Characterization of late acyltransferase genes of Yersinia pestis and their role in temperature-dependent lipid A variation

Journal of Bacteriology

Volumn 188, Issue 4, 2006, Pages 1381-1388

  Rebeil, Roberto ^a,c   Ernst, Robert K ^b   Jarrett, Clayton O ^a   Adams, Kristin N ^b   Miller, Samuel I ^b   Hinnebusch, B Joseph ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

^c SANDIA NATIONAL LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; CECROPIN A; LIPID A;

ADAPTATION; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM MUTANT; CONTROLLED STUDY; DISEASE CARRIER; ENVIRONMENTAL FACTOR; FLEA; GENE EXPRESSION REGULATION; GENETIC ANALYSIS; HOST; IN VITRO STUDY; IN VIVO STUDY; LIPOGENESIS; MIDGUT; NONHUMAN; PRIORITY JOURNAL; TEMPERATURE DEPENDENCE; YERSINIA PESTIS;

ACYLTRANSFERASES; ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS; ANTIMICROBIAL CATIONIC PEPTIDES; FEMALE; FLEAS; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; LIPID A; MALE; MICROBIAL SENSITIVITY TESTS; MUTATION; POLYMYXIN B; TEMPERATURE; UP-REGULATION; YERSINIA PESTIS;

BACTERIA (MICROORGANISMS); INSECTA; MAMMALIA; RODENTIA; SIPHONAPTERA (FLEAS); YERSINIA PESTIS;

EID: 32444440799     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.188.4.1381-1388.2006     Document Type: Article

References (40)

1. Ahn, V. E., E. I. Lo, C. K. Engel, L. Chen, P. M. Hwang, L. E. Kay, R. E. Bishop, and G. G. Privé. 2004. A hydrocarbon ruler measures palmitate in the enzymatic acylation of endotoxin. EMBO J. 23:2931-2941.
2. Aussel, L., H. Therisod, D. Karibian, M. B. Perry, M. Bruneteau, and M. Caroff. 2000. Novel variation of lipid A structures in strains of different Yersinia species. FEBS Lett. 465:87-92.
3. Caroff, M., A. Tacken, and L. Szabo. 1988. Detergent-accelerated hydrolysis of bacterial endotoxins and determination of the anomeric configuration of the glycosyl phosphate present in the "isolated lipid A" fragment of the Bordetella pertussis endotoxin. Carbohydr. Res. 175:273-282.
4. Carty, S. M., K. R. Sreekumar, and C. R. H. Raetz. 1999. Effect of cold shock on lipid A biosynthesis in Escherichia coli: Induction at 12°C of an acyltransferase specific for palmitoleoyl-acyl carrier protein. J. Biol. Chem. 274:9677-9685.
5. Cavanaugh, D. C., and R. Randall. 1959. The role of multiplication of Pasteurella pestis in mononuclear phagocytes in the pathogenesis of flea-borne plague. J. Immunol. 83:348-363.
6. Chaussee, M. S., R. O. Watson, J. C. Smoot, and J. M. Musser. 2001. Identification of Rgg-regulated exoproteins of Streptococcus pyogenes. Infect. Immun. 69:822-831.
7. Clementz, T., J. J. Bednarski, and C. R. H. Raetz. 1996. Function of the htrB high temperature requirement gene of Escherichia coli in the acylation of lipid A: HtrB catalyzed incorporation of laurate. J. Biol. Chem. 271:12095-12102.
8. Clementz, T., Z. Zhou, and C. R. H. 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.
9. Darveau, R. P., and Hancock. 1983. Procedure for isolation of bacterial lipopolysaccharides from both smooth and rough Pseudomonas aeruginosa and Salmonella typhimurium strains. J. Bacteriol. 155:831-838.
10. Donnenberg, M. S., and J. B. Kaper. 1991. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector. Infect. Immun. 59:4310-4317.
11. Du, Y., E. Galyov, and Å. Forsberg. 1995. Genetic analysis of virulence determinants unique to Yersinia pestis. Contrib. Microbiol. Immunol. 13:321-324.
12. Ernst, R. K., E. C. Yi, L. Guo, K. B. Lim, J. L. Burns, M. Hackett, and S. I. Miller. 1999. Specific lipopolysaccharide found in cystic fibrosis airway Pseudomonas aeruginosa. Science 286:1561-1565.
13. 2+ environments. J. Bacteriol. 179:7040-7045.
14. Gunn, J. S., K. B. Lim, J. Krueger, K. Kim, L. Guo, M. Hackett, and S. I. Miller. 1998. PmrA-PmrB-regulated genes necessary for 4-aminoarabinose lipid A modification and polymyxin resistance. Mol. Microbiol. 27:1171-1182.
15. 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.
16. Hinnebusch, B. J., R. D. Perry, and T. G. Schwan. 1996. Role of the Yersinia pestis hemin storage (hms) locus in the transmission of plague by fleas. Science 273:367-370.
17. Hinnebusch, B. J., A. E. Rudolph, P. Cherepanov, J. E. Dixon, T. G. Schwan, and Å. Forsberg. 2002. Role of the Yersinia murine toxin in the survival of Yersinia pestis in the midgut of the flea vector. Science 296:733-735.
18. Holst, O. 2003. Lipopolysaccharides of Yersinia. Adv. Exp. Med. Biol. 529:219-228.
19. Hudson, B. W., L. Kartman, and F. M. Prince. 1966. Pasteurella pestis detection in fleas by fluorescent antibody staining. Bull. W.H.O. 34:709-714.
20. Jarrett, C. O., E. Deak, K. E. Isherwood, P. C. Oyston, E. R. Fischer, A. R. Whitney, S. D. Kobayashi, F. R. DeLeo, and B. J. Hinnebusch. 2004. Transmission of Yersinia pestis from an infectious biofilm in the flea vector. J. Infect. Dis. 190:783-792.
21. Jones, B. D., W. A. Nichols, B. W. Gibson, M. G. Sunshine, and M. A. Apicella. 1997. Study of the role of the htrB gene in Salmonella typhimurium virulence. Infect. Immun. 65:4778-4783.
22. Karow, M., O. Fayet, A. Cegielska, T. Ziegelhoffer, and C. Georgopoulos. 1991. Isolation and characterization of the Escherichia coli htrB gene, whose product is essential for bacterial viability above 33°C in rich media. J. Bacteriol. 173:741-750.
23. Kawahara, K., H. Tsukano, H. Watanabe, B. Lindner, and M. Matsuura. 2002. Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect. Immun. 70:4092-4098.
24. Knirel, Y. A., B. Lindner, E. V. Vinogradov, N. A. Kocharova, S. N. Senchenkova, R. Z. Shaikhutdinova, S. V. Dentovskaya, N. K. Fursova, I. V. Bakhteeva, G. M. Titareva, S. V. Balakhonov, O. Holst, T. A. Gremyakova, G. B. Pier, and A. P. Anisimov. 2005. Temperature-dependent variations and intraspecies diversity of the structure of the lipopolysaccharide of Yersinia pestis. Biochemistry 44:1731-1743.
25. 24a. Motin, V. L., A. M. Georgescu, J. P. Fitch, P. P. Gu, D. O. Nelson, S. L. Mabery, J. B. Garnham, B. A. Sokhansanj, L. L. Oh, M. A. Coleman, J. M. Elliott, L. M. Kegelmeyer, A. J. Wyrobek, T. R. Slezak, R. R. Brubaker, and E. Garcia. 2004. Temporal global changes in gene expression during temperature transition in Yersinia pestis. J. Bacteriol. 186:6298-6305.
26. Nikaido, H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 67:593-656.
27. Parkhill, J., B. W. Wren, N. R. Thomson, R. W. Titball, M. T. Holden, M. B. Prentice, M. Sebaihia, K. D. James, C. Churcher, K. L. Mungall, S. Baker, D. Basham, S. D. Bentley, K. Brooks, A. M. Cerdeno-Tarraga, T. Chillingworth, A. Cronin, R. M. Davies, P. Davis, G. Dougan, T. Feltwell, N. Hamlin, S. Holroyd, K. Jagels, A. V. Karlyshev, S. Leather, S. Moule, P. C. Oyston, M. Quail, K. Rutherford, M. Simmonds, J. Skelton, K. Stevens, S. Whitehead, and B. G. Barrell. 2001. Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523-527.
28. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis-etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
29. Rebeil, R., R. K. Ernst, B. B. Gowen, S. I. Miller, and B. J. Hinnebusch. 2004. Variation in lipid A structure in the pathogenic yersiniae. Mol. Microbiol. 52:1363-1373.
30. Simon, R., U. Priefer, and A. Pülher. 1983. A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in gram-negative bacteria. Biotechnology 1:784-791.
31. Somerville, J. E., L. Cassiano, and R. P. Darveau. 1999. Escherichia coli msbB gene as a virulence factor and a therapeutic target. Infect. Immun. 67:6583-6590.
32. Somerville, J. E. J., L. Cassiano, B. Bainbridge, M. D. Cunningham, and R. P. Darveau. 1996. A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J. Clin. Investig. 97:359-365.
33. Stoker, N. G., N. F. Fairweather, and B. G. Spratt. 1982. Versatile low-copy-number plasmid vectors for cloning Escherichia coli. Gene 18:335-341.
34. Straley, S. C., and R. D. Perry. 1995. Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol. 3:310-317.
35. Terra, W. R., B. P. Ferreira, and R. J. Dillon. 1996. Digestive enzymes, p. 153-194. In M. J. Lehane and P. F. Billingsley (ed.), Biology of the insect midgut. Chapman & Hall, London, England.
36. r phenotypes of yersiniae. Infect. Immun. 43:895-900.
37. 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.
38. Vorachek-Warren, M. K., S. Ramirez, R. J. Cotter, and C. R. H. Raetz. 2002. A triple mutant of Escherichia coli lacking secondary acyl chains on lipid A. J. Biol. Chem. 277:14194-14205.
39. Wang, J., and M. F. Wilkinson. 2001. Deletion mutagenesis of large (12-kb) plasmids by a one step PCR protocol. BioTechniques 31:722-724.
40. Wyckoff, T. J. O., S. Lin, R. J. Cotter, G. D. Dotson, and C. R. H. Raetz. 1998. Hydrocarbon rulers in UDP-N-acetylglucosamine acyltransferases. J. Biol. Chem. 273:32369-32372.