Carbon monoxide differentially inhibits TLR signaling pathways by regulating ROS-induced trafficking of TLRs to lipid rafts

Journal of Experimental Medicine

Volumn 203, Issue 10, 2006, Pages 2377-2389

  Nakahira, Kiichi ^a   Hong, Pyo Kim ^a   Xue, Hui Geng ^a   Nakao, Atsunori ^a   Wang, Xue ^a   Murase, Noriko ^a   Drain, Peter F ^a   Wang, Xiaomei ^a   Sasidhar, Madhu ^b   Nabel, Elizabeth G ^c   Takahashi, Toru ^d   Lukacs, Nicholas W ^e   Ryter, Stefan W ^a   Morita, Kiyoshi ^d   Choi, Augustine M K ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d OKAYAMA UNIVERSITY MEDICAL SCHOOL   (Japan)

^e UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON MONOXIDE; DIPHENYLIODONIUM SALT; HEME OXYGENASE; POLYINOSINIC POLYCYTIDYLIC ACID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL DIFFERENTIATION; IMMUNOCOMPETENT CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; LIPID RAFT; MACROPHAGE; PRIORITY JOURNAL; PROTEIN BINDING; SIGNAL PROCESSING; TRANSLATION REGULATION; WILD TYPE;

ANIMALS; CARBON MONOXIDE; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEME OXYGENASE-1; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MACROPHAGES; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED C57BL; MICROSCOPY, FLUORESCENCE; PROTEIN TRANSPORT; REACTIVE OXYGEN SPECIES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS;

EID: 33749322644     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20060845     Document Type: Article

References (59)

1. Ryter, S.W., D. Morse, and A.M. Choi. 2004. Carbon monoxide: to boldly go where NO has gone before. Sci. STKE. 2004:RE6.
2. Yachie, A., Y. Niida, T. Wada, N. Igarashi, H. Kaneda, T. Toma, K. Ohta, Y. Kasahara, and S. Koizumi. 1999. Oxidative stress causes enhanced endothelial cell injury in human heme oxygenase-1 deficiency. J. Clin. Invest. 103:129-135.
3. Poss, K.D., and S. Tonegawa. 1997. Reduced stress defense in heme oxygenase 1-deficient cells. Proc. Natl. Acad. Sci. USA. 94:10925-10930.
4. Kawashima, A., Y. Oda, A. Yachie, S. Koizumi, and I. Nakanishi. 2002. Heme oxygenase-1 deficiency: the first autopsy case. Hum. Pathol. 33:125-130.
5. Otterbein, L.E., F.H. Bach, J. Alam, M. Soares, H. Tao Lu, M. Wysk, R.J. Davis, R.A. Flavell, and A.M. Choi. 2000. Carbon monoxide has anti-inflammatory effects involving the mitogen-activated protein kinase pathway. Nat. Med. 6:422-428.
6. Morse, D., S.E. Pischke, Z. Zhou, R.J. Davis, R.A. Flavell, T. Loop, S.L. Otterbein, L.E. Otterbein, and A.M. Choi. 2003. Suppression of inflammatory cytokine production by carbon monoxide involves the JNK pathway and AP-1. J. Biol. Chem. 278:36993-36998.
7. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511.
8. Liew, F.Y., D. Xu, E.K. Brint, and L.A. O'Neill. 2005. Negative regulation of toll-like receptor-mediated immune responses. Nat. Rev. Immunol. 5:446-458.
9. Dykstra, M., A. Cherukuri, H.W. Sohn, S.J. Tzeng, and S.K. Pierce. 2003. Location is everything: lipid rafts and immune cell signaling. Annu. Rev. Immunol. 21:457-481.
10. Manes, S., G. del Real, and A.C. Martinez. 2003. Pathogens: raft hijackers. Nat. Rev. Immunol. 3:557-568.
11. Triantafilou, M., K. Miyake, D.T. Golenbock, and K. Triantafilou. 2002. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 115:2603-2611.
12. Soong, G., B. Reddy, S. Sokol, R. Adamo, and A. Prince. 2004. TLR2 is mobilized into an apical lipid raft receptor complex to signal infection in airway epithelial cells. J. Clin. Invest. 113:1482-1489.
13. Chauveau, C., S. Remy, P.J. Royer, M. Hill, S. Tanguy-Royer, F.X. Hubert, L. Tesson, R. Brion, G. Beriou, M. Gregoire, et al. 2005. Heme oxygenase-1 expression inhibits dendritic cell maturation and proinflammatory function but conserves IL-10 expression. Blood. 106:1694-1702.
14. Lee, T.S., and L.Y. Chau. 2002. Heme oxygenase-1 mediates the antiinflammatory effect of interleukin-10 in mice. Nat. Med. 8:240-246.
15. Meylan, E., and J. Tschopp. 2006. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol. Cell. 22:561-569.
16. Alexopoulou, L., A.C. Holt, R. Medzhitov, and R.A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature. 413:732-738.
17. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131-137.
18. Doyle, S., S. Vaidya, R. O'Connell, H. Dadgostar, P. Dempsey, T. Wu, G. Rao, R. Sun, M. Haberland, R. Modlin, and G. Cheng. 2002. IRF3 mediates a TLR3/TLR4-specific antiviral gene program. Immunity. 17:251-263.
19. Sarady, J.K., S.L. Otterbein, F. Liu, L.E. Otterbein, and A.M. Choi. 2002. Carbon monoxide modulates endotoxin-induced production of granulocyte macrophage colony-stimulating factor in macrophages. Am. J. Respir. Cell Mol. Biol. 27:739-745.
20. Medvedev, A.E., A. Lentschat, L.M. Wahl, D.T. Golenbock, and S.N. Vogel. 2002. Dysregulation of LPS-induced Toll-like receptor 4-MyD88 complex formation and IL-1 receptor-associated kinase 1 activation in endotoxin-tolerant cells. J. Immunol. 169:5209-5216.
21. Hornef, M.W., B.H. Normark, A. Vandewalle, and S. Normark. 2003. Intracellular recognition of lipopolysaccharide by Toll-like receptor 4 in intestinal epithelial cells. J. Exp. Med. 198:1225-1235.
22. Bi, K., Y. Tanaka, N. Coudronniere, K. Sugie, S. Hong, M.J. van Stipdonk, and A. Altman. 2001. Antigen-induced translocation of PKC-theta to membrane rafts is required for T cell activation. Nat. Immunol. 2:556-563.
23. Gaide, O., B. Favier, D.F. Legler, D. Bonnet, B. Brissoni, S. Valitutti, C. Bron, J. Tschopp, and M. Thome. 2002. CARMA1 is a critical lipid raft-associated regulator of TCR-induced NF-kappa B activation. Nat. Immunol. 3:836-843.
24. 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.
25. Harder, T., P. Scheiffele, P. Verkade, and K. Simons. 1998. Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141:929-942.
26. Fessler, M.B., P.G. Arndt, S.C. Frasch, J.G. Lieber, C.A. Johnson, R.C. Murphy, J.A. Nick, D.L. Bratton, K.C. Malcolm, and G.S. Worthen. 2004. Lipid rafts regulate lipopolysaccharide-induced activation of Cdc42 and inflammatory functions of the human neutrophil. J. Biol. Chem. 279:39989-39998.
27. Triantafilou, M., K. Brandenburg, S. Kusumoto, K. Fukase, A. Mackie, U. Seydel, and K. Triantafilou. 2004. Combinational clustering of receptors following stimulation by bacterial products determines lipopolysaccharide responses. Biochem. J. 381:527-536.
28. Dai, Q., J. Zhang, and S.B. Pruett. 2005. Ethanol alters cellular activation and CD14 partitioning in lipid rafts. Biochem. Biophys. Res. Commun. 332:37-42.
29. Ahmad-Nejad, P., H. Hacker, M. Rutz, S. Bauer, R.M. Vabulas, and H. Wagner. 2002. Bacterial CpG-DNA and lipopolysaccharides activate Toll-like receptors at distinct cellular compartments. Eur. J. Immunol. 32:1958-1968.
30. Park, H.S., H.Y. Jung, E.Y. Park, J. Kim, W.J. Lee, and Y.S. Bae. 2004. Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-kappa B. J. Immunol. 173:3589-3593.
31. Matsuzawa, A., K. Saegusa, T. Noguchi, C. Sadamitsu, H. Nishitoh, S. Nagai, S. Koyasu, K. Matsumoto, K. Takeda, and H. Ichijo. 2005. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat. Immunol. 6:587-592.
32. Powers, K.A., K. Szaszi, R.G. Khadaroo, P.S. Tawadros, J.C. Marshall, A. Kapus, and O.D. Rotstein. 2006. Oxidative stress generated by hemorrhagic shock recruits Toll-like receptor 4 to the plasma membrane in macrophages. J. Exp. Med. 203:1951-1961.
33. Li, J.M., and A.M. Shah. 2002. Intracellular localization and preassembly of the NADPH oxidase complex in cultured endothelial cells. J. Biol. Chem. 277:19952-19960.
34. Sumimoto, H., K. Miyano, and R. Takeya. 2005. Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem. Biophys. Res. Commun. 338:677-686.
35. Taille, C., J. El-Benna, S. Lanone, J. Boczkowski, and R. Motterlini. 2005. Mitochondrial respiratory chain and NAD(P)H oxidase are targets for the antiproliferative effect of carbon monoxide in human airway smooth muscle. J. Biol. Chem. 280:25350-25360.
36. Reinking, J., M.M. Lam, K. Pardee, H.M. Sampson, S. Liu, P. Yang, S. Williams, W. White, G. Lajoie, A. Edwards, and H.M. Krause. 2005. The Drosophila nuclear receptor e75 contains heme and is gas responsive. Cell. 122:195-207.
37. Peng, T., X. Lu, and Q. Feng. 2005. Pivotal role of gp91phox-containing NADH oxidase in lipopolysaccharide-induced tumor necrosis factor-alpha expression and myocardial depression. Circulation. 111:1637-1644.
38. Kato, H., O. Takeuchi, S. Sato, M. Yoneyama, M. Yamamoto, K. Matsui, S. Uematsu, A. Jung, T. Kawai, K.J. Ishii, et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature. 441:101-105.
39. Brint, E.K., D. Xu, H. Liu, A. Dunne, A.N. McKenzie, L.A. O'Neill, and F.Y. Liew. 2004. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nat. Immunol. 5:373-379.
40. Chuang, T.H., and R.J. Ulevitch. 2004. Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat. Immunol. 5:495-502.
41. Su, T.T., B. Guo, Y. Kawakami, K. Sommer, K. Chae, L.A. Humphries, R.M. Kato, S. Kang, L. Patrone, R. Wall, et al. 2002. PKC-beta controls I kappa B kinase lipid raft recruitment and activation in response to BCR signaling. Nat. Immunol. 3:780-786.
42. Arron, J.R., Y. Pewzner-Jung, M.C. Walsh, T. Kobayashi, and Y. Choi. 2002. Regulation of the subcellular localization of tumor necrosis factor receptor-associated factor (TRAF)2 by TRAF1 reveals mechanisms of TRAF2 signaling. J. Exp. Med. 196:923-934.
43. Latz, E., A. Schoenemeyer, A. Visintin, K.A. Fitzgerald, B.G. Monks, C.F. Knetter, E. Lien, N.J. Nilsen, T. Espevik, and D.T. Golenbock. 2004. TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat. Immunol. 5:190-198.
44. Leifer, C.A., M.N. Kennedy, A. Mazzoni, C. Lee, M.J. Kruhlak, and D.M. Segal. 2004. TLR9 is localized in the endoplasmic reticulum prior to stimulation. J. Immunol. 173:1179-1183.
45. Janes, P.W., S.C. Ley, and A.I. Magee. 1999. Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147:447-461.
46. Qin, S., Y. Minami, M. Hibi, T. Kurosaki, and H. Yamamura. 1997. Syk-dependent and -independent signaling cascades in B cells elicited by osmotic and oxidative stress. J. Biol. Chem. 272:2098-2103.
47. Srisook, K., S.S. Han, H.S. Choi, M.H. Li, H. Ueda, C. Kim, and Y.N. Cha. 2006. CO from enhanced HO activity or from CORM-2 inhibits both O2- and NO production and downregulates HO-1 expression in LPS-stimulated macrophages. Biochem. Pharmacol. 71:307-318.
48. Jaggar, J.H., A. Li, H. Parfenova, J. Liu, E.S. Umstot, A.M. Dopico, and C.W. Leffler. 2005. Heme is a carbon monoxide receptor for large-conductance Ca2+-activated K+ channels. Circ. Res. 97:805-812.
49. Taille, C., J. El-Benna, S. Lanone, M.C. Dang, E. Ogier-Denis, M. Aubier, and J. Boczkowski. 2004. Induction of heme oxygenase-1 inhibits NAD(P)H oxidase activity by down-regulating cytochrome b558 expression via the reduction of heme availability. J. Biol. Chem. 279:28681-28688.
50. Jenner, R.G., and R.A. Young. 2005. Insights into host responses against pathogens from transcriptional profiling. Nat. Rev. Microbiol. 3:281-294.
51. Riedemann, N.C., R.F. Guo, and P.A. Ward. 2003. Novel strategies for the treatment of sepsis. Nat. Med. 9:517-524.
52. Bilban, M., F.H. Bach, S.L. Otterbein, E. Ifedigbo, J. de Costa d'Avila, H. Esterbauer, B.Y. Chin, A. Usheva, S.C. Robson, O. Wagner, and L.E. Otterbein. 2006. Carbon monoxide orchestrates a protective response through PPARgamma. Immunity. 24:601-610.
53. Yet, S.F., M.A. Perrella, M.D. Layne, C.M. Hsieh, K. Maemura, L. Kobzik, P. Wiesel, H. Christou, S. Kourembanas, and M.E. Lee. 1999. Hypoxia induces severe right ventricular dilatation and infarction in heme oxygenase-1 null mice. J. Clin. Invest. 103:R23-R29.
54. 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.
55. Kim, H.P., X. Wang, F. Galbiati, S.W. Ryter, and A.M. Choi. 2004. Caveolae compartmentalization of heme oxygenase-1 in endothelial cells. FASEB J. 18:1080-1089.
56. Nakao, A., K. Kimizuka, D.B. Stolz, J.S. Neto, T. Kaizu, A.M. Choi, T. Uchiyama, B.S. Zuckerbraun, M.A. Nalesnik, L.E. Otterbein, and N. Murase. 2003. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am. J. Pathol. 163:1587-1598.
57. Wang, X., Y. Wang, J. Zhang, H.P. Kim, S.W. Ryter, and A.M. Choi. 2005. FLIP protects against hypoxia/reoxygenation-induced endothelial cell apoptosis by inhibiting Bax activation. Mol. Cell. Biol. 25:4742-4751.
58. Sekhar, K.R., P.A. Crooks, V.N. Sonar, D.B. Friedman, J.Y. Chan, M.J. Meredith, J.H. Starnes, K.R. Kelton, S.R. Summar, S. Sasi, and M.L. Freeman. 2003. NADPH oxidase activity is essential for Keap1/Nrf2-mediated induction of GCLC in response to 2-indol-3-yl-methylenequinuclidin-3-ols. Cancer Res. 63:5636-5645.
59. Quinn, M.T., C.A. Parkos, and A.J. Jesaitis. 1995. Purification of human neutrophil NADPH oxidase cytochrome b-558 and association with Rap 1A. Methods Enzymol. 255:476-487.