Neisseria meningitidis PorB, a toll-like receptor 2 ligand, improves the capacity of Francisella tularensis lipopolysaccharide to protect mice against experimental tularemia

Clinical and Vaccine Immunology

Volumn 15, Issue 9, 2008, Pages 1322-1329

  Chiavolini, Damiana ^a   Weir, Susan ^a   Murphy, John R ^a   Wetzler, Lee M ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BACTERIUM LIPOPOLYSACCHARIDE; FRANCISELLA TULARENSIS HOLARCTICA LIVE VACCINE; IMMUNOGLOBULIN M; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; PORIN; PROTEIN PORB; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; ARTICLE; BIOLOGICAL WARFARE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DRUG EFFICACY; EXPERIMENTAL INFECTION; FEMALE; FRANCISELLA TULARENSIS; FRANCISELLA TULARENSIS HOLARCTICA; FRANCISELLA TULARENSIS TULARENSIS; IN VITRO STUDY; IN VIVO STUDY; INFECTION PREVENTION; LIGAND BINDING; MORTALITY; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; STRAIN DIFFERENCE; SURVIVAL; TULAREMIA; VACCINATION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, BACTERIAL; CYTOKINES; FEMALE; FRANCISELLA TULARENSIS; HUMANS; IMMUNOGLOBULIN M; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED BALB C; PORINS; SURVIVAL ANALYSIS; TULAREMIA;

EID: 51649099771     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.00125-08     Document Type: Article

References (45)

1. Ancuta, P., T. Pedron, R. Girard, G. Sandstrom, and R. Chaby. 1996. Inability of the Francisella tularensis lipopolysaccharide to mimic or to antagonize the induction of cell activation by endotoxins. Infect. Immun. 64:2041-2046.
2. Baron, S. D., R. Singh, and D. W. Metzger. 2007. Inactivated Francisella tularensis LVS protects against respiratory tularemia by intranasal vaccination in an immunoglobulin A-dependent fashion. Infect. Immun. 75:2152-2162.
3. Bolger, C. E., C. A. Forestal, J. K. Italo, J. L. Benach, and M. B. Furie. 2005. The live vaccine strain of Francisella tularensis replicates in human and murine macrophages but induces only the human cells to secrete proinflammatory cytokines. J. Leukoc. Biol. 77:893-897.
4. Burke, J. M., L. M. Ganley-Leal, K. Khatri, and L. M. Wetzler. 2007. Neisseria meningitidis PorB, a TLR2 ligand, induces an antigen-specific eosinophil recall response: potential adjuvant for helminth vaccines? J. Immunol. 179:3222-3230.
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. Cole, L. E., K. L. Elkins, S. M. Michalek, N. Qureshi, L. J. Eaton, P. Rallabhandi, N. Cuesta, and S. N. Vogel. 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.
7. Cole, L. E., K. A. Shirey, E. Barry, A. Santiago, P. Rallabhandi, K. L. Elkins, A. C. Puche, S. M. Michalek, and S. N. Vogel. 2007. Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect. Immun. 75:4127-4137.
8. Conlan, J. W., H. Shen, A. Webb, and M. B. Perry. 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 20:3465-3470.
9. Conlan, J. W., E. Vinogradov, M. A. Monteiro, and M. B. Perry. 2003. Mice intradermally-inoculated with the intact lipopolysaccharide, but not the lipid A or O-chain, from Francisella tularensis LVS rapidly acquire varying degrees of enhanced resistance against systemic or aerogenic challenge with virulent strains of the pathogen. Microb. Pathog. 34:39-45.
10. Cox, J. C., and A. R. Coulter. 1997. Adjuvants - a classification and review of their modes of action. Vaccine 15:248-256.
11. Dreisbach, V. C., S. C. Cowley, and K. L. Elkins. 2000. Purified lipopolysaccharide from Francisella tularensis live vaccine strain (LVS) induces protective immunity against LVS infection that requires B cells and gamma interferon. Infect. Immun. 68:1988-1996.
12. Duckett, N. S., S. Olmos, D. M. Durrent, and D. W. Metzger. 2005. Intranasal interleukin-12 treatment for protection against respiratory infection with the Francisella tularensis live vaccine strain. Infect. Immun. 73:2306-2311.
13. Eigelsbach, H. T., and C. M. Downs. 1961. Prophylactic effectiveness of live and killed tularemia vaccines. Part I. Production of vaccine and evaluation of in the white mouse and guinea pig. J. Immunol. 87:415-425.
14. Eyles, J. E., M. G. Hartley, T. R. Laws, P. C. F. Oyston, K. F. Griffin, and R. W. Titball. 2008. Protection afforded against aerosol challenge by systemic immunisation with inactivated Francisella tularensis live vaccine strain (LVS). Microb. Pathog. 44:164-168.
15. Finn, A. 2004. Bacterial polysaccharide-protein conjugate vaccines. Br. Med. Bull. 70:1-14.
16. Foshay, L., W. H. Hesselbrock, H. J. Wittenberg, and A. H. Rodenberg. 1942. Vaccine prophylaxis against tularemia in man. Am. J. Public Health 32:1131-1145.
17. Fulop, M., R. Manchee, and R. W. Titball. 1995. Role of lipopolysaccharide and a major outer membrane protein from Francisella tularensis in the induction of immunity against tularemia. Vaccine 13:1220-1225.
18. Gavrilin, M. A., I. J. Bouskl, N. L. Knatz, M. D. Duncan, M. W. Hall, J. S. Gunn, and M. D. Wewers. 2006. Internalization and phagosome escape required for Francisella to induce human monocyte IL-1beta processing and release. Proc. Natl. Acad. Sci. USA 103:141-146.
19. Golovliov, I., M. Ericsson, L. Akerblom, G. Sandstrom, A. Tarnvik, and A. Sjostedt. 1995. Adjuvanticity of ISCOMs incorporating a T cell-reactive lipoprotein of the facultative intracellular pathogen Francisella tularensis. Vaccine 13:261-267.
20. Griffin, K. F., P. C. F. Oyston, and R. W. Titball. 2007. Francisella tularensis vaccines. FEMS Immunol. Med. Microbiol. 49:315-323.
21. Guy, B. 2007. The perfect mix: recent progress in adjuvant research. Nat. Rev. Microbiol. 5:505-517.
22. Hartley, M. G., M. Green, G. Choules, D. Rogers, D. G. Rees, S. Newsted, A. Sjostedt, and R. W. Titball. 2004. Protection afforded by heat shock protein 60 from Francisella tularensis is due to copurified lipopolysaccharide. Infect. Immun. 72:4109-4113.
23. Hornick, R. B., and H. T. Eigelsbach. 1966. Aerogenic immunization of man with live tularemia vaccine. Bacteriol. Rev. 30:532-538.
24. Katz, J., P. Zhang, M. Martin, S. N. Vogel, and S. M. Michalek. 2006. Toll-like receptor 2 is required for inflammatory responses to Francisella tularensis LVS. Infect. Immun. 74:2809-2816.
25. Latz, E., J. Franko, D. T. Golenbock, and J. R. Schreiber. 2004. Haemophilus influenzae type b-outer membrane protein complex glycoconjugate vaccine induces cytokine production by engaging human Toll-like receptor 2 (TLR2) and requires the presence of TLR2 for optimal immunogenicity. J. Immunol. 172:2431-2438.
26. Mackinnon, F. G., Y. Ho, M. S. Blake, F. Michon, A. Chandraker, M. H. Sayegh, and L. M. Wetzler. 1999. The role of B/T costimulatory signals in the immunopotentiating activity of neisserial porin. J. Infect. Dis. 180:755-761.
27. MacLeod, H., and L. M. Wetzler. 2007. T cell activation by TLRs: a role for TLRs in the adaptive immune response. Sci. STKE 402:pe48.
28. Malik, M., C. S. Bakshi, B. Sahay, A. Shah, S. A. Lotz, and T. J. Sellati. 2006. Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis. Infect. Immun. 74:3657-3662.
29. Martin, M., S. M. Michalek, and J. Katz. 2003. Role of innate immune factors in the adjuvant activity of monophosphoryl lipid A. Infect. Immun. 71:2498-2507.
30. Massari, P., P. Henneke, Y. Ho, E. Latz, D. T. Golenbock, and L. M. Wetzler. 2002. Cutting edge: immune stimulation by neisserial porins is Toll-like receptor 2 and MyD88 dependent. J. Immunol. 168:1533-1537.
31. Massari, P., C. A. King, H. MacLeod, and L. M. Wetzler. 2005. Improved purification of native meningococcal porin PorB and studies on its structure/function. Protein Expr. Purif. 44:136-146.
32. Massari, P., A. Visintin, J. Gunawardana, K. A. Halmen, C. A. King, D. T. Golenbock, and L. M. Wetzler. 2006. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J. Immunol. 176:2373-2380.
33. McCrumb, F. R. 1961. Aerosol infection of man with Francisella tularensis. Bacteriol. Rev. 25:262-267.
34. Michelsen, K. S., A. Aicher, and M. Mohaupt. 2001. The role of Toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCs). Peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J. Immunol. 276:25680-25686.
35. O'Hagan, D. T., M. L. MacKichan, and M. Singh. 2001. Recent developments in adjuvants for vaccines against infectious diseases. Biomol. Eng. 18:69-85.
36. Pantosti, A., A. O. Tzianabos, A. B. Onderdonk, and D. L. Kasper. 1991. Immunochemical characterization of two surface polysaccharides of Bacteroides fragilis. Infect. Immun. 59:2075-2082.
37. Pulendran, B. 2004. Modulating vaccine responses with dendritic cells and Toll-like receptors. Immunol. Rev. 199:227-250.
38. Sandstrom, G., A. Sjostedt, T. Johansson, K. Kuoppa, and J. C. Williams. 1992. Immunogenicity and toxicity of lipopolysaccharide from Francisella tularensis LVS. FEMS Microbiol. Immunol. 5:201-210.
39. Saslaw, S., H. T. Eigelsbach, J. A. Prior, H. E. Wilson, and S. Carhart. 1961. Tularemia vaccine study. Part II. Respiratory challenge. Arch. Intern. Med. 107:689-701.
40. Singleton, T. E., P. Massari, and L. M. Wetzler. 2005. Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J. Immunol. 174:3545-3550.
41. Tarnvik, A. 1989. Nature of protective immunity to Francisella tularensis. Rev. Infect. Dis. 11:440-451.
42. Tarnvik, A., M. Ericsson, I. Golovliov, G. Sandstrom, and A. Sjostedt. 1996. Orchestration of the protective immune response to intracellular bacteria: Francisella tularensis as a model organism. FEMS Immunol. Med. Microbiol. 13:221-225.
43. Van der Kleij, D., E. Latz, J. F. Brouwers, Y. C. Kruize, M. Schmitz, E. A. Kurt-Jones, T. Espevik, E. C. De Jong, M. L. Kapsenberg, D. T. Golenbock, A. G. Tielens, and M. Yazdanbakhsh. 2002. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates Toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 277:48122-48129.
44. Weeratna, R. D., S. R. Makinen, M. J. McCluskie, and H. L. Davis. 2005. TLR agonists as vaccine adjuvants: comparison of CpG ODN and Resiquimod (R-848). Vaccine 23:5263-5270.
45. Wetzler, L. M. 2003. The role of Toll-like receptors 2 in microbial disease and immunity. Vaccine 21(Suppl. 2):S55-S60.