T cell Ig Mucin-3 promotes homeostasis of sepsis by negatively regulating the TLR response

Journal of Immunology

Volumn 190, Issue 5, 2013, Pages 2068-2079

  Yang, Xiaomei ^a,b   Jiang, Xingwei ^a   Chen, Guojiang ^a   Xiao, Yan ^c   Geng, Shaoxia ^a,b   Kang, Chunyan ^c   Zhou, Tingting ^a   Li, Yurong ^a   Guo, Xiaoqin ^a   Xiao, He ^a   Hou, Chunmei ^a   Wang, Renxi ^a   Lin, Zhou ^a   Li, Xinying ^a   Feng, Jiannan ^a   Ma, Yuanfang ^b   Shen, Beifen ^a   Li, Yan ^a   Han, Gencheng ^a  

^a INSTITUTE OF BASIC MEDICAL SCIENCES   (China)

^b HENAN UNIVERSITY   (China)

^c CHINESE PLA GENERAL HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; CD36 ANTIGEN; CD48 ANTIGEN; CXCL16 CHEMOKINE; IMMUNOGLOBULIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; MUCIN 3; MUCIN DOMAIN PROTEIN 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RECOMBINANT BLOOD CLOTTING FACTOR 8; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE SEVERITY; DOWN REGULATION; ENZYME ACTIVITY; HOMEOSTASIS; HUMAN; HUMAN CELL; INNATE IMMUNITY; MACROPHAGE ACTIVATION; MOLECULAR INTERACTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SEPSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE; UPREGULATION;

ADULT; AGED; ANIMALS; BIOLOGICAL MARKERS; CELL LINE; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; LIPOPOLYSACCHARIDES; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; NF-KAPPA B; PHOSPHATIDYLINOSITOL 3-KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SEPSIS; SEVERITY OF ILLNESS INDEX; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84874269629     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202661     Document Type: Article

References (58)

1. Martin, G. S., D. M. Mannino, S. Eaton, and M. Moss. 2003. The epidemiology of sepsis in the United States from 1979 through 2000. N. Engl. J. Med. 348: 1546-1554.
2. Gustot, T. 2011. Multiple organ failure in sepsis: prognosis and role of systemic inflammatory response. Curr. Opin. Crit. Care 17: 153-159.
3. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
4. Takeda, K., T. Kaisho, and S. Akira. 2003. Toll-like receptors. Annu. Rev. Immunol. 21: 335-376.
5. Moss, M., and G. S. Martin. 2004. A global perspective on the epidemiology of sepsis. Intensive Care Med. 30: 526-529.
6. Rasmussen, S. B., L. S. Reinert, and S. R. Paludan. 2009. Innate recognition of intracellular pathogens: detection and activation of the first line of defense. APMIS 117: 323-337.
7. 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.
8. O'Neill, L. A. 2003. Therapeutic targeting of Toll-like receptors for inflammatory and infectious diseases. Curr. Opin. Pharmacol. 3: 396-403.
9. Ehrentraut, S., R. Lohner, M. Schwederski, H. Ehrentraut, O. Boehm, S. Noga, P. Langhoff, G. Baumgarten, R. Meyer, and P. Knuefermann. 2011. In vivo Tolllike receptor 4 antagonism restores cardiac function during endotoxemia. Shock 36: 613-620.
10. Schwandt, T., B. Schumak, G. H. Gielen, F. Jüngerkes, P. Schmidbauer, K. Klocke, A. Staratschek-Jox, N. van Rooijen, G. Kraal, I. Ludwig-Portugall, et al. 2012. Expression of type I interferon by splenic macrophages suppresses adaptive immunity during sepsis. EMBO J. 31: 201-213.
11. Wittebole, X., D. Castanares-Zapatero, and P. F. Laterre. 2010. Toll-like receptor 4 modulation as a strategy to treat sepsis. Mediators Inflamm. 2010: 568396.
12. Hennessy, E. J., A. E. Parker, and L. A. O'Neill. 2010. Targeting Toll-like receptors: emerging therapeutics? Nat. Rev. Drug Discov. 9: 293-307.
13. Sánchez-Fueyo, A., J. Tian, D. Picarella, C. Domenig, X. X. Zheng, C. A. Sabatos, N. Manlongat, O. Bender, T. Kamradt, V. K. Kuchroo, et al. 2003. Tim-3 inhibits T helper type 1-mediated auto- and alloimmune responses and promotes immunological tolerance. Nat. Immunol. 4: 1093-1101.
14. Hastings, W. D., D. E. Anderson, N. Kassam, K. Koguchi, E. A. Greenfield, S. C. Kent, X. X. Zheng, T. B. Strom, D. A. Hafler, and V. K. Kuchroo. 2009. TIM-3 is expressed on activated human CD4+ T cells and regulates Th1 and Th17 cytokines. Eur. J. Immunol. 39: 2492-2501.
15. Zhu, C., A. C. Anderson, A. Schubart, H. Xiong, J. Imitola, S. J. Khoury, X. X. Zheng, T. B. Strom, and V. K. Kuchroo. 2005. The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity. Nat. Immunol. 6: 1245-1252.
16. Niwa, H., T. Satoh, Y. Matsushima, K. Hosoya, K. Saeki, T. Niki, M. Hirashima, and H. Yokozeki. 2009. Stable form of galectin-9, a Tim-3 ligand, inhibits contact hypersensitivity and psoriatic reactions: a potent therapeutic tool for Th1- and/or Th17-mediated skin inflammation. Clin. Immunol. 132: 184-194.
17. Anderson, A. C., D. E. Anderson, L. Bregoli, W. D. Hastings, N. Kassam, C. Lei, R. Chandwaskar, J. Karman, E. W. Su, M. Hirashima, et al. 2007. Promotion of tissue inflammation by the immune receptor Tim-3 expressed on innate immune cells. Science 318: 1141-1143.
18. Nagahara, K., T. Arikawa, S. Oomizu, K. Kontani, A. Nobumoto, H. Tateno, K. Watanabe, T. Niki, S. Katoh, M. Miyake, et al. 2008. Galectin-9 increases Tim-3+ dendritic cells and CD8+ T cells and enhances antitumor immunity via galectin-9-Tim-3 interactions. J. Immunol. 181: 7660-7669.
19. Chiba, S., M. Baghdadi, H. Akiba, H. Yoshiyama, I. Kinoshita, H. Dosaka-Akita, Y. Fujioka, Y. Ohba, J. V. Gorman, J. D. Colgan, et al. 2012. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat. Immunol. 13: 832-842.
20. Koguchi, K., D. E. Anderson, L. Yang, K. C. O'Connor, V. K. Kuchroo, and D. A. Hafler. 2006. Dysregulated T cell expression of TIM3 in multiple sclerosis. J. Exp. Med. 203: 1413-1418.
21. Liberal, R., C. R. Grant, B. S. Holder, Y. Ma, G. Mieli-Vergani, D. Vergani, and M. S. Longhi. 2012. The impaired immune regulation of autoimmune hepatitis is linked to a defective galectin-9/tim-3 pathway. Hepatology 56: 677-686.
22. Elahi, S., W. L. Dinges, N. Lejarcegui, K. J. Laing, A. C. Collier, D. M. Koelle, M. J. McElrath, and H. Horton. 2011. Protective HIV-specific CD8+ T cells evade Treg cell suppression. Nat. Med. 17: 989-995.
23. Li, H., K.Wu, K. Tao, L. Chen, Q. Zheng, X. Lu, J. Liu, L. Shi, C. Liu, G. Wang, and W. Zou. 2012. Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma. Hepatology 56: 1342-1351.
24. Frisancho-Kiss, S., S. E. Davis, J. F. Nyland, J. A. Frisancho, D. Cihakova, M. A. Barrett, N. R. Rose, and D. Fairweather. 2007. Cutting edge: crossregulation by TLR4 and T cell Ig mucin-3 determines sex differences in inflammatory heart disease. J. Immunol. 178: 6710-6714.
25. Uchida, Y., B. Ke, M. C. Freitas, H. Yagita, H. Akiba, R. W. Busuttil, N. Najafian, and J. W. Kupiec-Weglinski. 2010. T-cell immunoglobulin mucin-3 determines severity of liver ischemia/reperfusion injury in mice in a TLR4- dependent manner. Gastroenterology 139: 2195-2206.
26. Hotchkiss, R. S., C. M. Coopersmith, J. E. McDunn, and T. A. Ferguson. 2009. The sepsis seesaw: tilting toward immunosuppression. Nat. Med. 15: 496-497.
27. Bone, R. C., R. A. Balk, F. B. Cerra, R. P. Dellinger, A. M. Fein, W. A. Knaus, R. M. Schein, and W. J. Sibbald; The ACCP/SCCM Consensus Conference Committee. American College of Chest Physicians/Society of Critical Care Medicine. 1992. Definitions for sepsis and organ failure and guidelines for the use of innovative therapies in sepsis. Chest 101: 1644-1655.
28. Monney, L., C. A. Sabatos, J. L. Gaglia, A. Ryu, H. Waldner, T. Chernova, S. Manning, E. A. Greenfield, A. J. Coyle, R. A. Sobel, et al. 2002. Th1-specific cell surface protein Tim-3 regulates macrophage activation and severity of an autoimmune disease. Nature 415: 536-541.
29. Li, X., G. Chen, Y. Li, R. Wang, L. Wang, Z. Lin, X. Gao, J. Feng, Y. Ma, B. Shen, et al. 2010. Involvement of T cell Ig Mucin-3 (Tim-3) in the negative regulation of inflammatory bowel disease. Clin. Immunol. 134: 169-177.
30. Kashio, Y., K. Nakamura, M. J. Abedin, M. Seki, N. Nishi, N. Yoshida, T. Nakamura, and M. Hirashima. 2003. Galectin-9 induces apoptosis through the calcium-calpain-caspase-1 pathway. J. Immunol. 170: 3631-3636.
31. Weng, T. I., H. Y. Wu, C. W. Kuo, and S. H. Liu. 2011. Honokiol rescues sepsisassociated acute lung injury and lethality via the inhibition of oxidative stress and inflammation. Intensive Care Med. 37: 533-541.
32. Geng, H., G. M. Zhang, D. Li, H. Zhang, Y. Yuan, H. G. Zhu, H. Xiao, L. F. Han, and Z. H. Feng. 2006. Soluble form of T cell Ig mucin 3 is an inhibitory molecule in T cell-mediated immune response. J. Immunol. 176: 1411-1420.
33. Shaw, D. R., and F. M. Griffin, Jr. 1982. Thioglycollate-elicited mouse peritoneal macrophages are less efficient than resident macrophages in antibody-dependent cell-mediated cytolysis. J. Immunol. 128: 433-440.
34. Li, Y., J. Feng, S. Geng, S. Geng, H. Wei, G. Chen, X. Li, L. Wang, R. Wang, H. Peng, et al. 2011. The N- and C-terminal carbohydrate recognition domains of galectin-9 contribute differently to its multiple functions in innate immunity and adaptive immunity. Mol. Immunol. 48: 670-677.
35. Xu, R., R. Wang, G. Han, J. Wang, G. Chen, L. Wang, X. Li, R. Guo, B. Shen, and Y. Li. 2010. Complement C5a regulates IL-17 by affecting the crosstalk between DC and gammadelta T cells in CLP-induced sepsis. Eur. J. Immunol. 40: 1079-1088.
36. Castoldi, A., T. T. Braga, M. Correa-Costa, C. F. Aguiar, Ê. J. Bassi, R. Correa- Silva, R. M. Elias, F. Salvador, P. M. Moraes-Vieira, M. A. Cenedeze, et al. 2012. TLR2, TLR4 and the MYD88 signaling pathway are crucial for neutrophil migration in acute kidney injury induced by sepsis. PLoS ONE 7: e37584.
37. O'Neill, L. A. 2002. Signal transduction pathways activated by the IL-1 receptor/ toll-like receptor superfamily. Curr. Top. Microbiol. Immunol. 270: 47-61.
38. Polumuri, S. K., V. Y. Toshchakov, and S. N. Vogel. 2007. Role of phosphatidylinositol- 3 kinase in transcriptional regulation of TLR-induced IL-12 and IL-10 by Fc g receptor ligation in murine macrophages. J. Immunol. 179: 236-246.
39. Fukao, T., M. Tanabe, Y. Terauchi, T. Ota, S. Matsuda, T. Asano, T. Kadowaki, T. Takeuchi, and S. Koyasu. 2002. PI3K-mediated negative feedback regulation of IL-12 production in DCs. Nat. Immunol. 3: 875-881.
40. Guha, M., and N. Mackman. 2002. The phosphatidylinositol 3-kinase-Akt pathway limits lipopolysaccharide activation of signaling pathways and expression of inflammatory mediators in human monocytic cells. J. Biol. Chem. 277: 32124-32132.
41. Kinjyo, I., T. Hanada, K. Inagaki-Ohara, H. Mori, D. Aki, M. Ohishi, H. Yoshida, M. Kubo, and A. Yoshimura. 2002. SOCS1/JAB is a negative regulator of LPSinduced macrophage activation. Immunity 17: 583-591.
42. Mashima, R., K. Saeki, D. Aki, Y. Minoda, H. Takaki, T. Sanada, T. Kobayashi, H. Aburatani, Y. Yamanashi, and A. Yoshimura. 2005. FLN29, a novel interferon- and LPS-inducible gene acting as a negative regulator of toll-like receptor signaling. J. Biol. Chem. 280: 41289-41297.
43. Heyninck, K., and R. Beyaert. 1999. The cytokine-inducible zinc finger protein A20 inhibits IL-1-induced NF-kappaB activation at the level of TRAF6. FEBS Lett. 442: 147-150.
44. Lee, J., E. W. Su, C. Zhu, S. Hainline, J. Phuah, J. A. Moroco, T. E. Smithgall, V. K. Kuchroo, and L. P. Kane. 2011. Phosphotyrosine-dependent coupling of Tim-3 to T-cell receptor signaling pathways. Mol. Cell. Biol. 31: 3963-3974.
45. Hawkes, M., X. Li, M. Crockett, A. Diassiti, C. Finney, G. Min-Oo, W. C. Liles, J. Liu, and K. C. Kain. 2010. CD36 deficiency attenuates experimental mycobacterial infection. BMC Infect. Dis. 10: 299.
46. Abadía-Molina, A. C., H. Ji, W. A. Faubion, A. Julien, Y. Latchman, H. Yagita, A. Sharpe, A. K. Bhan, and C. Terhorst. 2006. CD48 controls T-cell and antigenpresenting cell functions in experimental colitis. Gastroenterology 130: 424-434.
47. Fitzgerald, K. A., D. C. Rowe, B. J. Barnes, D. R. Caffrey, A. Visintin, E. Latz, B. Monks, P. M. Pitha, and D. T. Golenbock. 2003. LPS-TLR4 signaling to IRF- 3/7 and NF-kappaB involves the toll adapters TRAM and TRIF. J. Exp. Med. 198: 1043-1055.
48. Kuchroo, V. K., D. T. Umetsu, R. H. DeKruyff, and G. J. Freeman. 2003. The TIM gene family: emerging roles in immunity and disease. Nat. Rev. Immunol. 3: 454-462.
49. Rodriguez-Manzanet, R., R. DeKruyff, V. K. Kuchroo, and D. T. Umetsu. 2009. The costimulatory role of TIM molecules. Immunol. Rev. 229: 259-270.
50. Andersson, U., and K. J. Tracey. 2011. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu. Rev. Immunol. 29: 139-162.
51. Zhang, Y., C. J. Ma, J. M. Wang, X. J. Ji, X. Y. Wu, J. P. Moorman, and Z. Q. Yao. 2012. Tim-3 regulates pro- and anti-inflammatory cytokine expression in human CD14+ monocytes. J. Leukoc. Biol. 91: 189-196.
52. Anderson, A. C. 2012. Editorial: Tim-3 puts on the brakes. J. Leukoc. Biol. 91: 183-185.
53. Moore, K. W., R. de Waal Malefyt, R. L. Coffman, and A. O'Garra. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19: 683-765.
54. Varma, T. K., M. Durham, E. D. Murphey, W. Cui, Z. Huang, C. Y. Lin, T. Toliver-Kinsky, and E. R. Sherwood. 2005. Endotoxin priming improves clearance of Pseudomonas aeruginosa in wild-type and interleukin-10 knockout mice. Infect. Immun. 73: 7340-7347.
55. Gogos, C. A., E. Drosou, H. P. Bassaris, and A. Skoutelis. 2000. Pro- versus antiinflammatory cytokine profile in patients with severe sepsis: a marker for prognosis and future therapeutic options. J. Infect. Dis. 181: 176-180.
56. Boone, D. L., E. E. Turer, E. G. Lee, R. C. Ahmad, M. T. Wheeler, C. Tsui, P. Hurley, M. Chien, S. Chai, O. Hitotsumatsu, et al. 2004. The ubiquitinmodifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5: 1052-1060.
57. Karaghiosoff, M., R. Steinborn, P. Kovarik, G. Kriegshäuser, M. Baccarini, B. Donabauer, U. Reichart, T. Kolbe, C. Bogdan, T. Leanderson, et al. 2003. Central role for type I interferons and Tyk2 in lipopolysaccharide- induced endotoxin shock. Nat. Immunol. 4: 471-477.
58. Weighardt, H., S. Kaiser-Moore, S. Schlautkötter, T. Rossmann-Bloeck, U. Schleicher, C. Bogdan, and B. Holzmann. 2006. Type I IFN modulates host defense and late hyperinflammation in septic peritonitis. J. Immunol. 177: 5623-5630.