Human TLRs 10 and 1 share common mechanisms of innate immune sensing but not signaling

Journal of Immunology

Volumn 184, Issue 9, 2010, Pages 5094-5103

  Guan, Yue ^a   Ranoa, Diana Rose E ^a   Jiang, Song ^a   Mutha, Sarita K ^a   Li, Xinyan ^a   Baudry, Jerome ^c   Tapping, Richard I ^a,b  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c OAK RIDGE NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 8; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 10; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6; HYBRID PROTEIN; LIPOPEPTIDE; TLR10 PROTEIN, HUMAN; TLR2 PROTEIN, HUMAN;

ANTIGEN RECOGNITION; ARTICLE; CELL STRAIN HEK293; COLON MUCOSA; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOPRECIPITATION; INNATE IMMUNITY; MUTATIONAL ANALYSIS; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; WESTERN BLOTTING; AMINO ACID SEQUENCE; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CHEMISTRY; COMPARATIVE STUDY; DRUG POTENTIATION; EXTRACELLULAR SPACE; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; PSEUDOGENE; SYNTHESIS; TUMOR CELL LINE;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE; CELL LINE, TUMOR; EXTRACELLULAR SPACE; HUMANS; IMMUNITY, INNATE; LIPOPEPTIDES; MICE; MICE, KNOCKOUT; MODELS, IMMUNOLOGICAL; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; PSEUDOGENES; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 10; TOLL-LIKE RECEPTOR 2;

EID: 77954480383     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901888     Document Type: Article

References (74)

1. Fearon, D. T. 1997. Seeking wisdom in innate immunity. Nature 388: 323-324.
2. Medzhitov, R., and C. A. Janeway, Jr. 1997. Innate immunity: impact on the adaptive immune response. Curr. Opin. Immunol. 9: 4-9.
3. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801.
4. Iwasaki, A., and R. Medzhitov. 2004. Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5: 987-995.
5. Zhang, Z., and H. J. Schluesener. 2006. Mammalian toll-like receptors: from endogenous ligands to tissue regeneration. Cell. Mol. Life Sci. 63: 2901-2907.
6. Muzio, M., D. Bosisio, N. Polentarutti, G. D'amico, A. Stoppacciaro, R. Mancinelli, C. van't Veer, G. Penton-Rol, L. P. Ruco, P. Allavena, and A. Mantovani. 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.
7. Zarember, K. A., and P. J. Godowski. 2002. Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J. Immunol. 168: 554-561.
8. Faure, E., O. Equils, P. A. Sieling, L. Thomas, F. X. Zhang, C. J. Kirschning, N. Polentarutti, M. Muzio, and M. Arditi. 2000. Bacterial lipopolysaccharide activates NF-kappaB through toll-like receptor 4 (TLR-4) in cultured human dermal endothelial cells. Differential expression of TLR-4 and TLR-2 in endothelial cells. J. Biol. Chem. 275: 11058-11063.
9. Kadowaki, N., S. Ho, S. Antonenko, R. W. Malefyt, R. A. Kastelein, F. Bazan, and Y. J. Liu. 2001. Subsets of human dendritic cell precursors express different toll-like receptors and respond to different microbial antigens. J. Exp. Med. 194: 863-869.
10. Barton, G. M., and R. Medzhitov. 2002. Control of adaptive immune responses by Toll-like receptors. Curr. Opin. Immunol. 14: 380-383.
11. Krieg, A. M., and J. Vollmer. 2007. Toll-like receptors 7, 8, and 9: linking innate immunity to autoimmunity. Immunol. Rev. 220: 251-269.
12. Uematsu, S., and S. Akira. 2007. Toll-like receptors and Type I interferons. J. Biol. Chem. 282: 15319-15323.
13. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc. Natl. Acad. Sci. USA 97: 13766-13771.
14. O'Neill, L. A., and A. G. Bowie. 2007. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7: 353-364.
15. Chuang, T., and R. J. Ulevitch. 2001. Identification of hTLR10: a novel human Toll-like receptor preferentially expressed in immune cells. Biochim. Biophys. Acta 1518: 157-161.
16. Roach, J. C., G. Glusman, L. Rowen, A. Kaur, M. K. Purcell, K. D. Smith, L. E. Hood, and A. Aderem. 2005. The evolution of vertebrate Toll-like receptors. Proc. Natl. Acad. Sci. USA 102: 9577-9582.
17. Zhou, H., J. Gu, S. J. Lamont, and X. Gu. 2007. Evolutionary analysis for functional divergence of the toll-like receptor gene family and altered functional constraints. J. Mol. Evol. 65: 119-123.
18. Temperley, N. D., S. Berlin, I. R. Paton, D. K. Griffin, and D. W. Burt. 2008. Evolution of the chicken Toll-like receptor gene family: a story of gene gain and gene loss. BMC Genomics 9: 62.
19. Hughes, A. L., and H. Piontkivska. 2008. Functional diversification of the toll-like receptor gene family. Immunogenetics 60: 249-256.
20. Nakajima, T., H. Ohtani, Y. Satta, Y. Uno, H. Akari, T. Ishida, and A. Kimura. 2008. Natural selection in the TLR-related genes in the course of primate evolution. Immunogenetics 60: 727-735.
21. Ferrer-Admetlla, A., E. Bosch, M. Sikora, T. Marquès-Bonet, A. Ramírez-Soriano, A. Muntasell, A. Navarro, R. Lazarus, F. Calafell, J. Bertranpetit, and F. Casals. 2008. Balancing selection is the main force shaping the evolution of innate immunity genes. J. Immunol. 181: 1315-1322.
22. Corbett, M. S., I. Schmitt, O. Riess, and A. Walz. 1994. Characterization of the gene for human neutrophil-activating peptide 78 (ENA-78). Biochem. Biophys. Res. Commun. 205: 612-617.
23. Horton, R. M., Z. L. Cai, S. N. Ho, and L. R. Pease. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8: 528-535.
24. Omueti, K. O., J. M. Beyer, C. M. Johnson, E. A. Lyle, and R. I. Tapping. 2005. Domain exchange between human toll-like receptors 1 and 6 reveals a region required for lipopeptide discrimination. J. Biol. Chem. 280: 36616-36625.
25. Kim, H. M., B. S. Park, J. I. Kim, S. E. Kim, J. Lee, S. C. Oh, P. Enkhbayar, N. Matsushima, H. Lee, O. J. Yoo, and J. O. Lee. 2007. Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130: 906-917.
26. Jin, M. S., S. E. Kim, J. Y. Heo, M. E. Lee, H. M. Kim, S. G. Paik, H. Lee, and J. O. Lee. 2007. Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130: 1071-1082.
27. Hoover, D. M., and J. Lubkowski. 2002. DNAWorks: an automated method for designing oligonucleotides for PCR-based gene synthesis. Nucleic Acids Res. 30: e43.
28. Brooks, B. R., C. L. Brooks 3rd, A. D. Mackerell, Jr., L. Nilsson, R. J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, et al. 2009. CHARMM: The biomolecular simulation program. J. Comput. Chem. 30: 1545-1614.
29. Medzhitov, R., P. Preston-Hurlburt, and C. A. Janeway, Jr. 1997. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
30. Takeuchi, O., S. Sato, T. Horiuchi, K. Hoshino, K. Takeda, Z. Dong, R. L. Modlin, and S. Akira. 2002. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J. Immunol. 169: 10-14.
31. Takeuchi, O., T. Kawai, P. F. Mühlradt, M. Morr, J. D. Radolf, A. Zychlinsky, K. Takeda, and S. Akira. 2001. Discrimination of bacterial lipoproteins by Tolllike receptor 6. Int. Immunol. 13: 933-940.
32. Sandor, F., E. Latz, F. Re, L. Mandell, G. Repik, D. T. Golenbock, T. Espevik, E. A. Kurt-Jones, and R. W. Finberg. 2003. Importance of extra- and intracellular domains of TLR1 and TLR2 in NFkappa B signaling. J. Cell Biol. 162: 1099-1110.
33. Underhill, D. M., A. Ozinsky, A. M. Hajjar, A. Stevens, C. B. Wilson, M. Bassetti, and A. Aderem. 1999. The Toll-like receptor 2 is recruited to macrophage phagosomes and discriminates between pathogens. Nature 401: 811-815.
34. Jiang, Z., P. Georgel, C. Li, J. Choe, K. Crozat, S. Rutschmann, X. Du, T. Bigby, S. Mudd, S. Sovath, et al. 2006. Details of Toll-like receptor:adapter interaction revealed by germ-line mutagenesis. Proc. Natl. Acad. Sci. USA 103: 10961-10966.
35. Tapping, R. I., and P. S. Tobias. 2003. Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling. J. Endotoxin Res. 9: 264-268.
36. Johnson, C. M., E. A. Lyle, K. O. Omueti, V. A. Stepensky, O. Yegin, E. Alpsoy, L. Hamann, R. R. Schumann, and R. I. Tapping. 2007. Cutting edge: A common polymorphism impairs cell surface trafficking and functional responses of TLR1 but protects against leprosy. J. Immunol. 178: 7520-7524.
37. Meng, G., M. Rutz, M. Schiemann, J. Metzger, A. Grabiec, R. Schwandner, P. B. Luppa, F. Ebel, D. H. Busch, S. Bauer, et al. 2004. Antagonistic antibody prevents toll-like receptor 2-driven lethal shock-like syndromes. J. Clin. Invest. 113: 1473-1481.
38. Jin, M. S., and J. O. Lee. 2008. Structures of the toll-like receptor family and its ligand complexes. Immunity 29: 182-191.
39. Bella, J., K. L. Hindle, P. A. McEwan, and S. C. Lovell. 2008. The leucine-rich repeat structure. Cell. Mol. Life Sci. 65: 2307-2333.
40. Grabiec, A., G. Meng, S. Fichte, W. Bessler, H. Wagner, and C. J. Kirschning. 2004. Human but not murine toll-like receptor 2 discriminates between tri-palmitoylated and tri-lauroylated peptides. J. Biol. Chem. 279: 48004-48012.
41. Pettersen, E. F., T. D. Goddard, C. C. Huang, G. S. Couch, D. M. Greenblatt, E. C. Meng, and T. E. Ferrin. 2004. UCSF Chimera - a visualization system for exploratory research and analysis. J. Comput. Chem. 25: 1605-1612.
42. Omueti, K. O., D. J. Mazur, K. S. Thompson, E. A. Lyle, and R. I. Tapping. 2007. The polymorphism P315L of human toll-like receptor 1 impairs innate immune sensing of microbial cell wall components. J. Immunol. 178: 6387-6394.
43. Hasan, U., C. Chaffois, C. Gaillard, V. Saulnier, E. Merck, S. Tancredi, C. Guiet, F. Brière, J. Vlach, S. Lebecque, et al. 2005. Human TLR10 is a functional receptor, expressed by B cells and plasmacytoid dendritic cells, which activates gene transcription through MyD88. J. Immunol. 174: 2942-2950.
44. Zhang, H., P. N. Tay, W. Cao, W. Li, and J. Lu. 2002. Integrin-nucleated Toll-like receptor (TLR) dimerization reveals subcellular targeting of TLRs and distinct mechanisms of TLR4 activation and signaling. FEBS Lett. 532: 171-176.
45. 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.
46. Sheedy, F. J., and L. A. O'Neill. 2007. The Troll in Toll: Mal and Tram as bridges for TLR2 and TLR4 signaling. J. Leukoc. Biol. 82: 196-203.
47. Kawai, T., and S. Akira. 2007. Signaling to NF-kappaB by Toll-like receptors. Trends Mol. Med. 13: 460-469.
48. 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.
49. Nyman, T., P. Stenmark, S. Flodin, I. Johansson, M. Hammarström, and P. Nordlund. 2008. The crystal structure of the human toll-like receptor 10 cytoplasmic domain reveals a putative signaling dimer. J. Biol. Chem. 283: 11861-11865.
50. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. Van Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282: 2085-2088.
51. Toshchakov, V. U., S. Basu, M. J. Fenton, and S. N. Vogel. 2005. Differential involvement of BB loops of toll-IL-1 resistance (TIR) domain-containing adapter proteins in TLR4- versus TLR2-mediated signal transduction. J. Immunol. 175: 494-500.
52. Gautam, J. K., L. D. Ashish, J. K. Comeau, Krueger, and M. F. Smith, Jr. 2006. Structural and functional evidence for the role of the TLR2 DD loop in TLR1/ TLR2 heterodimerization and signaling. J. Biol. Chem. 281: 30132-30142.
53. 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.
54. Shinkai, H., Y. Muneta, K. Suzuki, T. Eguchi-Ogawa, T. Awata, and H. Uenishi. 2006. Porcine Toll-like receptor 1, 6, and 10 genes: complete sequencing of genomic region and expression analysis. Mol. Immunol. 43: 1474-1480.
55. Opsal, M. A., D. I. Våge, B. Hayes, I. Berget, and S. Lien. 2006. Genomic organization and transcript profiling of the bovine toll-like receptor gene cluster TLR6-TLR1-TLR10. Gene 384: 45-50.
56. Hornung, V., S. Rothenfusser, S. Britsch, A. Krug, B. Jahrsdörfer, T. Giese, S. Endres, and G. Hartmann. 2002. Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J. Immunol. 168: 4531-4537.
57. Bourke, E., D. Bosisio, J. Golay, N. Polentarutti, and A. Mantovani. 2003. The toll-like receptor repertoire of human B lymphocytes: inducible and selective expression of TLR9 and TLR10 in normal and transformed cells. Blood 102: 956-963.
58. Bernasconi, N. L., N. Onai, and A. Lanzavecchia. 2003. A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells. Blood 101: 4500-4504.
59. Vasilevsky, S., J. Colino, R. Puliaev, D. H. Canaday, and C. M. Snapper. 2008. Macrophages pulsed with Streptococcus pneumoniae elicit a T cell-dependent antibody response upon transfer into naive mice. J. Immunol. 181: 1787-1797.
60. Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438: 364-368.
61. Meyer-Bahlburg, A.,S. Khim, and D. J. Rawlings. 2007. B cell intrinsic TLR signals amplify but are not required for humoral immunity. J. Exp. Med. 204: 3095-3101.
62. Ruprecht, C. R., and A. Lanzavecchia. 2006. Toll-like receptor stimulation as a third signal required for activation of human naive B cells. Eur. J. Immunol. 36: 810-816.
63. Kanzler, H., F. J. Barrat, E. M. Hessel, and R. L. Coffman. 2007. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat. Med. 13: 552-559.
64. Marshak-Rothstein, A. 2006. Toll-like receptors in systemic autoimmune disease. Nat. Rev. Immunol. 6: 823-835.
65. Chiron, D., I. Bekeredjian-Ding, C. Pellat-Deceunynck, R. Bataille, and G. Jego. 2008. Toll-like receptors: lessons to learn from normal and malignant human B cells. Blood 112: 2205-2213.
66. Månsson, A., M. Adner, U. Höckerfelt, and L. O. Cardell. 2006. A distinct Tolllike receptor repertoire in human tonsillar B cells, directly activated by PamCSK, R-837 and CpG-2006 stimulation. Immunology 118: 539-548.
67. Ganley-Leal, L. M., X. Liu, and L. M. Wetzler. 2006. Toll-like receptor 2-mediated human B cell differentiation. Clin. Immunol. 120: 272-284.
68. Bohnhorst, J., T. Rasmussen, S. H. Moen, M. Fløttum, L. Knudsen, M. Børset, T. Espevik, and A. Sundan. 2006. Toll-like receptors mediate proliferation and survival of multiple myeloma cells. Leukemia 20: 1138-1144.
69. Muzio, M., C. Scielzo, M. T. Bertilaccio, M. Frenquelli, P. Ghia, and F. Caligaris-Cappio. 2009. Expression and function of toll like receptors in chronic lymphocytic leukaemia cells. Br. J. Haematol. 144: 507-516.
70. Marsland, B. J., and M. Kopf. 2007. Toll-like receptors: paving the path to T cell-driven autoimmunity? Curr. Opin. Immunol. 19: 611-614.
71. Komai-Koma, M., L. Jones, G. S. Ogg, D. Xu, and F. Y. Liew. 2004. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc. Natl. Acad. Sci. USA 101: 3029-3034.
72. Bell, M. P., P. A. Svingen, M. K. Rahman, Y. Xiong, andW. A. Faubion, Jr. 2007. FOXP3 regulates TLR10 expression in human T regulatory cells. J. Immunol. 179: 1893-1900.
73. Ma, X., Y. Liu, B. B. Gowen, E. A. Graviss, A. G. Clark, and J. M. Musser. 2007. Full-exon resequencing reveals toll-like receptor variants contribute to human susceptibility to tuberculosis disease. PLoS One 2: e1318.
74. Lazarus, R., B. A. Raby, C. Lange, E. K. Silverman, D. J. Kwiatkowski, D. Vercelli, W. J. Klimecki, F. D. Martinez, and S. T. Weiss. 2004. TOLL-like receptor 10 genetic variation is associated with asthma in two independent samples. Am. J. Respir. Crit. Care Med. 170: 594-600.