Perforin- and granzyme-mediated cytotoxic effector functions are essential for protection against francisella tularensis following vaccination by the defined F. Tularensis subsp. Novicida ΔfopC vaccine strain

Infection and Immunity

Volumn 80, Issue 6, 2012, Pages 2177-2185

  Sanapala, Shilpa ^a,c   Yu, Jieh Juen ^a   Murthy, Ashlesh K ^b   Li, Weidang ^a   Neal Guentzel, M ^a   Chambers, James P ^a   Klose, Karl E ^a   Arulanandam, Bernard P ^a  

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

^b MIDWESTERN UNIVERSITY   (United States)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GRANZYME; LIVE VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OUTER MEMBRANE LIPOPROTEIN FOPC; PERFORIN; PROTEIN IGLB; TULAREMIA VACCINE; UNCLASSIFIED DRUG; BACTERIAL VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIGEN PRESENTING CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; CELL DIFFERENTIATION; CELL GROWTH; COLONY FORMING UNIT; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME RELEASE; FRANCISELLA TULARENSIS; IN VITRO STUDY; INFECTION PREVENTION; MACROPHAGE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PATHOGENICITY ISLAND; PHAGOSOME; PHENOTYPE; PNEUMONIC TULAREMIA; PRIORITY JOURNAL; PROTEIN FUNCTION; T LYMPHOCYTE ACTIVATION; TULAREMIA; VACCINATION; WILD TYPE; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; COCULTURE; GENE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MOUSE MUTANT; PHYSIOLOGY;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL VACCINES; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; COCULTURE TECHNIQUES; FRANCISELLA TULARENSIS; GENE EXPRESSION REGULATION; GENES, MHC CLASS I; GENES, MHC CLASS II; GRANZYMES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PERFORIN; TULAREMIA; VACCINATION; VACCINES, ATTENUATED;

EID: 85047688492     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00036-12     Document Type: Article

References (73)

1. Ackerman AL, Cresswell P. 2004. Cellular mechanisms governing crosspresentation of exogenous antigens. Nat. Immunol. 5:678-684.
2. Anthony LS, Ghadirian E, Nestel FP, Kongshavn PA. 1989. The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb. Pathog. 7:421- 428.
3. Barnett ED. 2007. Yellow fever: epidemiology and prevention. Clin. Infect. Dis. 44:850-856.
4. Baxby D. 1999. Edward Jenner's inquiry; a bicentenary analysis. Vaccine 17:301-307.
5. Bokhari SM, et al. 2008. NK cells and gamma interferon coordinate the formation and function of hepatic granulomas in mice infected with the Francisella tularensis live vaccine strain. Infect. Immun. 76:1379 -1389.
6. Boltz-Nitulescu G, et al. 1987. Differentiation of rat bone marrow cells into macrophages under the influence of mouse L929 cell supernatant. J. Leukoc. Biol. 41:83-91.
7. Broms JE, Lavander M, Sjostedt A. 2009. A conserved alpha-helix essential for a type VI secretion-like system of Francisella tularensis. J. Bacteriol. 191:2431-2446.
8. 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.
9. Cong Y, et al. 2009. Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (DiglB) induces protective immunity against homotypic and heterotypic challenge. Vaccine 27: 5554-5561.
10. Darmon AJ, Nicholson DW, Bleackley RC. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377:446-448.
11. Dennis DT, et al. 2001. Tularemia as a biological weapon: medical and public health management. JAMA 285:2763-2773.
12. 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.
13. 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.
14. Feunou PF, Bertout J, Locht C. 2010. T- and B-cell-mediated protection induced by novel, live attenuated pertussis vaccine in mice. Cross protection against parapertussis. PLoS One 5:e10178.
15. Flynn JL, et al. 1993. An essential role for interferon gamma in resistance to Mycobacterium tuberculosis infection. J. Exp. Med. 178:2249 -2254.
16. Fortier AH, Slayter MV, Ziemba R, Meltzer MS, Nacy CA. 1991. Live vaccine strain of Francisella tularensis: infection and immunity in mice. Infect. Immun. 59:2922-2928.
17. Fulop M, Mastroeni P, Green M, Titball RW. 2001. Role of antibody to lipopolysaccharide in protection against low- and high-virulence strains of Francisella tularensis. Vaccine 19:4465- 4472.
18. Fung-Leung WP, et al. 1991. CD8 is needed for development of cytotoxic T cells but not helper T cells. Cell 65:443- 449.
19. Gagnon E, et al. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110:119 -131.
20. Gavrilin MA, et al. 2006. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1_ processing and release. Proc. Natl. Acad. Sci. U. S. A. 103:141-146.
21. Golovliov I, Baranov V, Krocova Z, Kovarova H, Sjostedt A. 2003. An attenuated strain of the facultative intracellular bacterium Francisella tularensis can escape the phagosome of monocytic cells. Infect. Immun. 71:5940 -5950.
22. Hamrick TS, et al. 2003. Influence of pregnancy on the pathogenesis of listeriosis in mice inoculated intragastrically. Infect. Immun. 71:5202- 5209.
23. Hartley G, et al. 2006. Grey variants of the live vaccine strain of Francisella tularensis lack lipopolysaccharide O-antigen, show reduced ability to survive in macrophages and do not induce protective immunity in mice. Vaccine 24:989 -996.
24. Jensen PE. 2007. Recent advances in antigen processing and presentation. Nat. Immunol. 8:1041-1048.
25. Kagi D, Ledermann B, Burki K, Hengartner H, Zinkernagel RM. 1994. CD8+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity. Eur. J. Immunol. 24:3068 -3072.
26. Kägi D, et al. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31-37.
27. Kaufmann SH. 1999. Cell-mediated immunity: dealing a direct blow to pathogens. Curr. Biol. 9:R97-R99.
28. 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.
29. Kitamura D, Roes J, Kühn R, Rajewsky K. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423- 426.
30. Koller BH, Marrack P, Kappler JW, Smithies O. 1990. Normal development of mice deficient in beta 2M, MHC class I proteins, and CD8+ T cells. Science 248:1227-1230.
31. Levine MM, Ferreccio C, Black RE, Germanier R. 1987. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet i:1049 -1052.
32. Levine MM, Kaper JB. 1993. Live oral vaccines against cholera: an update. Vaccine 11:207-212.
33. Lieberman J. 2003. The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3:361-370.
34. Lindberg AA. 1995. The history of live bacterial vaccines. Dev. Biol. Stand. 84:211-219.
35. Lindgren H, et al. 2009. The 58-kilodalton major virulence factor of Francisella tularensis is required for efficient utilization of iron. Infect. Immun. 77:4429-4436.
36. Liu J, Zogaj X, Barker JR, Klose KE. 2007. Construction of targeted insertion mutations in Francisella tularensis subsp. novicida. BioTechniques 43:487- 490, 492.
37. 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.
38. Lowy DR, Schiller JT. 2006. Prophylactic human papillomavirus vaccines. J. Clin. Invest. 116:1167-1173.
39. Madsen L, et al. 1999. Mice lacking all conventional MHC class II genes. Proc. Natl. Acad. Sci. U. S. A. 96:10338 -10343.
40. Mares CA, Ojeda SS, Morris EG, Li Q, Teale JM. 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, Weiss DS, Dixit VM, Monack DM. 2005. Innate immu-nity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J. Exp. Med. 202:1043-1049.
42. Masson D, Tschopp J. 1985. Isolation of a lytic, pore-forming protein (perforin) from cytolytic T-lymphocytes. J. Biol. Chem. 260:9069 -9072.
43. McCarrick JW, III, Parnes JR, Seong RH, Solter D, Knowles BB. 1993. Positive-negative selection gene targeting with the diphtheria toxin Achain gene in mouse embryonic stem cells. Transgenic Res. 2:183-190.
44. McCullers JA. 2007. Evolution, benefits, and shortcomings of vaccine management. J. Manag. Care Pharm. 13:S2- 6.
45. Metkar SS, et al. 2002. Cytotoxic cell granule-mediated apoptosis: perforin delivers granzyme B-serglycin complexes into target cells without plasma membrane pore formation. Immunity 16:417- 428.
46. Nallaparaju KC, et al. 2011. Evasion of IFN-gamma signaling by Francisella novicida is dependent upon Francisella outer membrane protein C. PLoS One 6:e18201.
47. Nano FE, et al. 2004. A Francisella tularensis pathogenicity island required for intramacrophage growth. J. Bacteriol. 186:6430-6436.
48. Pammit MA, Raulie EK, Lauriano CM, Klose KE, Arulanandam BP. 2006. Intranasal vaccination with a defined attenuated Francisella novicida strain induces gamma interferon-dependent antibody-mediated protection against tularemia. Infect. Immun. 74:2063-2071.
49. Pasetti MF, Levine MM, Sztein MB. 2003. Animal models paving the way for clinical trials of attenuated Salmonella enterica serovar Typhi live oral vaccines and live vectors. Vaccine 21:401- 418.
50. Pinkoski MJ, et al. 1998. Entry and trafficking of granzyme B in target cells during granzyme B-perforin-mediated apoptosis. Blood 92:1044- 1054.
51. Podack ER, Young JD, Cohn ZA. 1985. Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl. Acad. Sci. U. S. A. 82:8629-8633.
52. Powell HJ, et al. 2008. CD4+ T cells are required during priming but not the effector phase of antibody-mediated IFN-gamma-dependent protective immunity against pulmonary Francisella novicida infection. Immunol. Cell Biol. 86:515-522.
53. Ray HJ, et al. 2010. The Fischer 344 rat reflects human susceptibility to Francisella pulmonary challenge and provides a new platform for virulence and protection studies. PLoS One 5:e9952.
54. Ray HJ, et al. 2009. Oral live vaccine strain-induced protective immunity against pulmonary Francisella tularensis challenge is mediated by CD4+T cells and antibodies, including immunoglobulin A. Clin. Vaccine Immunol. 16:444-452.
55. Rohmer L, et al. 2007. Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol. 8:R102.
56. Salomonsson E, et al. 2009. Reintroduction of two deleted virulence loci restores full virulence to the live vaccine strain of Francisella tularensis. Infect. Immun. 77:3424 -3431.
57. 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.
58. Santic M, et al. 2007. A Francisella tularensis pathogenicity island protein essential for bacterial proliferation within the host cell cytosol. Cell Microbiol. 9:2391-2403.
59. Santic M, Molmeret M, Klose KE, Jones S, Kwaik YA. 2005. The Francisella tularensis pathogenicity island protein IglC and its regulator MglA are essential for modulating phagosome biogenesis and subsequent bacterial escape into the cytoplasm. Cell Microbiol. 7:969 -979.
60. Shafer WM, Pohl J, Onunka VC, Bangalore N, Travis J. 1991. Human lysosomal cathepsin G and granzyme B share a functionally conserved broad spectrum antibacterial peptide. J. Biol. Chem. 266:112-116.
61. Shinkai Y, Takio K, Okumura K. 1988. Homology of perforin to the ninth component of complement (C9). Nature 334:525-527.
62. Sjostedt A. 2007. Tularemia: history, epidemiology, pathogen physiology, and clinical manifestations. Ann. N. Y. Acad. Sci. 1105:1-29.
63. Stegelmann F, et al. 2005. Coordinate expression of CC chemokine ligand 5, granulysin, and perforin in CD8_T cells provides a host defense mechanism against Mycobacterium tuberculosis. J. Immunol. 175:7474 -7483.
64. Stenger S, et al. 1998. An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 282:121-125.
65. Stenmark S, Lindgren H, Tarnvik A, Sjostedt A. 2003. Specific antibodies contribute to the host protection against strains of Francisella tularensis subspecies holarctica. Microb. Pathog. 35:73- 80.
66. Stuart BM. 1945. Tularemic pneumonia: review of American literature and report of 15 additional cases. Am. J. Med. Sci. 210:223-236.
67. Takai T. 1996. Multiple loss of effector cell functions in FcR gammadeficient mice. Int. Rev. Immunol. 13:369 -381.
68. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. 1994. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 76:519 -529.
69. Tarnvik A. 1989. Nature of protective immunity to Francisella tularensis. Rev. Infect. Dis. 11:440-451.
70. Viret JF, Dietrich G, Favre D. 2004. Biosafety aspects of the recombinant live oral Vibrio cholerae vaccine strain CVD 103-HgR. Vaccine 22:2457- 2469.
71. Watanabe S, Watanabe T, Kawaoka Y. 2009. Influenza A virus lacking M2 protein as a live attenuated vaccine. J. Virol. 83:5947-5950.
72. Wiertz EJ, et al. 1996. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384:432- 438.
73. Wu TH, et al. 2005. Intranasal vaccination induces protective immunity against intranasal infection with virulent Francisella tularensis biovar A. Infect. Immun. 73:2644 -2654.