1887

Abstract

has been recognized as the causative agent of tularaemia for almost a century. Since its discovery in 1911, it has been shown to infect a wide range of hosts, including humans. As early as the 1920s it was suggested to be an intracellular pathogen, but it has proven to be an enigmatic organism, whose interaction with the host has been difficult to elucidate, and we still have a very limited understanding of the molecular mechanisms of virulence. However, the recent availability of genome sequence data and molecular tools has allowed us to start to understand the molecular basis of pathogenicity, and will facilitate the development of a vaccine to protect against infection.

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2008-08-01
2019-11-14
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References

  1. Ancuta, P., Pedron, T., Girard, R., Sandstrom, G. & Chaby, R. ( 1996; ). Inability of the Francisella tularensis lipopolysaccharide to mimic or to antagonize the induction of the cell activation by endotoxins. Infect Immun 64, 2041–2046.
    [Google Scholar]
  2. Anthony, L. D., Burke, R. D. & Nano, F. E. ( 1991; ). Growth of Francisella spp. in rodent macrophages. Infect Immun 59, 3291–3296.
    [Google Scholar]
  3. Barker, J. H., Weiss, J., Apicella, M. A. & Nauseef, W. M. ( 2006; ). Basis for the failure of Francisella tularensis lipopolysaccharide to prime human polymorphonuclear leukocytes. Infect Immun 74, 3277–3284.[CrossRef]
    [Google Scholar]
  4. Baron, G. S. & Nano, F. E. ( 1998; ). MgIA and MgIB are required for the intramacrophage growth of Francisella novicida. Mol Microbiol 29, 247–259.[CrossRef]
    [Google Scholar]
  5. Baron, G. S. & Nano, F. E. ( 1999; ). An erythromycin resistance cassette and mini-transposon for constructing transcriptional fusions to cat. Gene 229, 59–65.[CrossRef]
    [Google Scholar]
  6. Beckstrom-Sternberg, S. M., Auerbach, R. K., Godbole, S., Pearson, J. V., Beckstrom-Sternberg, J. S., Deng, Z., Munk, C., Kubota, K., Zhou, Y. & other authors ( 2007; ). Complete genomic characterization of a pathogenic A.II strain of Francisella tularensis subspecies tularensis. PLoS ONE 2, e947 [CrossRef]
    [Google Scholar]
  7. Ben Nasr, A., Haithcoat, J., Masterson, J. E., Gunn, J. S., Eaves-Pyles, T. & Klimpel, G. R. ( 2006; ). Critical role for serum opsonins and complement receptors CR3 (CD11b/CD18) and CR4 (CD11c/CD18) in phagocytosis of Francisella tularensis by human dendritic cells (DC): uptake of Francisella leads to activation of immature DC and intracellular survival of the bacteria. J Leukoc Biol 80, 774–786.[CrossRef]
    [Google Scholar]
  8. Bina, X. R., Wang, C., Miller, M. A. & Bina, J. E. ( 2006; ). The Bla2 β-lactamase from the live-vaccine strain of Francisella tularensis encodes a functional protein that is only active against penicillin-class beta-lactam antibiotics. Arch Microbiol 186, 219–228.[CrossRef]
    [Google Scholar]
  9. Boyce, J. M. ( 1975; ). Recent trends in the epidemiology of tularemia in the United States. J Infect Dis 131, 197–199.[CrossRef]
    [Google Scholar]
  10. Brotcke, A., Weiss, D. S., Kim, C. C., Chain, P., Malfatti, S., Garcia, E. & Monack, D. M. ( 2006; ). Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect Immun 74, 6642–6655.[CrossRef]
    [Google Scholar]
  11. Buddingh, G. J. & Womack, F. C., Jr ( 1941; ). Observations on the infection of chick embryos with Bacterium tularense, Brucella, and Pasteurella pestis. J Exp Med 74, 213–222.[CrossRef]
    [Google Scholar]
  12. 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.[CrossRef]
    [Google Scholar]
  13. Checroun, C., Wehrly, T. D., Fischer, E. R., Hayes, S. F. & Celli, J. ( 2006; ). Autophagy-mediated reentry of Francisella tularensis into the endocytic compartment after cytoplasmic replication. Proc Natl Acad Sci U S A 103, 14578–14583.[CrossRef]
    [Google Scholar]
  14. Clemens, D. L., Lee, B. Y. & Horwitz, M. A. ( 2004; ). Virulent and avirulent strains of Francisella tularensis prevent acidification and maturation of their phagosomes and escape into the cytoplasm in human macrophages. Infect Immun 72, 3204–3217.[CrossRef]
    [Google Scholar]
  15. Clemens, D. L., Lee, B. Y. & Horwitz, M. A. ( 2005; ). Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect Immun 73, 5892–5902.[CrossRef]
    [Google Scholar]
  16. Conlan, J. W., Shen, H., Webb, A. & Perry, M. B. ( 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.[CrossRef]
    [Google Scholar]
  17. Councilman, W. T. & Strong, R. P. ( 1921; ). Plague-like infections in rodents. Trans Assoc Am Physicians 36, 135–143.
    [Google Scholar]
  18. Craig, L., Pique, M. E. & Tainer, J. A. ( 2004; ). Type IV pilus structure and bacterial pathogenicity. Nat Rev Microbiol 2, 363–378.[CrossRef]
    [Google Scholar]
  19. de Bruin, O. M., Ludu, J. S. & Nano, F. E. ( 2007; ). The Francisella pathogenicity island protein IglA localizes to the bacterial cytoplasm and is needed for intracellular growth. BMC Microbiol 7, 1 [CrossRef]
    [Google Scholar]
  20. Deng, K., Blick, R. J., Liu, W. & Hansen, E. J. ( 2006; ). Identification of Francisella tularensis genes affected by iron limitation. Infect Immun 74, 4224–4236.[CrossRef]
    [Google Scholar]
  21. Dennis, D. T., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Friedlander, A. M., Hauer, J. & other authors ( 2001; ). Tularemia as a biological weapon: Medical and Public Health Management. JAMA 285, 2763–2773.[CrossRef]
    [Google Scholar]
  22. Dorofe'ev, K. A. ( 1947; ). Classification of the causative agent of tularemia. Symp Res Works Inst Epidemiol Mikrobiol Chita 1, 170–180.
    [Google Scholar]
  23. Ellis, J., Oyston, P. C. F., Green, M. & Titball, R. W. ( 2002; ). Tularemia. Clin Microbiol Rev 15, 631–646.[CrossRef]
    [Google Scholar]
  24. Evans, M. E., Gregory, D. W., Schaffner, W. & McGee, Z. A. ( 1985; ). Tularemia: a 30 year experience with 88 cases. Medicine (Baltimore) 64, 251–269.
    [Google Scholar]
  25. Farlow, J., Wagner, D. M., Dukerich, M., Stanley, M., Chu, M., Kubota, K., Petersen, J. & Keim, P. ( 2005; ). Francisella tularensis in the United States. Emerg Infect Dis 11, 1835–1841.[CrossRef]
    [Google Scholar]
  26. Feldman, K. A., Enscore, R. E., Lathrop, S. L., Matyas, B. T., McGuill, M., Schriefer, M. E., Stiles-Enos, D., Dennis, D. T., Petersen, L. R. & Hayes, E. B. ( 2001; ). An outbreak of primary pneumonic tularemia on Martha's Vineyard. N Engl J Med 345, 1601–1637.[CrossRef]
    [Google Scholar]
  27. Fink, S. L. & Cookson, B. T. ( 2005; ). Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73, 1907–1916.[CrossRef]
    [Google Scholar]
  28. Forsberg, A. & Guina, T. ( 2007; ). Type II secretion and type IV pili of Francisella. Ann N Y Acad Sci 1105, 187–201.[CrossRef]
    [Google Scholar]
  29. Forslund, A. L., Kuoppa, K., Svensson, K., Salomonsson, E., Johansson, A., Byström, M., Oyston, P. C. F., Michell, S. L., Titball, R. W. & other authors ( 2006; ). Direct repeat-mediated deletion of a type IV pilin gene results in major virulence attenuation of Francisella tularensis. Mol Microbiol 59, 1818–1830.[CrossRef]
    [Google Scholar]
  30. Forsman, M., Sandstrom, G. & Sjostedt, A. ( 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.[CrossRef]
    [Google Scholar]
  31. Fortier, A. H., Green, S. J., Polsinelli, T., Jones, T. R., Crawford, R. M., Leiby, D. A., Elkins, K. L., Meltzer, M. S. & Nacy, C. A. ( 1994; ). Life and death of an intracellular pathogen: Francisella tularensis and the macrophage. Immunol Ser 60, 349–361.
    [Google Scholar]
  32. Foshay, L. ( 1950; ). Tularemia. Annu Rev Microbiol 4, 313–330.[CrossRef]
    [Google Scholar]
  33. Foshay, L., Hesselbrock, W. H., Wittenberg, H. J. & Rodenberg, A. H. ( 1942; ). Vaccine prophylaxis against tularemia in man. Am J Public Health 32, 1131–1145.[CrossRef]
    [Google Scholar]
  34. Francis, E. ( 1927; ). Microscopic changes of tularemia in the tick Dermacentor andersoni and the bedbug Cimex lectularius. Public Health Rep 42, 2763–2772.[CrossRef]
    [Google Scholar]
  35. Fulop, M., Manchee, R. & Titball, R. ( 1995; ). Role of lipopolysaccharide and a major outer-membrane protein from Francisella tularensis in the induction of immunity against tularemia. Vaccine 13, 1220–1225.[CrossRef]
    [Google Scholar]
  36. Fulop, M., Mastroeni, P., Green, M. & Titball, R. W. ( 2001; ). Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis. Vaccine 19, 4465–4472.[CrossRef]
    [Google Scholar]
  37. Gallagher, L. A., Ramage, E., Jacobst, M. A., Kaul, R., Brittnacher, M. & Manoil, C. ( 2007; ). A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc Natl Acad Sci U S A 104, 1009–1014.[CrossRef]
    [Google Scholar]
  38. Gil, H., Platz, G. J., Forestal, C. A., Monfett, M., Bakshi, C. S., Seliati, T. J., Furie, M. B., Benach, J. L. & Thanassi, D. G. ( 2006; ). Deletion of TolC orthologs in Francisella tularensis identifies roles in multidrug resistance and virulence. Proc Natl Acad Sci U S A 103, 12897–12902.[CrossRef]
    [Google Scholar]
  39. Golovliov, I., Sjostedt, A., Mokrievich, A. & Pavlov, V. ( 2003; ). A method for allelic replacement in Francisella tularensis. FEMS Microbiol Lett 222, 273–280.[CrossRef]
    [Google Scholar]
  40. Gray, C. G., Cowley, S. C., Cheung, K. K. M. & Nano, F. E. ( 2002; ). The identification of five genetic loci of Francisella novicida associated with intracellular growth. FEMS Microbiol Lett 215, 53–56.[CrossRef]
    [Google Scholar]
  41. Hager, A. J., Bolton, D. L., Pelletier, M. R., Brittnacher, M. J., Gallagher, L. A., Kaul, R., Skerrett, S. J., Miller, S. I. & Guina, T. ( 2006; ). Type IV pili-mediated secretion modulates Francisella virulence. Mol Microbiol 62, 227–237.[CrossRef]
    [Google Scholar]
  42. Hajjar, A. M., Harvey, M. D., Shaffer, S. A., Goodlett, D. R., Sjostedt, A., Edebro, H., Forsman, M., Bystrom, M., Pelletier, M. & other authors ( 2006; ). Lack of in vitro and in vivo recognition of Francisella tularensis subspecies lipopolysaccharide by Toll-like receptors. Infect Immun 74, 6730–6738.[CrossRef]
    [Google Scholar]
  43. Helvaci, S., Gedikoglu, S., Akalin, H. & Oral, H. B. ( 2000; ). Tularemia in Bursa, Turkey: 205 cases in ten years. Eur J Epidemiol 16, 271–276.[CrossRef]
    [Google Scholar]
  44. Hood, A. M. ( 1977; ). Virulence factors of Francisella tularensis. J Hyg (Lond) 79, 47–65.[CrossRef]
    [Google Scholar]
  45. Johansson, A., Ibrahim, A., Goransson, I., Eriksson, U., Gurycova, D., Clarridge, J. E., III & Sjostedt, A. ( 2000; ). Evaluation of PCR-based methods for discrimination of Francisella species and subspecies and development of a specific PCR that distinguishes the two major subspecies of Francisella tularensis. J Clin Microbiol 38, 4180–4185.
    [Google Scholar]
  46. Johansson, A., Berglund, L., Sjostedt, A. & Tarnvik, A. ( 2001; ). Ciprofloxacin for treatment of tularemia. Clin Infect Dis 33, 267–268.
    [Google Scholar]
  47. Johansson, A., Farlow, J., Larsson, P., Dukerich, M., Chambers, E., Bystrom, M., Fox, J., Chu, M., Forsman, M. & other authors ( 2004; ). Worldwide genetic relationships among Francisella tularensis isolates determined by multiple-locus variable-number tandem repeat analysis. J Bacteriol 186, 5808–5818.[CrossRef]
    [Google Scholar]
  48. Kadull, P. J., Reames, H. R., Coriell, L. L. & Foshay, L. ( 1950; ). Studies on tularemia. V. Immunisation of man. J Immunol 65, 425–435.
    [Google Scholar]
  49. Kavanaugh, C. N. ( 1935; ). Tularemia. A consideration of one hundred and twenty-three cases, with observations at autopsy in one. Arch Intern Med 55, 61–85.[CrossRef]
    [Google Scholar]
  50. Kawula, T. H., Hall, J. D., Fuller, J. R. & Craven, R. R. ( 2004; ). Use of transposon-transposase complexes to create stable insertion mutant strains of Francisella tularensis LVS. Appl Environ Microbiol 70, 6901–6904.[CrossRef]
    [Google Scholar]
  51. Keim, P., Johansson, A. & Wagner, D. M. ( 2007; ). Molecular epidemiology, evolution, and ecology of Francisella. Ann N Y Acad Sci 1105, 30–66.[CrossRef]
    [Google Scholar]
  52. Lai, X. H., Golovliov, I. & Sjostedt, A. ( 2001; ). Francisella tularensis induces cytopathogenicity and apoptosis in murine macrophages via a mechanism that requires intracellular bacterial multiplication. Infect Immun 69, 4691–4694.[CrossRef]
    [Google Scholar]
  53. Lai, X. H., Golovliov, I. & Sjostedt, A. ( 2004; ). Expression of IglC is necessary for intracellular growth and induction of apoptosis in murine macrophages by Francisella tularensis. Microb Pathog 37, 225–230.[CrossRef]
    [Google Scholar]
  54. Larsson, P., Oyston, P. C. F., Chain, P., Chu, M., Duffield, M. L., Gabbert, N. M., Fuxelius, H. H., Garcia, E., Halltorp, G. & other authors ( 2005; ). The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 37, 153–159.[CrossRef]
    [Google Scholar]
  55. Lauriano, C. M., Barker, J. R., Nano, F. E., Arulanandarn, B. P. & Klose, K. E. ( 2003; ). Allelic exchange in Francisella tularensis using PCR products. FEMS Microbiol Lett 229, 195–202.[CrossRef]
    [Google Scholar]
  56. Lauriano, C. M., Barker, J. R., Yoon, S. S., Nano, F. E., Arulanandam, B. P., Hassettt, D. J. & Klose, K. E. ( 2004; ). MglA regulates transcription of virulence factors necessary for Francisella tularensis intraamoebae and intramacrophage survival. Proc Natl Acad Sci U S A 101, 4246–4249.[CrossRef]
    [Google Scholar]
  57. Lee, B. Y., Horwitz, M. A. & Clemens, D. L. ( 2006; ). Identification, recombinant expression, immuno localization in macrophages, and T-cell responsiveness of the major extracellular proteins of Francisella tularensis. Infect Immun 74, 4002–4013.[CrossRef]
    [Google Scholar]
  58. Levesque, B., de Serres, G., Higgins, R., D'Halewyn, M. A., Atsorb, H., Grondin, J., Major, M., Garvie, M. & Duval, B. ( 1995; ). Seroepidemiologic study of three zoonoses (leptospirosis, Q fever, and tularemia) among trappers in Québec, Canada. Clin Diagn Lab Immunol 2, 496–498.
    [Google Scholar]
  59. Lindemann, S. R., McLendon, M. K., Apicella, M. A. & Jones, B. D. ( 2007; ). An in vitro model system used to study adherence and invasion of Francisella tularensis live vaccine strain in nonphagocytic cells. Infect Immun 75, 3178–3182.[CrossRef]
    [Google Scholar]
  60. LoVullo, E. D., Sherrill, L. A., Perez, L. L. & Pavelka, M. S. ( 2006; ). Genetic tools for highly pathogenic Francisella tularensis subsp. tularensis. Microbiology 152, 3425–3435.[CrossRef]
    [Google Scholar]
  61. Maier, T. M., Havig, A., Casey, M., Nano, F. E., Frank, D. W. & Zahrt, T. C. ( 2004; ). Construction and characterisation of a highly efficient Francisella shuttle plasmid. Appl Environ Microbiol 70, 7511–7519.[CrossRef]
    [Google Scholar]
  62. Maier, T. M., Pechous, R., Casey, M., Zahrt, T. C. & Frank, D. W. ( 2006; ). In vivo Himar1-based transposon mutagenesis of Francisella tularensis. Appl Environ Microbiol 72, 1878–1885.[CrossRef]
    [Google Scholar]
  63. Maier, T. M., Casey, M., Becker, R., Dorsey, C., Glass, E., Maltsev, N., Zahrt, T. C. & Frank, D. W. ( 2007; ). Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 75, 5376–5389.[CrossRef]
    [Google Scholar]
  64. Malik, M., Bakshi, C. S., Sahay, B., Shah, A., Lotz, S. A. & Sellati, T. J. ( 2006; ). Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis. Infect Immun 74, 3657–3662.[CrossRef]
    [Google Scholar]
  65. Malik, M., Bakshi, C. S., McCabe, K., Catlett, S. V., Shah, A., Singh, R., Jackson, P. L., Gaggar, A., Metzger, D. W. & other authors ( 2007; ). Matrix metalloproteinase 9 activity enhances host susceptibility to pulmonary infection with type A and B strains of Francisella tularensis. J Immunol 178, 1013–1020.[CrossRef]
    [Google Scholar]
  66. Mariathasan, S., Weiss, D. S., Dixit, V. M. & Monack, D. M. ( 2005; ). Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202, 1043–1049.[CrossRef]
    [Google Scholar]
  67. Matyas, B. T., Nieder, H. S. & Telford, S. R., III ( 2007; ). Pneumonic tularemia on Martha's Vineyard - clinical, epidemiologic, and ecological characteristics. Ann N Y Acad Sci 1105, 351–377.[CrossRef]
    [Google Scholar]
  68. McCaffrey, R. L. & Allen, L.-A. H. ( 2006; ). Pivotal advance: Francisella tularensis LVS evades killing by human neutrophils via inhibition of the respiratory burst and phagosome escape. J Leukoc Biol 80, 1224–1230.[CrossRef]
    [Google Scholar]
  69. McCoy, G. W. & Chapin, C. W. ( 1912; ). Further observations on a plague-like disease of rodents with a preliminary note on the causative agent, Bacterium tularense. J Infect Dis 10, 61–72.[CrossRef]
    [Google Scholar]
  70. McCrumb, F. R. ( 1961; ). Aerosol infection of man with Pasteurella tularensis. Bacteriol Rev 25, 262–267.
    [Google Scholar]
  71. Mecsas, J., Bilis, I. & Falkow, S. ( 2001; ). Identification of attenuated Yersinia pseudotuberculosis strains and characterization of an orogastric infection in BALB/c mice on day 5 postinfection by signature-tagged mutagenesis. Infect Immun 69, 2779–2787.[CrossRef]
    [Google Scholar]
  72. Milne, T. S., Michell, S. L., Diaper, H., Wikstrom, P., Svensson, K., Oyston, P. C. F. & Titball, R. W. ( 2007; ). A 55 kDa hypothetical membrane protein is an iron-regulated virulence factor of Francisella tularensis subsp. novicida U112. J Med Microbiol 56, 1268–1276.[CrossRef]
    [Google Scholar]
  73. Mohapatra, N. P., Balagopal, A., Soni, S., Schlesinger, L. S. & Gunn, J. S. ( 2007; ). AcpA is a Francisella acid phosphatase that affects intramacrophage survival and virulence. Infect Immun 75, 390–396.[CrossRef]
    [Google Scholar]
  74. Mörner, T. ( 1992; ). The ecology of tularemia. Rev Sci Tech 11, 1123–1130.
    [Google Scholar]
  75. Mougous, J. D., Cuff, M. E., Raunser, S., Shen, A., Zhou, M., Gifford, C. A., Goodman, A. L., Joachimiak, G., Ordonez, C. L. & other authors ( 2006; ). A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312, 1526–1530.[CrossRef]
    [Google Scholar]
  76. Nano, F. E., Zhang, N., Cowley, S. C., Klose, K. E., Cheung, K. K. M., Roberts, M. J., Ludu, J. S., Letendre, G. W., Meierovics, A. I. & other authors ( 2004; ). A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 186, 6430–6436.[CrossRef]
    [Google Scholar]
  77. Nylund, A., Ottem, K. F., Watanabe, K., Karlsbakk, E. & Krossoy, B. ( 2006; ). Francisella sp (family Francisellaceae) causing mortality in Norwegian cod (Gadus morhua) farming. Arch Microbiol 185, 383–392.[CrossRef]
    [Google Scholar]
  78. Ohara, Y., Sato, T., Fujita, H., Ueno, T. & Homma, M. ( 1991; ). Clinical manifestations of tularemia in Japan - analysis of 1355 cases observed between 1924 and 1987. Infection 19, 14–17.[CrossRef]
    [Google Scholar]
  79. Ostland, V. E., Stannard, J. A., Creek, J. J., Hedrick, R. P., Ferguson, H. W., Carlberg, J. M. & Westerman, M. E. ( 2006; ). Aquatic Francisella-like bacterium associated with mortality of intensively cultured hybrid striped bass Morone chrysops × M. saxatilis. Dis Aquat Organ 72, 135–145.[CrossRef]
    [Google Scholar]
  80. Oyston, P. C. F., Sjostedt, A. & Titball, R. W. ( 2004; ). Tularemia: bioterrorism defence renews interest in Francisella tularensis. Nat Rev Microbiol 2, 967–978.[CrossRef]
    [Google Scholar]
  81. Petrosino, J. F., Xiang, Q., Karpathy, S. E., Jiang, H. Y., Yerrapragada, S., Liu, Y. M., Gioia, J., Hemphill, L., Gonzalez, A. & other authors ( 2006; ). Chromosome rearrangement and diversification of Francisella tularensis revealed by the type B (OSU18) genome sequence. J Bacteriol 188, 6977–6985.[CrossRef]
    [Google Scholar]
  82. Phillips, N. J., Schilling, B., McLendon, M. K., Apicella, M. A. & Gibson, B. W. ( 2004; ). Novel modification of lipid A of Francisella tularensis. Infect Immun 72, 5340–5348.[CrossRef]
    [Google Scholar]
  83. Prior, J. L., Prior, R. G., Hitchen, P. G., Diaper, H., Griffin, K. F., Morris, H. R., Dell, A. & Titball, R. W. ( 2003; ). Characterization of the O antigen gene cluster and structural analysis of the O antigen of Francisella tularensis subsp. tularensis. J Med Microbiol 52, 845–851.[CrossRef]
    [Google Scholar]
  84. Pukatzki, S., Ma, A. T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W. C., Heidelberg, J. F. & Mekalanos, J. J. ( 2006; ). Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103, 1528–1533.[CrossRef]
    [Google Scholar]
  85. Qin, A. & Mann, B. J. ( 2006; ). Identification of transposon insertion mutants of Francisella tularensis tularensis strain Schu S4 deficient in intracellular replication in the hepatic cell line HepG2. BMC Microbiol 6, 69 [CrossRef]
    [Google Scholar]
  86. Rahhal, R. M., Bush, T. J. V., McLendon, M. K., Apicella, M. A. & Bishop, G. A. ( 2007; ). Differential effects of Francisella tularensis lipopolysaccharide on B lymphocytes. J Leukoc Biol 82, 813–820.[CrossRef]
    [Google Scholar]
  87. Rasko, D. A., Esteban, C. D. & Sperandio, V. ( 2007; ). Development of novel plasmid vectors and a promoter trap system in Francisella tularensis compatible with the pFLN10 based plasmids. Plasmid 58, 159–166.[CrossRef]
    [Google Scholar]
  88. Raynaud, C., Meibom, K. L., Lety, M. A., Dubail, I., Candela, T., Frapy, E. & Charbit, A. ( 2007; ). Role of the wbt locus of Francisella tularensis in lipopolysaccharide O-antigen biogenesis and pathogenicity. Infect Immun 75, 536–541.[CrossRef]
    [Google Scholar]
  89. Reilly, T. J., Baron, G. S., Nano, F. E. & Kuhlenschmidt, M. S. ( 1996; ). Characterization and sequencing of a respiratory burst-inhibiting acid phosphatase from Francisella tularensis. J Biol Chem 271, 10973–10983.[CrossRef]
    [Google Scholar]
  90. Rohmer, L., Brittnacher, M., Svensson, K., Buckley, D., Haugen, E., Zhou, Y., Chang, J., Levy, R., Hayden, H. & other authors ( 2006; ). Potential source of Francisella tularensis live vaccine strain attenuation determined by genome comparison. Infect Immun 74, 6895–6906.[CrossRef]
    [Google Scholar]
  91. Sandstrom, G., Sjostedt, A., Johansson, T., Kuoppa, K. & Williams, J. C. ( 1992; ). Immunogenicity and toxicity of lipopolysaccharide from Francisella tularensis LVS. FEMS Microbiol Immunol 5, 201–210.
    [Google Scholar]
  92. Santic, M., Molmeret, M., Barker, J. R., Klose, K. E., Dekanic, A., Doric, M. & Abu Kwaik, Y. ( 2007; ). A Francisella tularensis pathogenicity island protein essential for bacterial proliferation within the host cell cytosol. Cell Microbiol 9, 2391–2403.[CrossRef]
    [Google Scholar]
  93. Santic, M., Asare, R., Skrobonja, I., Jones, S. & Kwaik, Y. A. ( 2008; ). Acquisition of the vATPase proton pump and phagosome acidification is essential for escape of Francisella tularensis into the macrophage cytosol. Infect Immun in press
    [Google Scholar]
  94. Shen, H., Chen, W. X. & Conlan, J. W. ( 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 of F. tularensis. Microb Pathog 37, 107–110.[CrossRef]
    [Google Scholar]
  95. Shepard, C. C. ( 1959; ). Nonacid-fast bacteria and HeLa cells: their uptake and subsequent intracellular growth. J Bacteriol 77, 701–714.
    [Google Scholar]
  96. Sjostedt, A. ( 2005; ). Family XVII. Francisellaceae, genus I. Francisella. In Bergey's Manual of Systematic Bacteriology, pp. 200–210. Edited by D. J. Brenner, N. R. Krieg, J. T. Staley & G. M. Garrity. New York: Springer.
  97. Sjostedt, A. ( 2007; ). Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann N Y Acad Sci 1105, 1–29.[CrossRef]
    [Google Scholar]
  98. Staples, J. E., Kubota, K. A., Chalcraft, L. G., Mead, P. S. & Petersen, J. M. ( 2006; ). Epidemiologic and molecular analysis of human tularemia, United States, 1964–2004. Emerg Infect Dis 12, 1113–1118.[CrossRef]
    [Google Scholar]
  99. Steinemann, T. L., Sheikholeslami, M. R., Brown, H. H. & Bradsher, R. W. ( 1999; ). Oculoglandular tularemia. Arch Ophthalmol 117, 132–133.[CrossRef]
    [Google Scholar]
  100. Stewart, S. J. ( 1996; ). Tularemia: association with hunting and farming. FEMS Immunol Med Microbiol 13, 197–199.[CrossRef]
    [Google Scholar]
  101. Stover, C. K., Pham, X. Q., Erwin, A. L., Mizoguchi, S. D., Warrener, P., Hickey, M. J., Brinkman, F. S. L., Hufnagle, W. O., Kowalik, D. J. & other authors ( 2000; ). Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406, 959–964.[CrossRef]
    [Google Scholar]
  102. 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.[CrossRef]
    [Google Scholar]
  103. Syrjala, H., Kujala, P., Myllyla, V. & Salminen, A. ( 1985; ). Airborne transmission of tularemia in farmers. Scand J Infect Dis 17, 371–375.
    [Google Scholar]
  104. Syrjala, H., Schildt, R. & Raisainen, S. ( 1991; ). In vitro susceptibility of Francisella tularensis to fluoroquinolones and treatment of tularemia with norfloxacin and ciprofloxacin. Eur J Clin Microbiol Infect Dis 10, 68–70.[CrossRef]
    [Google Scholar]
  105. Tarnvik, A. ( 1989; ). Nature of protective immunity to Francisella tularensis. Rev Infect Dis 11, 440–451.[CrossRef]
    [Google Scholar]
  106. Tarnvik, A. & Chu, M. C. ( 2007; ). New approaches to diagnosis and therapy of tularemia. Ann N Y Acad Sci 1105, 378–404.[CrossRef]
    [Google Scholar]
  107. Tarnvik, A., Sandstrom, G. & Sjostedt, A. ( 1996; ). Epidemiological analysis of tularemia in Sweden 1931–1993. FEMS Immunol Med Microbiol 13, 201–204.
    [Google Scholar]
  108. Telepnev, M., Golovliov, I., Grundstrom, T., Tarnvik, A. & Sjostedt, A. ( 2003; ). Francisella tularensis inhibits Toll-like receptor-mediated activation of intracellular signalling and secretion of TNF-α and IL-1 from murine macrophages. Cell Microbiol 5, 41–51.[CrossRef]
    [Google Scholar]
  109. Tempel, R., Lai, X. H., Crosa, L., Kozlowicz, B. & Heffron, F. ( 2006; ). Attenuated Francisella novicida transposon mutants protect mice against wild-type challenge. Infect Immun 74, 5095–5105.[CrossRef]
    [Google Scholar]
  110. Thakran, S., Li, H., Lavine, C. L., Miller, M. A., Bina, J. E., Bina, X. R. & Re, F. ( 2007; ). Identification of Francisella tularensis lipoproteins that stimulate the Toll-like receptor (TLR) 2/TLR1 heterodimer. J Biol Chem 283, 3751–3760.
    [Google Scholar]
  111. 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.[CrossRef]
    [Google Scholar]
  112. Titball, R. W. & Petrosino, J. F. ( 2007; ). Francisella tularensis genomics and proteomics. Ann N Y Acad Sci 1105, 98–121.[CrossRef]
    [Google Scholar]
  113. Titball, R. W., Sjostedt, A. & Pavelka, M. S., Jr & Nano, F. E. ( 2007; ). Biosafety and selectable markers. Francisella tularensis: biology, pathogenicity, epidemiology, and biodefense. Ann N Y Acad Sci 1105, 405–417.[CrossRef]
    [Google Scholar]
  114. Twine, S., Bystrom, M., Chen, W. X., 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.[CrossRef]
    [Google Scholar]
  115. Vinogradov, E., Perry, M. B. & Conlan, J. W. ( 2002; ). Structural analysis of Francisella tularensis lipopolysaccharide. Eur J Biochem 269, 6112–6118.[CrossRef]
    [Google Scholar]
  116. Vinogradov, E., Conlan, W., Gunn, J. S. & Perry, M. B. ( 2004; ). Characterisation of the lipopolysaccharide O-antigen of Francisella novicida. Carbohydr Res 339, 649–654.[CrossRef]
    [Google Scholar]
  117. Wang, X., Ribeiro, A. A., Guan, Z., McGrath, S. C., Cotter, R. J. & Raetz, C. R. H. ( 2006; ). Structure and biosynthesis of free lipid A molecules that replace lipopolysaccharide in Francisella tularensis subsp. novicida. Biochemistry 45, 14427–14440.[CrossRef]
    [Google Scholar]
  118. 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.[CrossRef]
    [Google Scholar]
  119. Whipp, M. J., Davis, J. M., Lum, G., de Boer, J., Zhou, Y., Bearden, S. W., Petersen, J. M., Chu, M. C. & Hogg, G. ( 2003; ). Characterization of a novicida-like subspecies of Francisella tularensis isolated in Australia. J Med Microbiol 52, 839–842.[CrossRef]
    [Google Scholar]
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