Enhancement of vaccine efficacy by expression of a TLR5 ligand in the defined live attenuated Francisella tularensis subsp. Novicida strain U112δiglB :: FljB

Vaccine

Volumn 32, Issue 40, 2014, Pages 5234-5240

  Cunningham, Aimee L ^a,b   Dang, Kim Minh ^a   Yu, Jieh Juen ^a   Guentzel, M Neal ^a   Heidner, Hans W ^a   Klose, Karl E ^a   Arulanandam, Bernard P ^a  

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

^b Mays Cancer Center at UT Health San Antonio   (United States)

Author keywords

Fischer 344 rat; Flagellin; Francisella tularensis; TLR5; Vaccine

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL VACCINE; FLAGELLIN; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIVE ATTENUATED FRANCISELLA NOVICIDA VACCINE; LIVE VACCINE; TOLL LIKE RECEPTOR 5; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BACTERIUM ANTIBODY; FLJB PROTEIN, SALMONELLA; LIGAND; VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; BACTERIAL STRAIN; CELL DIVISION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOSOL; DRUG EFFICACY; FRANCISELLA NOVICIDA; FRANCISELLA TULARENSIS; HEK293 CELL LINE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; INFECTION; LYMPHOCYTE; MACROPHAGE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SALMONELLA TYPHIMURIUM; SINGLE DRUG DOSE; SPLEEN CELL; TULAREMIA; VACCINATION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; CELL LINE; FISCHER 344 RAT; IMMUNOLOGY; MICROBIOLOGY;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL VACCINES; CELL LINE; FLAGELLIN; FRANCISELLA TULARENSIS; HUMANS; LIGANDS; MACROPHAGES; MICE, INBRED BALB C; RATS, INBRED F344; TOLL-LIKE RECEPTOR 5; TULAREMIA; VACCINE POTENCY; VACCINES, ATTENUATED;

EID: 84906057185     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2014.07.038     Document Type: Article

References (48)

1. KuoLee R., Harris G., Conlan J.W., Chen W. Oral immunization of mice with the live vaccine strain (LVS) of Francisella tularensis protects mice against respiratory challenge with virulent type A F. tularensis. Vaccine 2007, 25(19):3781-3791.
2. Ray H.J., Cong Y., Murthy A.K., Selby D.M., Klose K.E., Barker J.R., et al. 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 2009, 16(4):444-452.
3. Sanapala S., Yu J.J., Murthy A.K., Li W., Guentzel M.N., Chambers J.P., et al. 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. Infect Immun 2012, 80(6):2177-2185.
4. Signarovitz A.L., Ray H.J., Yu J.J., Guentzel M.N., Chambers J.P., Klose K.E., et al. Mucosal immunization with live attenuated Francisella novicida U112δiglB protects against pulmonary F. tularensis SCHU S4 in the Fischer 344 rat model. PLoS One 2012, 7(10):e47639.
5. Cong Y., Yu J.J., Guentzel M.N., Berton M.T., Seshu J., Klose K.E., et al. Vaccination with a defined Francisella tularensis subsp. novicida pathogenicity island mutant (δiglB) induces protective immunity against homotypic and heterotypic challenge. Vaccine 2009, 27(41):5554-5561.
6. Liu J., Zogaj X., Barker J.R., Klose K.E. Construction of targeted insertion mutations in Francisella tularensis subsp. novicida. Biotechniques 2007, 43(4):487-490. 92.
7. Barker J.R., Chong A., Wehrly T.D., Yu J.J., Rodriguez S.A., Liu J., et al. The Francisella tularensis pathogenicity island encodes a secretion system that is required for phagosome escape and virulence. Mol Microbiol 2009, 74(6):1459-1470.
8. de Bruin O.M., Duplantis B.N., Ludu J.S., Hare R.F., Nix E.B., Schmerk C.L., et al. The biochemical properties of the Francisella pathogenicity island (FPI)-encoded proteins IglA, IglB, IglC, PdpB and DotU suggest roles in type VI secretion. Microbiology 2011, 157(Pt 12):3483-3491.
9. Nguyen C.T., Kim S.Y., Kim M.S., Lee S.E., Rhee J.H. Intranasal immunization with recombinant PspA fused with a flagellin enhances cross-protective immunity against Streptococcus pneumoniae infection in mice. Vaccine 2011, 29(34):5731-5739.
10. Hong S.H., Byun Y.H., Nguyen C.T., Kim S.Y., Seong B.L., Park S., et al. Intranasal administration of a flagellin-adjuvanted inactivated influenza vaccine enhances mucosal immune responses to protect mice against lethal infection. Vaccine 2012, 30(2):466-474.
11. Leal M.T., Camacho A.G., Teixeira L.H., Bargieri D.Y., Soares I.S., Tararam C.A., et al. Immunogenicity of recombinant proteins consisting of Plasmodium vivax circumsporozoite protein allelic variant-derived epitopes fused with Salmonella Typhimurium flagellin. Clin Vaccine Immunol 2013.
12. Le Moigne V., Robreau G., Mahana W. Flagellin as a good carrier and potent adjuvant for Th1 response: study of mice immune response to the p27 (Rv2108) Mycobacterium tuberculosis antigen. Mol Immunol 2008, 45(9):2499-2507.
13. Ben-Yedidia T., Arnon R. Effect of pre-existing carrier immunity on the efficacy of synthetic influenza vaccine. Immunol Lett 1998, 64(1):9-15.
14. Honko A.N., Sriranganathan N., Lees C.J., Mizel S.B. Flagellin is an effective adjuvant for immunization against lethal respiratory challenge with Yersinia pestis. Infect Immun 2006, 74(2):1113-1120.
15. + lamina propria cells. Nat Immunol 2006, 7(8):868-874.
16. McDonald W.F., Huleatt J.W., Foellmer H.G., Hewitt D., Tang J., Desai P., et al. A West Nile virus recombinant protein vaccine that coactivates innate and adaptive immunity. J Infect Dis 2007, 195(11):1607-1617.
17. Samatey F.A., Imada K., Nagashima S., Vonderviszt F., Kumasaka T., Yamamoto M., et al. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 2001, 410(6826):331-337.
18. Lauriano C.M., Barker J.R., Nano F.E., Arulanandam B.P., Klose K.E. Allelic exchange in Francisella tularensis using PCR products. FEMS Microbiol Lett 2003, 229(2):195-202.
19. Ray H.J., Chu P., Wu T.H., Lyons C.R., Murthy A.K., Guentzel M.N., et al. The Fischer 344 rat reflects human susceptibility to Francisella pulmonary challenge and provides a new platform for virulence and protection studies. PLoS One 2010, 5(4):e9952.
20. Nguyen J., Gilley R.P., Zogaj X., Rodriguez S.A., Klose K.E. Lipidation of the FPI Protein IglE contributes to Francisella tularensis subsp. novicida intramacrophage replication and virulence. Pathog Dis 2014.
21. Rohmer L., Fong C., Abmayr S., Wasnick M., Larson Freeman T.J., Radey M., et al. Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol 2007, 8(6):R102.
22. Bhatnagar N., Getachew E., Straley S., Williams J., Meltzer M., Fortier A. Reduced virulence of rifampicin-resistant mutants of Francisella tularensis. J Infect Dis 1994, 170(4):841-847.
23. Zogaj X., Wyatt G.C., Klose K.E. Cyclic di-GMP stimulates biofilm formation and inhibits virulence of Francisella novicida. Infect Immun 2012, 80(12):4239-4247.
24. Bazzoni F., Beutler B. The tumor necrosis factor ligand and receptor families. N Engl J Med 1996, 334(26):1717-1725.
25. Elkins K.L., Cowley S.C., Bosio C.M. Innate and adaptive immune responses to an intracellular bacterium, Francisella tularensis live vaccine strain. Microbes Infect 2003, 5(2):135-142.
26. Mara-Koosham G., Hutt J.A., Lyons C.R., Wu T.H. Antibodies contribute to effective vaccination against respiratory infection by type A Francisella tularensis strains. Infect Immun 2011, 79(4):1770-1778.
27. Anthony L.S., Ghadirian E., Nestel F.P., Kongshavn P.A. The requirement for gamma interferon in resistance of mice to experimental tularemia. Microb Pathog 1989, 7(6):421-428.
28. Pammit M.A., Raulie E.K., Lauriano C.M., Klose K.E., Arulanandam B.P. Intranasal vaccination with a defined attenuated Francisella novicida strain induces gamma interferon-dependent antibody-mediated protection against tularemia. Infect Immun 2006, 74(4):2063-2071.
29. Kirimanjeswara G.S., Golden J.M., Bakshi C.S., Metzger D.W. Prophylactic and therapeutic use of antibodies for protection against respiratory infection with Francisella tularensis. J Immunol 2007, 179(1):532-539.
30. Lavine C.L., Clinton S.R., Angelova-Fischer I., Marion T.N., Bina X.R., Bina J.E., et al. Immunization with heat-killed Francisella tularensis LVS elicits protective antibody-mediated immunity. Eur J Immunol 2007, 37(11):3007-3020.
31. Lu Z., Roche M.I., Hui J.H., Unal B., Felgner P.L., Gulati S., et al. Generation and characterization of hybridoma antibodies for immunotherapy of tularemia. Immunol Lett 2007, 112(2):92-103.
32. Casadevall A., Pirofski L.A. A reappraisal of humoral immunity based on mechanisms of antibody-mediated protection against intracellular pathogens. Adv Immunol 2006, 91:1-44.
33. Drabick J.J., Narayanan R.B., Williams J.C., Leduc J.W., Nacy C.A. Passive protection of mice against lethal Francisella tularensis (live tularemia vaccine strain) infection by the sera of human recipients of the live tularemia vaccine. Am J Med Sci 1994, 308(2):83-87.
34. Stenmark S., Lindgren H., Tarnvik A., Sjostedt A. Specific antibodies contribute to the host protection against strains of Francisella tularensis subspecies holarctica. Microb Pathog 2003, 35(2):73-80.
35. Kubelkova K., Krocova Z., Balonova L., Pejchal J., Stulik J., Macela A. Specific antibodies protect gamma-irradiated mice against Francisella tularensis infection. Microb Pathog 2012, 53(5-6):259-268.
36. Mizel S.B., Graff A.H., Sriranganathan N., Ervin S., Lees C.J., Lively M.O., et al. Flagellin-F1-V fusion protein is an effective plague vaccine in mice and two species of nonhuman primates. Clin Vaccine Immunol 2009, 16(1):21-28.
37. Sanders C.J., Yu Y., Moore D.A., Williams I.R., Gewirtz A.T. Humoral immune response to flagellin requires T cells and activation of innate immunity. J Immunol 2006, 177(5):2810-2818.
38. Adar Y., Singer Y., Levi R., Tzehoval E., Perk S., Banet-Noach C., et al. A universal epitope-based influenza vaccine and its efficacy against H5N1. Vaccine 2009, 27(15):2099-2107.
39. Lee L.H., Burg E., Baqar S., Bourgeois A.L., Burr D.H., Ewing C.P., et al. Evaluation of a truncated recombinant flagellin subunit vaccine against Campylobacter jejuni. Infect Immun 1999, 67(11):5799-5805.
40. Pino O., Martin M., Michalek S.M. Cellular mechanisms of the adjuvant activity of the flagellin component FljB of Salmonella enterica Serovar Typhimurium to potentiate mucosal and systemic responses. Infect Immun 2005, 73(10):6763-6770.
41. Geier H., Celli J. Phagocytic receptors dictate phagosomal escape and intracellular proliferation of Francisella tularensis. Infect Immun 2011, 79(6):2204-2214.
42. Ben Nasr A., Haithcoat J., Masterson J.E., Gunn J.S., Eaves-Pyles T., Klimpel G.R. 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 2006, 80(4):774-786.
43. Clay C.D., Soni S., Gunn J.S., Schlesinger L.S. Evasion of complement-mediated lysis and complement C3 deposition are regulated by Francisella tularensis lipopolysaccharide O antigen. J Immunol 2008, 181(8):5568-5578.
44. Schwartz J.T., Barker J.H., Long M.E., Kaufman J., McCracken J., Allen L.A. Natural IgM mediates complement-dependent uptake of Francisella tularensis by human neutrophils via complement receptors 1 and 3 in nonimmune serum. J Immunol 2012, 189(6):3064-3077.
45. Clemens D.L., Lee B.Y., Horwitz M.A. Francisella tularensis enters macrophages via a novel process involving pseudopod loops. Infect Immun 2005, 73(9):5892-5902.
46. Miao E.A., Alpuche-Aranda C.M., Dors M., Clark A.E., Bader M.W., Miller S.I., et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 2006, 7(6):569-575.
47. Lu C., Wang A., Wang L., Dorsch M., Ocain T.D., Xu Y. Nucleotide binding to CARD12 and its role in CARD12-mediated caspase-1 activation. Biochem Biophys Res Commun 2005, 331(4):1114-1119.
48. Carvalho F.A., Nalbantoglu I., Aitken J.D., Uchiyama R., Su Y., Doho G.H., et al. Cytosolic flagellin receptor NLRC4 protects mice against mucosal and systemic challenges. Mucosal Immunol 2012, 5(3):288-298.