Regulation of TLR3 activation by S100A9

Journal of Immunology

Volumn 195, Issue 9, 2015, Pages 4426-4437

  Tsai, Su Yu ^a,b   Segovia, Jesus A ^b   Chang, Te Hung ^b   Shil, Niraj K ^a   Pokharel, Swechha M ^a   Kannan, T R ^b   Baseman, Joel B ^b   Defrêne, Joan ^c   Pagé, Nathalie ^c   Cesaro, Annabelle ^c,d   Tessier, Philippe A ^c   Bose, Santanu ^a  

^a WASHINGTON STATE UNIVERSITY   (United States)

^b University of Texas Health Science Center   (United States)

^c LAVAL UNIVERSITY   (Canada)

^d UNIVERSITÉ D'ORLÉANS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CALGRANULIN B; POLYINOSINIC POLYCYTIDYLIC ACID; TOLL LIKE RECEPTOR 3; S100A9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOSOME; FEMALE; IN VIVO STUDY; LYSOSOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; RNA VIRUS INFECTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL LINE; CONFOCAL MICROSCOPY; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA VIRUS; TUMOR CELL LINE; VIROLOGY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CALGRANULIN B; CELL LINE; CELL LINE, TUMOR; CELLS, CULTURED; FEMALE; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-BETA; MACROPHAGES; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; POLY I-C; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA VIRUSES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 3;

EID: 84945156937     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1500378     Document Type: Article

References (65)

1. Bose, S., and A. K. Banerjee. 2003. Innate immune response against nonsegmented negative strand RNA viruses. J. Interferon Cytokine Res. 23: 401-412.
2. Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67: 227-264.
3. Uematsu, S., and S. Akira. 2007. Toll-like receptors and Type I interferons. J. Biol. Chem. 282: 15319-15323.
4. Versteeg, G. A., and A. García-Sastre. 2010. Viral tricks to grid-lock the type I interferon system. Curr. Opin. Microbiol. 13: 508-516.
5. Schmolke, M., and A. García-Sastre. 2010. Evasion of innate and adaptive immune responses by influenza A virus. Cell. Microbiol. 12: 873-880.
6. Wilkins, C., and M. Gale, Jr. 2010. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 22: 41-47.
7. Bose, S., N. Kar, R. Maitra, J. A. DiDonato, and A. K. Banerjee. 2003. Temporal activation of NF-kappaB regulates an interferon-independent innate antiviral response against cytoplasmic RNA viruses. Proc. Natl. Acad. Sci. USA 100: 10890-10895.
8. Kota, S., A. Sabbah, T. H. Chang, R. Harnack, Y. Xiang, X. Meng, and S. Bose. 2008. Role of human β-defensin-2 during tumor necrosis factor-α/NF-kappaB-mediated innate antiviral response against human respiratory syncytial virus. J. Biol. Chem. 283: 22417-22429.
9. Sabbah, A., T. H. Chang, R. Harnack, V. Frohlich, K. Tominaga, P. H. Dube, Y. Xiang, and S. Bose. 2009. Activation of innate immune antiviral responses by Nod2. Nat. Immunol. 10: 1073-1080.
10. Segovia, J., A. Sabbah, V. Mgbemena, S. Y. Tsai, T. H. Chang, M. T. Berton, I. R. Morris, I. C. Allen, J. P. Ting, and S. Bose. 2012. TLR2/MyD88/NF-κB pathway, reactive oxygen species, potassium efflux activates NLRP3/ASC inflammasome during respiratory syncytial virus infection. PLoS One 7: e29695.
11. 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.
12. Brencicova, E., and S. S. Diebold. 2013. Nucleic acids and endosomal pattern recognition: how to tell friend from foe? Front. Cell. Infect. Microbiol. 3: 37.
13. Matsumoto, M., and T. Seya. 2008. TLR3: interferon induction by double-stranded RNA including poly(I:C). Adv. Drug Deliv. Rev. 60: 805-812.
14. Zhang, S. Y., M. Herman, M. J. Ciancanelli, R. Pérez de Diego, V. Sancho-Shimizu, L. Abel, and J. L. Casanova. 2013. TLR3 immunity to infection in mice and humans. Curr. Opin. Immunol. 25: 19-33.
15. Perales-Linares, R., and S. Navas-Martin. 2013. Toll-like receptor 3 in viral pathogenesis: friend or foe? Immunology 140: 153-167.
16. Wang, Q., D. J. Miller, E. R. Bowman, D. R. Nagarkar, D. Schneider, Y. Zhao, M. J. Linn, A. M. Goldsmith, J. K. Bentley, U. S. Sajjan, and M. B. Hershenson. 2011. MDA5 and TLR3 initiate pro-inflammatory signaling pathways leading to rhinovirus-induced airways inflammation and hyperresponsiveness. PLoS Pathog. 7: e1002070.
17. Le Goffic, R., V. Balloy, M. Lagranderie, L. Alexopoulou, N. Escriou, R. Flavell, M. Chignard, and M. Si-Tahar. 2006. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog. 2: e53.
18. Groskreutz, D. J., M. M. Monick, L. S. Powers, T. O. Yarovinsky, D. C. Look, and G. W. Hunninghake. 2006. Respiratory syncytial virus induces TLR3 protein and protein kinase R, leading to increased double-stranded RNA responsiveness in airway epithelial cells. J. Immunol. 176: 1733-1740.
19. Aeffner, F., Z. P. Traylor, E. N. Yu, and I. C. Davis. 2011. Double-stranded RNA induces similar pulmonary dysfunction to respiratory syncytial virus in BALB/c mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 301: L99-L109.
20. Rudd, B. D., J. J. Smit, R. A. Flavell, L. Alexopoulou, M. A. Schaller, A. Gruber, A. A. Berlin, and N. W. Lukacs. 2006. Deletion of TLR3 alters the pulmonary immune environment and mucus production during respiratory syncytial virus infection. J. Immunol. 176: 1937-1942.
21. Her, Z., T. S. Teng, J. J. Tan, T. H. Teo, Y. W. Kam, F. M. Lum, W. W. Lee, C. Gabriel, R. Melchiotti, A. K. Andiappan, et al. 2015. Loss of TLR3 aggravates CHIKV replication and pathology due to an altered virus-specific neutralizing antibody response. EMBO Mol. Med. 7: 24-41.
22. Wang, N., Y. Liang, S. Devaraj, J. Wang, S. M. Lemon, and K. Li. 2009. Toll-like receptor 3 mediates establishment of an antiviral state against hepatitis C virus in hepatoma cells. J. Virol. 83: 9824-9834.
23. Wu, J., S. Huang, X. Zhao, M. Chen, Y. Lin, Y. Xia, C. Sun, X. Yang, J. Wang, Y. Guo, et al. 2014. Poly(I:C) treatment leads to interferon-dependent clearance of hepatitis B virus in a hydrodynamic injection mouse model. J. Virol. 88: 10421-10431.
24. Karimi-Googheri, M., and M. K. Arababadi. 2014. TLR3 plays significant roles against hepatitis B virus. Mol. Biol. Rep. 41: 3279-3286.
25. Jelinek, I., J. N. Leonard, G. E. Price, K. N. Brown, A. Meyer-Manlapat, P. K. Goldsmith, Y. Wang, D. Venzon, S. L. Epstein, and D. M. Segal. 2011. TLR3-specific double-stranded RNA oligonucleotide adjuvants induce dendritic cell cross-presentation, CTL responses, and antiviral protection. J. Immunol. 186: 2422-2429.
26. Matsumoto, M., K. Funami, M. Tanabe, H. Oshiumi, M. Shingai, Y. Seto, A. Yamamoto, and T. Seya. 2003. Subcellular localization of Toll-like receptor 3 in human dendritic cells. J. Immunol. 171: 3154-3162.
27. Crozat, K., and B. Beutler. 2004. TLR7: A new sensor of viral infection. Proc. Natl. Acad. Sci. USA 101: 6835-6836.
28. 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.
29. Barton, G. M., and J. C. Kagan. 2009. A cell biological view of Toll-like receptor function: regulation through compartmentalization. Nat. Rev. Immunol. 9: 535-542.
30. Lee, B. L., and G. M. Barton. 2014. Trafficking of endosomal Toll-like receptors. Trends Cell Biol. 24: 360-369.
31. Takahashi, K., T. Shibata, S. Akashi-Takamura, T. Kiyokawa, Y. Wakabayashi, N. Tanimura, T. Kobayashi, F. Matsumoto, R. Fukui, T. Kouro, et al. 2007. A protein associated with Toll-like receptor (TLR) 4 (PRAT4A) is required for TLR-dependent immune responses. J. Exp. Med. 204: 2963-2976.
32. 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.
33. Johnsen, I. B., T. T. Nguyen, M. Ringdal, A. M. Tryggestad, O. Bakke, E. Lien, T. Espevik, and M. W. Anthonsen. 2006. Toll-like receptor 3 associates with c-Src tyrosine kinase on endosomes to initiate antiviral signaling. EMBO J. 25: 3335-3346.
34. Lee, H. K., S. Dunzendorfer, K. Soldau, and P. S. Tobias. 2006. Double-stranded RNA-mediated TLR3 activation is enhanced by CD14. Immunity 24: 153-163.
35. Niimi, K., K. Asano, Y. Shiraishi, T. Nakajima, M. Wakaki, J. Kagyo, T. Takihara, Y. Suzuki, K. Fukunaga, T. Shiomi, et al. 2007. TLR3-mediated synthesis and release of eotaxin-1/CCL11 from human bronchial smooth muscle cells stimulated with double-stranded RNA. J. Immunol. 178: 489-495.
36. Funami, K., M. Sasai, Y. Ohba, H. Oshiumi, T. Seya, and M. Matsumoto. 2007. Spatiotemporal mobilization of Toll/IL-1 receptor domain-containing adaptor molecule-1 in response to dsRNA. J. Immunol. 179: 6867-6872.
37. Qi, R., D. Singh, and C. C. Kao. 2012. Proteolytic processing regulates Toll-like receptor 3 stability and endosomal localization. J. Biol. Chem. 287: 32617-32629.
38. Tsai, S. Y., J. A. Segovia, T. H. Chang, I. R. Morris, M. T. Berton, P. A. Tessier, M. R. Tardif, A. Cesaro, and S. Bose. 2014. DAMP molecule S100A9 acts as a molecular pattern to enhance inflammation during influenza A virus infection: role of DDX21-TRIF-TLR4-MyD88 pathway. PLoS Pathog. 10: e1003848.
39. Donato, R., B. R. Cannon, G. Sorci, F. Riuzzi, K. Hsu, D. J. Weber, and C. L. Geczy. 2013. Functions of S100 proteins. Curr. Mol. Med. 13: 24-57.
40. Hermann, A., R. Donato, T. M. Weiger, and W. J. Chazin. 2012. S100 calcium binding proteins and ion channels. Front. Pharmacol. 3: 67.
41. Segovia, J. A., S. Y. Tsai, T. H. Chang, N. K. Shil, S. T. Weintraub, J. D. Short, and S. Bose. 2015. Nedd8 regulates inflammasome-dependent caspase-1 activation. Mol. Cell. Biol. 35: 582-597.
42. Bose, S., M. Mathur, P. Bates, N. Joshi, and A. K. Banerjee. 2003. Requirement for cyclophilin A for the replication of vesicular stomatitis virus New Jersey serotype. J. Gen. Virol. 84: 1687-1699.
43. Manitz, M. P., B. Horst, S. Seeliger, A. Strey, B. V. Skryabin, M. Gunzer, W. Frings, F. Schönlau, J. Roth, C. Sorg, and W. Nacken. 2003. Loss of S100A9 (MRP14) results in reduced interleukin-8-induced CD11b surface expression, a polarized microfilament system, and diminished responsiveness to chemoattractants in vitro. Mol. Cell. Biol. 23: 1034-1043.
44. Halayko, A. J., and S. Ghavami. 2009. S100A8/A9: a mediator of severe asthma pathogenesis and morbidity? Can. J. Physiol. Pharmacol. 87: 743-755.
45. Simard, J. C., D. Girard, and P. A. Tessier. 2010. Induction of neutrophil degranulation by S100A9 via a MAPK-dependent mechanism. J. Leukoc. Biol. 87: 905-914.
46. Simard, J. C., M. M. Simon, P. A. Tessier, and D. Girard. 2011. Damage-associated molecular pattern S100A9 increases bactericidal activity of human neutrophils by enhancing phagocytosis. J. Immunol. 186: 3622-3631.
47. Raquil, M. A., N. Anceriz, P. Rouleau, and P. A. Tessier. 2008. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia. J. Immunol. 180: 3366-3374.
48. Vandal, K., P. Rouleau, A. Boivin, C. Ryckman, M. Talbot, and P. A. Tessier. 2003. Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J. Immunol. 171: 2602-2609.
49. Kalia, M., S. Kumari, R. Chadda, M. M. Hill, R. G. Parton, and S. Mayor. 2006. Arf6-independent GPI-anchored protein-enriched early endosomal compartments fuse with sorting endosomes via a Rab5/phosphatidylinositol-3'-kinase-dependent machinery. Mol. Biol. Cell 17: 3689-3704.
50. Sugimoto, Y., H. Ninomiya, Y. Ohsaki, K. Higaki, J. P. Davies, Y. A. Ioannou, and K. Ohno. 2001. Accumulation of cholera toxin and GM1 ganglioside in the early endosome of Niemann-Pick C1-deficient cells. Proc. Natl. Acad. Sci. USA 98: 12391-12396.
51. Bastin, G., and S. P. Heximer. 2013. Rab family proteins regulate the endosomal trafficking and function of RGS4. J. Biol. Chem. 288: 21836-21849.
52. Kumar, H., S. Koyama, K. J. Ishii, T. Kawai, and S. Akira. 2008. Cutting edge: cooperation of IPS-1- and TRIF-dependent pathways in poly IC-enhanced antibody production and cytotoxic T cell responses. J. Immunol. 180: 683-687.
53. Murakami, Y., R. Fukui, Y. Motoi, A. Kanno, T. Shibata, N. Tanimura, S. Saitoh, and K. Miyake. 2014. Roles of the cleaved N-terminal TLR3 fragment and cell surface TLR3 in double-stranded RNA sensing. J. Immunol. 193: 5208-5217.
54. Ewald, S. E., A. Engel, J. Lee, M. Wang, M. Bogyo, and G. M. Barton. 2011. Nucleic acid recognition by Toll-like receptors is coupled to stepwise processing by cathepsins and asparagine endopeptidase. J. Exp. Med. 208: 643-651.
55. Watanabe, A., M. Tatematsu, K. Saeki, S. Shibata, H. Shime, A. Yoshimura, C. Obuse, T. Seya, and M. Matsumoto. 2011. Raftlin is involved in the nucleocapture complex to induce poly(I:C)-mediated TLR3 activation. J. Biol. Chem. 286: 10702-10711.
56. Garcia-Cattaneo, A., F. X. Gobert, M. Müller, F. Toscano, M. Flores, A. Lescure, E. Del Nery, and P. Benaroch. 2012. Cleavage of Toll-like receptor 3 by cathepsins B and H is essential for signaling. Proc. Natl. Acad. Sci. USA 109: 9053-9058.
57. Sun, Q., L. Sun, H. H. Liu, X. Chen, R. B. Seth, J. Forman, and Z. J. Chen. 2006. The specific and essential role of MAVS in antiviral innate immune responses. Immunity 24: 633-642.
58. Gitlin, L., W. Barchet, S. Gilfillan, M. Cella, B. Beutler, R. A. Flavell, M. S. Diamond, and M. Colonna. 2006. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. USA 103: 8459-8464.
59. Huotari, J., and A. Helenius. 2011. Endosome maturation. EMBO J. 30: 3481-3500.
60. Chavrier, P., R. G. Parton, H. P. Hauri, K. Simons, and M. Zerial. 1990. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell 62: 317-329.
61. Ullrich, O., H. Horiuchi, C. Bucci, and M. Zerial. 1994. Membrane association of Rab5 mediated by GDP-dissociation inhibitor and accompanied by GDP/GTP exchange. Nature 368: 157-160.
62. Rink, J., E. Ghigo, Y. Kalaidzidis, and M. Zerial. 2005. Rab conversion as a mechanism of progression from early to late endosomes. Cell 122: 735-749.
63. Méresse, S., J. P. Gorvel, and P. Chavrier. 1995. The rab7 GTPase resides on a vesicular compartment connected to lysosomes. J. Cell Sci. 108: 3349-3358.
64. Vonderheit, A., and A. Helenius. 2005. Rab7 associates with early endosomes to mediate sorting and transport of Semliki forest virus to late endosomes. PLoS Biol. 3: e233.
65. Del Conte-Zerial, P., L. Brusch, J. C. Rink, C. Collinet, Y. Kalaidzidis, M. Zerial, and A. Deutsch. 2008. Membrane identity and GTPase cascades regulated by toggle and cut-out switches. Mol. Syst. Biol. 4: 206.