Crystal structures of the Toll/Interleukin-1 Receptor (TIR) domains from the brucella protein TcpB and host adaptor TIRAP reveal mechanisms of molecular mimicry

Journal of Biological Chemistry

Volumn 289, Issue 2, 2014, Pages 669-679

  Snyder, Greg A ^a,e   Deredge, Daniel ^b   Waldhuber, Anna ^c   Fresquez, Theresa ^a   Wilkins, David Z ^d   Smith, Patrick T ^a   Durr, Susi ^c   Cirl, Christine ^c   Jiang, Jiansheng ^a   Jennings, William ^a   Luchetti, Timothy ^a   Snyder, Nathaniel ^a   Sundberg, Eric J ^d,e   Wintrode, Patrick ^b   Miethke, Thomas ^f   Xiao, T Sam ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF PHARMACY   (United States)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^d INSTITUTE OF HUMAN VIROLOGY   (United States)

^e UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRUCELLA; DOMAIN STRUCTURE; INNATE IMMUNES; MOLECULAR MIMICRY;

BIOCHEMISTRY;

BIOLOGY;

BACTERIAL PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN TCPB; PROTEIN TIRAP; TOLL LIKE RECEPTOR ADAPTOR MOLECULE 1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL METABOLISM; BINDING SITE; BRUCELLA; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; DISULFIDE BOND; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INNATE IMMUNITY; MASS SPECTROMETRY; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

BACTERIAL PATHOGENESIS; CRYSTAL STRUCTURE; INNATE IMMUNITY; MAL TIRAP; SIGNAL TRANSDUCTION; TCPB; TOLL IL-1 RECEPTOR (TIR) DOMAIN;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BINDING SITES; BRUCELLA MELITENSIS; CRYSTALLOGRAPHY, X-RAY; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MEMBRANE GLYCOPROTEINS; MODELS, MOLECULAR; MOLECULAR MIMICRY; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, INTERLEUKIN-1; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; VIRULENCE FACTORS;

EID: 84891942344     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.523407     Document Type: Article

References (44)

1. Kenny, E. F., and O'Neill, L. A. (2008Signalling adaptors used by Toll-like receptors. An update. Cytokine 43, 342-349
2. Cirl, C., Wieser, A., Yadav, M., Duerr, S., Schubert, S., Fischer, H., Stappert, D., Wantia, N., Rodriguez, N., Wagner, H., Svanborg, C., and Miethke, T. (2008Subversion of Toll-like receptor signaling by a unique family of bacterial Toll/interleukin-1 receptor domain-containing proteins. Nat. Med. 14, 399-406
3. Radhakrishnan, G. K., Yu, Q., Harms, J. S., and Splitter, G. A. (2009Brucella TIR domain-containing protein mimics properties of the Toll-like receptor adaptor protein TIRAP. J. Biol. Chem. 284, 9892-9898
4. Salcedo, S. P., Marchesini, M. I., Lelouard, H., Fugier, E., Jolly, G., Balor, S., Muller, A., Lapaque, N., Demaria, O., Alexopoulou, L., Comerci, D. J., Ugalde, R. A., Pierre, P., and Gorvel, J.-P. (2008Brucella control of dendritic cell maturation is dependent on the TIR-containing protein Btp1. PLoS Pathog. 4, e21
5. Newman, R. M., Salunkhe, P., Godzik, A., and Reed, J. C. (2006Identification and characterization of a novel bacterial virulence factor that shares homology with mammalian Toll/interleukin-1 receptor family proteins. Infect. Immun. 74, 594-601
6. Low, L. Y., Mukasa, T., Reed, J. C., and Pascual, J. (2007Characterization of a TIR-like protein from Paracoccus denitrificans. Biochem. Biophys. Res. Commun. 356, 481-486
7. Rana, R. R., Simpson, P., Zhang, M., Jennions, M., Ukegbu, C., Spear, A. M., Alguel, Y., Matthews, S. J., Atkins, H. S., and Byrne, B. (2011Yersinia pestis TIR-domain protein forms dimers that interact with the human adaptor protein MyD88. Microb. Pathog. 51, 89-95
8. Cirl, C., and Miethke, T. (2010Microbial Toll/interleukin 1 receptor proteins. A new class of virulence factors. Int. J. Med. Microbiol. 300, 396-401
9. Yadav, M., Zhang, J., Fischer, H., Huang, W., Lutay, N., Cirl, C., Lum, J., Miethke, T., and Svanborg, C. (2010Inhibition of TIR domain signaling by TcpC. MyD88-dependent and independent effects on Escherichia coli virulence. PLoS Pathog. 6, e1001120
10. Snyder, G. A., and Sundberg, E. J. (May 22, 2013Molecular interactions in interleukin and Toll-like receptor signaling pathways. Curr. Pharm. Des. 10.2174.13816128113199990069
11. Xiao, T. S. (2010Subversion of innate immune signaling through molec-ular mimicry. J. Clin. Immunol. 30, 638-642
12. Snyder, G. A., Cirl, C., Jiang, J., Chen, K., Waldhuber, A., Smith, P., Römmler, F., Snyder, N., Fresquez, T., and Dürr, S. (2013Molecular mechanisms for the subversion of MyD88 signaling by TcpC from virulent uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. U.S.A. 110, 6985-6990
13. O'Neill, L. A., and Bowie, A. G. (2007The family of five. TIR-domaincontaining adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7, 353-364
14. Campos, M. A., Rosinha, G. M., Almeida, I. C., Salgueiro, X. S., Jarvis, B. W., Splitter, G. A., Qureshi, N., Bruna-Romero, O., Gazzinelli, R. T., and Oliveira, S. C. (2004Role of Toll-like receptor 4 in induction of cellmediated immunity and resistance to Brucella abortus infection in mice. Infect. Immun. 72, 176-186
15. Sengupta, D., Koblansky, A., Gaines, J., Brown, T., West, A. P., Zhang, D., Nishikawa, T., Park, S.-G., Roop, R. M., 2nd, and Ghosh, S. (2010Subversion of innate immune responses by Brucella through the targeted degradation of the TLR signaling adapter, MAL. J. Immunol. 184, 956-964
16. Kagan, J. C., and Medzhitov, R. (2006Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125, 943-955
17. Chaudhary, A., Ganguly, K., Cabantous, S., Waldo, G. S., Micheva-Viteva, S. N., Nag, K., Hlavacek, W. S., and Tung, C.-S. (2012The Brucella TIRlike protein TcpB interacts with the death domain of MyD88. Biochem. Biophys. Res. Commun. 417, 299-304
18. Radhakrishnan, G. K., Harms, J. S., and Splitter, G. A. (2011Modulation of microtubule dynamics by a TIR domain protein from the intracellular pathogen Brucella melitensis. Biochem. J. 439, 79-83
19. Schmidt, T. G., and Skerra, A. (2007The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat. Protoc. 2, 1528-1535
20. Radhakrishnan, G. K., and Splitter, G. A. (2010Biochemical and functional analysis of TIR domain containing protein from Brucella melitensis. Biochem. Biophys. Res. Commun. 397, 59-63
21. Otwinowski, Z., and Minor, W. (1997Processing of X-ray diffraction data. Methods Enzymol. 276, 307-326
22. Kabsch, W. (2010XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
23. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
24. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
25. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
26. Sheldrick, G. M. (2008A short history of SHELX. Acta Crystallogr. A 64, 112-122
27. Snyder, G., Jiang, J., Chen, K., Fresquez, T., Smith, P., Snyder, N., Luchetti, T., Cirl, C., Miethke, T., Tjandra, N., and Xiao, T. (2010Structural studies of Toll like receptor signaling adapters. J. Immunol. 184, 136.45
28. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
29. Yang, H., Guranovic, V., Dutta, S., Feng, Z., Berman, H. M., and Westbrook, J. D. (2004Automated and accurate deposition of structures solved by X-ray diffraction to the Protein Data Bank. Acta Crystallogr. D Biol. Crystallogr. 60, 1833-1839
30. DeLano, W. L. (2010The PyMOL Molecular Graphics System, version 1.3r1, Schrodinger, LLC, New York
31. Holm, L., and Rosenström, P. (2010Dali server. Conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549
32. Lee, B., and Richards, F. M. (1971The interpretation of protein structures. Estimation of static accessibility. J. Mol. Biol. 55, 379-400
33. Potterton, L., McNicholas, S., Krissinel, E., Gruber, J., Cowtan, K., Emsley, P., Murshudov, G. N., Cohen, S., Perrakis, A., and Noble, M. (2004Developments in the CCP4 molecular-graphics project. Acta Crystallogr. D Biol. Crystallogr. 60, 2288-2294
34. Krissinel, E., and Henrick, K. (2007Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797
35. Valkov, E., Stamp, A., Dimaio, F., Baker, D., Verstak, B., Roversi, P., Kellie, S., Sweet, M. J., Mansell, A., Gay, N. J., Martin, J. L., and Kobe, B. (2011Crystal structure of Toll-like receptor adaptor MAL/TIRAP reveals the molecular basis for signal transduction and disease protection. Proc. Natl. Acad. Sci. U.S.A. 108, 14879-14884
36. Lin, Z., Lu, J., Zhou, W., and Shen, Y. (2012Structural insights into TIR domain specificity of the bridging adaptor Mal in TLR4 signaling. PLoS One 7, e34202
37. Kaplan-Türköz, B., Koelblen, T., Felix, C., Candusso, M.-P., O'Callaghan, D., Vergunst, A. C., and Terradot, L. (2013Structure of the Toll/interleukin 1 receptor (TIRdomain of the immunosuppressive Brucella effector BtpA/Btp1/TcpB. FEBS Lett. 587, 3412-3416
38. Jiang, Z., Georgel, P., Li, C., Choe, J., Crozat, K., Rutschmann, S., Du, X., Bigby, T., Mudd, S., Sovath, S., Wilson, I. A., Olson, A., and Beutler, B. (2006Details of Toll-like receptor:adapter interaction revealed by germline mutagenesis. Proc. Natl. Acad. Sci. U.S.A. 103, 10961-10966
39. Kissner, T. L., Moisan, L., Mann, E., Alam, S., Ruthel, G., Ulrich, R. G., Rebek, M., Rebek, J., Jr., and Saikh, K. U. (2011A small molecule that mimics the BB-loop in the Toll interleukin-1 (IL-1receptor domain of MyD88 attenuates staphylococcal enterotoxin B-induced pro-inflammatory cytokine production and toxicity in mice. J. Biol. Chem. 286, 31385-31396
40. Loiarro, M., Capolunghi, F., Fantò, N., Gallo, G., Campo, S., Arseni, B., Carsetti, R., Carminati, P., De Santis, R., Ruggiero, V., and Sette, C. (2007Pivotal advance. Inhibition of MyD88 dimerization and recruitment of IRAK1 and IRAK4 by a novel peptidomimetic compound. J. Leukocyte Biol. 82, 801-810
41. Loiarro, M. (2005Peptide-mediated interference of TIR domain dimerization in MyD88 inhibits interleukin-1-dependent activation of NF-B. J. Biol. Chem. 280, 15809-15814
42. Tao, X., Xu, Y., Zheng, Y., Beg, A. A., and Tong, L. (2002An extensively associated dimer in the structure of the C713S mutant of the TIR domain of human TLR2. Biochem. Biophys. Res. Commun. 299, 216-221
43. Kavan, D., and Man, P. (2011MSTools. Web based application for visualization and presentation of HXMS data. Int. J. Mass Spectrom. 302, 53-58
44. Alaidarous, M., Ve, T., Casey, L. W., Valkov, E., Ericsson, D. J., Ullah, M. O., Schembri, M. A., Mansell, A., Sweet, M. J., and Kobe, B. (2014Mechanism of bacterial interference with TLR4 signaling by Brucella Toll/interleukin-1 receptor domain-containing protein TcpB. J. Biol. Chem. 289, 654-668