Fine-tuning synthesis of yersinia pestis lcrv from runaway-like replication balanced-lethal plasmid in a salmonella enterica serovar typhimurium vaccine induces protection against a lethal y. pestis challenge in mice

Infection and Immunity

Volumn 78, Issue 6, 2010, Pages 2529-2543

  Torres Escobar, Ascención ^a   Juárez Rodríguez, María Dolores ^a   Gunn, Bronwyn M ^a,c   Branger, Christine G ^a   Tinge, Steven A ^b,d   Curtiss III, Roy ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b Megan Health Inc   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d SAINT LOUIS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABINOSE; BACTERIAL ANTIGEN; BACTERIUM ANTIBODY; BETA LACTAMASE; GAMMA INTERFERON; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 4; LCRV ANTIGEN; PLAGUE VACCINE; PLASMID VECTOR; SALMONELLOSIS VACCINE; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ALLELE; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY RESPONSE; ANTIGEN EXPRESSION; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL GENE; BACTERIAL IMMUNITY; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CARBOXY TERMINAL SEQUENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; COPY NUMBER VARIATION; CYTOKINE PRODUCTION; DRUG SYNTHESIS; FEMALE; GENE CONTROL; GENE SWITCHING; IMMUNOSTIMULATION; IN VIVO STUDY; MOLECULAR CLONING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERATOR GENE; PLAGUE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROVOCATION TEST; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS; SEROTYPE; TH1 CELL; TH2 CELL; VACCINE PRODUCTION; YERSINIA PESTIS;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL VACCINES; FEMALE; GENETIC VECTORS; MICE; MICE, INBRED BALB C; PLAGUE; PLASMIDS; PORE FORMING CYTOTOXIC PROTEINS; SALMONELLA TYPHIMURIUM; SURVIVAL ANALYSIS; TH1 CELLS; TH2 CELLS; YERSINIA PESTIS;

EID: 77952688329     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00005-10     Document Type: Article

References (68)

1. Abramov, V. M., V. S. Khlebnikov, A. M. Vasiliev, I. V. Kosarev, R. N. Vasilenko, N. L. Kulikova, A. V. Khodyakova, V. I. Evstigneev, V. N. Uversky, V. L. Motin, G. B. Smirnov, and R. R. Brubaker. 2007. Attachment of LcrV from Yersinia pestis at dual binding sites to human TLR-2 and human IFN-gamma receptor. J. Proteome Res. 6:2222-2231.
2. Bertani, G. 1951. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 62:293-300.
3. Bochner, B. R. 1984. Curing bacterial cells of lysogenic viruses by using UCB indicator plates. Biotechniques 2:234-240.
4. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
5. Branger, C. G., J. D. Fetherston, R. D. Perry, and R. Curtiss III. 2007. Oral vaccination with different antigens from Yersinia pestis KIM delivered by live attenuated Salmonella Typhimurium elicits a protective immune response against plague. Adv. Exp. Med. Biol. 603:387-399.
6. Branger, C. G., A. Torres-Escobar, W. Sun, R. Perry, J. Fetherston, K. L. Roland, and R. Curtiss III. 2009. Oral vaccination with LcrV from Yersinia pestis KIM delivered by live attenuated Salmonella enterica serovar Typhimurium elicits a protective immune response against challenge with Yersinia pseudotuberculosis and Yersinia enterocolitica. Vaccine 27:5363-5370.
7. Brown, E. D., E. I. Vivas, C. T. Walsh, and R. Kolter. 1995. MurA (MurZ), the enzyme that catalyzes the first committed step in peptidoglycan biosynthesis, is essential in Escherichia coli. J. Bacteriol. 177:4194-4197.
8. Brubaker, R. R. 2003. Interleukin-10 and inhibition of innate immunity to yersiniae: roles of Yops and LcrV (V antigen). Infect. Immun. 71:3673-3681.
9. Cárdenas, L., and J. D. Clements. 1992. Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens. Clin. Microbiol. Rev. 5:328-342.
10. Curtiss, R., III. 1965. Chromosomal aberrations associated with mutations to bacteriophage resistance in Escherichia coli. J. Bacteriol. 89:28-40.
11. Curtiss, R., III, 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.
12. Curtiss, R., III. April 2003. Regulation of attenuation of live vaccines to enhance cross protective immunity. International patent WO 03/096812.
13. Curtiss, R., III, and W. Kong. August 2006. Regulated bacterial lysis for gene vaccine vector delivery and antigen release. U.S. patent 2006/0140975 A1.
14. Curtiss, R., III, X. Zhang, S. Y. Wanda, H. Y. Kang, V. Konjufca, Y. Li, B. Gunn, S. Wang, G. Scarpellini, and I. S. Lee. 2007. Induction of host immune responses using Salmonella-vectored vaccines, p. 297-313. In K. A. Brogden, F. C. Minion, N. Cornick, T. B. Stanton, Q. Zhang, L. K. Nolan, and M. J. Wannemuehler (ed.), Virulence mechanism of bacterial pathogens, 4th ed. ASM Press, Washington, DC.
15. 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.
16. Depaolo, R. W., F. Tang, I. Kim, M. Han, N. Levin, N. Ciletti, A. Lin, D. Anderson, O. Schneewind, and B. Jabri. 2008. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4:350-361.
17. Derewenda, U., A. Mateja, Y. Devedjiev, K. M. Routzahn, A. G. Evdokimov, Z. S. Derewenda, and D. S. Waugh. 2004. The structure of Yersinia pestis V-antigen, an essential virulence factor and mediator of immunity against plague. Structure 12:301-306.
18. Dozois, C. M., F. Daigle, and R. Curtiss III. 2003. Identification of pathogen-specific and conserved genes expressed in vivo by an avian pathogenic Escherichia coli strain. Proc. Natl. Acad. Sci. U. S. A. 100:247-252.
19. 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.
20. Eisele, N. A., and D. M. Anderson. 2009. Dual function antibodies to Y. pestis LcrV required for pulmonary clearance of plague. Clin. Vaccine Immunol. 16:1720-1727.
21. Ewen, C., and M. E. Baca-Estrada. 2001. Evaluation of interleukin-4 concentration by ELISA is influenced by the consumption of IL-4 by cultured cells. J. Interferon Cytokine Res. 21:39-43. (Pubitemid 32106089)
22. Fields, K. A., M. L. Nilles, C. Cowan, and S. C. Straley. 1999. Virulence role of V antigen of Yersinia pestis at the bacterial surface. Infect. Immun. 67:5395-5408.
23. Garmory, H. S., K. F. Griffin, K. A. Brown, and R. W. Titball. 2003. Oral immunisation with live aroA attenuated Salmonella enterica serovar Typhimurium expressing the Yersinia pestis V antigen protects mice against plague. Vaccine 21:3051-3057.
24. Getahun, A., J. Dahlström, S. Wernersson, and B. Heyman. 2004. IgG2a-mediated enhancement of antibody and T cell responses and its relation to inhibitory and activating Fc gamma receptors. J. Immunol. 172:5269-5276. (Pubitemid 38542024)
25. Gunn, B. M., S.-Y. Wanda, D. Burshell, C. 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.
26. Hill, J., S. E. Leary, K. F. Griffin, E. D. Williamson, and R. W. Titball. 1997. Regions of Yersinia pestis V antigen that contribute to protection against plague identified by passive and active immunization. Infect. Immun. 65:4476-4482.
27. Hinnebusch, B. J. 2005. The evolution of flea-borne transmission in Yersinia pestis. Curr. Issues Mol. Biol. 7:197-212.
28. Hitchcock, P. J., and T. M. Brown. 1983. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154:269-277.
29. Holmström, A., J. Olsson, P. Cherepanov, E. Maier, R. Nordfelth, J. Pettersson, R. Benz, H. Wolf-Watz, and A. Forsberg. 2001. LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol. Microbiol. 39:620-632. (Pubitemid 32158142)
30. Husseiny, M. I., and M. Hensel. 2009. Evaluation of Salmonella live vaccines with chromosomal expression cassettes for translocated fusion proteins. Vaccine 27:3780-3787.
31. Iankov, I. D., D. P. Petrov, I. V. Mladenov, I. H. Haralambieva, R. Ivanova, L. Sechanova, and I. G. Mitov. 2001. Monoclonal antibodies of IgA isotype specific for lipopolysaccharide of Salmonella enteritidis: production, purification, characterization and application as serotyping reagents. FEMS Microbiol. Lett. 196:215-221.
32. Inglesby, T. V., D. T. Dennis, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, J. F. Koerner, M. Layton, J. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. M. Perl, P. K. Russell, M. Schoch-Spana, and K. Tonat. 2000. Plague as a biological weapon: medical and public health management. JAMA 283:2281-2290.
33. Kadonaga, J. T., A. Plückthun, and J. R. Knowles. 1985. Signal sequence mutants of beta-lactamase. J. Biol. Chem. 260:16192-16199.
34. 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.
35. Khan, A. A., J. P. Babu, G. Gupta, and D. N. Rao. 2008. Identifying B and T cell epitopes and studying humoral, mucosal and cellular immune responses of peptides derived from V antigen of Yersinia pestis. Vaccine 26:316-332.
36. Kong, W., S. Y. Wanda, X. Zhang, W. Bollen, S. A. Tinge, K. L. Roland, and R. Curtiss III. 2008. Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc. Natl. Acad. Sci. U. S. A. 105:9361-9366.
37. Koshland, D., and D. Botstein. 1980. Secretion of beta-lactamase requires the carboxy end of the protein. Cell 20:749-760. (Pubitemid 10078554)
38. Kummer, L. W., F. M. Szaba, M. A. Parent, J. J. Adamovicz, J. Hill, L. L. Johnson, and S. T. Smiley. 2008. Antibodies and cytokines independently protect against pneumonic plague. Vaccine 26:6901-6907.
39. Lennox, E. S. 1955. Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1:190-206.
40. 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. U. S. A. 106:593-598.
41. Liu, T., and A. K. Chopra. 28 August 2009, posting date. An enteric pathogen Salmonella enterica serovar Typhimurium suppresses tumor growth by downregulating CD44(high) and CD4T regulatory (T(reg)) cell expression in mice: the critical role of lipopolysaccharide and Braun lipoprotein in modulating tumor growth. Cancer Gene Ther. doi:10.1038/cgt.2009.58.
42. Liu, W. T., H. L. Hsu, C. C. Liang, C. C. Chuang, H. C. Lin, and Y. T. Liu. 2007. A comparison of immunogenicity and protective immunity against experimental plague by intranasal and/or combined with oral immunization of mice with attenuated Salmonella serovar Typhimurium expressing secreted Yersinia pestis F1 and V antigen. FEMS Immunol. Med. Microbiol. 51:58-69.
43. Lo-Man, R., J. P. Langeveld, E. Dériaud, M. Jehanno, M. Rojas, J. M. Clément, R. H. Meloen, M. Hofnung, and C. Leclerc. 2000. Extending the CD4(+) T-cell epitope specificity of the Th1 immune response to an antigen using a Salmonella enterica serovar Typhimurium delivery vehicle. Infect. Immun. 68:3079-3089.
44. Matson, J. S., and M. L. Nilles. 2001. LcrG-LcrV interaction is required for control of Yops secretion in Yersinia pestis. J. Bacteriol. 183:5082-5091.
45. Matsuyama, S., K. Inokuchi, and S. Mizushima. 1984. Promoter exchange between ompF and ompC, genes for osmoregulated major outer membrane proteins of Escherichia coli K-12. J. Bacteriol. 158:1041-1047. (Pubitemid 14088676)
46. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
47. Motin, V. L., R. Nakajima, G. B. Smirnov, and R. R. Brubaker. 1994. Passive immunity to yersiniae mediated by anti-recombinant V antigen and protein A-V antigen fusion peptide. Infect. Immun. 62:4192-4201.
48. Mueller, C. A., P. Broz, S. A. Müller, P. Ringler, F. Erne-Brand, I. Sorg, M. Kuhn, A. Engel, and G. R. Cornelis. 2005. The V-antigen of Yersinia forms a distinct structure at the tip of injectisome needles. Science 310:674-676.
49. Nakayama, K., S. M. Kelly, and R. Curtiss III. 1988. Construction of an ASD+ expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Biotechnology 6:693-697.
50. Overheim, K. A., R. W. Depaolo, K. L. Debord, E. M. Morrin, D. M. Anderson, N. M. Green, R. R. Brubaker, B. Jabri, and O. Schneewind. 2005. LcrV plague vaccine with altered immunomodulatory properties. Infect. Immun. 73:5152-5159.
51. Parsa, S., and B. Pfeifer. 2007. Engineering bacterial vectors for delivery of genes and proteins to antigen-presenting cells. Mol. Pharm. 4:4-17.
52. Perry, R. D., and J. D. Fetherston. 1997. Yersinia pestis - etiologic agent of plague. Clin. Microbiol. Rev. 10:35-66.
53. Perry, R. D., S. C. Straley, J. D. Fetherston, D. J. Rose, J. Gregor, and F. R. Blattner. 1998. DNA sequencing and analysis of the low-Ca2+-response plasmid pCD1 of Yersinia pestis KIM5. Infect. Immun. 66:4611-4623.
54. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
55. Schmidt-Weber, C. B., S. I. Alexander, L. E. Henault, L. James, and A. H. Lichtman. 1999. IL-4 enhances IL-10 gene expression in murine Th2 cells in the absence of TCR engagement. J. Immunol. 162:238-244.
56. Schwyn, B., and J. B. Neilands. 1987. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 160:47-56.
57. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300:337-339. (Pubitemid 36433726)
58. Shi, H., S. Wang, K. L. Roland, B. M. Gunn, and R. Curtiss III. 2010. Immunogenicity of a live recombinant Salmonella enterica serovar Typhimurium vaccine expressing pspA in neonates and infant mice born from naïve and immunized mothers. Clin. Vaccine Immunol. 17:363-371.
59. Sing, A., D. Reithmeier-Rost, K. Granfors, J. Hill, A. Roggenkamp, and J. Heesemann. 2005. A hypervariable N-terminal region of Yersinia LcrV determines Toll-like receptor 2-mediated IL-10 induction and mouse virulence. Proc. Natl. Acad. Sci. U. S. A. 102:16049-16054.
60. Smiley, S. T. 2008. Immune defense against pneumonic plague. Immunol. Rev. 225:256-271.
61. Summers, R. G., and J. R. Knowles. 1989. Illicit secretion of a cytoplasmic protein into the periplasm of Escherichia coli requires a signal peptide plus a portion of the cognate secreted protein. Demarcation of the critical region of the mature protein. J. Biol. Chem. 264:20074-20081.
62. Sun, W., K. L. Roland, X. Kuang, C. G. Branger, and R. Curtiss III. 2010. Yersinia pestis with regulated delayed attenuation as a vaccine candidate to induce protective immunity against plague. Infect. Immun. 78:1304-1313.
63. Uhlin, B. E., and K. Nordström. 1978. A runaway-replication mutant of plasmid R1drd-19: temperature-dependent loss of copy number control. Mol. Gen. Genet. 165:167-179.
64. Vander Byl, C., and A. M. Kropinski. 2000. Sequence of the genome of Salmonella bacteriophage P22. J. Bacteriol. 182:6472-6481.
65. Vernazza, C., B. Lingard, H. C. Flick-Smith, L. W. Baillie, J. Hill, and H. S. Atkins. 2009. Small protective fragments of the Yersinia pestis V antigen. Vaccine 27:2775-2780.
66. Wang, S., D. Heilman, F. Liu, T. Giehl, S. Joshi, X. Huang, T. H. Chou, J. Goguen, and S. Lu. 2004. A DNA vaccine producing LcrV antigen in oligomers is effective in protecting mice from lethal mucosal challenge of plague. Vaccine 22:3348-3357.
67. 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.
68. 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. (Pubitemid 15122816)