Subversion of innate immune responses by brucella through the targeted degradation of the TLR signaling adapter, MAL

Journal of Immunology

Volumn 184, Issue 2, 2010, Pages 956-964

  Sengupta, Dola ^a   Koblansky, Alicia ^a,b   Gaines, Jennifer ^c   Brown, Tim ^c   West, A Phillip ^a   Zhang, Dekai ^a,d   Nishikawa, Tak ^a   Park, Sung Gyoo ^a,b   Roop II, R Martin ^c   Ghosh, Sankar ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Columbia University ^*  (United States)

^c EAST CAROLINA UNIVERSITY   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; INTERLEUKIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR; INTERLEUKIN 1 RECEPTOR; MEMBRANE PROTEIN; TIRAP PROTEIN, HUMAN; TLR4 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 4; UBIQUITIN; VIRUS PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRUCELLA ABORTUS; BRUCELLOSIS; CONTROLLED STUDY; FEMALE; GRAM NEGATIVE BACTERIUM; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MACROPHAGE; MUTANT; NONHUMAN; OSTEOMYELITIS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; BRUCELLA; CELL LINE; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; PHYSIOLOGY; SEQUENCE HOMOLOGY;

BRUCELLA; CELL LINE; HUMANS; IMMUNITY, INNATE; MEMBRANE GLYCOPROTEINS; PHOSPHORYLATION; RECEPTORS, INTERLEUKIN-1; SEQUENCE HOMOLOGY, AMINO ACID; TOLL-LIKE RECEPTOR 4; UBIQUITIN; VIRAL PROTEINS;

EID: 76249100903     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0902008     Document Type: Article

References (54)

1. O'Neill, L. A. 2006. How Toll-like receptors signal: what we know and what we don't know. Curr. Opin. Immunol. 18: 3-9.
2. West, A. P., A. A. Koblansky, and S. Ghosh. 2006. Recognition and signaling by toll-like receptors. Annu. Rev. Cell Dev. Biol. 22: 409-437.
3. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
4. O'Neill, L. A., K. A. Fitzgerald, and A. G. Bowie. 2003. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol. 24: 286-290.
5. Medzhitov, R., P. Preston-Hurlburt, E. Kopp, A. Stadlen, C. Chen, S. Ghosh, and C. A. Janeway, Jr. 1998. MyD88 is an adaptor protein in the hToll/IL-1 receptor family signaling pathways. Mol. Cell 2: 253-258. (Pubitemid 128373651)
6. Fitzgerald, K. A., E. M. Palsson-McDermott, A. G. Bowie, C. A. Jefferies, A. S. Mansell, G. Brady, E. Brint, A. Dunne, P. Gray, and M. T. Harte. 2001. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 413: 78-83.
7. Horng, T., G. M. Barton, and R. Medzhitov. 2001. TIRAP: an adapter molecule in the Toll signaling pathway. Nat. Immunol. 2: 835-841.
8. Yamamoto, M., S. Sato, K. Mori, K. Hoshino, O. Takeuchi, K. Takeda, and S. Akira. 2002. Cutting edge: a novel Toll/IL-1 receptor domain-containing adapter that preferentially activates the IFN-β promoter in the Toll-like receptor signaling. J. Immunol. 169: 6668-6672. (Pubitemid 36899248)
9. Oshiumi, H., M. Matsumoto, K. Funami, T. Akazawa, and T. Seya. 2003. TICAM-1, an adaptor molecule that participates in Toll-like receptor 3-mediated interferon-β induction. Nat. Immunol. 4: 161-167.
10. Fitzgerald, K. A., D. C. Rowe, B. J. Barnes, D. R. Caffrey, A. Visintin, E. Latz, B. Monks, P. M. Pitha, and D. T. Golenbock. 2003. LPS-TLR4 signaling to IRF-3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198: 1043-1055.
11. Yamamoto, M., S. Sato, H. Hemmi, S. Uematsu, K. Hoshino, T. Kaisho, O. Takeuchi, K. Takeda, and S. Akira. 2003. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4: 1144-1150.
12. Oshiumi, H., M. Sasai, K. Shida, T. Fujita, M. Matsumoto, and T. Seya. 2003. TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to toll-like receptor 4 TICAM-1 that induces interferon-β. J. Biol. Chem. 278: 49751-49762.
13. Mink, M., B. Fogelgren, K. Olszewski, P. Maroy, and K. Csiszar. 2001. A novel human gene (SARM) at chromosome 17q11 encodes a protein with a SAM motif and structural similarity to Armadillo/β-catenin that is conserved in mouse, Drosophila, and Caenorhabditis elegans. Genomics 74: 234-244.
14. Liberati, N. T., K. A. Fitzgerald, D. H. Kim, R. Feinbaum, D. T. Golenbock, and F. M. Ausubel. 2004. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. U.S.A. 101: 6593-6598.
15. Horng, T., G. M. Barton, R. A. Flavell, and R. Medzhitov. 2002. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420: 329-333.
16. Carty, M., R. Goodbody, M. Schröder, J. Stack, P. N. Moynagh, and A. G. Bowie. 2006. The human adaptor SARM negatively regulates adaptor protein TRIF-dependent Toll-like receptor signaling. Nat. Immunol. 7: 1074-1081.
17. O'Neill, L. A., and A. G. Bowie. 2007. The family of five: TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7: 353-364.
18. Roop, R. M., 2nd, B. H. Bellaire, M. W. Valderas, and J. A. Cardelli. 2004. Adaptation of the Brucellae to their intracellular niche. Mol. Microbiol. 52: 621-630.
19. Franco, M. P., M. Mulder, R. H. Gilman, and H. L. Smits. 2007. Human brucellosis. Lancet Infect. Dis. 7: 775-786.
20. Pappas, G., N. Akritidis, M. Bosilkovski, and E. Tsianos. 2005. Brucellosis. N. Engl. J. Med. 352: 2325-2336.
21. Nicoletti, P., R. P. Lenk, M. C. Popescu, and C. E. Swenson. 1989. Efficacy of various treatment regimens, using liposomal streptomycin in cows with brucellosis. Am. J. Vet. Res. 50: 1004-1007.
22. Franz, D. R., P. B. Jahrling, A. M. Friedlander, D. J. McClain, D. L. Hoover, W. R. Bryne, J. A. Pavlin, G. W. Christopher, and E. M. Eitzen, Jr. 1997. Clinical recognition and management of patients exposed to biological warfare agents. JAMA 278: 399-411.
23. Pappas, G., and P. Papadimitriou. 2007. Challenges in Brucella bacteraemia. Int. J. Antimicrob. Agents 30(Suppl 1): S29-S31.
24. Greenfield, R. A., D. A. Drevets, L. J. Machado, G. W. Voskuhl, P. Cornea, and M. S. Bronze. 2002. Bacterial pathogens as biological weapons and agents of bioterrorism. Am. J. Med. Sci. 323: 299-315.
25. Pappas, G., P. Panagopoulou, L. Christou, and N. Akritidis. 2006. Brucella as a biological weapon. Cell. Mol. Life Sci. 63: 2229-2236.
26. Barquero-Calvo, E., E. Chaves-Olarte, D. S. Weiss, C. Guzmán-Verri, C. Chacón-Díaz, A. Rucavado, I. Moriyón, and E. Moreno. 2007. Brucella abortus uses a stealthy strategy to avoid activation of the innate immune system during the onset of infection. PLoS One 2: e631.
27. Forestier, C., F. Deleuil, N. Lapaque, E. Moreno, and J. P. Gorvel. 2000. Brucella abortus lipopolysaccharide in murine peritoneal macrophages acts as a down-regulator of T cell activation. J. Immunol. 165: 5202-5210.
28. Pizarro-Cerdá, J., S. Méresse, R. G. Parton, G. van der Goot, A. Sola-Landa, I. Lopez-Goñi, E. Moreno, and J. P. Gorvel. 1998. Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes. Infect. Immun. 66: 5711-5724.
29. Celli, J., C. de Chastellier, D. M. Franchini, J. Pizarro-Cerda, E. Moreno, and J. P. Gorvel. 2003. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 198: 545-556.
30. Celli, J., and J. P. Gorvel. 2004. Organelle robbery: Brucella interactions with the endoplasmic reticulum. Curr. Opin. Microbiol. 7: 93-97.
31. Backert, S., and T. F. Meyer. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr. Opin. Microbiol. 9: 207-217.
32. Lavigne, J. P., G. Patey, F. J. Sangari, G. Bourg, M. Ramuz, D. O'Callaghan, and S. Michaux-Charachon. 2005. Identification of a new virulence factor, BvfA, in Brucella suis. Infect. Immun. 73: 5524-5529.
33. Arellano-Reynoso, B., N. Lapaque, S. Salcedo, G. Briones, A. E. Ciocchini, R. Ugalde, E. Moreno, I. Moriyón, and J. P. Gorvel. 2005. Cyclic β-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat. Immunol. 6: 618-625.
34. Oliveira, S. C., F. S. de Oliveira, G. C. Macedo, L. A. de Almeida, and N. B. Carvalho. 2008. The role of innate immune receptors in the control of Brucella abortus infection: toll-like receptors and beyond. Microbes Infect. 10: 1005-1009.
35. Cirl, C., A. Wieser, M. Yadav, S. Duerr, S. Schubert, H. Fischer, D. Stappert, N. Wantia, N. Rodriguez, H. Wagner, et al. 2008. Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 14: 399-406.
36. Newman, R. M., P. Salunkhe, A. Godzik, and J. C. Reed. 2006. Identification and characterization of a novel bacterial virulence factor that shares homology with mammalian Toll/interleukin-1 receptor family proteins. Infect. Immun. 74: 594-601.
37. Radhakrishnan, G. K., Q. Yu, J. S. Harms, and G. A. Splitter. 2009. Brucella TIR domain-containing protein mimics properties of the toll-like receptor adaptor protein TIRAP. J. Biol. Chem. 284: 9892-9898.
38. Elzer, P. H., R. W. Phillips, M. E. Kovach, K. M. Peterson, and R. M. Roop 2nd. 1994. Characterization and genetic complementation of a Brucella abortus high-temperature- requirement A (htrA) deletionmutant. Infect. Immun. 62: 4135-4139.
39. Alton, G. G., L. M. Jones, R. D. Angus, and J. M. Verger. 1988. Techniques for the brucellosis laboratory. Paris, France.
40. Gee, J. M., M.W. Valderas, M. E. Kovach, V. K. Grippe, G. T. Robertson, W. Ng, J. M. Richardson, M. E. Winkler, and R. M. Roop. 2005. The Brucella abortus Cu, Zn superoxide dismutase is required for optimal resistance to oxidative killing by murine macrophages and wild-type virulence in experimentally infected mice. Infect. Immun. 73: 2873-2880.
41. Salcedo, S. P., M. I. Marchesini, H. Lelouard, E. Fugier, G. Jolly, S. Balor, A. Muller, N. Lapaque, O. Demaria, L. Alexopoulou, et al. 2008. Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog. 4: e21.
42. Xu, Y., X. Tao, B. Shen, T. Horng, R. Medzhitov, J. L. Manley, and L. Tong. 2000. Structural basis for signal transduction by the Toll/interleukin-1 receptor domains. Nature 408: 111-115.
43. Dunne, A., M. Ejdeback, P. L. Ludidi, L. A. O'Neill, and N. J. Gay. 2003. Structural complementarity of Toll/interleukin-1 receptor domains in Toll-like receptors and the adaptors Mal and MyD88. J. Biol. Chem. 278: 41443-41451.
44. Campos, M. A., G. M. Rosinha, I. C. Almeida, X. S. Salgueiro, B. W. Jarvis, G. A. Splitter, N. Qureshi, O. Bruna-Romero, R. T. Gazzinelli, and S. C. Oliveira. 2004. Role of Toll-like receptor 4 in induction of cell-mediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 72: 176-186.
45. Dueñas, A. I., A. Orduña, M. S. Crespo, and C. García-Rodríguez. 2004. Interaction of endotoxins with Toll-like receptor 4 correlates with their endotoxic potential and may explain the proinflammatory effect of Brucella spp. LPS. Int. Immunol. 16: 1467-1475.
46. Kagan, J. C., and R. Medzhitov. 2006. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955.
47. Gray, P., A. Dunne, C. Brikos, C. A. Jefferies, S. L. Doyle, and L. A. O'Neill. 2006. MyD88 adapter-like (Mal) is phosphorylated by Bruton's tyrosine kinase during TLR2 and TLR4 signal transduction. J. Biol. Chem. 281: 10489-10495.
48. Piao, W., C. Song, H. Chen, L. M. Wahl, K. A. Fitzgerald, L. A. O'Neill, and A. E. Medvedev. 2008. Tyrosine phosphorylation of MyD88 adapter-like (Mal) is critical for signal transduction and blocked in endotoxin tolerance. J. Biol. Chem. 283: 3109-3119.
49. Mansell, A., R. Smith, S. L. Doyle, P. Gray, J. E. Fenner, P. J. Crack, S. E. Nicholson, D. J. Hilton, L. A. O'Neill, and P. J. Hertzog. 2006. Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat. Immunol. 7: 148-155.
50. Kamizono, S., T. Hanada, H. Yasukawa, S. Minoguchi, R. Kato, M. Minoguchi, K. Hattori, S. Hatakeyama, M. Yada, S. Morita, et al. 2001. The SOCS box of SOCS-1 accelerates ubiquitin-dependent proteolysis of TEL-JAK2. J. Biol. Chem. 276: 12530-12538.
51. Zhang, J. G., A. Farley, S. E. Nicholson, T. A. Willson, L. M. Zugaro, R. J. Simpson, R. L. Moritz, D. Cary, R. Richardson, G. Hausmann, et al. 1999. The conserved SOCS box motif in suppressors of cytokine signaling binds to elongins B and C and may couple bound proteins to proteasomal degradation. Proc. Natl. Acad. Sci. U.S.A. 96: 2071-2076.
52. Arenas, G. N., A. S. Staskevich, A. Aballay, and L. S. Mayorga. 2000. Intracellular trafficking of Brucella abortus in J774 macrophages. Infect. Immun. 68: 4255-4263.
53. Jefferies, C. A., S. Doyle, C. Brunner, A. Dunne, E. Brint, C. Wietek, E. Walch, T. Wirth, and L. A. O'Neill. 2003. Bruton's tyrosine kinase is a Toll/interleukin-1 receptor domain-binding protein that participates in nuclear factor kappaB activation by Toll-like receptor 4. J. Biol. Chem. 278: 26258-26264.
54. Núñez Miguel, R., J. Wong, J. F. Westoll, H. J. Brooks, L. A. O'Neill, N. J. Gay, C. E. Bryant, and T. P. Monie. 2007. A dimer of the Toll-like receptor 4 cytoplasmic domain provides a specific scaffold for the recruitment of signalling adaptor proteins. PLoS One 2: e788.