Adaptor protein-3-mediated trafficking of TLR2 ligands controls specificity of inflammatory responses but not adaptor complex assembly

Journal of Immunology

Volumn 195, Issue 9, 2015, Pages 4331-4340

  Petnicki Ocwieja, Tanja ^a   Kern, Aurelie ^a   Killpack, Tess L ^a   Bunnell, Stephen C ^a   Hu, Linden T ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN 3; GAMMA INTERFERON; INTERLEUKIN 6; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AUTACOID; CYTOKINE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN RECEPTOR; LIPOPEPTIDE; MEMBRANE PROTEIN; MYD88 PROTEIN, MOUSE; PAM(3)CSK(4) PEPTIDE; TIRAP PROTEIN, MOUSE; TIRP PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINE RESPONSE; IN VIVO STUDY; INFLAMMATION; LYME DISEASE; MOUSE; NONHUMAN; PHAGOSOME; PHENOTYPE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; BORRELIA BURGDORFERI; C3H MOUSE; C57BL MOUSE; CELL CULTURE; CONFOCAL MICROSCOPY; GENETICS; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; L CELL LINE; LYSOSOME; MACROPHAGE; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT;

ADAPTOR PROTEIN COMPLEX 3; ANIMALS; BORRELIA BURGDORFERI; CELLS, CULTURED; CYTOKINES; HOST-PATHOGEN INTERACTIONS; INFLAMMATION MEDIATORS; L CELLS (CELL LINE); LIPOPEPTIDES; LYSOSOMES; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; MYELOID DIFFERENTIATION FACTOR 88; PHAGOSOMES; PROTEIN TRANSPORT; RECEPTORS, INTERLEUKIN; RECEPTORS, INTERLEUKIN-1; TOLL-LIKE RECEPTOR 2;

EID: 84945156923     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1501268     Document Type: Article

References (39)

1. Kawai, T., and S. Akira. 2009. The roles of TLRs, RLRs and NLRs in pathogen recognition. Int. Immunol. 21: 317-337.
2. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11: 373-384.
3. Kagan, J. C., T. Su, T. Horng, A. Chow, S. Akira, and R. Medzhitov. 2008. Tram couples endocytosis of Toll-like receptor 4 to the induction of interferon β. Nat. Immunol. 9: 343-345.
4. Husebye, H., M. H. Aune, J. Stenvik, E. Samstad, F. Skjeldal, O. Halaas, N. J. Nilsen, H. Stenmark, E. Latz, E. Lien, et al. 2010. The Rab11a GTPase controls Toll-like receptor 4-induced activation of interferon regulatory factor-3 on phagosomes. Immunity 33: 583-596.
5. Sasai, M., M. M. Linehan, and A. Iwasaki. 2010. Bifurcation of Toll-like receptor 9 signaling by adaptor protein 3. Science 329: 1530-1534.
6. Underhill, D. M., A. Ozinsky, A. M. Haijar, 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.
7. Barbalat, R., L. Lau, R. M. Locksley, and G. M. Barton. 2009. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol. 10: 1200-1207.
8. Dietrich, N., S. Lienenklaus, S. Weiss, and N. O. Gekara. 2010. Murine toll-like receptor 2 activation induces type I interferon responses from endolysosomal compartments. PLoS One 5: e10250.
9. 1 regulates TLR2 recognition of lipopeptides from endosomal compartments. PLoS One 5: e12871.
10. Ip, W. K. E., K. Takahashi, K. J. Moore, L. M. Stuart, and R. A. B. Ezekowitz. 2008. Mannose-binding lectin enhances toll-like receptors 2 and 6 signaling from the phagosome. J. Exp. Med. 205: 169-181.
11. Cervantes, J. L., S. M. Dunham-Ems, C. J. La Vake, M. M. Petzke, B. Sahay, T. J. Sellati, J. D. Radolf, and J. C. Salazar. 2011. Phagosomal signaling by Borrelia burgdorferi in human monocytes involves Toll-like receptor (TLR) 2 and TLR8 cooperativity and TLR8-mediated induction of IFN-β. Proc. Natl. Acad. Sci. USA 108: 3683-3688.
12. Wolf, A. J., A. Arruda, C. N. Reyes, A. T. Kaplan, T. Shimada, K. Shimada, M. Arditi, G. Liu, and D. M. Underhill. 2011. Phagosomal degradation increases TLR access to bacterial ligands and enhances macrophage sensitivity to bacteria. J. Immunol. 187: 6002-6010.
13. Ip, W. K., A. Sokolovska, G. M. Charriere, L. Boyer, S. Dejardin, M. P. Cappillino, L. M. Yantosca, K. Takahashi, K. J. Moore, A. Lacy-Hulbert, and L. M. Stuart. 2010. Phagocytosis and phagosome acidification are required for pathogen processing and MyD88-dependent responses to Staphylococcus aureus. J. Immunol. 184: 7071-7081.
14. Petnicki-Ocwieja, T., E. Chung, D. I. Acosta, L. T. Ramos, O. S. Shin, S. Ghosh, L. Kobzik, X. Li, and L. T. Hu. 2013. TRIF mediates Toll-like receptor 2-dependent inflammatory responses to Borrelia burgdorferi. Infect. Immun. 81: 402-410.
15. Nilsen, N. J., G. I. Vladimer, J. Stenvik, M. P. Orning, M. V. Zeid-Kilani, M. Bugge, B. Bergstroem, J. Conlon, H. Husebye, A. G. Hise, et al. 2015. A role for the adaptor proteins TRAM and TRIF in Toll-like receptor 2 signaling. J. Biol. Chem. 290: 3209-3222.
16. Kagan, J. C., and R. Medzhitov. 2006. Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125: 943-955.
17. Bonham, K. S., M. H. Orzalli, K. Hayashi, A. I. Wolf, C. Glanemann, W. Weninger, A. Iwasaki, D. M. Knipe, and J. C. Kagan. 2014. A promiscuous lipid-binding protein diversifies the subcellular sites of Toll-like receptor signal transduction. Cell 156: 705-716.
18. Kawai, T., and S. Akira. 2011. Regulation of innate immune signalling pathways by the tripartite motif (TRIM) family proteins. EMBO Mol. Med. 3: 513-527.
19. + T cells. Immunity 36: 782-794.
20. McGettrick, A. F., and L. A. O'Neill. 2010. Localisation and trafficking of Toll-like receptors: an important mode of regulation. Curr. Opin. Immunol. 22: 20-27.
21. Sasai, M., and A. Iwasaki. 2011. Love triangle between Unc93B1, TLR7, and TLR9 prevents fatal attraction. Immunity 35: 3-5.
22. Ewald, S. E., B. L. Lee, L. Lau, K. E. Wickliffe, G. P. Shi, H. A. Chapman, and G. M. Barton. 2008. The ectodomain of Toll-like receptor 9 is cleaved to generate a functional receptor. Nature 456: 658-662.
23. Lee, B. L., J. E. Moon, J. H. Shu, L. Yuan, Z. R. Newman, R. Schekman, and G. M. Barton. 2013. UNC93B1 mediates differential trafficking of endosomal TLRs. Elife 2: e00291.
24. Bonifacino, J. S., M. S. Marks, H. Ohno, and T. Kirchhausen. 1996. Mechanisms of signal-mediated protein sorting in the endocytic and secretory pathways. Proc. Assoc. Am. Physicians 108: 285-295.
25. Bonifacino, J. S. 2004. Insights into the biogenesis of lysosome-related organelles from the study of the Hermansky-Pudlak syndrome. Ann. N.Y. Acad. Sci. 1038: 103-114.
26. Dell'Angelica, E. C., V. Shotelersuk, R. C. Aguilar, W. A. Gahl, and J. S. Bonifacino. 1999. Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the β 3A subunit of the AP-3 adaptor. Mol. Cell 3: 11-21.
27. Pinto, L. H., M. A. Williams, H. Suzuki, N. Mangini, G. W. Balkema, Jr., and J. W. Vanable, Jr. 1985. Visual defects in mouse hypopigmentation mutants. Neurosci. Res. Suppl. 2: S239-S251.
28. Feng, L., A. B. Seymour, S. Jiang, A. To, A. A. Peden, E. K. Novak, L. Zhen, M. E. Rusiniak, E. M. Eicher, M. S. Robinson, et al. 1999. The β 3A subunit gene (Ap3b1) of the AP-3 adaptor complex is altered in the mouse hypopigmentation mutant pearl, a model for Hermansky-Pudlak syndrome and night blindness. Hum. Mol. Genet. 8: 323-330.
29. Behera, A. K., E. Hildebrand, R. T. Bronson, G. Perides, S. Uematsu, S. Akira, and L. T. Hu. 2006. MyD88 deficiency results in tissue-specific changes in cytokine induction and inflammation in interleukin-18-independent mice infected with Borrelia burgdorferi. Infect. Immun. 74: 1462-1470.
30. Stack, J., S. L. Doyle, D. J. Connolly, L. S. Reinert, K. M. O'Keeffe, R. M. McLoughlin, S. R. Paludan, and A. G. Bowie. 2014. TRAM is required for TLR2 endosomal signaling to type I IFN induction. J. Immunol. 193: 6090-6102.
31. Cruz, A. R., M. W. Moore, C. J. La Vake, C. H. Eggers, J. C. Salazar, and J. D. Radolf. 2008. Phagocytosis of Borrelia burgdorferi, the Lyme disease spirochete, potentiates innate immune activation and induces apoptosis in human monocytes. Infect. Immun. 76: 56-70.
32. Salazar, J. C., S. Duhnam-Ems, C. La Vake, A. R. Cruz, M. W. Moore, M. J. Caimano, L. Velez-Climent, J. Shupe, W. Krueger, and J. D. Radolf. 2009. Activation of human monocytes by live Borrelia burgdorferi generates TLR2- dependent and -independent responses which include induction of IFN-β. PLoS Pathog. 5: e1000444.
33. Ohnishi, H., H. Tochio, Z. Kato, N. Kawamoto, T. Kimura, K. Kubota, T. Yamamoto, T. Funasaka, H. Nakano, R. W. Wong, et al. 2012. TRAM is involved in IL-18 signaling and functions as a sorting adaptor for MyD88. PLoS One 7: e38423.
34. Henault, J., J. Martinez, J. M. Riggs, J. Tian, P. Mehta, L. Clarke, M. Sasai, E. Latz, M. M. Brinkmann, A. Iwasaki, et al. 2012. Noncanonical autophagy is required for type I interferon secretion in response to DNA-immune complexes. Immunity 37: 986-997.
35. Wooten, R. M., Y. Ma, R. A. Yoder, J. P. Brown, J. H. Weis, J. F. Zachary, C. J. Kirschning, and J. J. Weis. 2002. Toll-like receptor 2 is required for innate, but not acquired, host defense to Borrelia burgdorferi. J. Immunol. 168: 348-355.
36. Sahay, B., R. L. Patsey, C. H. Eggers, J. C. Salazar, J. D. Radolf, and T. J. Sellati. 2009. CD14 signaling restrains chronic inflammation through induction of p38-MAPK/SOCS-dependent tolerance. PLoS Pathog. 5: e1000687.
37. -/- mice. FEMS Immunol. Med. Microbiol. 52: 124-133.
38. Bolz, D. D., R. S. Sundsbak, Y. Ma, S. Akira, C. J. Kirschning, J. F. Zachary, J. H. Weis, and J. J. Weis. 2004. MyD88 plays a unique role in host defense but not arthritis development in Lyme disease. J. Immunol. 173: 2003-2010.
39. Liu, N., R. R. Montgomery, S. W. Barthold, and L. K. Bockenstedt. 2004. Myeloid differentiation antigen 88 deficiency impairs pathogen clearance but does not alter inflammation in Borrelia burgdorferi-infected mice. Infect. Immun. 72: 3195-3203.