Generation of a convalescent model of virulent francisella tularensis infection for assessment of host requirements for survival of tularemia

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Crane, Deborah D ^a   Scott, Dana P ^a   Bosio, Catharine M ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC AGENT; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; LEVOFLOXACIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; ANTIINFECTIVE AGENT; LYMPHOCYTE ANTIGEN RECEPTOR;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FRANCISELLA TULARENSIS; IMMUNE RESPONSE; IMMUNE SYSTEM; INTRACELLULAR BACTERIUM; LOW DRUG DOSE; MOUSE; NATURAL KILLER CELL; NONHUMAN; TULAREMIA; ANALYSIS OF VARIANCE; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; CELLULAR IMMUNITY; DISEASE MODEL; FLOW CYTOMETRY; IMMUNOLOGY; KINETICS; METABOLISM; T LYMPHOCYTE;

ANIMALIA; BACTERIA (MICROORGANISMS); FRANCISELLA TULARENSIS; MUS;

ANALYSIS OF VARIANCE; ANIMALS; ANTI-BACTERIAL AGENTS; B-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; IMMUNITY, CELLULAR; INTERFERON-GAMMA; INTERLEUKIN-12; KINETICS; MICE; MICE, INBRED C57BL; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTES; TULAREMIA;

EID: 84858022942     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033349     Document Type: Article

References (89)

1. Wenger JD, Hollis DG, Weaver RE, Baker CN, Brown GR, et al. (1989) Infection caused by Francisella philomiragia (formerly Yersinia philomiragia). A newly recognized human pathogen. Ann Intern Med 110: 888-892.
2. Olsufjev NG, Meshcheryakova IS, (1982) Infraspecific taxonomy of tularemia agent Francisella tularensis McCoy et Chapin. J Hyg Epidemiol Microbiol Immunol 26: 291-299.
3. Chen W, Shen H, Webb A, KuoLee R, Conlan JW, (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.
4. Sjostedt A, eds. (2005) (2005) Francisella New York Springer pp. 200-210.
5. Eigelsbach HT, Downs CM, (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.
6. Anthony LS, Kongshavn PA, (1987) Experimental murine tularemia caused by Francisella tularensis, live vaccine strain: a model of acquired cellular resistance. Microb Pathog 2: 3-14.
7. McCoy GW, Chapin CW, (1912) Bacterium tularense the cause of a plague-like disease of rodents. Journal if Infectious Diseases 10: 17-23.
8. McCrumb FR, (1961) Aerosol Infection of Man with Pasteurella Tularensis. Bacteriol Rev 25: 262-267.
9. Bosio CM, Bielefeldt-Ohmann H, Belisle JT, (2007) Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J Immunol 178: 4538-4547.
10. Tarnvik A, Berglund L, (2003) Tularaemia. Eur Respir J 21: 361-373.
11. Anthony LD, Burke RD, Nano FE, (1991) Growth of Francisella spp. in rodent macrophages. Infect Immun 59: 3291-3296.
12. Clemens DL, Lee BY, Horwitz MA, (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.
13. Chase JC, Bosio CM, (2010) The presence of CD14 overcomes evasion of innate immune responses by virulent Francisella tularensis in human dendritic cells in vitro and pulmonary cells in vivo. Infect Immun 78: 154-167.
14. Chase JC, Celli J, Bosio CM, (2009) Direct and indirect impairment of human dendritic cell function by virulent Francisella tularensis Schu S4. Infect Immun 77: 180-195.
15. Hall JD, Woolard MD, Gunn BM, Craven RR, Taft-Benz S, et al. (2008) Infected-host-cell repertoire and cellular response in the lung following inhalation of Francisella tularensis Schu S4, LVS, or U112. Infect Immun 76: 5843-5852.
16. Huang MT, Mortensen BL, Taxman DJ, Craven RR, Taft-Benz S, et al. (2010) Deletion of ripA alleviates suppression of the inflammasome and MAPK by Francisella tularensis. J Immunol 185: 5476-5485.
17. Ben Nasr A, Haithcoat J, Masterson JE, Gunn JS, Eaves-Pyles T, et al. (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.
18. Butchar JP, Cremer TJ, Clay CD, Gavrilin MA, Wewers MD, et al. (2008) Microarray analysis of human monocytes infected with Francisella tularensis identifies new targets of host response subversion. PLoS ONE 3: e2924.
19. Parsa KV, Ganesan LP, Rajaram MV, Gavrilin MA, Balagopal A, et al. (2006) Macrophage pro-inflammatory response to Francisella novicida infection is regulated by SHIP. PLoS Pathog 2: e71.
20. Bauler TJ, Chase JC, Bosio CM, (2011) IFN-{beta} Mediates Suppression of IL-12p40 in Human Dendritic Cells following Infection with Virulent Francisella tularensis. J Immunol 187: 1845-1855.
21. Crane DD, Warner SL, Bosio CM, (2009) A novel role for plasmin-mediated degradation of opsonizing antibody in the evasion of host immunity by virulent, but not attenuated, Francisella tularensis. J Immunol 183: 4593-4600.
22. Elkins KL, Cooper A, Colombini SM, Cowley SC, Kieffer TL, (2002) In vivo clearance of an intracellular bacterium, Francisella tularensis LVS, is dependent on the p40 subunit of interleukin-12 (IL-12) but not on IL-12 p70. Infect Immun 70: 1936-1948.
23. Duckett NS, Olmos S, Durrant DM, Metzger DW, (2005) Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect Immun 73: 2306-2311.
24. Shirey KA, Cole LE, Keegan AD, Vogel SN, (2008) Francisella tularensis live vaccine strain induces macrophage alternative activation as a survival mechanism. J Immunol 181: 4159-4167.
25. Ketavarapu JM, Rodriguez AR, Yu JJ, Cong Y, Murthy AK, et al. (2008) Mast cells inhibit intramacrophage Francisella tularensis replication via contact and secreted products including IL-4. Proc Natl Acad Sci U S A 105: 9313-9318.
26. KuoLee R, Zhou H, Harris G, Zhao X, Qiu H, et al. (2008) Inhibition of airway eosinophilia and pulmonary pathology in a mouse model of allergic asthma by the live vaccine strain of Francisella tularensis. Clin Exp Allergy 38: 1003-1015.
27. 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-alpha and IL-1 from murine macrophages. Cell Microbiol 5: 41-51.
28. Cole LE, Elkins KL, Michalek SM, Qureshi N, Eaton LJ, et al. (2006) Immunologic consequences of Francisella tularensis live vaccine strain infection: role of the innate immune response in infection and immunity. J Immunol 176: 6888-6899.
29. Cole LE, Santiago A, Barry E, Kang TJ, Shirey KA, et al. (2008) Macrophage proinflammatory response to Francisella tularensis live vaccine strain requires coordination of multiple signaling pathways. J Immunol 180: 6885-6891.
30. Ulland TK, Buchan BW, Ketterer MR, Fernandes-Alnemri T, Meyerholz DK, et al. (2010) Cutting edge: mutation of Francisella tularensis mviN leads to increased macrophage absent in melanoma 2 inflammasome activation and a loss of virulence. J Immunol 185: 2670-2674.
31. Conlan JW, KuoLee R, Shen H, Webb A, (2002) Different host defences are required to protect mice from primary systemic vs pulmonary infection with the facultative intracellular bacterial pathogen, Francisella tularensis LVS. Microb Pathog 32: 127-134.
32. Conlan JW, Sjostedt A, North RJ, (1994) CD4+ and CD8+ 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.
33. Elkins KL, Rhinehart-Jones TR, Culkin SJ, Yee D, Winegar RK, (1996) Minimal requirements for murine resistance to infection with Francisella tularensis LVS. Infect Immun 64: 3288-3293.
34. Wayne Conlan J, Shen H, Kuolee R, Zhao X, Chen W, (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.
35. Malik M, Bakshi CS, McCabe K, Catlett SV, Shah A, et al. (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.
36. Klimpel GR, Eaves-Pyles T, Moen ST, Taormina J, Peterson JW, et al. (2008) Levofloxacin rescues mice from lethal intra-nasal infections with virulent Francisella tularensis and induces immunity and production of protective antibody. Vaccine 26: 6874-6882.
37. Aranda EA, (2001) Treatment of tularemia with levofloxacin. Clin Microbiol Infect 7: 167-168.
38. Foshay L, (1946) A Comparative Study of the Treatment of Tularemia with Immune Serum, Hyperimmune Serum and Streptomycin. American Jorunal of Medicine 1: 180-188.
39. Mc CF Jr, Snyder MJ, Woodward TE, (1957) Studies on human infection with Pasteurella tularensis; comparison of streptomycin and chloramphenicol in the prophylaxis of clinical disease. Trans Assoc Am Physicians 70: 74-79; discussion 79-80.
40. Chen W, KuoLee R, Shen H, Busa M, Conlan JW, (2004) Toll-like receptor 4 (TLR4) does not confer a resistance advantage on mice against low-dose aerosol infection with virulent type A Francisella tularensis. Microb Pathog 37: 185-191.
41. Chen W, KuoLee R, Shen H, Conlan JW, (2004) Susceptibility of immunodeficient mice to aerosol and systemic infection with virulent strains of Francisella tularensis. Microb Pathog 36: 311-318.
42. Zhang D, Kuolee R, Harris G, Zhang Q, Conlan JW, et al. (2008) Lymphotoxin-alpha plays only a minor role in host resistance to respiratory infection with virulent type A Francisella tularensis in mice. Mediators Inflamm 2008: 239740.
43. Conlan JW, Chen W, Shen H, Webb A, KuoLee R, (2003) Experimental tularemia in mice challenged by aerosol or intradermally with virulent strains of Francisella tularensis: bacteriologic and histopathologic studies. Microb Pathog 34: 239-248.
44. Bosio CM, Elkins KL, (2001) Susceptibility to secondary Francisella tularensis live vaccine strain infection in B-cell-deficient mice is associated with neutrophilia but not with defects in specific T-cell-mediated immunity. Infect Immun 69: 194-203.
45. Elkins KL, Bosio CM, Rhinehart-Jones TR, (1999) Importance of B cells, but not specific antibodies, in primary and secondary protective immunity to the intracellular bacterium Francisella tularensis live vaccine strain. Infect Immun 67: 6002-6007.
46. Yee D, Rhinehart-Jones TR, Elkins KL, (1996) Loss of either CD4+ or CD8+ T cells does not affect the magnitude of protective immunity to an intracellular pathogen, Francisella tularensis strain LVS. J Immunol 157: 5042-5048.
47. Andersson H, Hartmanova B, Kuolee R, Ryden P, Conlan W, et al. (2006) Transcriptional profiling of host responses in mouse lungs following aerosol infection with type A Francisella tularensis. J Med Microbiol 55: 263-271.
48. Sharma J, Mares CA, Li Q, Morris EG, Teale JM, Features of sepsis caused by pulmonary infection with Francisella tularensis Type A strain. Microb Pathog 51: 39-47.
49. Trinchieri G, (1995) Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu Rev Immunol 13: 251-276.
50. Fortier AH, Polsinelli T, Green SJ, Nacy CA, (1992) Activation of macrophages for destruction of Francisella tularensis: identification of cytokines, effector cells, and effector molecules. Infect Immun 60: 817-825.
51. Ireland R, Olivares-Zavaleta N, Warawa JM, Gherardini FC, Jarrett C, et al. (2010) Effective, broad spectrum control of virulent bacterial infections using cationic DNA liposome complexes combined with bacterial antigens. PLoS Pathog 6: e1000921.
52. Lindgren H, Shen H, Zingmark C, Golovliov I, Conlan W, et al. (2007) Resistance of Francisella tularensis strains against reactive nitrogen and oxygen species with special reference to the role of KatG. Infect Immun 75: 1303-1309.
53. Novelli F, Casanova JL, (2004) The role of IL-12, IL-23 and IFN-gamma in immunity to viruses. Cytokine Growth Factor Rev 15: 367-377.
54. Reljic R, (2007) IFN-gamma therapy of tuberculosis and related infections. J Interferon Cytokine Res 27: 353-364.
55. Cowley SC, Meierovics AI, Frelinger JA, Iwakura Y, Elkins KL, (2010) Lung CD4-CD8- double-negative T cells are prominent producers of IL-17A and IFN-gamma during primary respiratory murine infection with Francisella tularensis live vaccine strain. J Immunol 184: 5791-5801.
56. Lin Y, Ritchea S, Logar A, Slight S, Messmer M, et al. (2009) Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31: 799-810.
57. Lopez MC, Duckett NS, Baron SD, Metzger DW, (2004) Early activation of NK cells after lung infection with the intracellular bacterium, Francisella tularensis LVS. Cell Immunol 232: 75-85.
58. Woolard MD, Hensley LL, Kawula TH, Frelinger JA, (2008) Respiratory Francisella tularensis live vaccine strain infection induces Th17 cells and prostaglandin E2, which inhibits generation of gamma interferon-positive T cells. Infect Immun 76: 2651-2659.
59. Harty JT, Bevan MJ, (1995) Specific immunity to Listeria monocytogenes in the absence of IFN gamma. Immunity 3: 109-117.
60. Cooper AM, Dalton DK, Stewart TA, Griffin JP, Russell DG, et al. (1993) Disseminated tuberculosis in interferon gamma gene-disrupted mice. J Exp Med 178: 2243-2247.
61. Buchmeier NA, Schreiber RD, (1985) Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc Natl Acad Sci U S A 82: 7404-7408.
62. Denis M, (1991) Involvement of cytokines in determining resistance and acquired immunity in murine tuberculosis. J Leukoc Biol 50: 495-501.
63. Santic M, Molmeret M, Abu Kwaik Y, (2005) Modulation of biogenesis of the Francisella tularensis subsp. novicida-containing phagosome in quiescent human macrophages and its maturation into a phagolysosome upon activation by IFN-gamma. Cell Microbiol 7: 957-967.
64. Lindgren H, Golovliov I, Baranov V, Ernst RK, Telepnev M, et al. (2004) Factors affecting the escape of Francisella tularensis from the phagolysosome. J Med Microbiol 53: 953-958.
65. Henry T, Kirimanjeswara GS, Ruby T, Jones JW, Peng K, et al. (2010) Type I IFN signaling constrains IL-17A/F secretion by gammadelta T cells during bacterial infections. J Immunol 184: 3755-3767.
66. Pappu R, Ramirez-Carrozzi V, Sambandam A, (2011) The interleukin-17 cytokine family: critical players in host defence and inflammatory diseases. Immunology.
67. Kaufmann SH, Ladel CH, (1994) Role of T cell subsets in immunity against intracellular bacteria: experimental infections of knock-out mice with Listeria monocytogenes and Mycobacterium bovis BCG. Immunobiology 191: 509-519.
68. Ladel CH, Flesch IE, Arnoldi J, Kaufmann SH, (1994) Studies with MHC-deficient knock-out mice reveal impact of both MHC I- and MHC II-dependent T cell responses on Listeria monocytogenes infection. J Immunol 153: 3116-3122.
69. Oliveira SC, Harms JS, Rech EL, Rodarte RS, Bocca AL, et al. (1998) The role of T cell subsets and cytokines in the regulation of intracellular bacterial infection. Braz J Med Biol Res 31: 77-84.
70. Skold M, Behar SM, (2003) Role of CD1d-restricted NKT cells in microbial immunity. Infect Immun 71: 5447-5455.
71. Sada-Ovalle I, Chiba A, Gonzales A, Brenner MB, Behar SM, (2008) Innate invariant NKT cells recognize Mycobacterium tuberculosis-infected macrophages, produce interferon-gamma, and kill intracellular bacteria. PLoS Pathog 4: e1000239.
72. Ho LP, Denney L, Luhn K, Teoh D, Clelland C, et al. (2008) Activation of invariant NKT cells enhances the innate immune response and improves the disease course in influenza A virus infection. Eur J Immunol 38: 1913-1922.
73. Joyee AG, Qiu H, Fan Y, Wang S, Yang X, (2008) Natural killer T cells are critical for dendritic cells to induce immunity in Chlamydial pneumonia. Am J Respir Crit Care Med 178: 745-756.
74. Anderson RV, Crane DD, Bosio CM, (2010) Long lived protection against pneumonic tularemia is correlated with cellular immunity in peripheral, not pulmonary, organs. Vaccine 28: 6562-6572.
75. Gillessen S, Carvajal D, Ling P, Podlaski FJ, Stremlo DL, et al. (1995) Mouse interleukin-12 (IL-12) p40 homodimer: a potent IL-12 antagonist. Eur J Immunol 25: 200-206.
76. Aggarwal S, Ghilardi N, Xie MH, de Sauvage FJ, Gurney AL, (2003) Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 278: 1910-1914.
77. Frank GM, Divito SJ, Maker DM, Xu M, Hendricks RL, (2010) A novel p40-independent function of IL-12p35 is required for progression and maintenance of herpes stromal keratitis. Invest Ophthalmol Vis Sci 51: 3591-3598.
78. Hunter CA, (2005) New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat Rev Immunol 5: 521-531.
79. Bakshi CS, Malik M, Mahawar M, Kirimanjeswara GS, Hazlett KR, et al. (2008) An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis SchuS4 strain. Vaccine 26: 5276-5288.
80. Kirimanjeswara GS, Golden JM, Bakshi CS, Metzger DW, (2007) Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J Immunol 179: 532-539.
81. Rhinehart-Jones TR, Fortier AH, Elkins KL, (1994) Transfer of immunity against lethal murine Francisella infection by specific antibody depends on host gamma interferon and T cells. Infect Immun 62: 3129-3137.
82. Savitt AG, Mena-Taboada P, Monsalve G, Benach JL, (2009) Francisella tularensis infection-derived monoclonal antibodies provide detection, protection, and therapy. Clin Vaccine Immunol 16: 414-422.
83. Mara-Koosham G, Hutt JA, Lyons CR, Wu TH, (2011) Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains. Infect Immun 79: 1770-1778.
84. LeBien TW, Tedder TF, (2008) B lymphocytes: how they develop and function. Blood 112: 1570-1580.
85. Harris S, (1992) Japanese biological warfare research on humans: a case study of microbiology and ethics. Ann N Y Acad Sci 666: 21-52.
86. Enderlin G, Morales L, Jacobs RF, Cross JT, (1994) Streptomycin and alternative agents for the treatment of tularemia: review of the literature. Clin Infect Dis 19: 42-47.
87. Risi GF, Pombo DJ, (1995) Relapse of tularemia after aminoglycoside therapy: case report and discussion of therapeutic options. Clin Infect Dis 20: 174-175.
88. Parker RR, Spencer RR, (1926) Six Additional Cases of Laboratory Infection of Tularemia in Man. Public Health Reports 41: 1341-1357.
89. Burke DS, (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.