Regulated delayed expression of rfaH in an attenuated Salmonella enterica serovar typhimurium vaccine enhances immunogenicity of outer membrane proteins and a heterologous antigen

Infection and Immunity

Volumn 77, Issue 12, 2009, Pages 5572-5582

  Kong, Qingke ^a   Liu, Qing ^a   Roland, Kenneth L ^a   Curtiss III, Roy ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSIDE; BACTERIAL PROTEIN; IMMUNOGLOBULIN G; LIVE VACCINE; O ANTIGEN; OUTER MEMBRANE PROTEIN; PNEUMOCOCCAL PROTEIN PSPA; PROTEIN BAD; RFAH PROTEIN; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM VACCINE; SALMONELLOSIS VACCINE; SUGAR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL VIRULENCE; CODON; CONTROLLED STUDY; ENTEROBACTERIACEAE; FEMALE; GENE CONSTRUCT; HOST; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; LD 50; LYMPHOID TISSUE; MOUSE; MUTANT; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROVOCATION TEST; RIBOSOME; SALMONELLA ENTERICA; SEQUENCE ANALYSIS; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTIBODIES, BACTERIAL; ANTIGENS, HETEROPHILE; ARABINOSE; BACTERIAL OUTER MEMBRANE PROTEINS; BACTERIAL PROTEINS; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION, BACTERIAL; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; PNEUMOCOCCAL INFECTIONS; PROMOTER REGIONS, GENETIC; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; STREPTOCOCCUS PNEUMONIAE; SURVIVAL ANALYSIS; TRANSCRIPTIONAL ACTIVATION; VACCINES, ATTENUATED;

EID: 72449190072     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00831-09     Document Type: Article

References (51)

1. Artsimovitch, I., and R. Landick. 2002. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109:193-203. (Erratum, 110:801.) (Pubitemid 35283967)
2. Atkins, H. S., M. Morton, K. F. Griffin, M. G. M. Stokes, J. P. Nataro, and R. W. Titball. 2006. Recombinant Salmonella vaccines for biodefence. Vaccine 24:2710-2717.
3. Bailey, M. J. A., C. Hughes, and V. Koronakis. 1997. RfaH and the ops element, components of a novel system controlling bacterial transcription elongation. Mol. Microbiol. 26:845-851.
4. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:293-300.
5. Briles, D. E., J. D. King, M. A. Gray, L. S. McDaniel, E. Swiatlo, and K. A. Benton. 1996. PspA, a protection-eliciting pneumococcal protein: immunogenicity of isolated native PspA in mice. Vaccine 14:858-867.
6. Brown, J. S., T. Hussell, S. M. Gilliland, D. W. Holden, J. C. Paton, M. R. Ehrenstein, M. J. Walport, and M. Botto. 2002. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc. Natl. Acad. Sci. USA 99:16969-16974.
7. Chatfield, S. N., M. Roberts, G. Dougan, C. Hormaeche, and C. M. A. Khan. 1995. The development of oral vaccines against parasitic diseases utilizing live attenuated Salmonella. Parasitology 110:S17-S24.
8. Cheminay, C., and M. Hensel. 2008. Rational design of Salmonella recombinant vaccines. Int. J. Med. Microbiol. 298:87-98.
9. Collins, L. V., S. Attridge, and J. Hackett. 1991. Mutations at rfc or pmi attenuate Salmonella typhimurium virulence for mice. Infect. Immun. 59:1079-1085.
10. Curtiss, R., III. 2002. Bacterial infectious disease control by vaccine development. J. Clin. Investig. 110:1061-1066.
11. Curtiss, R., III, S.-Y. Wanda, B. M. Gunn, X. Zhang, S. A. Tinge, V. Ananthnarayan, H. Mo, S. Wang, and W. Kong. 2009. Salmonella enterica serovar Typhimurium strains with regulated delayed attenuation in vivo. Infect. Immun. 77:1071-1082.
12. Curtiss, R., III, X. Zhang, S. Y. Wanda, H. Y. Kang, V. Konjufca, Y. Li., B. Gunn, S. Wang, G. Scarpellini, and L. I. Soo. 2007. Induction of host immune responses using Salmonella-vectored vaccines, p. 297-313. In Virulence mechanisms of bacterial pathogens, 4th ed. ASM Press, Washington, DC.
13. Curtiss, R., and S. M. Kelly. 1987. Salmonella typhimurium deletion mutants lacking adenylate-cyclase and cyclic-AMP receptor protein are avirulent and immunogenic. Infect. Immun. 55:3035-3043.
14. 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.
15. Germanier, R., and E. Fürer. 1971. Immunity in experimental salmonellosis. 2. Basis for avirulence and protective capacity of galE mutants of Salmonella typhimurium. Infect. Immun. 4:663-673.
16. Hassan, J. O., and R. Curtiss. 1990. Control of colonization by virulent Salmonella Typhimurium by oral immunization of chickens with avirulent delta-Cya delta-Crp Salmonella Typhimurium. Res. Microbiol. 141:839-850.
17. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver stained polyacrylamide gels. J. Bacteriol. 154:269-277.
18. Hone, D., R. Morona, S. Attridge, and J. Hackett. 1987. Construction of defined galE mutants of Salmonella for use as vaccines. J. Infect. Dis. 156:167-174.
19. Hone, D. M., S. R. Attridge, B. Forrest, R. Morona, D. Daniels, J. T. Labrooy, R. C. A. Bartholomeusz, D. J. C. Shearman, and J. Hackett. 1988. A galE-via (Vi-antigen-negative) mutant of Salmonella typhi Ty2 retains virulence in humans. Infect. Immun. 56:1326-1333.
20. 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.
21. Kong, W., S. Y. Wanda, X. Zhang, W. Bollen, S. A. Tinge, K. L. Roland, and R. Curtiss. 2008. Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc. Natl. Acad. Sci. USA 105:9361-9366.
22. Li, Y., S. Wang, G. Scarpellini, B. Gunn, W. Xin, S. Y. Wanda, K. L. Roland, and R. Curtiss III. 2009. Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc. Natl. Acad. Sci. USA 106:593-598.
23. Li, Y., S. Wang, W. Xin, G. Scarpellini, Z. Shi, B. Gunn, K. L. Roland, and R. Curtiss III. 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.
24. Lindberg, A. A., and C. G. Hellerqvist. 1980. Rough mutants of Salmonella typhimurium - immunochemical and structural analysis of lipopolysaccharides from rfaH mutants. J. Gen. Microbiol. 116:25-32.
25. McDaniel, L. S., J. S. Sheffield, P. Delucchi, and D. E. Briles. 1991. PspA, a surface protein of Streptococcus pneumoniae, is capable of eliciting protection against pneumococci of more than one capsular type. Infect. Immun. 59:222-228.
26. Nagy, G., V. Danino, U. Dobrindt, M. Pallen, R. Chaudhuri, L. Emody, J. C. Hinton, and J. Hacker. 2006. Down-regulation of key virulence factors makes the Salmonella enterica serovar Typhimurium rfaH mutant a promising live-attenuated vaccine candidate. Infect. Immun. 74:5914-5925.
27. Nagy, G., U. Dobrindt, J. Hacker, and L. Emody. 2004. Oral immunization with an rfaH mutant elicits protection against salmonellosis in mice. Infect. Immun. 72:4297-4301.
28. Nagy, G., L. Emody, and T. Pal. 2008. Strategies for the development of vaccines conferring broad-spectrum protection. Int. J. Med. Microbiol. 298:379-395.
29. Nagy, G., T. Palkovics, A. Otto, H. Kusch, B. Kocsis, U. Dobrindt, S. Engelmann, M. Hecker, L. Emody, T. Pal, and J. Hacker. 2008. "Gently rough": The vaccine potential of a Salmonella enterica regulatory lipopolysaccharide mutant. J. Infect. Dis. 198:1699-1706.
30. + expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Nat. Biotechnol. 6:693-697.
31. Nayak, A. R., S. A. Tinge, R. C. Tart, L. S. McDaniel, D. E. Briles, and R. Curtiss III. 1998. A live recombinant avirulent oral Salmonella vaccine expressing pneumococcal surface protein A induces protective responses against Streptococcus pneumoniae. Infect. Immun. 66:3744-3751.
32. Neidhardt, F. C., P. L. Bloch, and D. F. Smith. 1974. Culture medium for enterobacteria. J. Bacteriol. 119:736-747.
33. Rojas, G., S. Saldias, M. Bittner, M. Zaldivar, and I. Contreras. 2001. The rfaH gene, which affects lipopolysaccharide synthesis in Salmonella enterica serovar Typhi, is differentially expressed during the bacterial growth phase. FEMS Microbiol. Lett. 204:123-128.
34. Roland, K., R. Curtiss III, and D. Sizemore. 1999. Construction and evaluation of a delta cya delta crp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis. 43:429-441.
35. Sambandamurthy, V. K., and W. R. Jacobs. 2005. Live attenuated mutants of Mycobacterium tuberculosis as candidate vaccines against tuberculosis. Microbes Infect. 7:955-961.
36. 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.
37. Samuel, G., and P. Reeves. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519.
38. Sanderson, K. E., and B. A. D. Stocker. 1981. Gene rfaH, which affects lipopolysaccharide core structure in Salmonella typhimurium, is required also for expression of F-factor functions. J. Bacteriol. 146:535-541.
39. Santangelo, T. J., and J. W. Roberts. 2002. RfaH, a bacterial transcription antiterminator. Mol. Cell 9:698-700.
40. Schmieger, H. 1972. Phage P22 mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:75-88.
41. Singh, S. P., Y. U. Williams, P. E. Klebba, P. Macchia, and S. Miller. 2000. Immune recognition of porin and lipopolysaccharide epitopes of Salmonella typhimurium in mice. Microb. Pathog. 28:157-167.
42. Stevenson, G., and P. A. Manning. 1985. Galactose epimeraseless (galE) mutant G30 of Salmonella typhimurium is a good potential live oral vaccine carrier for fimbrial antigens. FEMS Microbiol. Lett. 28:317-321.
43. Stocker, B. A. D., and P. H. Makela. 1986. Genetic determination of bacterial virulence, with special reference to Salmonella. Curr. Top. Microbiol. Immunol. 124:149-172.
44. Stocker, B. A. D., and P. H. Makela. 1978. Genetics of (Gram-negative) bacterial surface. Philos. Trans. R. Soc. Lond. B 202:5-30.
45. Stocker, B. A. D., B. M. Males, and W. Takano. 1980. Salmonella typhimurium mutants of rfaH - phenotype, genetics and antibiotic sensitivities. J. Gen. Microbiol. 116:17-24.
46. Sun, W., S. Wang, and R. Curtiss III. 2008. Highly efficient method for introducing successive multiple scarless gene deletions and markerless gene insertions into the Yersinia pestis chromosome. Appl. Environ. Microbiol. 74:4241-4245. (Pubitemid 351962452)
47. 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.
48. Valentine, P. J., B. P. Devore, and F. Heffron. 1998. Identification of three highly attenuated Salmonella typhimurium mutants that are more immunogenic and protective in mice than a prototypical aroA mutant. Infect. Immun. 66:3378-3383.
49. Whitfield, C., N. Kaniuk, and E. Frirdich. 2003. Molecular insights into the assembly and diversity of the outer core oligosaccharide in lipopolysaccharides from Escherichia coli and Salmonella. J. Endoxin Res. 9:244-249.
50. 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. Protocols 3:163-175.
51. Xin, W., S. Y. Wanda, Y. Li, S. Wang, H. Mo, and R. Curtiss III. 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.