Toll-like receptor 3 ligand dampens liver inflammation by stimulating Vα14 invariant natural killer T cells to negatively regulate γδT cells

American Journal of Pathology

Volumn 176, Issue 4, 2010, Pages 1779-1789

  Gardner, Tommy R ^a   Chen, Qingling ^a   Jin, Yijun ^a   Ajuebor, Maureen N ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; POLYINOSINIC POLYCYTIDYLIC ACID; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 3;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; GAMMA DELTA T CELL; HEPATITIS; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; UPREGULATION;

EID: 77950587866     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090738     Document Type: Article

References (69)

1. Van Kaer L: α-Galactosylceramide therapy for autoimmune diseases: prospects and obstacles. Nat Rev Immunol 2005, 5:31-42 (Pubitemid 40070329)
2. Kronenberg M: Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol 2005, 23:877-900
3. Wilson MT, Singh AK, Van Kaer L: Immunotherapy with ligands of natural killer T cells. Trends Mol Med 2002, 8:225-231 (Pubitemid 34493640)
4. Wilson MT, Van Kaer L: Natural killer T cells as targets for therapeutic intervention in autoimmune diseases. Curr Pharm Des 2003, 9:201-220 (Pubitemid 36131715)
5. Bendelac A, Savage PB, Teyton L: The biology of NKT cells. Annu Rev Immunol 2007, 25:297-336
6. Rogers L, Burchat S, Gage J, Hasu M, Thabet M, Wilcox L, Ramsamy TA, Whitman SC: Deficiency of invariant Vα14 natural killer T cells decreases atherosclerosis in LDL receptor null mice. Cardiovasc Res 2008, 78:167-174 (Pubitemid 351430959)
7. VanderLaan PA, Reardon CA, Sagiv Y, Blachowicz L, Lukens J, Nissenbaum M, Wang CR, Getz GS: Characterization of the natural killer T-cell response in an adoptive transfer model of atherosclerosis. Am J Pathol 2007, 170:1100-1107 (Pubitemid 47339376)
8. Godfrey DI, MacDonald HR, Kronenberg M, Smyth MJ, Van Kaer L: NKT cells: what's in a name?. Nat Rev Immunol 2004, 4:231-237
9. Seino K, Taniguchi M: Functional roles of NKT cell in the immune system. Front Biosci 2004, 9:2577-2587
10. Tessmer MS, Fatima A, Paget C, Trottein F, Brossay L: NKT cell immune responses to viral infection. Expert Opin Ther Targets 2009, 13:153-162
11. Burdin N, Kronenberg M: CD1-mediated immune responses to glycolipids. Curr Opin Immunol 1999, 11:326-331
12. Gumperz JE, Roy C, Makowska A, Lum D, Sugita M, Podrebarac T, Koezuka Y, Porcelli SA, Cardell S, Brenner MB, Behar SM: Murine CD1d-restricted T cell recognition of cellular lipids. Immunity 2000, 12:211-221 (Pubitemid 30398635)
13. Matsuda JL, Mallevaey T, Scott-Browne J, Gapin L: CD1d-restricted iNKT cells, the 'Swiss-Army knife' of the immune system. Curr Opin Immunol 2008, 20:358-368
14. Brigl M, Bry L, Kent SC, Gumperz JE, Brenner MB: Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol 2003, 4:1230-1237 (Pubitemid 37540692)
15. Taniguchi M, Seino K, Nakayama T: The NKT cell system: bridging innate and acquired immunity. Nat Immunol 2003, 4:1164-1165 (Pubitemid 37540684)
16. Ajuebor MN, Aspinall AI, Zhou F, Le T, Yang Y, Urbanski SJ, Sidobre S, Kronenberg M, Hogaboam CM, Swain MG: Lack of chemokine receptor CCR5 promotes murine fulminant liver failure by preventing the apoptosis of activated CD1d-restricted NKT cells. J Immunol 2005, 174:8027-8037 (Pubitemid 40806314)
17. Ajuebor MN, Jin Y, Gremillion GL, Strieter RM, Chen Q, Adegboyega PA: γδT cells initiate acute inflammation and injury in adenovirus-infected liver via cytokine-chemokine cross talk. J Virol 2008, 82:9564-9576
18. Matsuda JL, Gapin L, Baron JL, Sidobre S, Stetson DB, Mohrs M, Locksley RM, Kronenberg M: Mouse Vα14i natural killer T cells are resistant to cytokine polarization in vivo, Proc Natl Acad Sci USA 2003, 100:8395-8400 (Pubitemid 36842556)
19. Crowe NY, Coquet JM, Berzins SP, Kyparissoudis K, Keating R, Pellicci DG, Hayakawa Y, Godfrey DI, Smyth MJ: Differential antitumor immunity mediated by NKT cell subsets in vivo. J Exp Med 2005, 202:1279-1288 (Pubitemid 41586958)
20. Carnaud C, Lee D, Donnars O, Park SH, Beavis A, Koezuka Y, Bendelac A: Cutting edge: Cross-talk between cells of the innate immune system: nKT cells rapidly activate NK cells. J Immunol 1999, 163:4647-4650 (Pubitemid 29501223)
21. Ajuebor MN, Wondimu Z, Hogaboam CM, Le T, Proudfoot AE, Swain MG: CCR5 deficiency drives enhanced natural killer cell trafficking to and activation within the liver in murine T cell-mediated hepatitis. Am J Pathol 2007, 170:1975-1988 (Pubitemid 47339271)
22. Schwabe RF, Seki E, Brenner DA: Toll-like receptor signaling in the liver. Gastroenterology 2006, 130:1886-1900
23. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA: Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 2001, 413:732-738 (Pubitemid 33009951)
24. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA: Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci USA 2004, 101:5598-5603 (Pubitemid 38481202)
25. Heil F, Hemmi H, Hochrein H, Ampenberger F, Kirschning C, Akira S, Lipford G, Wagner H, Bauer S: Species-specific recognition of single-stranded RNA via Toll-like receptor 7 and 8. Science 2004, 303:1526-1529 (Pubitemid 38314424)
26. Bauer S, Kirschning CJ, Hacker H, Redecke V, Hausmann S, Akira S, Wagner H, Lipford GB: Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition, Proc Natl Acad Sci USA 2001, 98:9237-9242 (Pubitemid 32743900)
27. Tyznik AJ, Tupin E, Nagarajan NA, Her MJ, Benedict CA, Kronenberg M: Cutting edge: The mechanism of invariant NKT cell responses to viral danger signals. J Immunol 2008, 181:4452-4456
28. Nagarajan NA, Kronenberg M: Invariant NKT cells amplify the innate immune response to lipopolysaccharide. J Immunol 2007, 178:2706-2713 (Pubitemid 46335652)
29. Londhe VA, Belperio JA, Keane MP, Burdick MD, Xue YY, Strieter RM: CXCR2 is critical for dsRNA-induced lung injury: relevance to viral lung infection. J Inflamm (Lond) 2005, 2:4
30. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR: Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 2006, 80:5059-5064
31. Guillot L, Le Goffic R, Bloch S, Escriou N, Akira S, Chignard M, Si-Tahar M: Involvement of Toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J Biol Chem 2005, 280:5571-5580 (Pubitemid 40280035)
32. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, Kaneko Y, Koseki H, Kanno M, Taniguchi M: Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science 1997, 278:1623-1626 (Pubitemid 27516281)
33. Wang J, Sun R, Wei H, Dong Z, Tian Z: Pre-activation of T lymphocytes by low dose of concanavalin A aggravates Toll-like receptor-3 ligand-induced NK cell-mediated liver injury. Int Immunopharmacol 2006, 6:800-807
34. Siegel M, Strnad P, Watts RE, Choi K, Jabri B, Omary MB, Khosla C: Extracellular transglutaminase 2 is catalytically inactive, but is transiently activated upon tissue injury. PLoS ONE 2008, 3:e1861 (Pubitemid 351943737)
35. Salminen WF Jr, Voellmy R, Roberts SM: Effect of N-acetylcysteine on heat shock protein induction by acetaminophen in mouse liver. J Pharmacol Exp Ther 1998, 286:519-524 (Pubitemid 28318028)
36. O'Brien RL, Roark CL, Born WK: IL-17-producing γδT cells. Eur J Immunol 2009, 39:662-666
37. Hobbs JA, Cho S, Roberts TJ, Sriram V, Zhang J, Xu M, Brutkiewicz RR: Selective loss of natural killer T cells by apoptosis following infection with lymphocytic choriomeningitis virus. J Virol 2001, 75:10746-10754 (Pubitemid 33031544)
38. Savage PB, Teyton L, Bendelac A: Glycolipids for natural killer T cells. Chem Soc Rev 2006, 35:771-779
39. Cho WG, Albuquerque RJ, Kleinman ME, Tarallo V, Greco A, Nozaki M, Green MG, Baffi JZ, Ambati BK, De Falco M, Alexander JS, Brunetti A, De Falco S, Ambati J: Small interfering RNA-induced TLR3 activation inhibits blood and lymphatic vessel growth, Proc Natl Acad Sci USA 2009, 106:7137-7142
40. O'Brien RL, Roark CL, Jin N, Aydintug MK, French JD, Chain JL, Wands JM, Johnston M, Born WK: γδT-cell receptors: functional correlations. Immunol Rev 2007, 215:77-88
41. + T cells and natural killer cells is essential for the antimetastatic effect of α-galactosylceramide. Blood 2002, 99:1259-1266
42. Wesley JD, Tessmer MS, Chaukos D, Brossay L: NK cell-like behavior of Vα14i NK T cells during MCMV infection. PLoS Pathog 2008, 4:e1000106
43. Gardner T, Chen Q, Jin Y, Ajuebor MN: Characterization of the role of TCR γδ in NK cell accumulation during viral liver inflammation. Exp Mol Pathol 2009, 86:32-35
44. Wang J, Sun R, Wei H, Dong Z, Gao B, Tian Z: Poly I:C prevents T cell-mediated hepatitis via an NK-dependent mechanism. J Hepatol 2006, 44:446-454 (Pubitemid 43227868)
45. Chiba A, Dascher CC, Besra GS, Brenner MB: Rapid NKT cell responses are self-terminating during the course of microbial infection. J Immunol 2008, 181:2292-2302
46. + T cells during mycobacterial infection to promote apoptosis by inducing components of the intracellular apoptosis machinery and by inducing extracellular proapoptotic signals. J Immunol 2007, 179:939-949
47. Kudo H, Takahara T, Yata Y, Kawai K, Zhang W, Sugiyama T: Lipopolysaccharide triggered TNF-α-induced hepatocyte apoptosis in a murine non-alcoholic steatohepatitis model, J Hepatol 2009, 51:168-175
48. Aggarwal S, Gollapudi S, Gupta S: Increased TNF-α-induced apoptosis in lymphocytes from aged humans: changes in TNF-α receptor expression and activation of caspases. J Immunol 1999, 162:2154-2161 (Pubitemid 29288837)
49. Hildeman DA, Mitchell T, Kappler J, Marrack P: T cell apoptosis and reactive oxygen species. J Clin Invest 2003, 111:575-581 (Pubitemid 36278573)
50. Cavassani KA, Ishii M, Wen H, Schaller MA, Lincoln PM, Lukacs NW, Hogaboam CM, Kunkel SL: TLR3 is an endogenous sensor of tissue necrosis during acute inflammatory events. J Exp Med 2008, 205:2609-2621
51. Paget C, Mallevaey T, Speak AO, Torres D, Fontaine J, Sheehan KC, Capron M, Ryffel B, Faveeuw C, Leite de Moraes M, Platt F, Trottein F: Activation of invariant NKT cells by Toll-like receptor 9-stimulated dendritic cells requires type I interferon and charged glycosphingolipids. Immunity 2007, 27:597-609 (Pubitemid 47628833)
52. Salio M, Speak AO, Shepherd D, Polzella P, Illarionov PA, Veerapen N, Besra GS, Platt FM, Cerundolo V: Modulation of human natural killer T cell ligands on TLR-mediated antigen-presenting cell activation, Proc Natl Acad Sci USA 2007, 104:20490-20495
53. Schmidt KN, Leung B, Kwong M, Zarember KA, Satyal S, Navas TA, Wang F, Godowski PJ: APC-independent activation of NK cells by the Toll-like receptor 3 agonist double-stranded RNA. J Immunol 2004, 172:138-143 (Pubitemid 38020465)
54. Isogawa M, Robek MD, Furuichi Y, Chisari FV: Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J Virol 2005, 79:7269-7272 (Pubitemid 40677357)
55. Wesch D, Beetz S, Oberg HH, Marget M, Krengel K, Kabelitz D: Direct costimulatory effect of TLR3 ligand poly(I:C) on human γδT lymphocytes. J Immunol 2006, 176:1348-1354 (Pubitemid 43134276)
56. Patole PS, Grone HJ, Segerer S, Ciubar R, Belemezova E, Henger A, Kretzler M, Schlondorff D, Anders HJ: Viral double-stranded RNA aggravates lupus nephritis through Toll-like receptor 3 on glomerular mesangial cells and antigen-presenting cells. J Am Soc Nephrol 2005, 16:1326-1338 (Pubitemid 41716517)
57. Niimi K, Asano K, Shiraishi Y, Nakajima T, Wakaki M, Kagyo J, Takihara T, Suzuki Y, Fukunaga K, Shiomi T, Oguma T, Sayama K, Yamaguchi K, Natori Y, Matsumoto M, Seya T, Yamaya M, Ishizaka A: TLR3-mediated synthesis and release of eotaxin-1/CCL11 from human bronchial smooth muscle cells stimulated with double-stranded RNA. J Immunol 2007, 178:489-495 (Pubitemid 46033633)
58. Negishi H, Osawa T, Ogami K, Ouyang X, Sakaguchi S, Koshiba R, Yanai H, Seko Y, Shitara H, Bishop K, Yonekawa H, Tamura T, Kaisho T, Taya C, Taniguchi T, Honda K: A critical link between Toll-like receptor 3 and type II interferon signaling pathways in antiviral innate immunity, Proc Natl Acad Sci USA 2008, 105:20446-20451
59. Biburger M, Tiegs G: α-Galactosylceramide-induced liver injury in mice is mediated by TNF-α but independent of Kupffer cells. J Immunol 2005, 175:1540-1550 (Pubitemid 41023055)
60. Wintermeyer P, Cheng CW, Gehring S, Hoffman BL, Holub M, Brossay L, Gregory SH: Invariant natural killer T cells suppress the neutrophil inflammatory response in a mouse model of cholestatic liver damage. Gastroenterology 2009, 136:1048-1059
61. Dong Z, Wei H, Sun R, Hu Z, Gao B, Tian Z: Involvement of natural killer cells in poly I:C-induced liver injury. J Hepatol 2004, 41:966-973 (Pubitemid 39575664)
62. Jin N, Miyahara N, Roark CL, French JD, Aydintug MK, Matsuda JL, Gapin L, O'Brien RL, Gelfand EW, Born WK: Airway hyperresponsiveness through synergy of γδT cells and NKT cells. J Immunol 2007, 179:2961-2968 (Pubitemid 46654182)
63. Matsuda JL, Naidenko OV, Gapin L, Nakayama T, Taniguchi M, Wang CR, Koezuka Y, Kronenberg M: Tracking the response of natural killer T cells to a glycolipid antigen using CD1d tetramers. J Exp Med 2000, 192:741-754
64. Taniai H, Hines IN, Bharwani S, Maloney RE, Nimura Y, Gao B, Flores SC, McCord JM, Grisham MB, Aw TY: Susceptibility of murine periportal hepatocytes to hypoxia-reoxygenation: role for NO and Kupffer cell-derived oxidants. Hepatology 2004, 39:1544-1552 (Pubitemid 38702655)
65. Jaeschke H, Bautista AP, Spolarics Z, Spitzer JJ: Superoxide generation by Kupffer cells and priming of neutrophils during reperfusion after hepatic ischemia. Free Radic Res Commun 1991, 15:277-284
66. Peck A, Mellins ED: Breaking old paradigms: Th17 cells in autoimmune arthritis. Clin Immunol 2009, 132:295-304
67. Iwakura Y, Nakae S, Saijo S, Ishigame H: The roles of IL-17A in inflammatory immune responses and host defense against pathogens. Immunol Rev 2008, 226:57-79
68. Johansson S, Berg L, Hall H, Hoglund P: NK cells: elusive players in autoimmunity. Trends Immunol 2005, 26:613-618
69. Smyth MJ, Cretney E, Takeda K, Wiltrout RH, Sedger LM, Kayagaki N, Yagita H, Okumura K: Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) contributes to interferon γ-dependent natural killer cell protection from tumor metastasis. J Exp Med 2001, 193:661-670 (Pubitemid 32524460)