Resolvin d1 attenuates polyinosinic-Polycytidylic acid-Induced inflammatory signaling in human airway epithelial cells via tak1

Journal of Immunology

Volumn 193, Issue 10, 2014, Pages 4980-4987

  Hsiao, Hsi Min ^a   Thatcher, Thomas H ^a   Levy, Elizabeth P ^a   Fulton, Robert A ^a   Owens, Kristina M ^a   Phipps, Richard P ^a   Sime, Patricia J ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; AUTACOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MEMBRANE PROTEIN; MEMBRANE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN ALX; PROTEIN FPR2; PROTEIN GPR32; RESOLVIN D1; TAK1 BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG; DOCOSAHEXAENOIC ACID; G PROTEIN COUPLED RECEPTOR; GPR32 PROTEIN, HUMAN; HSH2D PROTEIN, HUMAN; IL6 PROTEIN, HUMAN; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SMALL INTERFERING RNA; TAB1 PROTEIN, HUMAN;

ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; DRUG POTENCY; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LUNG ALVEOLUS EPITHELIUM; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; RESPIRATORY TRACT INFLAMMATION; SIGNAL TRANSDUCTION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BRONCHUS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; INFLAMMATION; PATHOLOGY; PRIMARY CELL CULTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BRONCHI; DOCOSAHEXAENOIC ACIDS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; INTERLEUKIN-6; INTERLEUKIN-8; MAP KINASE KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; POLY I-C; PRIMARY CELL CULTURE; RECEPTORS, G-PROTEIN-COUPLED; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED FACTOR 6;

EID: 84910115222     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400313     Document Type: Article

References (46)

1. Serhan, C.N., and N. Chiang.2013.Resolution phase lipid mediators of inflammation: agonists of resolution.Curr. Opin. Pharmacol.13: 632-640.
2. Dalli, J., R.A.Colas, and C.N.Serhan.2013.Novel n-3 immunoresolvents: structures and actions.Sci. Rep.3: 1940.
3. Henson, P.M.1991.Resolution of inflammation.A perspective.Chest 99(3, Suppl)2S-6S.
4. Serhan, C.N.2010.Novel lipid mediators and resolution mechanisms in acute inflammation: to resolve or not? Am. J. Pathol.177: 1576-1591.
5. Hsiao, H.M., R.E. Sapinoro, T.H. Thatcher, A. Croasdell, E.P. Levy, R.A. Fulton, K.C. Olsen, S.J. Pollock, C.N. Serhan, R.P. Phipps, and P.J. Sime.2013.A novel anti-inflammatory and pro-resolving role for resolving D1 in acute cigarette smoke-induced lung inflammation.PLoS ONE 8: e58258.
6. Campbell, E.L., N.A. Louis, S.E. Tomassetti, G.O. Canny, M. Arita, C.N. Serhan, and S.P. Colgan.2007.Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution.FASEB J.21: 3162-3170.
7. Godson, C., S. Mitchell, K. Harvey, N.A. Petasis, N. Hogg, and H.R. Brady.2000.Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages.J. Immunol. 164: 1663-1667.
8. Canny, G., O. Levy, G.T. Furuta, S. Narravula-Alipati, R.B. Sisson, C.N. Serhan, and S.P. Colgan.2002.Lipid mediator-induced expression of bactericidal/ permeability-increasing protein (BPI) in human mucosal epithelia.Proc. Natl. Acad. Sci. USA 99: 3902-3907.
9. Mickleborough, T.D.2005.Dietary omega-3 polyunsaturated fatty acid supplementation and airway hyperresponsiveness in asthma.J. Asthma 42: 305-314.
10. Arm, J.P., C.E. Horton, B.W. Spur, J.M. Mencia-Huerta, and T.H. Lee.1989.The effects of dietary supplementation with fish oil lipids on the airways response to inhaled allergen in bronchial asthma.Am. Rev. Respir. Dis.139: 1395-1400.
11. Shahar, E., A.R. Folsom, S.L. Melnick, M.S. Tockman, G.W. Comstock, V. Gennaro, M.W. Higgins, P.D. Sorlie, W.J. Ko, and M. Szklo, Atherosclerosis Risk in Communities Study Investigators.1994.Dietary n-3 polyunsaturated fatty acids and smoking-related chronic obstructive pulmonary disease.N. Engl. J. Med.331: 228-233.
12. Wang, B., X. Gong, J.Y. Wan, L. Zhang, Z. Zhang, H.Z. Li, and S. Min.2011.Resolvin D1 protects mice from LPS-induced acute lung injury.Pulm. Pharmacol. Ther. 24: 434-441.
13. Rogerio, A.P., O. Haworth, R. Croze, S.F.Oh, M. Uddin, T. Carlo, M.A. Pfeffer, R. Priluck, C.N. Serhan, and B.D. Levy.2012.Resolvin D1 and aspirin-Triggered resolvin D1 promote resolution of allergic airways responses.J. Immunol. 189: 1983-1991.
14. Vareille, M., E. Kieninger, M.R. Edwards, and N. Regamey.2011.The airway epithelium: soldier in the fight against respiratory viruses.Clin. Microbiol. Rev.24: 210-229.
15. Norling, L.V., J. Dalli, R.J. Flower, C.N. Serhan, and M. Perretti.2012.Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions.Arterioscler.Thromb. Vasc. Biol.32: 1970-1978.
16. Ritter, M., D. Mennerich, A. Weith, and P. Seither.2005.Characterization of Toll-like receptors in primary lung epithelial cells: strong impact of the TLR3 ligand poly(I:C) on the regulation of Toll-like receptors, adaptor proteins and inflammatory response.J. Inflamm.(Lond.) 2: 16.
17. Takaesu, G., J. Ninomiya-Tsuji, S. Kishida, X. Li, G.R. Stark, and K. Matsumoto.2001.Interleukin-1 (IL-1) receptor-associated kinase leads to activation of TAK1 by inducing TAB2 translocation in the IL-1 signaling pathway.Mol. Cell. Biol.21: 2475-2484.
18. Rezaee, F., N. Meednu, J.A. Emo, B. Saatian, T.J. Chapman, N.G. Naydenov, A. De Benedetto, L.A. Beck, A.I. Ivanov, and S.N. Georas.2011.Polyinosinic: polycytidylic acid induces protein kinase D-dependent disassembly of apical junctions and barrier dysfunction in airway epithelial cells.J. Allergy Clin. Immunol. 128: 1216-1224 e1211.
19. Krishnamoorthy, S., A. Recchiuti, N. Chiang, S. Yacoubian, C.H. Lee, R. Yang, N.A. Petasis, and C.N. Serhan.2010.Resolvin D1 binds human phagocytes with evidence for proresolving receptors.Proc. Natl. Acad. Sci. USA 107: 1660-1665.
20. Stenfeldt, A.L., J. Karlsson, C. Wennerås, J. Bylund, H. Fu, and C. Dahlgren.2007.Cyclosporin H, Boc-MLF and Boc-FLFLF are antagonists that preferentially inhibit activity triggered through the formyl peptide receptor.Inflammation 30: 224-229.
21. Jiang, Z., M. Zamanian-Daryoush, H. Nie, A.M. Silva, B.R. Williams, and X. Li.2003.Poly(I-C)-induced Toll-like receptor 3 (TLR3)-mediated activation of NFkappa B and MAP kinase is through an interleukin-1 receptor-associated kinase (IRAK)-independent pathway employing the signaling components TLR3-TRAF6-TAK1-TAB2-PKR.J. Biol. Chem.278: 16713-16719.
22. Ninomiya-Tsuji, J., K. Kishimoto, A. Hiyama, J. Inoue, Z. Cao, and K. Matsumoto.1999.The kinase TAK1 can activate the NIK-I kappaB as well as the MAP kinase cascade in the IL-1 signalling pathway.Nature 398: 252-256.
23. Xu, M.X., B.C. Tan, W. Zhou, T. Wei, W.H. Lai, J.W. Tan, and J.H. Dong.2013.Resolvin D1, an endogenous lipid mediator for inactivation of inflammation-related signaling pathways in microglial cells, prevents lipopolysaccharide-induced inflammatory responses.CNS Neurosci. Ther. 19: 235-243.
24. Levy, B.D.2012.Resolvin D1 and Resolvin E1 promote the resolution of allergic airway inflammation via shared and distinct molecular counter-regulatory pathways.Front. Immunol. 3: 390.
25. Webster Marketon, J.I., and J. Corry.2013.Poly I:C and respiratory syncytial virus (RSV) inhibit glucocorticoid receptor (GR)-mediated transactivation in lung epithelial, but not monocytic, cell lines.Virus Res.176: 303-306.
26. Lindh, H.F., H.L. Lindsay, B.R. Mayberry, and M. Forbes.1969.Polyinosiniccytidylic acid complex (poly I:C) and viral infections in mice.Proc. Soc. Exp. Biol. Med.132: 83-87.
27. Numata, M., H.W. Chu, A. Dakhama, and D.R. Voelker.2010.Pulmonary surfactant phosphatidylglycerol inhibits respiratory syncytial virus-induced inflammation and infection.Proc. Natl. Acad. Sci. USA 107: 320-325.
28. Dakhama, A., M.Kraft, R.J.Martin, and E.W.Gelfand.2003.Induction of regulated upon activation, normal T cells expressed and secreted (RANTES) and transforming growth factor-beta 1 in airway epithelial cells by Mycoplasma pneumoniae.Am. J. Respir. Cell Mol. Biol.29: 344-351.
29. Yadav, U.C., K.V.Ramana, L.Aguilera-Aguirre, I.Boldogh, H.A.Boulares, and S.K.Srivastava.2009.Inhibition of aldose reductase prevents experimental allergic airway inflammation in mice.PLoS ONE 4: e6535.
30. Wedzicha, J.A. 2004.Role of viruses in exacerbations of chronic obstructive pulmonary disease.Proc. Am. Thorac. Soc.1: 115-120.
31. Cooray, S.N., T. Gobbetti, T. Montero-Melendez, S. McArthur, D. Thompson, A.J. Clark, R.J. Flower, and M. Perretti.2013.Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses.Proc. Natl. Acad. Sci. USA 110: 18232-18237.
32. Filep, J.G.2013.Biasing the lipoxin A4/formyl peptide receptor 2 pushes inflammatory resolution.Proc. Natl. Acad. Sci. USA 110: 18033-18034.
33. Bozinovski, S., M. Uddin, R. Vlahos, M. Thompson, J.L. McQualter, A.S. Merritt, P.A. Wark, A. Hutchinson, L.B. Irving, B.D. Levy, and G.P. Anderson.2012.Serum amyloid A opposes lipoxin A4 to mediate glucocorticoid refractory lung inflammation in chronic obstructive pulmonary disease.Proc. Natl. Acad. Sci. USA 109: 935-940.
34. Bozinovski, S., D. Anthony, G.P. Anderson, L.B. Irving, B.D. Levy, and R. Vlahos.2013.Treating neutrophilic inflammation in COPD by targeting ALX/FPR2 resolution pathways.Pharmacol. Ther. 140: 280-289.
35. Chiang, N., G.Fredman, F.Bäckhed, S.F.Oh, T.Vickery, B.A.Schmidt, and C.N.Serhan.2012.Infection regulates pro-resolving mediators that lower antibiotic requirements.Nature 484: 524-528.
36. Morita, M., K. Kuba, A. Ichikawa, M. Nakayama, J. Katahira, R. Iwamoto, T. Watanebe, S. Sakabe, T. Daidoji, S. Nakamura, et al.2013.The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza.Cell 153: 112-125.
37. Sakurai, H. 2012.Targeting of TAK1 in inflammatory disorders and cancer.Trends Pharmacol. Sci.33: 522-530.
38. Oh, D.Y., S. Talukdar, E.J. Bae, T. Imamura, H. Morinaga, W. Fan, P. Li, W.J. Lu, S.M. Watkins, and J.M. Olefsky.2010.GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects.Cell 142: 687-698.
39. Kajino, T., H. Ren, S. Iemura, T. Natsume, B. Stefansson, D.L. Brautigan, K. Matsumoto, and J. Ninomiya-Tsuji.2006.Protein phosphatase 6 downregulates TAK1 kinase activation in the IL-1 signaling pathway.J. Biol. Chem.281: 39891-39896.
40. Zheng, H., Q. Li, R. Chen, J. Zhang, Y. Ran, X. He, S. Li, and H.B. Shu.2013.The dual-specificity phosphatase DUSP14 negatively regulates tumor necrosis factor-and interleukin-1-induced nuclear factor-kB activation by dephosphorylating the protein kinase TAK1.J. Biol. Chem.288: 819-825.
41. Barnes, P.J. 2009.The cytokine network in chronic obstructive pulmonary disease.Am. J. Respir. Cell Mol. Biol.41: 631-638.
42. Wedzicha, J.A., and G.C. Donaldson.2003.Exacerbations of chronic obstructive pulmonary disease.Respir.Care 48: 1204-1213; discussion 1213-1205.
43. Schwab, J.M., N. Chiang, M. Arita, and C.N. Serhan.2007.Resolvin E1 and protectin D1 activate inflammation-resolution programmes.Nature 447: 869-874.
44. Levy, B.D., C.B. Clish, B. Schmidt, K. Gronert, and C.N. Serhan.2001.Lipid mediator class switching during acute inflammation: signals in resolution.Nat. Immunol. 2: 612-619.
45. Serhan, C.N., and N. Chiang.2008.Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus.Br.J.Pharmacol.153(Suppl 1): S200-S215.
46. Lee, H.N., J.K. Kundu, Y.N. Cha, and Y.J. Surh.2013.Resolvin D1 stimulates efferocytosis through p50/p50-mediated suppression of tumor necrosis factor-α expression.J.Cell Sci.126: 4037-4047.