Palmitoylation state impacts induction of innate and acquired immunity by the Salmonella enterica serovar Typhimurium msbB mutant

Infection and Immunity

Volumn 79, Issue 12, 2011, Pages 5027-5038

  Kong, Qingke ^a   Six, David A ^b   Liu, Qing ^a   Gu, Lillian ^b   Roland, Kenneth L ^a   Raetz, Christian R H ^b   Curtiss, Roy ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; CYTOKINE; IMMUNOGLOBULIN G; LIPID A; LIPOPOLYSACCHARIDE; SALMONELLOSIS VACCINE; ANTIINFECTIVE AGENT; BACTERIAL PROTEIN;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE MUTATION; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; INFECTION PREVENTION; INNATE IMMUNITY; LPXR GENE; MACROPHAGE; MOUSE; MSBB GENE; NONHUMAN; PAGL GENE; PAGP GENE; PALMITOYLATION; PHENOTYPE; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROTYPE; STREPTOCOCCUS PNEUMONIA; ANIMAL; ANIMAL SALMONELLOSIS; CELL LINE; DRUG EFFECT; GENETICS; HUMAN; IMMUNOLOGY; LIPOYLATION; METABOLISM; MUTATION; PATHOGENICITY; VIRULENCE;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; CELL LINE; HUMANS; IMMUNITY, INNATE; LIPOYLATION; MICE; MUTATION; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; VIRULENCE;

EID: 84862917689     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.05524-11     Document Type: Article

References (64)

1. Abrahams, G. L., and M. Hensel. 2006. Manipulating cellular transport and immune responses: dynamic interactions between intracellular Salmonella enterica and its host cells. Cell Microbiol. 8:728-737.
2. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:293-300.
3. Bishop, R. E., et al. 2000. Transfer of palmitate from phospholipids to lipid A in outer membranes of Gram-negative bacteria. EMBO J. 19:5071-5080.
4. Bligh, E. G., and W. J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Phys. 37:911-917.
5. Brandenburg, K., and A. Wiese. 2004. Endotoxins: relationships between structure, function, and activity. Curr. Top. Med. Chem. 4:1127-1146.
6. Briles, D. E., et al. 1996. PspA, a protection-eliciting pneumococcal protein: immunogenicity of isolated native PspA in mice. Vaccine 14:858-867.
7. 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.
8. Clairmont, C., et al. 2000. Biodistribution and genetic stability of the novel antitumor agent VNP20009, a genetically modified strain of Salmonella typhimurium. J. Infect. Dis. 181:1996-2002.
9. Dofferhoff, A. S., et al. 1991. Effects of different types and combinations of antimicrobial agents on endotoxin release from gram-negative bacteria: an in vitro and in vivo study. Scand. J. Infect. Dis. 23:745-754.
10. Edwards, R. A., L. H. Keller, and D. M. Schifferli. 1998. Improved allelic exchange vectors and their use to analyze 987P fimbria gene expression. Gene 207:149-157.
11. Elson, G., I. Dunn-Siegrist, B. Daubeuf, and J. Pugin. 2007. Contribution of Toll-like receptors to the innate immune response to Gram-negative and Gram-positive bacteria. Blood 109:1574-1583.
12. Erridge, C., E. Bennett-Guerrero, and I. R. Poxton. 2002. Structure and function of lipopolysaccharides. Microbes Infect. 4:837-851.
13. Evans, M. E., and M. Pollack. 1993. Effect of antibiotic class and concentration on the release of lipopolysaccharide from Escherichia coli. J. Infect. Dis. 167:1336-1343.
14. 2+ and pH in the modification of Salmonella lipid A after endocytosis by macrophage tumour cells. Mol. Microbiol. 55:425-440.
15. Gunn, B. M., S. Y. Wanda, D. Burshell, C. H. Wang, and R. Curtiss III. 2010. Construction of recombinant attenuated Salmonella enterica serovar Typhimurium vaccine vector strains for safety in newborn and infant mice. Clin. Vaccine Immunol. 17:354-362.
16. Gunn, J. S., S. S. Ryan, J. C. Van Velkinburgh, R. K. Ernst, and S. I. Miller. 2000. Genetic and functional analysis of a PmrA-PmrB-regulated locus necessary for lipopolysaccharide modification, antimicrobial peptide resistance, and oral virulence of Salmonella enterica serovar Typhimurium. Infect. Immun. 68:6139-6146.
17. Guo, L., et al. 1997. Regulation of lipid A modifications by Salmonella typhimurium virulence genes phoP-phoQ. Science 276:250-253.
18. Guo, L., et al. 1998. Lipid A acylation and bacterial resistance against vertebrate antimicrobial peptides. Cell 95:189-198.
19. Hassan, J. O., and R. Curtiss III. 1990. Control of colonization by virulent Salmonella typhimurium by oral immunization of chickens with avirulent Δcya Δcrp Salmonella typhimurium. Res. Microbiol. 141:839-850.
20. Herrera, C. M., J. V. Hankins, and M. S. Trent. 2010. Activation of PmrA inhibits LpxT-dependent phosphorylation of lipid A promoting resistance to antimicrobial peptides. Mol. Microbiol. 76:1444-1460.
21. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J. Immunol. 165:618-622.
22. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver stained polyacrylamide gels. J. Bacteriol. 154:269-277.
23. Ibarra, J. A., and O. Steele-Mortimer. 2009. Salmonella-the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol. 11:1579-1586.
24. Iweala, O. I., et al. 2009. Vaccine-induced antibody isotypes are skewed by impaired CD4 T cell and invariant NKT cell effector responses in MyD88-deficient mice. J. Immunol. 183:2252-2260.
25. Kang, H. Y., J. Srinivasan, and R. Curtiss III. 2002. Immune responses to recombinant pneumococcal PspA antigen delivered by live attenuated Salmonella enterica serovar Typhimurium vaccine. Infect. Immun. 70:1739-1749.
26. Karsten, V., et al. 2009. msbB deletion confers acute sensitivity to CO2 in Salmonella enterica serovar Typhimurium that can be suppressed by a lossof-function mutation in zwf. BMC Microbiol. 9:170.
27. Khan, S. A., et al. 1998. A lethal role for lipid A in Salmonella infections. Mol. Microbiol. 29:571-579.
28. Kong, Q., Q. Liu, A. M. Jansen, and R. Curtiss III. 2010. Regulated delayed expression of rfc enhances the immunogenicity and protective efficacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Vaccine 28:6094-6103.
29. Kong, Q., Q. Liu, K. L. Roland, and R. Curtiss III. 2009. Regulated delayed expression of rfaH in an attenuated Salmonella enterica serovar Typhimurium vaccine enhances immunogenicity of outer membrane proteins and a heterologous antigen. Infect. Immun. 77:5572-5582.
30. Kong, Q., et al. 2011. Salmonella synthesizing 1-monophosphorylated lipopolysaccharide exhibits low endotoxic activity while retaining its immunogenicity. J. Immunol. 187:412-423.
31. Li, Y., et al. 2008. A sopB deletion mutation enhances the immunogenicity and protective efficacy of a heterologous antigen delivered by live attenuated Salmonella enterica vaccines. Infect. Immun. 76:5238-5246.
32. Liu, T., et al. 2008. Immunological responses against Salmonella enterica serovar Typhimurium Braun lipoprotein and lipid A mutant strains in Swiss-Webster mice: potential use as live-attenuated vaccines. Microb. Pathog. 44:224-237.
33. Low, K. B., et al. 1999. Lipid A mutant Salmonella with suppressed virulence and TNF alpha induction retain tumor-targeting in vivo. Nat. Biotechnol. 17:37-41.
34. Merighi, M., C. D. Ellermeier, J. M. Slauch, and J. S. Gunn. 2005. Resolvase-in vivo expression technology analysis of the Salmonella enterica serovar Typhimurium PhoP and PmrA regulons in BALB/c mice. J. Bacteriol. 187:7407-7416.
35. Miller, J. 1972. Experiments in molecular genetics, p. 352-355. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
36. Murray, S. R., D. Bermudes, K. S. de Felipe, and K. B. Low. 2001. Extragenic suppressors of growth defects in msbB Salmonella. J. Bacteriol. 183:5554-5561.
37. 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.
38. + expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Nat. Biotechnol. 6:693-697.
39. Nayak, A. R., et al. 1998. A live recombinant avirulent oral Salmonella vaccine expressing pneumococcal surface protein A induces protective responses against Streptococcus pneumoniae. Infect. Immun. 66:3744-3751.
40. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
41. Osborn, M. J. 1963. Studies on gram-negative cell wall. 1. Evidence for role of 2-keto-3-deoxyoctonate in lipopolysaccharide of Salmonella typhimurium. Proc. Natl. Acad. Sci. U. S. A. 50:499-506.
42. Osorio, C. G., et al. 2005. Second-generation recombination-based in vivo expression technology for large-scale screening for Vibrio cholerae genes induced during infection of the mouse small intestine. Infect. Immun. 73: 972-980.
43. Park, S. M., et al. 2008. MyD88 signaling is not essential for induction of antigen-specific B cell responses but is indispensable for protection against Streptococcus pneumoniae infection following oral vaccination with attenuated Salmonella expressing PspA antigen. J. Immunol. 181:6447-6455.
44. Pawelek, J. M., K. B. Low, and D. Bermudes. 1997. Tumor-targeted Salmonella as a novel anti-cancer vector. Cancer Res. 57:4537-4544.
45. Raetz, C. R. H., and C. Whitfield. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700.
46. Ranallo, R. T., et al. 2010. Virulence, inflammatory potential, and adaptive immunity induced by Shigella flexneri msbB mutants. Infect. Immun. 78:400-412.
47. Reynolds, C. M., et al. 2006. An outer membrane enzyme encoded by Salmonella typhimurium ipxR that removes the 3'-acyloxyacyl moiety of lipid A. J. Biol. Chem. 281:21974-21987.
48. Rietschel, E. T. 1994. Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J. 8:217-225.
49. Roger, T., et al. 2009. Protection from lethal Gram-negative bacterial sepsis by targeting Toll-like receptor 4. Proc. Natl. Acad. Sci. U. S. A. 106:2348-2352.
50. Roland, K., R. Curtiss III, and D. Sizemore. 1999. Construction and evaluation of a Δcya Δcrp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis. 43:429-441.
51. Rossignol, D. P., and M. Lynn. 2005. TLR4 antagonists for endotoxemia and beyond. Curr. Opin. Investig. Drugs 6:496-502.
52. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
53. Seibert, S. A., P. Mex, A. Kohler, S. H. E. Kaufmann, and H. W. Mittrucker. 2010. TLR2-, TLR4- and Myd88-independent acquired humoral and cellular immunity against Salmonella enterica serovar Typhimurium. Immunol. Lett. 127:126-134.
54. 2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J. Biol. Chem. 266:815-823.
55. Somerville, J. E., L. Cassiano, B. Bainbridge, M. D. Cunningham, and R. P. Darveau. 1996. A novel Escherichia coli lipid A mutant that produces an anti-inflammatory lipopolysaccharide. J. Clin. Invest. 97:359-365.
56. Toguchi, A., M. Siano, M. Burkart, and R. M. Harshey. 2000. Genetics of swarming motility in Salmonella enterica serovar Typhimurium: critical role for lipopolysaccharide. J. Bacteriol. 182:6308-6321.
57. Toso, J. F., et al. 2002. Phase I study of the intravenous administration of attenuated Salmonella typhimurium to patients with metastatic melanoma. J. Clin. Oncol. 20:142-152.
58. Tran, A. X., et al. 2005. Resistance to the antimicrobial peptide polymyxin requires myristoylation of Escherichia coli and Salmonella typhimurium lipid A. J. Biol. Chem. 280:28186-28194.
59. Trent, M. S., W. Pabich, C. R. H. Raetz, and S. I. Miller. 2001. A PhoP/PhoQinduced lipase (PagL) that catalyzes 3-O-deacylation of lipid A precursors in membranes of Salmonella typhimurium. J. Biol. Chem. 276:9083-9092.
60. Watson, P. R., et al. 2000. Mutation of waaN reduces Salmonella enterica serovar Typhimurium-induced enteritis and net secretion of type III secretion system 1-dependent proteins. Infect. Immun. 68:3768-3771.
61. Wiegand, I., K. Hilpert, and R. E. W. Hancock. 2008. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat. Protoc. 3:163-175.
62. Xin, W., et al. 2008. Analysis of type II secretion of recombinant pneumococcal PspA and PspC in a Salmonella enterica serovar Typhimurium vaccine with regulated delayed antigen synthesis. Infect. Immun. 76:3241-3254.
63. Yi, E. C., and M. Hackett. 2000. Rapid isolation method for lipopolysaccharide and lipid A from Gram-negative bacteria. Analyst 125:651-656.
64. Zhou, D. G., and J. Galan. 2001. Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect. 3:1293-1298.