Natural killer T cell-derived IL-17 mediates lung ischemia-reperfusion injury

American Journal of Respiratory and Critical Care Medicine

Volumn 183, Issue 11, 2011, Pages 1539-1549

  Sharma, Ashish K ^a   LaPar, Damien J ^a   Zhao, Yunge ^a   Li, Li ^a   Lau, Christine L ^a   Kron, Irving L ^a   Iwakura, Yoichiro ^b   Okusa, Mark D ^a   Laubach, Victor E ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Inflammation; Innate immunity; Lung transplant; Neutrophils; T cells

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; MONOCYTE CHEMOTACTIC PROTEIN 1; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ISCHEMIA; LUNG INJURY; MALE; MOUSE; NATURAL KILLER T CELL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY;

ACUTE LUNG INJURY; ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INFLAMMATION; INTERLEUKIN-17; LUNG; MALE; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; PULMONARY EDEMA; REPERFUSION INJURY; RESPIRATORY FUNCTION TESTS;

EID: 79957969252     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201007-1173OC     Document Type: Article

References (45)

1. Ailawadi G, Lau CL, Smith PW, Swenson BR, Hennessy SA, Kuhn CJ, Fedoruk LM, Kozower BD, Kron IL, Jones DR. Does reperfusion injury still cause significant mortality after lung transplantation? J Thorac Cardiovasc Surg 2009;137:688-694.
2. Christie JD, Edwards LB, Aurora P, Dobbels F, Kirk R, Rahmel AO, Stehlik J, Taylor DO, Kucheryavaya AY, Hertz MI. The Registry of the International Society for Heart and Lung Transplantation: Twenty-sixth Official Adult Lung and Heart-Lung Transplantation Report-2009. J Heart Lung Transplant 2009;28:1031-1049.
3. Granton J. Update of early respiratory failure in the lung transplant recipient. Curr Opin Crit Care 2006;12:19-24.
4. Fiser SM, Tribble CG, Long SM, Kaza AK, Kern JA, Jones DR, Robbins MK, Kron IL. Ischemia-reperfusion injury after lung transplantation increases risk of late bronchiolitis obliterans syndrome. Ann Thorac Surg 2002;73:1041-1047.
5. Land WG. The role of postischemic reperfusion injury and other nonantigen-dependent inflammatory pathways in transplantation. Transplantation 2005;79:505-514. (Pubitemid 40372243)
6. Eppinger MJ, Jones ML, Deeb GM, Bolling SF, Ward PA. Pattern of injury and the role of neutrophils in reperfusion injury of rat lung. J Surg Res 1995;58:713-718.
7. Fiser SM, Tribble CG, Long SM, Kaza AK, Cope JT, Laubach VE, Kern JA, Kron IL. Lung transplant reperfusion injury involves pulmonary macrophages and circulating leukocytes in a biphasic response. J Thorac Cardiovasc Surg 2001;121:1069-1075.
8. Yang Z, Sharma AK, Linden J, Kron IL, Laubach VE. CD4+ T lymphocytes mediate acute pulmonary ischemia-reperfusion injury. J Thorac Cardiovasc Surg 2009;137:695-702.
9. de Perrot M, Young K, Imai Y, Liu M, Waddell TK, Fischer S, Zhang L, Keshavjee S. Recipient T cells mediate reperfusion injury after lung transplantation in the rat. J Immunol 2003;171:4995-5002. (Pubitemid 37432779)
10. Debbabi H, Ghosh S, Kamath AB, Alt J, Demello DE, Dunsmore S, Behar SM. Primary type II alveolar epithelial cells present microbial antigens to antigen-specific CD4+ T cells. Am J Physiol Lung Cell Mol Physiol 2005;289:L274-L279. (Pubitemid 41008910)
11. Godfrey DI, Kronenberg M. Going both ways: immune regulation via CD1d-dependent NKT cells. J Clin Invest 2004;114:1379-1388. (Pubitemid 40385565)
12. Hanschen M, Zahler S, Krombach F, Khandoga A. Reciprocal activation between CD4+ T cells and Kupffer cells during hepatic ischemia-reperfusion. Transplantation 2008;86:710-718.
13. Yang Z, Sharma AK, Marshall M, Kron IL, Laubach VE. NADPH oxidase in bone marrow-derived cells mediates pulmonary ischemia-reperfusion injury. Am J Respir Cell Mol Biol 2009;40:375-381.
14. Jovanovic DV, Di Battista JA, Martel-Pelletier J, Jolicoeur FC, He Y, Zhang M, Mineau F, Pelletier JP. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 1998;160:3513-3521. (Pubitemid 28164746)
15. Laan M, Cui ZH, Hoshino H, Lotvall J, Sjostrand M, Gruenert DC, Skoogh BE, Linden A. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 1999;162:2347-2352. (Pubitemid 29288861)
16. Shichita T, Sugiyama Y, Ooboshi H, Sugimori H, Nakagawa R, Takada I, Iwaki T, Okada Y, Iida M, Cua DJ, et al. Pivotal role of cerebral interleukin-17-producing gammadeltaT cells in the delayed phase of ischemic brain injury. Nat Med 2009;15:946-950.
17. Caldwell CC, Okaya T, Martignoni A, Husted T, Schuster R, Lentsch AB. Divergent functions of CD4+ T lymphocytes in acute liver inflammation and injury after ischemia-reperfusion. Am J Physiol Gastrointest Liver Physiol 2005;289:G969-G976. (Pubitemid 41532590)
18. Edgerton C, Crispin JC, Moratz CM, Bettelli E, Oukka M, Simovic M, Zacharia A, Egan R, Chen J, Dalle Lucca JJ, et al. IL-17 producing CD4+ T cells mediate accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice. Clin Immunol 2009;130:313-321.
19. Min SI, Ha J, Park CG, Won JK, Park YJ, Min SK, Kim SJ. Sequential evolution of IL-17 responses in the early period of allograft rejection. Exp Mol Med 2009;41:707-716.
20. Li L, Huang L, Sung SS, Lobo PI, Brown MG, Gregg RK, Engelhard VH, Okusa MD. NKT cell activation mediates neutrophil IFN-gamma production and renal ischemia-reperfusion injury. J Immunol 2007;178:5899-5911. (Pubitemid 46674387)
21. Lappas CM, Day YJ, Marshall MA, Engelhard VH, Linden J. Adenosine A2A receptor activation reduces hepatic ischemia reperfusion injury by inhibiting CD1d-dependent NKT cell activation. J Exp Med 2006;203:2639-2648. (Pubitemid 44833340)
22. Sharma AK, Zhao Y, LaPar D, Lau C, Kron I, Laubach V. Pivotal role of NKT cells and IL-17 In pulmonary ischemia-reperfusion injury [abstract]. Am J Respir Crit Care Med 2010;181:A1099.
23. Nakae S, Komiyama Y, Nambu A, Sudo K, Iwase M, Homma I, Sekikawa K, Asano M, Iwakura Y. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 2002;17:375-387. (Pubitemid 35279557)
24. Cui J, Shin T, Kawano T, Sato H, Kondo E, Toura I, Kaneko Y, Koseki H, Kanno M, Taniguchi M. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science 1997;278:1623-1626. (Pubitemid 27516281)
25. Institute of Laboratory Animal Resources. Guide for the care and use of laboratory animals, 8th ed. Washington, DC: National Academies Press; 2011.
26. Li L, Huang L, Vergis AL, Ye H, Bajwa A, Narayan V, Strieter RM, Rosin DL, Okusa MD. IL-17 produced by neutrophils regulates IFN-gamma-mediated neutrophil migration in mouse kidney ischemia-reperfusion injury. J Clin Invest 2010;120:331-342.
27. Weaver CT, Hatton RD, Mangan PR, Harrington LE. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu Rev Immunol 2007;25:821-852. (Pubitemid 46697925)
28. Benlagha K, Weiss A, Beavis A, Teyton L, Bendelac A. In vivo identification of glycolipid antigen-specific T cells using fluorescent CD1d tetramers. J Exp Med 2000;191:1895-1903.
29. Ye P, Rodriguez FH, Kanaly S, Stocking KL, Schurr J, Schwarzenberger P, Oliver P, Huang W, Zhang P, Zhang J, et al. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J Exp Med 2001;194:519-527. (Pubitemid 32835046)
30. Korn T, Oukka M, Kuchroo V, Bettelli E. Th17 cells: effector T cells with inflammatory properties. Semin Immunol 2007;19:362-371. (Pubitemid 351274046)
31. Kolls JK, Linden A. Interleukin-17 family members and inflammation. Immunity 2004;21:467-476. (Pubitemid 39370503)
32. Braun RK, Ferrick C, Neubauer P, Sjoding M, Sterner-Kock A, Kock M, Putney L, Ferrick DA, Hyde DM, Love RB. IL-17 producing gamma-delta T cells are required for a controlled inflammatory response after bleomycin-induced lung injury. Inflammation 2008;31:167-179.
33. Michel ML, Keller AC, Paget C, Fujio M, Trottein F, Savage PB, Wong CH, Schneider E, Dy M, Leite-de-Moraes MC. Identification of an IL-17-producing NK1.1(neg) iNKT cell population involved in airway neutrophilia. J Exp Med 2007;204:995-1001. (Pubitemid 46798144)
34. Montoya CJ, Pollard D, Martinson J, Kumari K, Wasserfall C, Mulder CB, Rugeles MT, Atkinson MA, Landay AL, Wilson SB. Characterization of human invariant natural killer T subsets in health and disease using a novel invariant natural killer T cell-clonotypic monoclonal antibody, 6B11. Immunology 2007;122:1-14. (Pubitemid 47222606)
35. 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)
36. Gao B, Radaeva S, Park O. Liver natural killer and natural killer T cells: immunobiology and emerging roles in liver diseases. J Leukoc Biol 2009;86:513-528.
37. Day YJ, Huang L, Ye H, Li L, Linden J, Okusa MD. Renal ischemia-reperfusion injury and adenosine 2A receptor-mediated tissue protection: the role of CD4+ T cells and IFN-gamma. J Immunol 2006;176:3108-3114.
38. Sharma AK, Hajzus V, Kazemi A, Kron IL, Laubach VE. NADPH oxidase-dependent activation of CD4+ T cells modulates macrophage and alveolar epithelial cell activation during lung ischemiareperfusion injury. Am J Respir Crit Care Med 2010;181:A1095.
39. Linden A, Laan M, Anderson GP. Neutrophils, interleukin-17A and lung disease. Eur Respir J 2005;25:159-172. (Pubitemid 40207746)
40. Lockhart E, Green AM, Flynn JL. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006;177:4662-4669. (Pubitemid 44469799)
41. McGeachy MJ, Cua DJ. Th17 cell differentiation: the long and winding road. Immunity 2008;28:445-453. (Pubitemid 351467042)
42. Ferretti S, Bonneau O, Dubois GR, Jones CE, Trifilieff A. IL-17, produced by lymphocytes and neutrophils, is necessary for lipopolysaccharide-induced airway neutrophilia: IL-15 as a possible trigger. J Immunol 2003;170:2106-2112. (Pubitemid 36197433)
43. Hoshino A, Nagao T, Nagi-Miura N, Ohno N, Yasuhara M, Yamamoto K, Nakayama T, Suzuki K. MPO-ANCA induces IL-17 production by activated neutrophils in vitro via classical complement pathway-dependent manner. J Autoimmun 2008;31:79-89. (Pubitemid 351685761)
44. Yao Z, Fanslow WC, Seldin MF, Rousseau AM, Painter SL, Comeau MR, Cohen JI, Spriggs MK. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 1995;3:811-821. (Pubitemid 26091152)
45. Yao Z, Spriggs MK, Derry JM, Strockbine L, Park LS, VandenBos T, Zappone JD, Painter SL, Armitage RJ. Molecular characterization of the human interleukin (IL)-17 receptor. Cytokine 1997;9:794-800. (Pubitemid 27494143)