Dual anti-oxidant and anti-inflammatory actions of the electrophilic cyclooxygenase-2-derived 17-oxo-DHA in lipopolysaccharide- and cigarette smoke-induced inflammation

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 7, 2014, Pages 2299-2309

  Cipollina, Chiara ^a,b   Di Vincenzo, Serena ^b,c   Gerbino, Stefania ^b,c   Siena, Liboria ^b   Gjomarkaj, Mark ^b   Pace, Elisabetta ^b  

^a Fondazione RiMED   (Italy)

^b CNR Consiglio Nazionale delle Ricerche   (Italy)

^c UNIVERSITY OF PALERMO   (Italy)

Author keywords

Cigarette smoke; Electrophile; Inflammation; Omega 3 fatty acid; Oxidative stress

Indexed keywords

17 OXO DOCOSAHEXAENOIC ACID; CIGARETTE SMOKE; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; GLUTATHIONE; HEME OXYGENASE 1; INDOMETACIN; LIPOPOLYSACCHARIDE; REACTIVE OXYGEN METABOLITE; TOLL LIKE RECEPTOR 4; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

16HBE CELL LINE; ACUTE RESPIRATORY FAILURE; ARTICLE; BRONCHUS MUCOSA; CELL LINE; ENZYME ACTIVITY; EPITHELIUM CELL; INFLAMMATION; LUNG ALVEOLUS MACROPHAGE; LUNG LAVAGE; NONHUMAN; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

CIGARETTE SMOKE; ELECTROPHILE; INFLAMMATION; OMEGA-3 FATTY ACID; OXIDATIVE STRESS;

ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; CELL LINE; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACIDS; EPITHELIAL CELLS; HUMANS; INFLAMMATION; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MACROPHAGES; SMOKING;

EID: 84899791880     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2014.02.024     Document Type: Article

References (58)

1. G. Calviello, H.M. Su, K.H. Weylandt, E. Fasano, S. Serini, and A. Cittadini Experimental evidence of omega-3 polyunsaturated fatty acid modulation of inflammatory cytokines and bioactive lipid mediators: their potential role in inflammatory, neurodegenerative, and neoplastic diseases Biomed. Res. Int. 2013 2013 743171
2. J. Li, P. Xun, D. Zamora, A. Sood, K. Liu, M. Daviglus, C. Iribarren, D. Jacobs Jr., J.M. Shikany, and K. He Intakes of long-chain omega-3 (n - 3) PUFAs and fish in relation to incidence of asthma among American young adults: the CARDIA study Am. J. Clin. Nutr. 97 2013 173 178
3. R. Barros, A. Moreira, J. Fonseca, L. Delgado, M.G. Castel-Branco, T. Haahtela, C. Lopes, and P. Moreira Dietary intake of alpha-linolenic acid and low ratio of n - 6:n - 3 PUFA are associated with decreased exhaled NO and improved asthma control Br. J. Nutr. 106 2011 441 450
4. P.C. Calder n - 3 polyunsaturated fatty acids, inflammation, and inflammatory diseases Am. J. Clin. Nutr. 83 2006 1505S 1519S
5. P. Saravanan, N.C. Davidson, E.B. Schmidt, and P.C. Calder Cardiovascular effects of marine omega-3 fatty acids Lancet 376 2010 540 550
6. A.L. Groeger, C. Cipollina, M.P. Cole, S.R. Woodcock, G. Bonacci, T.K. Rudolph, V. Rudolph, B.A. Freeman, and F.J. Schopfer Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids Nat. Chem. Biol. 6 2010 433 441
7. Y. Isobe, M. Arita, S. Matsueda, R. Iwamoto, T. Fujihara, H. Nakanishi, R. Taguchi, K. Masuda, K. Sasaki, D. Urabe, M. Inoue, and H. Arai Identification and structure determination of a novel anti-inflammatory mediator resolvin E3: 17,18-dihydroxy-eicosapentaenoic acid J. Biol. Chem. 287 2012 10525 10534
8. Y. Lu, H. Tian, and S. Hong Novel 14,21-dihydroxy-docosahexaenoic acids: structures, formation pathways, and enhancement of wound healing J. Lipid Res. 51 2010 923 932
9. E.S. Musiek, J.D. Brooks, M. Joo, E. Brunoldi, A. Porta, G. Zanoni, G. Vidari, T.S. Blackwell, T.J. Montine, G.L. Milne, B. McLaughlin, and J.D. Morrow Electrophilic cyclopentenone neuroprostanes are anti-inflammatory mediators formed from the peroxidation of the omega-3 polyunsaturated fatty acid docosahexaenoic acid J. Biol. Chem. 283 2008 19927 19935
10. C.N. Serhan, S. Hong, K. Gronert, S.P. Colgan, P.R. Devchand, G. Mirick, and R.L. Moussignac Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals J. Exp. Med. 196 2002 1025 1037
11. S. Fujii, and T. Akaike Redox signaling by 8-nitro-cyclic guanosine monophosphate: nitric oxide- and reactive oxygen species-derived electrophilic messenger Antioxid. Redox Signal. 19 2013 1236 1246
12. F.J. Schopfer, C. Cipollina, and B.A. Freeman Formation and signaling actions of electrophilic lipids Chem. Rev. 111 2011 5997 6021
13. E. Kansanen, A.M. Kivela, and A.L. Levonen Regulation of Nrf2-dependent gene expression by 15-deoxy-delta12,14-prostaglandin J2 Free Radic. Biol. Med. 47 2009 1310 1317
14. T. Cui, F.J. Schopfer, J. Zhang, K. Chen, T. Ichikawa, P.R. Baker, C. Batthyany, B.K. Chacko, X. Feng, R.P. Patel, A. Agarwal, B.A. Freeman, and Y.E. Chen Nitrated fatty acids: endogenous anti-inflammatory signaling mediators J. Biol. Chem. 281 2006 35686 35698
15. D.S. Straus, G. Pascual, M. Li, J.S. Welch, M. Ricote, C.H. Hsiang, L.L. Sengchanthalangsy, G. Ghosh, and C.K. Glass 15-Deoxy-delta 12,14-prostaglandin J2 inhibits multiple steps in the NF-kappa B signaling pathway Proc. Natl. Acad. Sci. U. S. A. 97 2000 4844 4849
16. M. Decramer, W. Janssens, and M. Miravitlles Chronic obstructive pulmonary disease Lancet 379 2012 1341 1351
17. A. Tamimi, D. Serdarevic, and N.A. Hanania The effects of cigarette smoke on airway inflammation in asthma and COPD: therapeutic implications Respir. Med. 106 2012 319 328
18. E. Pace, M. Ferraro, L. Siena, M. Melis, A.M. Montalbano, M. Johnson, M.R. Bonsignore, G. Bonsignore, and M. Gjomarkaj Cigarette smoke increases Toll-like receptor 4 and modifies lipopolysaccharide-mediated responses in airway epithelial cells Immunology 124 2008 401 411
19. H. Sarir, E. Mortaz, K. Karimi, A.D. Kraneveld, I. Rahman, E. Caldenhoven, F.P. Nijkamp, and G. Folkerts Cigarette smoke regulates the expression of TLR4 and IL-8 production by human macrophages J. Inflamm. (Lond.) 6 2009 12
20. D. Malhotra, R. Thimmulappa, A. Navas-Acien, A. Sandford, M. Elliott, A. Singh, L. Chen, X. Zhuang, J. Hogg, P. Pare, R.M. Tuder, and S. Biswal Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1 Am. J. Respir. Crit. Care Med. 178 2008 592 604
21. D. Goven, A. Boutten, V. Lecon-Malas, J. Marchal-Somme, N. Amara, B. Crestani, M. Fournier, G. Leseche, P. Soler, J. Boczkowski, and M. Bonay Altered Nrf2/Keap1-Bach1 equilibrium in pulmonary emphysema Thorax 63 2008 916 924
22. A. Kode, S. Rajendrasozhan, S. Caito, S.R. Yang, I.L. Megson, and I. Rahman Resveratrol induces glutathione synthesis by activation of Nrf2 and protects against cigarette smoke-mediated oxidative stress in human lung epithelial cells Am. J. Physiol. Lung Cell. Mol. Physiol. 294 2008 L478 L488
23. A.J. Thorley, and T.D. Tetley Pulmonary epithelium, cigarette smoke, and chronic obstructive pulmonary disease Int. J. Chron. Obstruct. Pulmon. Dis. 2 2007 409 428
24. G.G. Brusselle, G.F. Joos, and K.R. Bracke New insights into the immunology of chronic obstructive pulmonary disease Lancet 378 2011 1015 1026
25. N. Roche, R. Marthan, P. Berger, A. Chambellan, P. Chanez, B. Aguilaniu, P.Y. Brillet, P.R. Burgel, A. Chaouat, P. Devillier, R. Escamilla, R. Louis, H. Mal, J.F. Muir, T. Perez, T. Similowski, B. Wallaert, and M. Aubier Beyond corticosteroids: future prospects in the management of inflammation in COPD Eur. Respir. Rev. 20 2011 175 182
26. A. Boutten, D. Goven, E. Artaud-Macari, J. Boczkowski, and M. Bonay NRF2 targeting: a promising therapeutic strategy in chronic obstructive pulmonary disease Trends Mol. Med. 17 2011 363 371
27. A.L. Cozens, M.J. Yezzi, M. Yamaya, D. Steiger, J.A. Wagner, S.S. Garber, L. Chin, E.M. Simon, G.R. Cutting, and P. Gardner et al. A transformed human epithelial cell line that retains tight junctions post crisis In Vitro Cell. Dev. Biol. 28A 1992 735 744
28. E. Pace, A. Giarratano, M. Ferraro, A. Bruno, L. Siena, S. Mangione, M. Johnson, and M. Gjomarkaj TLR4 upregulation underpins airway neutrophilia in smokers with chronic obstructive pulmonary disease and acute respiratory failure Hum. Immunol. 72 2011 54 62
29. I. Rahman, A. Kode, and S.K. Biswas Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method Nat. Protoc. 1 2006 3159 3165
30. E. Pace, M. Ferraro, S. Di Vincenzo, C. Cipollina, S. Gerbino, D. Cigna, V. Caputo, R. Balsamo, L. Lanata, and M. Gjomarkaj Comparative cytoprotective effects of carbocysteine and fluticasone propionate in cigarette smoke extract-stimulated bronchial epithelial cells Cell Stress Chaperones 18 2013 733 743
31. M. Profita, G. Chiappara, F. Mirabella, R. Di Giorgi, L. Chimenti, G. Costanzo, L. Riccobono, V. Bellia, J. Bousquet, and A.M. Vignola Effect of cilomilast (Ariflo) on TNF-alpha, IL-8, and GM-CSF release by airway cells of patients with COPD Thorax 58 2003 573 579
32. M.J. Walters, M.J. Paul-Clark, S.K. McMaster, K. Ito, I.M. Adcock, and J.A. Mitchell Cigarette smoke activates human monocytes by an oxidant-AP-1 signaling pathway: implications for steroid resistance Mol. Pharmacol. 68 2005 1343 1353
33. K. Karimi, H. Sarir, E. Mortaz, J.J. Smit, H. Hosseini, S.J. De Kimpe, F.P. Nijkamp, and G. Folkerts Toll-like receptor-4 mediates cigarette smoke-induced cytokine production by human macrophages Respir. Res. 7 2006 66
34. K.A. Zarember, and P.J. Godowski Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines J. Immunol. 168 2002 554 561
35. D. Adenuga, S. Caito, H. Yao, I.K. Sundar, J.W. Hwang, S. Chung, and I. Rahman Nrf2 deficiency influences susceptibility to steroid resistance via HDAC2 reduction Biochem. Biophys. Res. Commun. 403 2010 452 456
36. M. Suzuki, T. Betsuyaku, Y. Ito, K. Nagai, Y. Nasuhara, K. Kaga, S. Kondo, and M. Nishimura Down-regulated NF-E2-related factor 2 in pulmonary macrophages of aged smokers and patients with chronic obstructive pulmonary disease Am. J. Respir. Cell Mol. Biol. 39 2008 673 682
37. M.A. Birrell, S. Wong, M.C. Catley, and M.G. Belvisi Impact of tobacco-smoke on key signaling pathways in the innate immune response in lung macrophages J. Cell. Physiol. 214 2008 27 37
38. D. Goven, A. Boutten, V. Lecon-Malas, J. Boczkowski, and M. Bonay Prolonged cigarette smoke exposure decreases heme oxygenase-1 and alters Nrf2 and Bach1 expression in human macrophages: roles of the MAP kinases ERK(1/2) and JNK FEBS Lett. 583 2009 3508 3518
39. Y.C. Yang, C.K. Lii, Y.L. Wei, C.C. Li, C.Y. Lu, K.L. Liu, and H.W. Chen Docosahexaenoic acid inhibition of inflammation is partially via cross-talk between Nrf2/heme oxygenase 1 and IKK/NF-kappaB pathways J. Nutr. Biochem. 24 2013 204 212
40. J. Alam, and J.L. Cook How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am. J. Respir. Cell Mol. Biol. 36 2007 166 174
41. S. Koizumi, P. Gong, K. Suzuki, and M. Murata Cadmium-responsive element of the human heme oxygenase-1 gene mediates heat shock factor 1-dependent transcriptional activation J. Biol. Chem. 282 2007 8715 8723
42. E. Kansanen, H.K. Jyrkkanen, and A.L. Levonen Activation of stress signaling pathways by electrophilic oxidized and nitrated lipids Free Radic. Biol. Med. 52 2012 973 982
43. D. Goven, A. Boutten, V. Lecon-Malas, J. Marchal-Somme, P. Soler, J. Boczkowski, and M. Bonay Induction of heme oxygenase-1, biliverdin reductase and H-ferritin in lung macrophage in smokers with primary spontaneous pneumothorax: role of HIF-1alpha PLoS One 5 2010 e10886
44. G. Olmos, I. Conde, I. Arenas, L. Del Peso, C. Castellanos, M.O. Landazuri, and J. Lucio-Cazana Accumulation of hypoxia-inducible factor-1alpha through a novel electrophilic, thiol antioxidant-sensitive mechanism Cell. Signal. 19 2007 2098 2105
45. V.A. van Beelen, J.M. Aarts, A. Reus, H. Mooibroek, L. Sijtsma, D. Bosch, I.M. Rietjens, and G.M. Alink Differential induction of electrophile-responsive element-regulated genes by n - 3 and n - 6 polyunsaturated fatty acids FEBS Lett. 580 2006 4587 4590
46. B. Xue, Z. Yang, X. Wang, and H. Shi Omega-3 polyunsaturated fatty acids antagonize macrophage inflammation via activation of AMPK/SIRT1 pathway PLoS One 7 2012 e45990
47. Y. Zhao, and L.H. Chen Eicosapentaenoic acid prevents lipopolysaccharide-stimulated DNA binding of activator protein-1 and c-Jun N-terminal kinase activity J. Nutr. Biochem. 16 2005 78 84
48. L. Demirjian, R.T. Abboud, H. Li, and V. Duronio Acute effect of cigarette smoke on TNF-alpha release by macrophages mediated through the erk1/2 pathway Biochim. Biophys. Acta 1762 2006 592 597
49. Q. Qiu, W. Xiong, C. Yang, C. Gagnon, and P. Hardy Lymphocyte-derived microparticles induce bronchial epithelial cells' pro-inflammatory cytokine production and apoptosis Mol. Immunol. 55 2013 220 230
50. D.D. Gillette, P.A. Shah, T. Cremer, M.A. Gavrilin, B.Y. Besecker, A. Sarkar, D.L. Knoell, E. Cormet-Boyaka, M.D. Wewers, J.P. Butchar, and S. Tridandapani Analysis of human bronchial epithelial cell proinflammatory response to Burkholderia cenocepacia infection: inability to secrete il-1beta J. Biol. Chem. 288 2013 3691 3695
51. J. Yao, N. Mackman, T.S. Edgington, and S.T. Fan Lipopolysaccharide induction of the tumor necrosis factor-alpha promoter in human monocytic cells. Regulation by Egr-1, c-Jun, and NF-kappaB transcription factors J. Biol. Chem. 272 1997 17795 17801
52. L. Villacorta, L. Chang, S.R. Salvatore, T. Ichikawa, J. Zhang, D. Petrovic-Djergovic, L. Jia, H. Carlsen, F.J. Schopfer, B.A. Freeman, and Y.E. Chen Electrophilic nitro-fatty acids inhibit vascular inflammation by disrupting LPS-dependent TLR4 signalling in lipid rafts Cardiovasc. Res. 98 2013 116 124
53. R. Broekhuizen, E.F. Wouters, E.C. Creutzberg, C.A. Weling-Scheepers, and A.M. Schols Polyunsaturated fatty acids improve exercise capacity in chronic obstructive pulmonary disease Thorax 60 2005 376 382
54. J. de Batlle, J. Sauleda, E. Balcells, F.P. Gomez, M. Mendez, E. Rodriguez, E. Barreiro, J.J. Ferrer, I. Romieu, J. Gea, J.M. Anto, and J. Garcia-Aymerich Association between omega3 and omega6 fatty acid intakes and serum inflammatory markers in COPD J. Nutr. Biochem. 23 2012 817 821
55. F. Hirayama, A.H. Lee, C.W. Binns, N. Hiramatsu, M. Mori, and K. Nishimura Dietary intake of isoflavones and polyunsaturated fatty acids associated with lung function, breathlessness and the prevalence of chronic obstructive pulmonary disease: possible protective effect of traditional Japanese diet Mol. Nutr. Food Res. 54 2010 909 917
56. T.M. McKeever, S.A. Lewis, P.A. Cassano, M. Ocke, P. Burney, J. Britton, and H.A. Smit The relation between dietary intake of individual fatty acids, FEV1 and respiratory disease in Dutch adults Thorax 63 2008 208 214
57. G.R. Barr The Chronic Obstructive Pulmonary Disease Fish Oil Pilot Trial (COD-Fish) 2008
58. H.M. Hsiao, 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 A novel anti-inflammatory and pro-resolving role for resolvin D1 in acute cigarette smoke-induced lung inflammation PLoS One 8 2013 e58258