Attenuated Francisella novicida transposon mutants protect mice against wild-type challenge

Infection and Immunity

Volumn 74, Issue 9, 2006, Pages 5095-5105

  Tempel, Rebecca ^a   Lai, Xin He ^a   Crosa, Lidia ^a   Kozlowicz, Briana ^a   Heffron, Fred ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIVE VACCINE; TULAREMIA VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM IDENTIFICATION; BACTERIUM MUTANT; CARB GENE; CONTROLLED STUDY; DOSE RESPONSE; DRUG DESIGN; DSBB GENE; FEMALE; FRANCISELLA; FRANCISELLA NOVICIDA; FRANCISELLA TULARENSIS; FTT0742 GENE; FUMA GENE; GENE MUTATION; HOST CELL; IMMUNE RESPONSE; IMMUNIZATION; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PDPB GENE; PRIORITY JOURNAL; SCREENING TEST; TRANSPOSON; TULAREMIA; VACCINE PRODUCTION; WILD TYPE;

ANIMALS; BACTERIAL VACCINES; CELL LINE; DNA TRANSPOSABLE ELEMENTS; FEMALE; FRANCISELLA TULARENSIS; GENES, BACTERIAL; LETHAL DOSE 50; LIVER; LUNG; MACROPHAGES; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; MUTAGENESIS, INSERTIONAL; SPLEEN; TULAREMIA; VACCINES, ATTENUATED;

EID: 33748028835     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00598-06     Document Type: Article

References (50)

1. Ausubel, F. M. 2002. Short protocols in molecular biology: a compendium of methods from Current Protocols in Molecular Biology, 5th ed. Wiley, New York, NY.
2. Baron, G. S., and F. E. Nano. 1998. MglA and MglB are required for the intramacrophage growth of Francisella novicida. Mol. Microbiol. 29:247-259.
3. Broekhuijsen, M., P. Larsson, A. Johansson, M. Bystrom, U. Eriksson, E. Larsson, R. G. Prior, A. Sjostedt, R. W. Titball, and M. Forsman. 2003. Genome-wide DNA microarray analysis of Francisella tularensis strains demonstrates extensive genetic conservation within the species but identifies regions that are unique to the highly virulent F. tularensis subsp. tularensis. J. Clin. Microbiol. 41:2924-2931.
4. Chen, W., R. KuoLee, H. Shen, and J. W. Conlan. 2004. Susceptibility of immunodeficient mice to aerosol and systemic infection with virulent strains of Francisella tularensis. Microb. Pathog. 36:311-318.
5. Chen, W., H. Shen, A. Webb, R. KuoLee, and J. W. Conlan. 2003. Tularemia in BALB/c and C57BL/6 mice vaccinated with Francisella tularensis LVS and challenged intradermally or by aerosol with virulent isolates of the pathogen: protection varies depending on pathogen virulence, route of exposure, and host genetic background. Vaccine 21:3690-3700.
6. Conlan, J. W., H. Shen, R. Kuolee, X. Zhao, and W. Chen. 2005. Aerosol- but not intradermal-immunization with the live vaccine strain of Francisella tularensis protects mice against subsequent aerosol challenge with a highly virulent type A strain of the pathogen by an alphabeta T cell- and interferon gamma-dependent mechanism. Vaccine 23:2477-2485.
7. Conlan, J. W., H. Shen, A. Webb, and M. B. Perry. 2002. Mice vaccinated with the O-antigen of Francisella tularensis LVS lipopolysaccharide conjugated to bovine serum albumin develop varying degrees of protective immunity against systemic or aerosol challenge with virulent type A and type B strains of the pathogen. Vaccine 20:3465-3471.
8. Coriell, L. L., E. O. King, and M. G. Smith. 1948. Studies on tularemia IV. Observations on tularemia in control and vaccinated monkeys. J. Immunol. 58:183-202.
9. Cowley, S. C., S. V. Myltseva, and F. E. Nano. 1996. Phase variation in Francisella tularensis affecting intracellular growth, lipopolysaccharide antigenicity and nitric oxide production. Mol. Microbiol. 20:867-874.
10. Dennis, D. T., T. V. Inglesby, D. A. Henderson, J. G. Bartlett, M. S. Ascher, E. Eitzen, A. D. Fine, A. M. Friedlander, J. Hauer, M. Layton, S. R. Lillibridge, J. E. McDade, M. T. Osterholm, T. O'Toole, G. Parker, T. M. Perl, P. K. Russell, and K. Tonat. 2001. Tularemia as a biological weapon: medical and public health management. JAMA 285:2763-2773.
11. Eigelsbach, H. T., and C. M. Downs. 1961. Prophylactic effectiveness of live and killed tularemia vaccines. I. Production of vaccine and evaluation in the white mouse and guinea pig. J. Immunol. 87:415-425.
12. Forslund, A. L., K. Kuoppa, K. Svensson, E. Salomonsson, A. Johansson, M. Bystrom, P. C. Oyston, S. L. Michell, R. W. Titball, L. Noppa, E. Frithz-Lindsten, M. Forsman, and A. Forsberg. 2006. Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis. Mol. Microbiol. 59:1818-1830.
13. Forsman, M., G. Sandstrom, and A. Sjostedt. 1994. Analysis of 16S ribosomal DNA sequences of Francisella strains and utilization for determination of the phylogeny of the genus and for identification of strains by PCR. Int. J. Syst. Bacteriol. 44:38-46.
14. Fortier, A. H., S. J. Green, T. Polsinelli, T. R. Jones, R. M. Crawford, D. A. Leiby, K. L. Elkins, M. S. Meltzer, and C. A. Nacy. 1994. Life and death of an intracellular pathogen: Francisella tularensis and the macrophage. Immunol. Ser. 60:349-361.
15. Fulop, M., R. Manchee, and R. Titball. 1995. Role of lipopolysaccharide and a major outer membrane protein from Francisella tularensis in the induction of immunity against tularemia. Vaccine 13:1220-1225.
16. Fulop, M., P. Mastroeni, M. Green, and R. W. Titball. 2001. Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis. Vaccine 19:4465-4472.
17. Geddes, K., M. Worley, G. Niemann, and F. Heffron. 2005. Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect. Immun. 73:6260-6271.
18. Golovliov, I., A. Sjostedt, A. Mokrievich, and V. Pavlov. 2003. A method for allelic replacement in Francisella tularensis. FEMS Microbiol. Lett. 222:273-280.
19. Goryshin, I. Y., J. Jendrisak, L. M. Hoffman, R. Meis, and W. S. Reznikoff. 2000. Insertional transposon mutagenesis by electroporation of released Tn5 transposition complexes. Nat. Biotechnol. 18:97-100.
20. Gray, C. G., S. C. Cowley, K. K. Cheung, and F. E. Nano. 2002. The identification of five genetic loci of Francisella novicida associated with intracellular growth. FEMS Microbiol. Lett. 215:53-56.
21. Green, M., G. Choules, D. Rogers, and R. W. Titball. 2005. Efficacy of the live attenuated Francisella tularensis vaccine (LVS) in a murine model of disease. Vaccine 23:2680-2686.
22. Isherwood, K. E., R. W. Titball, D. H. Davies, P. L. Felgner, and W. J. Morrow. 2005. Vaccination strategies for Francisella tularensis. Adv. Drug Deliv. Rev. 57:1403-1414.
23. Kadokura, H., F. Katzen, and J. Beckwith. 2003. Protein disulfide bond formation in prokaryotes. Annu. Rev. Biochem. 72:111-135.
24. Kadull, P. J., H. R. Reames, L. L. Coriell, and L. Foshay. 1950. Studies on tularemia. V. Immunization of man. J. Immunol. 65:425-435.
25. Karlsson, J., R. G. Prior, K. Williams, L. Lindler, K. A. Brown, N. Chatwell, K. Hjalmarsson, N. Loman, K. A. Mack, M. Pallen, M. Popek, G. Sandstrom, A. Sjostedt, T. Svensson, I. Taraas, S. G. Andersson, B. W. Wren, P. C. Oyston, and R. W. Titball. 2000. Sequencing of the Francisella tularensis strain Schu 4 genome reveals the shikimate and purine metabolic pathways, targets for the construction of a rationally attenuated auxotrophic vaccine. Microb. Comp. Genomics 5:25-39.
26. Kawula, T. H., J. D. Hall, J. R. Fuller, and R. R. Craven. 2004. Use of transposon-transposase complexes to create stable insertion mutant strains of Francisella tularensis LVS. Appl. Environ. Microbiol. 70:6901-6904.
27. Kleffer, T. L., S. Cowley, F. E. Nano, and K. L. Elkins. 2003. Francisella novicida LPS has greater immunobiological activity in mice than F. tularensis LPS, and contributes to F. novicida murine pathogenesis. Microbes Infect. 5:397-403.
28. Koonin, E. V., and M. Y. Galperin. 2003. Sequence-evolution-function: computational approaches in comparative genomics. Kluwer Academic, Boston, MA.
29. Kudelina, R. I. 1978. Sensitivity of the causative agent of tularemia to antibiotics. Antibiotiki 23:710-714.
30. Kuoppa, K., A. Forsberg, and A. Norqvist. 2001. Construction of a reporter plasmid for screening in vivo promoter activity in Francisella tularensis. FEMS Microbiol. Lett. 205:77-81.
31. Lai, X. H., I. Golovliov, and A. Sjostedt. 2004. Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb. Pathog. 37:225-230.
32. Larsson, P., P. C. Oyston, P. Chain, M. C. Chu, M. Duffield, H. H. Fuxelius, E. Garcia, G. Halltorp, D. Johansson, K. E. Isherwood, P. D. Karp, E. Larsson, Y. Liu, S. Michell, J. Prior, R. Prior, S. Malfatti, A. Sjostedt, K. Svensson, N. Thompson, L. Vergez, J. K. Wagg, B. W. Wren, L. E. Lindler, S. G. Andersson, M. Forsman, and R. W. Titball. 2005. The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat. Genet. 37:153-159.
33. Lauriano, C. M., J. R. Barker, S. S. Yoon, F. E. Nano, B. P. Arulanandam, D. J. Hassett, and K. E. Klose. 2004. MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc. Natl. Acad. Sci. USA 101:4246-4249.
34. McCrumb, F. R. 1961. Aerosol infection of man with Pasteurella tularensis. Bacteriol. Rev. 25:262-267.
35. Nano, F. E., N. Zhang, S. C. Cowley, K. E. Klose, K. K. Cheung, M. J. Roberts, J. S. Ludu, G. W. Letendre, A. I. Meierovics, G. Stephens, and K. L. Elkins. 2004. A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186:6430-6436.
36. Oyston, P. C., and J. E. Quarry. 2005. Tularemia vaccine: past, present and future. Antonie Leeuwenhoek 87:277-281.
37. Pamer, E. G. 2004. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 4:812-823.
38. Pammit, M. A., E. K. Raulie, C. M. Lauriano, K. E. Klose, and B. P. Arulanandam. 2006. Intranasal vaccination with a defined attenuated Francisella novicida strain induces gamma interferon-dependent antibody-mediated protection against tularemia. Infect. Immun. 74:2063-2071.
39. Reed, L. J., and H. Muench. 1935. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 27:493-497.
40. Sam-Yellowe, T. Y. 1992. Molecular factors responsible for host cell recognition and invasion in Plasmodium falciparum. J. Protozool. 39:181-189.
41. Saslaw, S., H. T. Eigelsbach, J. A. Prior, H. E. Wilson, and S. Carhart. 1961. Tularemia vaccine study. II. Respiratory challenge. Arch. Intern. Med. 107:702-714.
42. Shen, H., W. Chen, and J. W. Conlan. 2004. Mice sublethally infected with Francisella novicida U112 develop only marginal protective immunity against systemic or aerosol challenge with virulent type A or B strains off. tularensis. Microb. Pathog. 37:107-110.
43. Shen, H., W. Chen, and J. W. Conlan. 2004. Susceptibility of various mouse strains to systemically- or aerosol-initiated tularemia by virulent type A Francisella tularensis before and after immunization with the attenuated live vaccine strain of the pathogen. Vaccine 22:2116-2121.
44. Tarnvik, A. 1989. Nature of protective immunity to Francisella tularensis. Rev. Infect. Dis. 11:440-451.
45. Tempel, R., K. Geddes, and F. Heffron. 2003. Presented at the Fourth International Conference on Tularemia, Bath, United Kingdom.
46. Tseng, C. P., C. C. Yu, H. H. Lin, C. Y. Chang, and J. T. Kuo. 2001. Oxygen- and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity. J. Bacteriol. 183:461-467.
47. Twine, S., M. Bystrom, W. Chen, M. Forsman, I. Golovliov, A. Johansson, J. Kelly, H. Lindgren, K. Svensson, C. Zingmark, W. Conlan, and A. Sjostedt. 2005. A mutant of Francisella tularensis strain SCHU S4 lacking the ability to express a 58-kilodalton protein is attenuated for virulence and is an effective live vaccine. Infect. Immun. 73:8345-8352.
48. van der Velden, A. W., S. W. Lindgren, M. J. Worley, and F. Heffron. 2000. Salmonella pathogenicity island 1-independent induction of apoptosis in infected macrophages by Salmonella enterica serotype Typhimurium. Infect. Immun. 68:5702-5709.
49. Wu, T. H., J. A. Hutt, K. A. Garrison, L. S. Berliba, Y. Zhou, and C. R. Lyons. 2005. Intranasal vaccination induces protective immunity against intranasal infection with virulent Francisella tularensis biovar A. Infect. Immun. 73:2644-2654.
50. Zusman, T., M. Feldman, E. Halperin, and G. Segal. 2004. Characterization of the icmH and icmF genes required for Legionella pneumophila intracellular growth, genes that are present in many bacteria associated with eukaryotic cells. Infect. Immun. 72:3398-3409.