Inflammatory impact of IFN-ƴ in CD8+ T cell-mediated lung injury is mediated by both Stat1-dependent and -independent pathways

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 308, Issue 7, 2015, Pages L650-L657

  Ramana, Chilakamarti V ^a   Deberge, Matthew P ^b   Kumar, Aseem ^c   Alia, Christopher S ^d   Durbin, Joan E ^e   Enelow, Richard I ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c LAURENTIAN UNIVERSITY   (Canada)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Acute lung injury; CD8+ T cell; Immunopathology; Interferon ; Stat1

Indexed keywords

GAMMA INTERFERON; STAT1 PROTEIN; STAT3 PROTEIN; STAT1 PROTEIN, MOUSE; STAT3 PROTEIN, MOUSE;

ACUTE LUNG INJURY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN RECOGNITION; ANTIVIRAL ACTIVITY; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EPITHELIUM CELL; IMMUNOPATHOLOGY; INFLAMMATORY CELL; INFLUENZA; INFLUENZA VIRUS; LUNG LAVAGE; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRAL CLEARANCE; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; ORTHOMYXOVIRUS INFECTION; PHYSIOLOGY; SIGNAL TRANSDUCTION; VIROLOGY;

ACUTE LUNG INJURY; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; INTERFERON-GAMMA; MICE, INBRED BALB C; MICE, KNOCKOUT; ORTHOMYXOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR;

EID: 84926338093     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00360.2014     Document Type: Article

References (33)

1. Baumgarth N, Kelso A. In vivo blockade of ƴ-interferon affects the influenza virus-induced humoral and the local cellular immune response in lung tissue. J Virol 70: 4411–4418, 1996.
2. Bot A, Bot S, Bona CA. Protective role of ƴ-interferon during the recall response to influenza virus. J Virol 72: 6637–6645, 1998.
3. Bradley LM, Douglass MF, Chatterjee D, Akira S, Baaten BJ. Matrix metalloprotease 9 mediates neutrophil migration into the airways in response to influenza virus-induced toll-like receptor signaling. PLoS Pathog 8: e1002641, 2012.
4. DeBerge MP, Ely KH, Cheng GS, Enelow RI. ADAM17-mediated processing of TNF-ƴ expressed by antiviral effector CD8+ T cells is required for severe T-cell-mediated lung injury. PLos One 8: e79340, 2013.
5. DeBerge MP, Ely KH, Enelow RI. Soluble, but not transmembrane, TNF-ƴ is required during influenza infection to limit the magnitude of immune responses and the extent of immunopathology. J Immunol 192:5839–5851, 2014.
6. Enelow RI, Mohammed AZ, Stoler MH, Liu AN, Young JS, Lou YH, Braciale TJ. Structural and functional consequences of alveolar cell recognition by CD8+ T lymphocytes in experimental lung disease. J Clin Invest 102: 1653–1661, 1998.
7. Faffe DS, Flynt L, Mellema M, Moore PE, Silverman ES, Subramaniam V, Jones MR, Mizgerd JP, Whitehead T, Imrich A, Panettieri RA Jr, Shore SA. Oncostatin M causes eotaxin-1 release from airway smooth muscle: synergy with IL-4 and IL-13. J Allergy Clin Immunol 115: 514–520, 2005.
8. Garcia-Sastre A, Durbin RK, Zheng H, Palese P, Gertner R, Levy DE, Durbin JE. The role of interferon in influenza virus tissue tropism. J Virol 72: 8550–8558, 1998.
9. Gil MP, Bohn E, O’Guin AK, Ramana CV, Levine B, Stark GR, Virgin HW, Schreiber RD. Biologic consequences of Stat1-independent IFN signaling. Proc Natl Acad Sci USA 98: 6680–6685, 2001.
10. Graham MB, Dalton DK, Giltinan D, Braciale VL, Stewart TA, Braciale TJ. Response to influenza infection in mice with a targeted disruption in the interferon-ƴ gene. J Exp Med 178: 1725–1732, 1993.
11. Hamada H, Bassity E, Flies A, Strutt TM, Garcia-Hernandez ML, McKinstry KK, Zou T, Swain SL, Dutton RW. Multiple redundant effector mechanisms of CD8+ T cells protect against influenza infection. J Immunol 190: 296–306, 2013.
12. Huang KJ, Su IJ, Theron M, Wu YC, Lai SK, Liu CC, Lei HY. An interferon-ƴ-related cytokine storm in SARS patients. J Med Virol 75: 185–194, 2005.
13. Jewell NA, Vaghefi N, Mertz SE, Akter P, Peebles RS Jr, Bakaletz LO, Durbin RK, Flano E, Durbin JE. Differential type I interferon induction by respiratory syncytial virus and influenza A virus in vivo. J Virol 81: 9790–9800, 2007.
14. Kreutzfeldt M, Bergthaler A, Fernandez M, Bruck W, Steinbach K, Vorm M, Coras R, Blumcke I, Bonilla WV, Fleige A, Forman R, Muller W, Becher B, Misgeld T, Kerschensteiner M, Pinschewer DD, Merkler D. Neuroprotective intervention by interferon-_ blockade prevents CD8+ T cell-mediated dendrite and synapse loss. J Exp Med 210: 2087–2103, 2013.
15. Li Y, Du H, Qin Y, Roberts J, Cummings OW, Yan C. Activation of the signal transducers and activators of the transcription 3 pathway in alveolar epithelial cells induces inflammation and adenocarcinomas in mouse lung. Cancer Res 67: 8494–8503, 2007.
16. Liu AN, Mohammed AZ, Rice WR, Fiedeldey DT, Liebermann JS, Whitsett JA, Braciale TJ, Enelow RI. Perforin-independent CD8+ T-cell-mediated cytotoxicity of alveolar epithelial cells is preferentially mediated by tumor necrosis factor-ƴ: Relative insensitivity to Fas ligand. Am J Respir Cell Mol Biol 20: 849–858, 1999.
17. Mauad T, Hajjar LA, Callegari GD, da Silva LF, Schout D, Galas FR, Alves VA, Malheiros DM, Auler JO Jr, Ferreira AF, Borsato MR, Bezerra SM, Gutierrez PS, Caldini ET, Pasqualucci CA, Dolhnikoff M, Saldiva PH. Lung pathology in fatal novel human influenza A (H1N1) infection. Am J Respir Crit Care Med 181: 72–79, 2010.
18. Moskophidis D, Kioussis D. Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med 188: 223–232, 1998.
19. Ostler T, Davidson W, Ehl S. Virus clearance and immunopathology by CD8+ T cells during infection with respiratory syncytial virus are mediated by IFN-ƴ. Eur J Immunol 32: 2117–2123, 2002.
20. Qing Y, Stark GR. Alternative activation of STAT1 and STAT3 in response to interferon-+. J Biol Chem 279: 41679–41685, 2004.
21. Ramana CV, Chatterjee-Kishore M, Nguyen H, Stark GR. Complex roles of Stat1 in regulating gene expression. Oncogene 19: 2619–2627, 2000.
22. Ramana CV, Cheng GS, Kumar A, Kwon HJ, Enelow RI. Role of alveolar epithelial early growth response-1 (Egr-1) in CD8+ T cellmediated lung injury. Mol Immunol 47: 623–631, 2009.
23. Ramana CV, Kumar A, Enelow R. Stat1-independent induction of SOCS-3 by interferon-_ is mediated by sustained activation of Stat3 in mouse embryonic fibroblasts. Biochem Biophys Res Commun 327: 727–733, 2005.
24. Regis G, Pensa S, Boselli D, Novelli F, Poli V. Ups and downs: the STAT1:STAT3 seesaw of interferon and gp130 receptor signalling. Semin Cell Dev Biol 19: 351–359, 2008.
25. Shenoy AR, Kim BH, Choi HP, Matsuzawa T, Tiwari S, MacMicking JD. Emerging themes in IFN-_-induced macrophage immunity by the p47 and p65 GTPase families. Immunobiology 212: 771–784, 2007.
26. Simeone-Penney MC, Severgnini M, Tu P, Homer RJ, Mariani TJ, Cohn L, Simon AR. Airway epithelial STAT3 is required for allergic inflammation in a murine model of asthma. J Immunol 178: 6191–6199, 2007.
27. Stow JL, Low PC, Offenhauser C, Sangermani D. Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology 214: 601–612, 2009.
28. Uetani K, Hiroi M, Meguro T, Ogawa H, Kamisako T, Ohmori Y, Erzurum SC. Influenza A virus abrogates IFN-+ response in respiratory epithelial cells by disruption of the Jak/Stat pathway. Eur J Immunol 38: 1559–1573, 2008.
29. Wang J, Schreiber RD, Campbell IL. STAT1 deficiency unexpectedly and markedly exacerbates the pathophysiological actions of IFN-+ in the central nervous system. Proc Natl Acad Sci USA 99: 16209–16214, 2002.
30. Whitmire JK, Tan JT, Whitton JL. Interferon-ƴ acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med 201: 1053–1059, 2005.
31. Wiley JA, Cerwenka A, Harkema JR, Dutton RW, Harmsen AG. Production of interferon-_ by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am J Pathol 158: 119–130, 2001.
32. Xu L, Yoon H, Zhao MQ, Liu J, Ramana CV, Enelow RI. Cutting edge: pulmonary immunopathology mediated by antigen-specific expression of TNF-ƴ by antiviral CD8+ T cells. J Immunol 173: 721–725, 2004.
33. Zhao MQ, Stoler MH, Liu AN, Wei B, Soguero C, Hahn YS, Enelow RI. Alveolar epithelial cell chemokine expression triggered by antigenspecific cytolytic CD8+ T cell recognition. J Clin Invest 106: R49–R58, 2000.