TNF superfamily receptor OX40 triggers invariant NKT cell pyroptosis and liver injury

Journal of Clinical Investigation

Volumn 127, Issue 6, 2017, Pages 2222-2234

  Lan, Peixiang ^a   Fan, Yihui ^a   Zhao, Yue ^a   Lou, Xiaohua ^a   Monsour, Howard P ^b   Zhang, Xiaolong ^a   Choi, Yongwon ^c   Dou, Yaling ^a   Ishii, Naoto ^d   Ghobrial, Rafik M ^a,e   Xiao, Xiang ^a   Li, Xian Chang ^a,e  

^a HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

^b HOUSTON METHODIST HOSPITAL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CASPASE 3; DEATH RECEPTOR; GASDERMIN D; INTERLEUKIN 1; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; OX40 LIGAND; PARACASPASE MALT1; PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; CD134 ANTIGEN; MALT1 PROTEIN, MOUSE; TNFRSF4 PROTEIN, MOUSE; TUMOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; CONCANAVALIN A-INDUCED HEPATITIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; ENZYME ACTIVATION; IMMUNOPATHOGENESIS; IMMUNOSTIMULATION; LIVER TISSUE; MALE; MOUSE; MURINE HEPATITIS; NATURAL KILLER T CELL; NONHUMAN; NUCLEAR PORE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PYROPTOSIS; SIGNAL TRANSDUCTION; T CELL DEPLETION; ANIMAL; C57BL MOUSE; CELL LINE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT; TOXIC HEPATITIS;

ANIMALS; CASPASE 1; CASPASES; CELL LINE; CHEMICAL AND DRUG INDUCED LIVER INJURY; ENZYME ACTIVATION; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; NEOPLASM PROTEINS; PROTEIN TRANSPORT; PYROPTOSIS; RECEPTORS, OX40;

EID: 85020206826     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI91075     Document Type: Article

References (47)

1. Bendelac A, Savage PB, Teyton L. The biology of NKT cells. Annu Rev Immunol. 2007;25:297-336.
2. Brennan PJ, Brigl M, Brenner MB. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol. 2013;13(2):101-117.
3. Kawano T, et al. CD1d-restricted and TCR-mediated activation of valpha14 NKT cells by glycosylceramides. Science. 1997;278(5343):1626-1629.
4. Godfrey DI, Stankovic S, Baxter AG. Raising the NKT cell family. Nat Immunol. 2010;11(3):197-206.
5. Brennan PJ, et al. Invariant natural killer T cells recognize lipid self antigen induced by microbial danger signals. Nat Immunol. 2011;12(12):1202-1211.
6. Frey AB, Rao TD. NKT cell cytokine imbalance in murine diabetes mellitus. Autoimmunity. 1999;29(3):201-214.
7. Tang ZH, Liang S, Potter J, Jiang X, Mao HQ, Li Z. Tim-3/galectin-9 regulate the homeostasis of hepatic NKT cells in a murine model of nonalcoholic fatty liver disease. J Immunol. 2013;190(4):1788-1796.
8. Cui K, et al. Invariant NKT cells promote alcoholinduced steatohepatitis through interleukin-1β in mice. J Hepatol. 2015;62(6):1311-1318.
9. Wang H, Feng D, Park O, Yin S, Gao B. Invariant NKT cell activation induces neutrophil accumulation and hepatitis: opposite regulation by IL-4 and IFN-γ. Hepatology. 2013;58(4):1474-1485.
10. Santodomingo-Garzon T, Swain MG. Role of NKT cells in autoimmune liver disease. Autoimmun Rev. 2011;10(12):793-800.
11. Robinson MW, Harmon C, O'Farrelly C. Liver immunology and its role in inflammation and homeostasis. Cell Mol Immunol. 2016;13(3):267-276.
12. Kronenberg M. Toward an understanding of NKT cell biology: progress and paradoxes. Annu Rev Immunol. 2005;23:877-900.
13. Croft M. Control of immunity by the TNFRrelated molecule OX40 (CD134). Annu Rev Immunol. 2010;28:57-78.
14. Li XC, Rothstein DM, Sayegh MH. Costimulatory pathways in transplantation: challenges and new developments. Immunol Rev. 2009;229(1):271-293.
15. Rogers PR, Song J, Gramaglia I, Killeen N, Croft M. OX40 promotes Bcl-xL and Bcl-2 expression and is essential for long-term survival of CD4 T cells. Immunity. 2001;15(3):445-455.
16. Kopf M, et al. OX40-deficient mice are defective in Th cell proliferation but are competent in generating B cell and CTL Responses after virus infection. Immunity. 1999;11(6):699-708.
17. Ito T, et al. TSLP-activated dendritic cells induce an inflammatory T helper type 2 cell response through OX40 ligand. J Exp Med. 2005;202(9):1213-1223.
18. Xiao X, et al. OX40 signaling favors the induction of T(H)9 cells and airway inflammation. Nat Immunol. 2012;13(10):981-990.
19. Vu MD, et al. OX40 costimulation turns off Foxp3+ Tregs. Blood. 2007;110(7):2501-2510.
20. Piconese S, Valzasina B, Colombo MP. OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection. J Exp Med. 2008;205(4):825-839.
21. Murata K, Nose M, Ndhlovu LC, Sato T, Sugamura K, Ishii N. Constitutive OX40/OX40 ligand interaction induces autoimmune-like diseases. J Immunol. 2002;169(8):4628-4636.
22. Xiao X, et al. New insights on OX40 in the control of T cell immunity and immune tolerance in vivo. J Immunol. 2012;188(2):892-901.
23. Elhai M, et al. OX40L blockade protects against inflammation-driven fibrosis. Proc Natl Acad Sci U S A. 2016;113(27):E3901-E3910.
24. Zaini J, et al. OX40 ligand expressed by DCs costimulates NKT and CD4+ Th cell antitumor immunity in mice. J Clin Invest. 2007;117(11):3330-3338.
25. Diana J, et al. NKT cell-plasmacytoid dendritic cell cooperation via OX40 controls viral infection in a tissue-specific manner. Immunity. 2009;30(2):289-299.
26. Damayanti T, et al. Serial OX40 engagement on CD4+ T cells and natural killer T cells causes allergic airway inflammation. Am J Respir Crit Care Med. 2010;181(7):688-698.
27. Fan Z, et al. In vivo tracking of 'color-coded' effector, natural and induced regulatory T cells in the allograft response. Nat Med. 2010;16(6):718-722.
28. Yuan J, Najafov A, Py BF. Roles of caspases in necrotic cell death. Cell. 2016;167(7):1693-1704.
29. Ashkenazi A, Salvesen G. Regulated cell death: signaling and mechanisms. Annu Rev Cell Dev Biol. 2014;30:337-356.
30. Doitsh G, et al. Cell death by pyroptosis drives CD4 T-cell depletion in HIV-1 infection. Nature. 2014;505(7484):509-514.
31. Shalini S, Dorstyn L, Dawar S, Kumar S. Old, new and emerging functions of caspases. Cell Death Differ. 2015;22(4):526-539.
32. Shi J, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015;526(7575):660-665.
33. Kayagaki N, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature. 2015;526(7575):666-671.
34. Croft M. Co-stimulatory members of the TNFR family: keys to effective T-cell immunity? Nat Rev Immunol. 2003;3(8):609-620.
35. Thome M. Multifunctional roles for MALT1 in T-cell activation. Nat Rev Immunol. 2008;8(7):495-500.
36. Teige A, Bockermann R, Hasan M, Olofsson KE, Liu Y, Issazadeh-Navikas S. CD1d-dependent NKT cells play a protective role in acute and chronic arthritis models by ameliorating antigen-specific Th1 responses. J Immunol. 2010;185(1):345-356.
37. Kim WR, Flamm SL, Di Bisceglie AM, Bodenheimer HC, Public Policy Committee of the American Association for the Study of Liver Disease. Serum activity of alanine aminotransferase (ALT) as an indicator of health and disease. Hepatology. 2008;47(4):1363-1370.
38. Takeda K, Hayakawa Y, Van Kaer L, Matsuda H, Yagita H, Okumura K. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc Natl Acad Sci U S A. 2000;97(10):5498-5503.
39. Miao EA, et al. Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol. 2010;11(12):1136-1142.
40. Swain MG. Fatigue in liver disease: pathophysiology and clinical management. Can J Gastroenterol. 2006;20(3):181-188.
41. Weinberg AD. The role of OX40 (CD134) in T-cell memory generation. Adv Exp Med Biol. 2010;684:57-68.
42. Ruby CE, Redmond WL, Haley D, Weinberg AD. Anti-OX40 stimulation in vivo enhances CD8+ memory T cell survival and significantly increases recall responses. Eur J Immunol. 2007;37(1):157-166.
43. Gaspal FM, Kim MY, McConnell FM, Raykundalia C, Bekiaris V, Lane PJ. Mice deficient in OX40 and CD30 signals lack memory antibody responses because of deficient CD4 T cell memory. J Immunol. 2005;174(7):3891-3896.
44. Huang LR, et al. Intrahepatic myeloid-cell aggregates enable local proliferation of CD8(+) T cells and successful immunotherapy against chronic viral liver infection. Nat Immunol. 2013;14(6):574-583.
45. Broz P, von Moltke J, Jones JW, Vance RE, Monack DM. Differential requirement for caspase-1 autoproteolysis in pathogen-induced cell death and cytokine processing. Cell Host Microbe. 2010;8(6):471-483.
46. Sugamura K, Ishii N, Weinberg AD. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol. 2004;4(6):420-431.
47. Jensen SM, et al. Signaling through OX40 enhances antitumor immunity. Semin Oncol. 2010;37(5):524-532.