Differential regulation by magnesium of the two MsbB paralogs of shigella flexneri

Journal of Bacteriology

Volumn 190, Issue 10, 2008, Pages 3526-3537

  Goldman, Seth R ^a,b   Tu, Yupeng ^a   Goldberg, Marcia B ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; LIPID A; LIPOPOLYSACCHARIDE; MAGNESIUM; MSBB PROTEIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; ESCHERICHIA COLI PROTEIN; MSBB PROTEIN, E COLI; PHOP PROTEIN, BACTERIA; PHOQ PROTEIN, BACTERIA;

ACYLATION; ARTICLE; BINDING SITE; CATALYSIS; ENZYME ACTIVITY; GENE DUPLICATION; LIPOGENESIS; MUTATION; NONHUMAN; PARALOGY; PRIORITY JOURNAL; PROTEIN MODIFICATION; SHIGELLA FLEXNERI; CHEMISTRY; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY;

ENTEROBACTERIACEAE; NEGIBACTERIA; SHIGELLA FLEXNERI;

ACYLTRANSFERASES; BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; LIPID A; MAGNESIUM; SHIGELLA FLEXNERI;

EID: 47049106441     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00151-08     Document Type: Article

References (67)

1. Alpuche Aranda, C. M., J. A. Swanson, W. P. Loomis, and S. I. Miller. 1992. Salmonella typhimurium activates virulence gene transcription within acidified macrophage phagosomes. Proc. Natl. Acad. Sci. USA 89:10079-10083.
2. Bader, M. W., S. Sanowar, M. E. Daley, A. R. Schneider, U. Cho, W. Xu, R. E. Klevit, H. Le Moual, and S. I. Miller, 2005. Recognition of antimicrobial peptides by a bacterial sensor kinase. Cell 122:461-472.
3. Bishop, R. E., H. S. Gibbons, T. Guina, M. S. Trent, S. I. Miller, and C. R. Raetz. 2000. Transfer of palmitate from phospholipids to lipid A in outer membranes of gram-negative bacteria. EMBO J. 19:5071-5080.
4. Bliska, J. B., K. L. Guan, J. E. Dixon, and S. Falkow. 1991. Tyrosine phosphate hydrolysis of host proteins by an essential Yersinia virulence determinant. Proc. Natl. Acad. Sci. USA 88:1187-1191.
5. Chang, A. C., and S. N. Cohen. 1978. Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J. Bacteriol. 134:1141-1156.
6. Clementz, T., Z. Zhou, and C. R. Raetz. 1997. Function of the Escherichia coli msbB gene, a multicopy suppressor of htrB knockouts, in the acylation of lipid A. Acylation by MsbB follows laurate incorporation by HtrB. J. Biol. Chem. 272:10353-10360.
7. Clerc, P., and P. J. Sansonetti. 1987. Entry of Shigella flexneri into HeLa cells: evidence for directed phagocytosis involving actin polymerization and myosin accumulation. Infect. Immun. 55:2681-2688.
8. Coats, S. R., C. T. Do, L. M. Karimi-Naser, P. H. Braham, and R. P. Darveau. 2007. Antagonistic lipopolysaccharides block E. coli lipopolysaccharide function at human TLR4 via interaction with the human MD-2 lipopolysaccharide binding site. Cell. Microbiol. 9:1191-1202.
9. 2+. Cell 125:71-84.
10. Dehio, C., and M. Meyer. 1997. Maintenance of broad-host-range incompatibility group P and group Q. plasmids and transposition of Tn5 in Bartonella henselae following conjugal plasmid transfer from Escherichia coli. J. Bacteriol. 179:538-540.
11. Deighan, P., A. Free, and C. J. Dorman. 2000. A role for the Escherichia coli H-NS-like protein StpA in OmpF porin expression through modulation of micF RNA stability. Mol. Microbiol. 38:126-139.
12. Derzelle, S., E. Turlin, E. Duchaud, S. Pages, F. Kunst, A. Givaudan, and A. Danchin. 2004. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J. Bacteriol. 186:1270-1279.
13. Detweiler, C. S., D. M. Monack, I. E. Brodsky, H. Mathew, and S. Falkow. 2003. virK, somA and rcsC are important for systemic Salmonella enterica serovar Typhimurium infection and cationic peptide resistance. Mol. Microbiol, 48:385-400.
14. D'Hauterille, H., S. Khan, D. J. Maskell, A. Kussak, A. Weintraub, J. Mathison, R. J. Ulevitch, N. Wuscher, C. Parsot, and P. J. Sansonetti. 2002. Two msbB genes encoding maximal acylation of lipid A are required for invasive Shigella flexneri to mediate inflammatory rupture and destruction of the intestinal epithelium. J. Immunol. 168:5240-5251.
15. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84:165-174.
16. 2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55:425-440.
17. Grabenstein, J. P., H. S. Fukuto, L. E. Palmer, and J. B. Bliska. 2006. Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect. Immun. 74:3727-3741.
18. 2+ environments. J. Bacteriol. 179:7040-7045.
19. Gunn, J. S., K. B. Lim, J. Krueger, K. Kim, L. Guo, M. Hackett, and S. I. Miller. 1998. PmrA-PmrB-regulated genes necessaiy for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
20. Gunn, J. S., and S. I. Miller. 1996. PhoP-PhoQ activates transcription of pmrAB, encoding a two-component regulatory system involved in Salmonella typhimurium antimicrobial peptide resistance. J. Bacteriol. 178:6857-6864.
21. Guo, L., K. B. Lim, J. S. Gunn, B. Bainbridge, R. P. Darveau, M. Hackett, and S. I. Miller. 1997. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276:250-253.
22. Guo, L., K. B. Lim, C. M. Poduje, M. Daniel, J. S. Gunn, M. Hackett, and S. I. Miller. 1998. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95:189-198.
23. Jayaraman, P. S., T. C. Peakman, S. J. Busby, R. V. Quincey, and J. A. Cole. 1987. Location and sequence of the promoter of the gene for the NADH-dependent nitrite reductase of Escherichia coli and its regulation by oxygen, the Fnr protein and nitrite. J. Mol. Biol. 196:781-788.
24. Johnson, C. R., J. Newcombe, S. Thorne, H. A. Borde, L. J. Eales-Reynolds, A. R. Gorringe, S. G. Funnell, and J. J. McFadden. 2001. Generation and characterization of a PhoP homologue mutant of Neisseria meningitidis. Mol. Microbiol, 39:1345-1355.
25. Karow, M., and C. Georgopoulos. 1992. Isolation and characterization of the Escherichia coli msbB gene, a multicopy suppressor of null mutations in the high-temperature requirement gene htrB. J. Bacteriol. 174:702-710.
26. 2+-responsive promoters. J. Bacteriol. 181:5516-5520.
27. Kim, S. H., W. Jia, R. E. Bishop, and C. Gyles. 2004. An msbB homologue carried in plasmid pO157 encodes an acyltransferase involved in lipid A biosynthesis in Escherichia coli O157:H7. Infect. Immun. 72:1174-1180.
28. Labischinski, H., G. Barnickel, H. Bradaczek, D. Naumann, E. T. Rietschel, and P. Giesbrecht. 1985. High state of order of isolated bacterial lipopolysaccharide and its possible contribution to the permeation barrier property of the outer membrane. J. Bacteriol. 162:9-20.
29. Labischinski, H., D. Naumann, C. Schultz, S. Kusumoto, T. Shiba, E. T. Rietschel, and P. Giesbrecht. 1989. Comparative X-ray and Fourier-transform-infrared investigations of conformational properties of bacterial and synthetic lipid A of Escherichia coli and Salmonella minnesota as well as partial structures and analogues there of. Eur. J. Biocfiem. 179:659-665.
30. 2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J. Bacteriol. 185:6287-6294.
31. Lodge, J., J. Fear, S. Busby, P. Gunasekaran, and N. R. Kamini. 1992. Broad host range plasmids carrying the Escherichia coli lactose and galactose operons. FEMS Microbiol. Lett. 74:271-276.
32. Low, K. B., M. Ittensohn, T. Le, J. Platt, S. Sodi, M. Amoss, O. Ash, E. Carmichael, A. Chakraborty, J. Fischer, S. L. Lin, X. Luo, S. I. Miller, L. Zheng, I. King, J. M. Pawelek, and D. Bermudes. 1999. Lipid A mutant Salmonella with suppressed virulence and TNFα induction retain tumortargeting in vivo. Nat. Biotechnol. 17:37-41.
33. Martin-Orozco, N., N. Touret, M. L. Zaharik, E. Park, R. Kopelman, S. Miller, B. B. Finlay, P. Gros, and S. Grinstein. 2006. Visualization of vacuolar acidification-induced transcription of genes of pathogens inside macrophages. Mol. Biol. Cell 17:498-510.
34. Maurelli, A. T., B. Baudry, H. d'Hauteville, T. L. Hale, and P. J. Sansonetti. 1985. Cloning of plasmid DNA sequences involved in invasion of HeLa cells by Shigella flexneri. Infect. Immun. 49:164-171.
35. Miller, S. I., W. S. Pulkkinen, M. E. Selsted, and J. J. Mekalanos. 1990. Characterization of defensin resistance phenotypes associated with mutations in the phoP virulence regulon of Salmonella typhimurium. Infect. Immun. 58:3706-3710.
36. Miller, V. L., and J. J. Mekalanos. 1988. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. I. Bacteriol. 170:2575-2583.
37. 2+ stimulon of Escherichia coli. J. Bacteriol. 185: 3696-3702.
38. Moss, J. E., P. E. Fisher, B. Vick, E. A. Groisman, and A. Zychlinsky. 2000. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell Microbiol. 2:443-452.
39. Murata, T., W. Tseng, T. Guina, S. I. Miller, and H. Nikaido. 2007. PhoPQ-mediated regulation produces a more robust permeability barrier in the outer membrane of Salmonella enterica serovar Typhimurium. J. Bacteriol. 189:7213-7222.
40. Murray, S. R., R. K. Ernst, D. Bermudes, S. I. Miller, and K. B. Low. 2007. PmrA(Con) confers pmrHFIJKL-dependent EGTA and polymyxin resistance on msbB Salmonella by decorating lipid A with phosphoethanolamine. J. Bacteriol. 189:5161-5169.
41. Navarre, W. W., T. A. Halsey, D. Walthers, J. Frye, M. McClelland, J. L. Potter, L. J. Kenney, J. S. Gunn, F. C. Fang, and S. J. Libby. 2005. Coregulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol. Microbiol. 56:492-508.
42. Nelson, D. L., and E. P. Kennedy. 1971. Magnesium transport in Escherichia coli. Inhibition by cobaltous ion. J. Biol. Chem. 246:3042-3049.
43. Newcombe, J., J. C. Jeynes, E. Mendoza, J. Hinds, G. L. Marsden, R. A. Stabler, M. Marti, and J. J. McFadden. 2005. Phenotypic and transcriptional characterization of the meningococcal PhoPQ system, a magnesium-sensing two-component regulatory system that controls genes involved in remodeling the meningococcal cell surface. J. Bacteriol. 187:4967-4975.
44. Nikaido, H., Y. Takeuchi, S. I. Ohnishi, and T. Nakae. 1977. Outer membrane of Salmonella typhimurium. Electron spin resonance studies. Biochim. Biophys. Acta 465:152-164.
45. Okada, N., C. Sasakawa, T. Tobe, M. Yamada, S. Nagai, K. A. Talukder, K. Komatsu, S. Kanegasaki, and M. Yoshikawa. 1991. Virulence-associated chromosomal loci of Shigella flexneri identified by random Tn5 insertion mutagenesis. Mol. Microbiol. 5:187-195.
46. Raetz, C. R., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
47. Sansonetti, P. J., A. Ryter, P. Clerc, A. T. Maurelli, and J. Mounier. 1986. Multiplication of Shigella flexneri within HeLa cells: lysis of the phagocytic vacuole and plasmid-mediated contact hemolysis. Infect. Immun. 51:461-469.
48. Snavely, M. D., S. A. Gravina, T. T. Cheung, C. G. Miller, and M. E. Maguire. 1991. Magnesium transport in Salmonella typhimurium. Regulation of mgtA and mgtB expression. J. Biol. Chem. 266:824-829.
49. Somerville, J. E., Jr., L. Cassiano, and R. P. Darveau. 1999. Escherichia coli msbB gene as a virulence factor and a therapeutic target. Infect. Immun. 67:6583-6590.
50. Soncini, F. C., E. Garcia Vescovi, F. Solomon, and E. A. Groisman. 1996. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J. Bacteriol. 178:5092-5099.
51. Steinhauer, J., R. Agha, T. Pham, A. W. Varga, and M. B. Goldberg. 1999. The unipolar Shigella surface protein IcsA is targeted directly to the bacterial old pole: IcsP cleavage of IcsA occurs over the entire bacterial surface. Mol. Microbiol. 32:367-377.
52. Tran, A. X., M. E. Lester, C. M. Stead, C. R. Raetz, D. J. Maskell, S. C. McGrath, R. J. Cotter, and M. S. Trent. 2005. Resistance to the antimicrobial peptide polymyxin requires myristoylation of Escherichia coli and Salmonella typhimurium lipid A. J. Biol. Chem. 280:28186-28194.
53. Trent, M. S., W. Pabich, C. R. Raetz, and S. I. Miller. 2001. 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.
54. Trent, M. S., A. A. Ribeiro, S. Lin, R. J. Cotter, and C. R. Raetz. 2001. 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.
55. Vaara, M., and M. Nurminen. 1999. Outer membrane permeability barrier in Escherichia coli mutants that are defective in the late acyltransferases of lipid A biosynthesis. Antimicrob. Agents Chemother. 43:1459-1462.
56. Venkatesan, M. M., M. B. Goldberg, D. J. Rose, E. J. Grotbeck, V. Burland, and F. R. Blattner. 2001. Complete DNA sequence and analysis of the large virulence plasmid of Shigella flexneri. Infect. Immun. 69:3271-3285.
57. Vorachek-Warren, M. K., S. Ramirez, R. J. Cotter, and C. R. Raetz. 2002, A triple mutant of Escherichia coli lacking secondaiy acyl chains on lipid A. J. Biol. Chem. 277:14194-14205.
58. Wehkamp, J., K. Fellermann, K. R. Herrlinger, C. L. Bevins, and E. F. Stange. 2005. Mechanisms of disease: defensins in gastrointestinal diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2:406-415.
59. Wei, J., M. B. Goldberg, V. Burland, M. M. Venkatesan, W. Deng, G. Fournier, G. F. Mayhew, G. Plunkett III, D. J. Rose, A. Darling, B. Mau, N. T. Perna, S. M. Payne, L. J. Runyen-Janecky, S. Zhou, D. C. Schwartz, and F. R. Blattner. 2003. Complete genome sequence and comparative genomics of Shigella flexneri serotype 2a strain 2457T. Infect. Immun. 71: 2775-2786.
60. Wing, H. J., A. W. Yan, S. R. Goldman, and M. B. Goldberg. 2004. Regulation of IcsP, the outer membrane protease of the Shigella actin tail assembly protein IcsA, by virulence plasmid regulators VirF and VirB. J. Bacteriol. 186:699-705.
61. Yamamoto, K., H. Ogasawara, N. Fujita, R. Utsumi, and A. Ishihama. 2002. Novel mode of transcription regulation of divergently overlapping promoters by PhoP, the regulator of two-component system sensing external magnesium availability. Mol. Microbiol. 45:423-438.
62. Yanisch-Perron, C., J. Vieira, and J. Messing. 1985. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103-119.
63. Yoon, J. W., S. A. Minnich, J. S. Ahn, Y. H. Park, A. Paszczynski, and C. J. Hovde. 2004. Thermoregulation of the Escherichia coli O157:H7 pO157 ecf operon and lipid A myristoyl transferase activity involves intrinsically curved DNA. Mol. Microbiol. 51:419-435.
64. 2+-responsive PhoP regulator in Yersinia pestis. FEMS Microbiol. Lett. 250: 85-95.
65. Zhou, Z., S. Lin, R. J. Cotter, and C. R. Raetz. 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.
66. Zhou, Z., A. A. Ribeiro, S. Lin, R. J. Cotter, S. I. Miller, and C. R. Raetz. 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.
67. Zwir, I., D. Shin, A. Kato, K. Nishino, T. Latifl, F. Solomon, J. M. Hare, H. Huang, and E. A. Groisman. 2005. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc. Natl. Acad. Sci. USA 102:2862-2867.