Deletion of the Bacillus anthracis capB homologue in Francisella tularensis subspecies tularensis generates an attenuated strain that protects mice against virulent tularaemia

Journal of Medical Microbiology

Volumn 59, Issue 11, 2010, Pages 1275-1284

  Michell, Stephen L ^a,b   Dean, Rachel E ^a   Eyles, Jim E ^a,c   Hartley, Margaret Gill ^a   Waters, Emma ^a   Prior, Joann L ^a   Titball, Richard W ^a   Oyston, Petra C F ^a  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^b UNIVERSITY OF EXETER   (United Kingdom)

^c PFIZER GLOBAL RESEARCH AND DEVELOPMENT   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAP BINDING PROTEIN; LIVE VACCINE; TULAREMIA VACCINE; BACTERIAL VACCINE; VIRULENCE FACTOR;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL GENE; BACTERIAL MUTATION; BACTERIAL STRAIN; CELLULAR IMMUNITY; FEMALE; FRANCISELLA TULARENSIS; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUBSPECIES; TULAREMIA; WILD TYPE; AMINO ACID SEQUENCE; ANIMAL; BAGG ALBINO MOUSE; BIOLOGY; GENE DELETION; GENETICS; IMMUNOLOGY; MOLECULAR GENETICS; OPERON; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; SURVIVAL; VIRULENCE;

AMINO ACID SEQUENCE; ANIMALS; BACILLUS ANTHRACIS; BACTERIAL VACCINES; COMPUTATIONAL BIOLOGY; FEMALE; FRANCISELLA TULARENSIS; GENES, BACTERIAL; MICE; MICE, INBRED BALB C; MOLECULAR SEQUENCE DATA; OPERON; SEQUENCE ALIGNMENT; SEQUENCE DELETION; SEQUENCE HOMOLOGY; SURVIVAL ANALYSIS; TULAREMIA; VACCINES, ATTENUATED; VIRULENCE; VIRULENCE FACTORS;

EID: 78049496555     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.018911-0     Document Type: Article

References (44)

1. Alkhuder, K., Meibom, K. L., Dubail, I., Dupuis, M. & Charbit, A. (2009). Glutathione provides a source of cysteine essential for intracellular multiplication of Francisella tularensis. PLoS Pathog 5, e1000284.
2. Anthony, L. S., Ghadirian, E., Nestel, F. P. & Kongshavn, P. A. (1989). The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathog 7, 421-428.
3. Burke, D. S. (1977). Immunization against tularemia: analysis of the effectiveness of live Francisella tularensis vaccine in prevention of laboratory-acquired tularemia. J Infect Dis 135, 55-60.
4. Candela, T. & Fouet, A. (2005). Bacillus anthracis CapD, belonging to the gamma-glutamyltranspeptidase family, is required for the covalent anchoring of capsule to peptidoglycan. Mol Microbiol 57, 717-726.
5. Candela, T. & Fouet, A. (2006). Poly-gamma-glutamate in bacteria. Mol Microbiol 60, 1091-1098.
6. Candela, T., Moya, M., Haustant, M. & Fouet, A. (2009). Fusobacterium nucleatum, the first Gram-negative bacterium demonstrated to produce polyglutamate. Can J Microbiol 55, 627-632.
7. Chamberlain, R. E. (1965). Evaluation of live tularemia vaccine prepared in a chemically defined medium. Appl Microbiol 13, 232-235.
8. Chen, W., Shen, H., Webb, A., KuoLee, R. & Conlan, J. W. (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.
9. Cherwonogrodzky, J. W., Knodel, M. H. & Spence, M. R. (1994). Increased encapsulation and virulence of Francisella tularensis live vaccine strain (LVS) by subculturing on synthetic medium. Vaccine 12, 773-775.
10. + T-cell-dependent and -independent host defense mechanisms can operate to control and resolve primary and secondary Francisella tularensis LVS infection in mice. Infect Immun 62, 5603-5607.
11. Conlan, J. W., Shen, H., Golovliov, I., Zingmark, C., Oyston, P. C., Chen, W., House, R. V. & Sjostedt, A. (2010). Differential ability of novel attenuated targeted deletion mutants of Francisella tularensis subspecies tularensis strain SCHU S4 to protect mice against aerosol challenge with virulent bacteria: effects of host background and route of immunization. Vaccine 28, 1824-1831.
12. Drysdale, M., Heninger, S., Hutt, J., Chen, Y., Lyons, C. R. & Koehler, T. M. (2005). Capsule synthesis by Bacillus anthracis is required for dissemination in murine inhalation anthrax. EMBO J 24, 221-227.
13. Eyles, J. E., Unal, B., Hartley, M. G., Newstead, S. L., Flick-Smith, H., Prior, J. L., Oyston, P. C. F., Randall, A., Mu, Y. & other authors (2007). Immunodominant Francisella tularensis antigens identified using proteome microarray. Proteomics 7, 2172-2183.
14. Fortier, A. H., Slayter, M. V., Ziemba, R., Meltzer, M. S. & Nacy, C. A. (1991). Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect Immun 59, 2922-2928.
15. Golovliov, I., Sjostedt, A., Mokrievich, A. & Pavlov, V. (2003). A method for allelic replacement in Francisella tularensis. FEMS Microbiol Lett 222, 273-280.
16. Hood, A. M. (1977). Virulence factors of Francisella tularensis. J Hyg (Lond) 79, 47-60.
17. Khan, A. S., Morse, S. & Lillibridge, S. (2000). Public-health preparedness for biological terrorism in the USA. Lancet 356, 1179-1182.
18. Kocianova, S., Vuong, C., Yao, Y., Voyich, J. M., Fischer, E. R., DeLeo, F. R. & Otto, M. (2005). Key role of poly-gamma-DL-glutamic acid in immune evasion and virulence of Staphylococcus epidermidis. J Clin Invest 115, 688-694.
19. Larsson, P., Oyston, P. C. F., Chain, P., Chu, M. C., Duffield, M., Fuxelius, H.-H., Garcia, E., Hälltorp, G., Johansson, D. & other authors (2005). The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37, 153-159.
20. T Method. Methods 25, 402-408.
21. Makino, S., Uchida, I., Terakado, N., Sasakawa, C. & Yoshikawa, M. (1989). Molecular characterization and protein analysis of the cap region, which is essential for encapsulation in Bacillus anthracis. J Bacteriol 171, 722-730.
22. McCrumb, F. R. (1961). Aerosol infection of man with Pasteurella tularensis. Bacteriol Rev 25, 262-267.
23. Meibom, K. L., Forslund, A. L., Kuoppa, K., Alkhuder, K., Dubail, I., Dupuis, M., Forsberg, A. & Charbit, A. (2009). Hfq, a novel pleiotropic regulator of virulence-associated genes in Francisella tularensis. Infect Immun 77, 1866-1880.
24. Merabishvili, M., Natidze, M., Rigvava, S., Brusetti, L., Raddadi, N., Borin, S., Chanishvili, N., Tediashvili, M., Sharp, R. & other authors (2006). Diversity of Bacillus anthracis strains in Georgia and of vaccine strains from the former Soviet Union. Appl Environ Microbiol 72, 5631-5636.
25. Norqvist, A., Kuoppa, K. & Sandström, G. (1996). Construction of a shuttle vector for use in Francisella tularensis. FEMS Immunol Med Microbiol 13, 257-260.
26. Olsufiev, N. G., Emelyanova, O. S. & Dunayeva, T. N. (1959). Comparative study of strains of B. tularense in the old and new world and their taxonomy. J Hyg Epidemiol Microbiol Immunol 3, 138-149.
27. Oyston, P. C. (2008). Francisella tularensis: unravelling the secrets of an intracellular pathogen. J Med Microbiol 57, 921-930.
28. Oyston, P. C. (2009). Francisella tularensis vaccines. Vaccine 27, D48-D51.
29. Oyston, P. C. F., Sjöstedt, A. & Titball, R. W. (2004). Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol 2, 967-978.
30. Pechous, R. D., McCarthy, T. R., Mohapatra, N. P., Soni, S., Penoske, R. M., Salzman, N. H., Frank, D. W., Gunn, J. S. & Zahrt, T. C. (2008). A Francisella tularensis Schu S4 purine auxotroph is highly attenuated in mice but offers limited protection against homologous intranasal challenge. PLoS ONE 3, e2487.
31. Qin, A., Scott, D. W. & Mann, B. J. (2008). Francisella tularensis subsp. tularensis Schu S4 disulfide bond formation protein B, but not an RND-type efflux pump, is required for virulence. Infect Immun 76, 3086-3092.
32. Qin, A., Scott, D. W., Thompson, J. A. & Mann, B. J. (2009). Identification of an essential Francisella tularensis subsp. tularensis virulence factor. Infect Immun 77, 152-161.
33. Ravel, J., Jiang, L., Stanley, S. T., Wilson, M. R., Decker, R. S., Read, T. D., Worsham, P., Keim, P. S., Salzberg, S. L. & other authors (2009). The complete genome sequence of Bacillus anthracis Ames "Ancestor". J Bacteriol 191, 445-446.
34. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
35. Sandström, G., Löfgren, S. & Tärnvik, A. (1988). A capsule-deficient mutant of Francisella tularensis LVS exhibits enhanced sensitivity to killing by serum but diminished sensitivity to killing by polymorphonuclear leukocytes. Infect Immun 56, 1194-1202.
36. Saslaw, S., Eigelsbach, H. T., Prior, J. A., Wilson, H. E. & Carhart, S. (1961a). Tularemia vaccine study. II. Respiratory challenge. Arch Intern Med 107, 702-714.
37. Saslaw, S., Eigelsbach, H. T., Wilson, H. E., Prior, J. A. & Carhart, S. (1961b). Tularemia vaccine study. I. Intracutaneous challenge. Arch Intern Med 107, 689-701.
38. Simon, P., Priefer, U. & Pühler, A. (1983). A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Nat Biotechnol 1, 784-791.
39. Straskova, A., Pavkova, I., Link, M., Forslund, A.-L., Kuoppa, K., Noppa, L., Kroca, M., Fucikova, A., Klimentova, J. & other authors (2009). Proteome analysis of an attenuated Francisella tularensis dsbA mutant: identification of potential DsbA substrate proteins. J Proteome Res 8, 5336-5346.
40. Su, J., Yang, J., Zhao, D., Kawula, T. H., Banas, J. A. & Zhang, J. R. (2007). Genome-wide identification of Francisella tularensis virulence determinants. Infect Immun 75, 3089-3101.
41. Tärnvik, A. (1989). Nature of protective immunity to Francisella tularensis. Rev Infect Dis 11, 440-451.
42. Thomas, R. M., Titball, R. W., Oyston, P. C. F., Griffin, K., Waters, E., Hitchen, P. G., Michell, S. L., Grice, I. D., Wilson, J. C. & Prior, J. L. (2007). The immunologically distinct O antigens from Francisella tularensis subspecies tularensis and Francisella novicida are both virulence determinants and protective antigens. Infect Immun 75, 371-378.
43. Twine, S., Byström, M., Chen, W., Forsman, M., Golovliov, I., Johansson, A., Kelly, J., Lindgren, H., Svensson, K. & other authors (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.
44. Weiss, D. S., Brotcke, A., Henry, T., Margolis, J. J., Chan, K. & Monack, D. M. (2007). In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci U S A 104, 6037-6042