Repression of bacterial lipoprotein production by francisella novicida facilitates evasion of innate immune recognition

Cellular Microbiology

Volumn 14, Issue 10, 2012, Pages 1531-1543

  Jones, Crystal L ^a,b   Sampson, Timothy R ^a,b   Nakaya, Helder I ^b   Pulendran, Bali ^a,b   Weiss, David S ^a,b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LIPOPROTEIN; TOLL LIKE RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ARTICLE; BACTERIAL VIRULENCE; CELL DIVISION; CELL SURVIVAL; CORRELATION ANALYSIS; CYTOKINE PRODUCTION; FRANCISELLA; FRANCISELLA NOVICIDA; HOST RESISTANCE; IMMUNE EVASION; IN VIVO STUDY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TULAREMIA;

ANIMALS; CELLS, CULTURED; CYTOKINES; FRANCISELLA TULARENSIS; GENE DELETION; IMMUNE EVASION; LIPOPROTEINS; MACROPHAGES; MICE; REPRESSOR PROTEINS; TOLL-LIKE RECEPTOR 2; VIRULENCE;

BACTERIA (MICROORGANISMS); FRANCISELLA; FRANCISELLA TULARENSIS SUBSP. NOVICIDA;

EID: 84866340552     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01816.x     Document Type: Article

References (51)

1. Abplanalp, A.L., Morris, I.R., Parida, B.K., Teale, J.M., and Berton, M.T. (2009) TLR-dependent control of Francisella tularensis infection and host inflammatory responses. PLoS ONE 4: e7920.
2. Akira, S., Uematsu, S., and Takeuchi, O. (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
3. Aliprantis, A.O., Yang, R.B., Mark, M.R., Suggett, S., Devaux, B., Radolf, J.D., etal. (1999) Cell activation and apoptosis by bacterial lipoproteins through Toll-like receptor-2. Science 285: 736-739.
4. Andersen-Nissen, E., Smith, K.D., Strobe, K.L., Barrett, S.L., Cookson, B.T., Logan, S.M., and Aderem, A. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc Natl Acad Sci USA 102: 9247-9252.
5. Anthony, L.D., Burke, R.D., and Nano, F.E. (1991) Growth of Francisella spp. in rodent macrophages. Infect Immun 59: 3291-3296.
6. Anthony, L.S., Gu, M.Z., Cowley, S.C., Leung, W.W., and Nano, F.E. (1991) Transformation and allelic replacement in Francisella spp. J Gen Microbiol 137: 2697-2703.
7. Bagos, P.G., Tsirigos, K.D., Liakopoulos, T.D., and Hamodrakas, S.J. (2008) Prediction of lipoprotein signal peptides in Gram-positive bacteria with a Hidden Markov Model. J Proteome Res 7: 5082-5093.
8. Brightbill, H.D., Libraty, D.H., Krutzik, S.R., Yang, R.B., Belisle, J.T., Bleharski, J.R., etal. (1999) Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285: 732-736.
9. Brotcke, A., Weiss, D.S., Kim, C.C., Chain, P., Malfatti, S., Garcia, E., and Monack, D.M. (2006) Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis Infect Immun 74: 6642-6655.
10. Cole, L.E., Elkins, K.L., Michalek, S.M., Qureshi, N., Eaton, L.J., Rallabhandi, P., etal. (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.
11. Cole, L.E., Shirey, K.A., Barry, E., Santiago, A., Rallabhandi, P., Elkins, K.L., etal. (2007) Toll-like receptor 2-mediated signaling requirements for Francisella tularensis live vaccine strain infection of murine macrophages. Infect Immun 75: 4127-4137.
12. De Pascalis, R., Taylor, B.C., and Elkins, K.L. (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.
13. Dickinson, G.S., Piccone, H., Sun, G., Lien, E., Gatto, L., and Alugupalli, K.R. (2010) Toll-like receptor 2 deficiency results in impaired antibody responses and septic shock during Borrelia hermsii infection. Infect Immun 78: 4579-4588.
14. Embers, M.E., Alvarez, X., Ooms, T., and Philipp, M.T. (2008) The failure of immune response evasion by linear plasmid 28-1-deficient Borrelia burgdorferi is attributable to persistent expression of an outer surface protein. Infect Immun 76: 3984-3991.
15. Follett, E.A., and Gordon, J. (1963) An electron microscope study of Vibrio flagella. J Gen Microbiol 32: 235-239.
16. Gallagher, L.A., McKevitt, M., Ramage, E.R., and Manoil, C. (2008) Genetic dissection of the Francisella novicida restriction barrier. J Bacteriol 190: 7830-7837.
17. Gozal, Y.M., Seyfried, N.T., Gearing, M., Glass, J.D., Heilman, C.J., Wuu, J., etal. (2011) Aberrant septin 11 is associated with sporadic frontotemporal lobar degeneration. Mol Neurodegener 6: 82.
18. Hall, J.D., Woolard, M.D., Gunn, B.M., Craven, R.R., Taft-Benz, S., Frelinger, J.A., and Kawula, T.H. (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.
19. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., etal. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
20. Hemmi, H., Takeuchi, O., Kawai, T., Kaisho, T., Sato, S., Sanjo, H., etal. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
21. Jones, J.D., Bourell, K.W., Norgard, M.V., and Radolf, J.D. (1995) Membrane topology of Borrelia burgdorferi and Treponema pallidum lipoproteins. Infect Immun 63: 2424-2434.
22. Kadzhaev, K., Zingmark, C., Golovliov, I., Bolanowski, M., Shen, H., Conlan, W., and Sjostedt, A. (2009) Identification of genes contributing to the virulence of Francisella tularensis SCHU S4 in a mouse intradermal infection model. PLoS ONE 4: e5463.
23. Kanistanon, D., Hajjar, A.M., Pelletier, M.R., Gallagher, L.A., Kalhorn, T., Shaffer, S.A., etal. (2008) A Francisella mutant in lipid A carbohydrate modification elicits protective immunity. PLoS Pathog 4: e24.
24. Kawahara, K., Tsukano, H., Watanabe, H., Lindner, B., and Matsuura, M. (2002) Modification of the structure and activity of lipid A in Yersinia pestis lipopolysaccharide by growth temperature. Infect Immun 70: 4092-4098.
25. Kraemer, P.S., Mitchell, A., Pelletier, M.R., Gallagher, L.A., Wasnick, M., Rohmer, L., etal. (2009) Genome-wide screen in Francisella novicida for genes required for pulmonary and systemic infection in mice. Infect Immun 77: 232-244.
26. Kumar, H., Kawai, T., and Akira, S. (2009) Toll-like receptors and innate immunity. Biochem Biophys Res Commun 388: 621-625.
27. Li, H., Nookala, S., Bina, X.R., Bina, J.E., and Re, F. (2006) Innate immune response to Francisella tularensis is mediated by TLR2 and caspase-1 activation. J Leukoc Biol 80: 766-773.
28. Liang, F.T., Jacobs, M.B., Bowers, L.C., and Philipp, M.T. (2002) An immune evasion mechanism for spirochetal persistence in Lyme borreliosis. J Exp Med 195: 415-422.
29. Lien, E., Means, T.K., Heine, H., Yoshimura, A., Kusumoto, S., Fukase, K., etal. (2000) Toll-like receptor 4 imparts ligand-specific recognition of bacterial lipopolysaccharide. J Clin Invest 105: 497-504.
30. Maier, T.M., Havig, A., Casey, M., Nano, F.E., Frank, D.W., and Zahrt, T.C. (2004) Construction and characterization of a highly efficient Francisella shuttle plasmid. Appl Environ Microbiol 70: 7511-7519.
31. Malik, M., Bakshi, C.S., Sahay, B., Shah, A., Lotz, S.A., and Sellati, T.J. (2006) Toll-like receptor 2 is required for control of pulmonary infection with Francisella tularensis Infect Immun 74: 3657-3662.
32. Muzio, M., Bosisio, D., Polentarutti, N., D'Amico, G., Stoppacciaro, A., Mancinelli, R., etal. (2000) Differential expression and regulation of Toll-like receptors (TLR) in human leukocytes: selective expression of TLR3 in dendritic cells. J Immunol 164: 5998-6004.
33. Nadler, C., Baruch, K., Kobi, S., Mills, E., Haviv, G., Farago, M., etal. (2010) The type III secretion effector NleE inhibits NF-kappaB activation. PLoS Pathog 6: e1000743.
34. Parsa, K.V., Butchar, J.P., Rajaram, M.V., Cremer, T.J., Gunn, J.S., Schlesinger, L.S., and Tridandapani, S. (2008) Francisella gains a survival advantage within mononuclear phagocytes by suppressing the host IFNgamma response. Mol Immunol 45: 3428-3437.
35. Peng, K., Broz, P., Jones, J., Joubert, L.M., and Monack, D. (2011) Elevated AIM2-mediated pyroptosis triggered by hypercytotoxic Francisella mutant strains is attributed to increased intracellular bacteriolysis. Cell Microbiol 13: 1586-1600.
36. Radhakrishnan, G.K., Yu, Q., Harms, J.S., and Splitter, G.A. (2009) Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J Biol Chem 284: 9892-9898.
37. Rohmer, L., Fong, C., Abmayr, S., Wasnick, M., Larson Freeman, T.J., Radey, M., etal. (2007) Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol 8: R102.
38. Salcedo, S.P., Marchesini, M.I., Lelouard, H., Fugier, E., Jolly, G., Balor, S., etal. (2008) Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog 4: e21.
39. Santic, M., Molmeret, M., and 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.
40. Santic, M., Asare, R., Skrobonja, I., Jones, S., and Abu Kwaik, Y. (2008) Acquisition of the vacuolar ATPase proton pump and phagosome acidification are essential for escape of Francisella tularensis into the macrophage cytosol. Infect Immun 76: 2671-2677.
41. Sjostedt, A., Conlan, J.W., and North, R.J. (1994) Neutrophils are critical for host defense against primary infection with the facultative intracellular bacterium Francisella tularensis in mice and participate in defense against reinfection. Infect Immun 62: 2779-2783.
42. Soehnlein, O., and Lindbom, L. (2010) Phagocyte partnership during the onset and resolution of inflammation. Nat Rev Immunol 10: 427-439.
43. Su, J., Yang, J., Zhao, D., Kawula, T.H., Banas, J.A., and Zhang, J.R. (2007) Genome-wide identification of Francisella tularensis virulence determinants. Infect Immun 75: 3089-3101.
44. Tanamoto, K., and Azumi, S. (2000) Salmonella-type heptaacylated lipid A is inactive and acts as an antagonist of lipopolysaccharide action on human line cells. J Immunol 164: 3149-3156.
45. Telepnev, M., Golovliov, I., Grundstrom, T., Tarnvik, A., and 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.
46. Thakran, S., Li, H., Lavine, C.L., Miller, M.A., Bina, J.E., Bina, X.R., and Re, F. (2008) Identification of Francisella tularensis lipoproteins that stimulate the Toll-like receptor (TLR) 2/TLR1 heterodimer. J Biol Chem 283: 3751-3760.
47. Vidal, V., Scragg, I.G., Cutler, S.J., Rockett, K.A., Fekade, D., Warrell, D.A., etal. (1998) Variable major lipoprotein is a principal TNF-inducing factor of louse-borne relapsing fever. Nat Med 4: 1416-1420.
48. Wang, X., Ribeiro, A.A., Guan, Z., Abraham, S.N., and Raetz, C.R. (2007) Attenuated virulence of a Francisella mutant lacking the lipid A 4′-phosphatase. Proc Natl Acad Sci USA 104: 4136-4141.
49. Weiss, D.S., Brotcke, A., Henry, T., Margolis, J.J., Chan, K., and Monack, D.M. (2007) In vivo negative selection screen identifies genes required for Francisella virulence. Proc Natl Acad Sci USA 104: 6037-6042.
50. Winter, S.E., Winter, M.G., Godinez, I., Yang, H.J., Russmann, H., Andrews-Polymenis, H.L., and Baumler, A.J. (2010) A rapid change in virulence gene expression during the transition from the intestinal lumen into tissue promotes systemic dissemination of Salmonella PLoS Pathog 6: e1001060.
51. Yoon, S.S., and Mekalanos, J.J. (2008) Decreased potency of the Vibrio cholerae sheathed flagellum to trigger host innate immunity. Infect Immun 76: 1282-1288.