Vaccination with an attenuated strain of Francisella novicida prevents T-cell depletion and protects mice infected with the wild-type strain from severe sepsis

Infection and Immunity

Volumn 77, Issue 10, 2009, Pages 4314-4326

  Sharma, Jyotika ^a   Li, Qun ^a   Mishra, Bibhuti B ^a   Georges, Michelle J ^a   Teale, Judy M ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; BACTERIUM ANTIBODY; CYTOKINE; FRANCISELLA NOVICIDA VACCINE; LIVE VACCINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CELL DEATH; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FRANCISELLA; FRANCISELLA NOVICIDA; GRAM NEGATIVE SEPSIS; HUMORAL IMMUNITY; IMMUNE RESPONSE; LETHALITY; LYMPHOCYTE COUNT; LYMPHOCYTE DEPLETION; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; T CELL DEPLETION; UPREGULATION; VACCINATION; WILD TYPE;

ANIMAL STRUCTURES; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; COLONY COUNT, MICROBIAL; CYTOKINES; FRANCISELLA TULARENSIS; LUNG; LYMPHOCYTE COUNT; MICE; MICE, INBRED C57BL; SEPSIS; SURVIVAL ANALYSIS; T-LYMPHOCYTES; TULAREMIA; VACCINES, ATTENUATED;

EID: 70349428437     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00654-09     Document Type: Article

References (67)

1. Bakshi, C. S., M. Malik, M. Mahawar, G. S. Kirimanjeswara, K. R. Hazlett, L. E. Palmer, M. B. Furie, R. Singh, J. A. Melendez, T. J. Sellati, and D. W. Metzger. 2008. An improved vaccine for prevention of respiratory tularemia caused by Francisella tularensis SchuS4 strain. Vaccine 26:5276-5288.
2. Bosio, C. M., H. Bielefeldt-Ohmann, and J. T. Belisle. 2007. Active suppression of the pulmonary immune response by Francisella tularensis Schu4. J. Immunol. 178:4538-4547.
3. Bosio, C. M., and S. W. Dow. 2005. Francisella tularensis induces aberrant activation of pulmonary dendritic cells. J. Immunol. 175:6792-6801.
4. Bosio, C. M., and K. L. Elkins. 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.
5. Chiavolini, D., J. Alroy, C. A. King, P. Jorth, S. Weir, G. Madico, J. R. Murphy, and L. M. Wetzler. 2008. Identification of immunologic and pathologic parameters of death versus survival in respiratory tularemia. Infect. Immun. 76:486-496.
6. Clark, I. A., L. M. Alleva, A. C. Budd, and W. B. Cowden. 2008. Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Med. Infect. Dis. 6:67-81.
7. Cowley, S. C., and K. L. Elkins. 2003. Multiple T cell subsets control Francisella tularensis LVS intracellular growth without stimulation through macrophage interferon gamma receptors. J. Exp. Med. 198:379-389.
8. - T cells control intracellular bacterial infections both in vitro and in vivo. J. Exp. Med. 202:309-319.
9. + T cells for soluble and membrane TNF in control of Francisella tularensis live vaccine strain intramacrophage growth. J. Immunol. 179:7709-7719.
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. (Pubitemid 32525374)
11. De Pascalis, R., B. C. Taylor, and K. L. Elkins. 2008. Diverse myeloid and lymphoid cell subpopulations produce gamma interferon during early innate immune responses to Francisella tularensis live vaccine strain. Infect. Immun. 76:4311-4321.
12. Dinarello, C. A. 1994. The interleukin-1 family: 10 years of discovery. FASEB J. 8:1314-1325.
13. Dube, P. H., P. A. Revell, D. D. Chaplin, R. G. Lorenz, and V. L. Miller. 2001. A role for IL-1 alpha in inducing pathologic inflammation during bacterial infection. Proc. Natl. Acad. Sci. USA 98:10880-10885.
14. Elkins, K. L., A. Cooper, S. M. Colombini, S. C. Cowley, and T. L. Kieffer. 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.
15. Elkins, K. L., S. C. Cowley, and C. M. Bosio. 2003. Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect. 5:135-142.
16. Elkins, K. L., S. C. Cowley, and C. M. Bosio. 2007. Innate and adaptive immunity to Francisella. Ann. N. Y. Acad. Sci. 1105:284-324.
17. Ericsson, M., G. Sandstrom, A. Sjostedt, and A. Tarnvik. 1994. Persistence of cell-mediated immunity and decline of humoral immunity to the intracellular bacterium Francisella tularensis 25 years after natural infection. J. Infect. Dis. 170:110-114.
18. Fink, M. P. 2001. Cytopathic hypoxia. Mitochondrial dysfunction as mechanism contributing to organ dysfunction in sepsis. Crit. Care Clin. 17:219-237.
19. Foell, D., H. Wittkowski, T. Vogl, and J. Roth. 2007. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J. Leukoc. Biol. 81:28-37.
20. Forsman, M., G. Sandstrom, and B. Jaurin. 1990. Identification of Francisella species and discrimination of type A and type B strains of F. tularensis by 16S rRNA analysis. Appl. Environ. Microbiol. 56:949-955.
21. Foulds, K. E., C. Y. Wu, and R. A. Seder. 2006. Th1 memory: implications for vaccine development. Immunol. Rev. 211:58-66.
22. Gallagher, L. A., E. Ramage, M. A. Jacobs, R. Kaul, M. Brittnacher, and C. Manoil. 2007. A comprehensive transposon mutant library of Francisella novicida, a bioweapon surrogate. Proc. Natl. Acad. Sci. USA 104:1009-1014.
23. Ghavami, S., C. Kerkhoff, M. Los, M. Hashemi, C. Sorg, and F. Karami- Tehrani. 2004. Mechanism of apoptosis induced by S100A8/A9 in colon cancer cell lines: the role of ROS and the effect of metal ions. J. Leukoc. Biol. 76:169-175.
24. Gonzalez-Juarrero, M., and I. M. Orme. 2001. Characterization of murine lung dendritic cells infected with Mycobacterium tuberculosis. Infect. Immun. 69:1127-1133.
25. Han, S., B. M. Bishop, and M. L. van Hoek. 2008. Antimicrobial activity of human beta-defensins and induction by Francisella. Biochem. Biophys. Res. Commun. 371:670-674.
26. Havlasova, J., L. Hernychova, M. Brychta, M. Hubalek, J. Lenco, P. Larsson, M. Lundqvist, M. Forsman, Z. Krocova, J. Stulik, and A. Macela. 2005. Proteomic analysis of anti-Francisella tularensis LVS antibody response in murine model of tularemia. Proteomics 5:2090-2103. (Pubitemid 40770573)
27. Herzum, I., and H. Renz. 2008. Inflammatory markers in SIRS, sepsis and septic shock. Curr. Med. Chem. 15:581-587.
28. Hiramatsu, M., R. S. Hotchkiss, I. E. Karl, and T. G. Buchman. 1997. Cecal ligation and puncture (CLP) induces apoptosis in thymus, spleen, lung, and gut by an endotoxin and TNF-independent pathway. Shock 7:247-253. (Pubitemid 127654275)
29. Hotchkiss, R. S., K. C. Chang, P. E. Swanson, K. W. Tinsley, J. J. Hui, P. Klender, S. Xanthoudakis, S. Roy, C. Black, E. Grimm, R. Aspiotis, Y. Han, D. W. Nicholson, and I. E. Karl. 2000. Caspase inhibitors improve survival in sepsis: a critical role of the lymphocyte. Nat. Immunol. 1:496-501.
30. Hotchkiss, R. S., P. E. Swanson, B. D. Freeman, K. W. Tinsley, J. P. Cobb, G. M. Matuschak, T. G. Buchman, and I. E. Karl. 1999. Apoptotic cell death in patients with sepsis, shock, and multiple organ dysfunction. Crit. Care Med. 27:1230-1251.
31. Hotchkiss, R. S., K. W. Tinsley, and I. E. Karl. 2003. Role of apoptotic cell death in sepsis. Scand. J. Infect. Dis. 35:585-592.
32. Hotchkiss, R. S., K. W. Tinsley, P. E. Swanson, K. C. Chang, J. P. Cobb, T. G. Buchman, S. J. Korsmeyer, and I. E. Karl. 1999. Prevention of lymphocyte cell death in sepsis improves survival in mice. Proc. Natl. Acad. Sci. USA 96:14541-14546.
33. + T lymphocytes in humans. J. Immunol. 166:6952-6963.
34. Isaksen, B., and M. K. Fagerhol. 2001. Calprotectin inhibits matrix metalloproteinases by sequestration of zinc. Mol. Pathol. 54:289-292.
35. Jia, Q., B. Y. Lee, D. L. Clemens, R. A. Bowen, and M. A. Horwitz. 2009. Recombinant attenuated Listeria monocytogenes vaccine expressing Francisella tularensis IglC induces protection in mice against aerosolized type A F. tularensis. Vaccine 27:1216-1229.
36. Kim, K. D., J. Zhao, S. Auh, X. Yang, P. Du, H. Tang, and Y. X. Fu. 2007. Adaptive immune cells temper initial innate responses. Nat. Med. 13:1248-1252.
37. Lamkanfi, M., L. O. Moreira, P. Makena, D. C. Spierings, K. Boyd, P. J. Murray, D. R. Green, and T. D. Kanneganti. 2009. Caspase-7 deficiency protects from endotoxin-induced lymphocyte apoptosis and improves survival. Blood 113:2742-2745.
38. 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.
39. Lembo, A., M. Pelletier, R. Iyer, M. Timko, J. C. Dudda, T. E. West, C. B. Wilson, A. M. Hajjar, and S. J. Skerrett. 2008. Administration of a synthetic TLR4 agonist protects mice from pneumonic tularemia. J. Immunol. 180: 7574-7581.
40. Mares, C. A., S. S. Ojeda, E. G. Morris, Q. Li, and J. M. Teale. 2008. Initial delay in the immune response to Francisella tularensis is followed by hypercytokinemia characteristic of severe sepsis and correlating with upregulation and release of damage-associated molecular patterns. Infect. Immun. 76: 3001-3010.
41. Mariathasan, S., D. S. Weiss, V. M. Dixit, and D. M. Monack. 2005. Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202:1043-1049.
42. Martignoni, A., J. Tschop, H. S. Goetzman, L. G. Choi, M. D. Reid, J. A. Johannigman, A. B. Lentsch, and C. C. Caldwell. 2008. CD4-expressing cells are early mediators of the innate immune system during sepsis. Shock 29: 591-597. (Pubitemid 351544079)
43. McLendon, M. K., M. A. Apicella, and L. A. Allen. 2006. Francisella tularensis: taxonomy, genetics, and immunopathogenesis of a potential agent of biowarfare. Annu. Rev. Microbiol. 60:167-185.
44. Metzger, D. W., C. S. Bakshi, and G. Kirimanjeswara. 2007. Mucosal immunopathogenesis of Francisella tularensis. Ann. N. Y. Acad. Sci. 1105:266-283.
45. Mizgerd, J. P. 2008. Acute lower respiratory tract infection. N. Engl. J. Med. 358:716-727.
46. Mizgerd, J. P. 2006. Lung infection - a public health priority. PLoS Med. 3:e76.
47. Oberholzer, C., A. Oberholzer, F. R. Bahjat, R. M. Minter, C. L. Tannahill, A. Abouhamze, D. LaFace, B. Hutchins, M. J. Clare-Salzler, and L. L. Moldawer. 2001. Targeted adenovirus-induced expression of IL-10 decreases thymic apoptosis and improves survival in murine sepsis. Proc. Natl. Acad. Sci. USA 98:11503-11508.
48. Oyston, P. C., A. Sjostedt, and R. W. Titball. 2004. Tularaemia: bioterrorism defence renews interest in Francisella tularensis. Nat. Rev. Microbiol. 2:967-978.
49. Park, J. S., D. Svetkauskaite, Q. He, J. Y. Kim, D. Strassheim, A. Ishizaka, and E. Abraham. 2004. Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279:7370-7377.
50. Pinheiro da Silva, F., and V. Nizet. 2009. Cell death during sepsis: integration of disintegration in the inflammatory response to overwhelming infection. Apoptosis 14:509-521.
51. Riedemann, N. C., R. F. Guo, and P. A. Ward. 2003. Novel strategies for the treatment of sepsis. Nat. Med. 9:517-524.
52. Ryckman, C., K. Vandal, P. Rouleau, M. Talbot, and P. A. Tessier. 2003. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J. Immunol. 170: 3233-3242. (Pubitemid 36302201)
53. Sebastian, S., J. T. Pinkham, J. G. Lynch, R. A. Ross, B. Reinap, L. T. Blalock, J. W. Conlan, and D. L. Kasper. 2009. Cellular and humoral immunity are synergistic in protection against types A and B Francisella tularensis. Vaccine 27:597-605.
54. Sharma, J., Q. Li, B. B. Mishra, C. Pena, and J. M. Teale. 2009. Lethal pulmonary infection with Francisella novicida is associated with severe sepsis. J. Leukoc. Biol. doi:10.1189/jlb.1208728.
55. Sharma, J., Q. Li, B. B. Mishra, and J. M.Teale. 2009. Lethal pulmonary infection with Francisella novicida causes depletion of alpha-beta T cells from lungs. Cell. Immunol. 257:1-4.
56. Sjostedt, A. 2007. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann. N. Y. Acad. Sci. 1105:1-29.
57. + T cells of primed humans. Immunology 76:584-592.
58. Sohnle, P. G., M. J. Hunter, B. Hahn, and W. J. Chazin. 2000. Zincreversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J. Infect. Dis. 182:1272-1275.
59. Sriskandan, S., and D. M. Altmann. 2008. The immunology of sepsis. J. Pathol. 214:211-223.
60. Sunahori, K., M. Yamamura, J. Yamana, K. Takasugi, M. Kawashima, H. Yamamoto, W. J. Chazin, Y. Nakatani, S. Yui, and H. Makino. 2006. The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor kappa B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res. Ther. 8:R69.
61. 2+- binding proteins S100A8 and S100A9 are encoded by novel injury-regulated genes. J. Biol. Chem. 276:35818-35825.
62. Tracey, K. J., B. Beutler, S. F. Lowry, J. Merryweather, S. Wolpe, I. W. Milsark, R. J. Hariri, T. J. Fahey III, A. Zentella, J. D. Albert, et al. 1986. Shock and tissue injury induced by recombinant human cachectin. Science 234:470-474.
63. 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.
64. Ulloa, L., and K. J. Tracey. 2005. The "cytokine profile": a code for sepsis. Trends Mol. Med. 11:56-63.
65. Wayne Conlan, J., and P. C. Oyston. 2007. Vaccines against Francisella tularensis. Ann. N. Y. Acad. Sci. 1105:325-350.
66. Wayne Conlan, J., 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.
67. Wu, N., and J. M. Davidson. 2004. Migration inhibitory factor-related protein (MRP)8 and MRP14 are differentially expressed in free-electron laser and scalpel incisions. Wound Repair Regen. 12:327-336. (Pubitemid 38880441)