M. (1996) Purification and characterization of diacylglycerol pyrophosphate phosphatase from Saccharomyces cerevisiae. J Biol Chem 271 : 1868 1876.
52. Zhou, Z., Lin, S., Cotter, R.J. Raetz, C.R. (1999) 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 274 : 18503 18514.
53. Zhou, Z., Ribeiro, A.A., Lin, S., Cotter, R.J., Miller, S.I. Raetz, C.R. (2001) Lipid A modifications in polymyxin-resistant Salmonella typhimurium: PMRA-dependent 4-amino-4-deoxy-L-arabinose, and phosphoethanolamine incorporation. J Biol Chem 276 : 43111 43121.