Inhaled carbon monoxide accelerates resolution of inflammation via unique proresolving mediator-heme oxygenase-1 circuits

Journal of Immunology

Volumn 190, Issue 12, 2013, Pages 6378-6388

  Chiang, Nan ^a   Shinohara, Masakazu ^a   Dalli, Jesmond ^a   Mirakaj, Valbona ^a   Kibi, Megumi ^a   Choi, Augustine M K ^b   Serhan, Charles N ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 15 LIPOXYGENASE; AUTACOID; CARBON MONOXIDE; HEME OXYGENASE 1; LEUKOTRIENE B4; MARESIN 1; RESOLVIN; RESOLVIN D1; RESOLVIN D5; SPECIALIZED PRORESOLVING MEDIATOR; UNCLASSIFIED DRUG; ZYMOSAN;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; ENZYME INHIBITION; HUMAN; HUMAN CELL; MACROPHAGE; MALE; MOUSE; NONHUMAN; PERITONEUM EXUDATE; PERITONITIS; PHAGOCYTOSIS; POLYMORPHONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ANIMALS; APOPTOSIS; CARBON MONOXIDE; CELLS, CULTURED; HEME OXYGENASE-1; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGES; MICE; NEUTROPHILS; SIGNAL TRANSDUCTION;

EID: 84879094995     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1202969     Document Type: Article

References (40)

1. Serhan, C. N. 2007. Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways. Annu. Rev. Immunol. 25: 101-137. (Pubitemid 46697904)
2. Medzhitov, R. 2010. Inflammation 2010: new adventures of an old flame. Cell 140: 771-776.
3. Nathan, C., and A. Ding. 2010. Nonresolving inflammation. Cell 140: 871-882.
4. Serhan, C. N., C. B. Clish, J. Brannon, S. P. Colgan, N. Chiang, and K. Gronert.Novel functional sets of lipid-derived mediators with antiinflammatory actions generated from γ-3 fatty acids via cyclooxygenase 2-nonsteroidal anti-inflammatory drugs and transcellular processing. J. Exp. Med. 192: 1197-1204.
5. Dinarello, C. A. 2010. Anti-inflammatory agents: present and future. Cell 140: 935-950.
6. Navarro-Xavier, R. A., J. Newson, V. L. F. Silveira, S. N. Farrow, D. W. Gilroy, and J. Bystrom. 2010. A new strategy for the identification of novel molecules with targeted proresolution of inflammation properties. J. Immunol. 184: 1516-1525.
7. Moncada, S., and E. A. Higgs. 2006. The discovery of nitric oxide and its role in vascular biology. Br. J. Pharmacol. 147(Suppl. 1): S193-S201. (Pubitemid 43077277)
8. Mustafa, A. K., M. M. Gadalla, and S. H. Snyder. 2009. Signaling by gasotransmitters. Sci. Signal. 2: re2.
9. Wallace, J. L., J. G. Ferraz, and M. N. Muscara. 2012. Hydrogen sulfide: an endogenous mediator of resolution of inflammation and injury. Antioxid. Redox Signal. 17: 58-67.
10. Abraham, N. G., and A. Kappas. 2008. Pharmacological and clinical aspects of heme oxygenase. Pharmacol. Rev. 60: 79-127. (Pubitemid 351439218)
11. Urquhart, P., G. Rosignoli, D. Cooper, R. Motterlini, and M. Perretti. 2007. Carbon monoxide-releasing molecules modulate leukocyte-endothelial interactions under flow. J. Pharmacol. Exp. Ther. 321: 656-662. (Pubitemid 46624509)
12. Nascimento-Silva, V., M. A. Arruda, C. Barja-Fidalgo, C. G. Villela, and I. M. Fierro. 2005. Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am. J. Physiol. Cell Physiol. 289: C557-C563. (Pubitemid 41192664)
13. Jin, S.-W., L. Zhang, Q.-Q. Lian, D. Liu, P. Wu, S.-L. Yao, and D.-Y. Ye. 2007. Posttreatment with aspirin-triggered lipoxin A4 analog attenuates lipopolysaccharideinduced acute lung injury in mice: the role of heme oxygenase-1. Anesth. Analg. 104: 369-377. (Pubitemid 46146744)
14. Biteman, B., I. R. Hassan, E. Walker, A. J. Leedom, M. Dunn, F. Seta, M. Laniado-Schwartzman, and K. Gronert. 2007. Interdependence of lipoxin A4 and heme-oxygenase in counter-regulating inflammation during corneal wound healing. FASEB J. 21: 2257-2266. (Pubitemid 47026460)
15. Dalli, J., and C. N. Serhan. 2012. Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and proresolving mediators. Blood 120: e60-e72.
16. 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.
17. Serhan, C. N., and N. A. Petasis. 2011. Resolvins and protectins in inflammation resolution. Chem. Rev. 111: 5922-5943.
18. Ryter, S. W., E. Kvam, and R. M. Tyrrell. 2000. Heme oxygenase activity: current methods and applications. Methods Mol. Biol. 99: 369-391.
19. 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. (Pubitemid 46920139)
20. Sun, D., and C. D. Funk. 1996. Disruption of 12/15-lipoxygenase expression in peritoneal macrophages: enhanced utilization of the 5-lipoxygenase pathway and diminished oxidation of low density lipoprotein. J. Biol. Chem. 271: 24055-24062. (Pubitemid 26327385)
21. Sekiya, K., and H. Okuda. 1982. Selective inhibition of platelet lipoxygenase by baicalein. Biochem. Biophys. Res. Commun. 105: 1090-1095. (Pubitemid 13219433)
22. Sun, Y.-P., S. F. Oh, J. Uddin, R. Yang, K. Gotlinger, E. Campbell, S. P. Colgan, N. A. Petasis, and C. N. Serhan. 2007. Resolvin D1 and its aspirin-triggered 17R epimer: stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J. Biol. Chem. 282: 9323-9334. (Pubitemid 47104612)
23. Buckley, C. D., D. W. Gilroy, C. N. Serhan, B. Stockinger, and P. P. Tak. 2013. The resolution of inflammation. Nat. Rev. Immunol. 13: 59-66.
24. El Kebir, D., P. Gjorstrup, and J. G. Filep. 2012. Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc. Natl. Acad. Sci. USA 109: 14983-14988.
25. Bonelli,M., A. Savitskaya, C.W. Steiner, E. Rath,M. Bilban, O.Wagner, F. H. Bach, J. S. Smolen, and C. Scheinecker. 2012. Heme oxygenase-1 end-products carbon monoxide and biliverdin ameliorate murine collagen induced arthritis. Clin. Exp. Rheumatol. 30: 73-78.
26. Patel, R., H. Albadawi, W. Steudel, F. F. Hashmi, J. Kang, H. J. Yoo, and M. T. Watkins. 2012. Inhalation of carbon monoxide reduces skeletal muscle injury after hind limb ischemia-reperfusion injury in mice. Am. J. Surg. 203: 488-495.
27. Mitchell, L. A., M. M. Channell, C. M. Royer, S. W. Ryter, A. M. Choi, and J. D. McDonald. 2010. Evaluation of inhaled carbon monoxide as an anti-inflammatory therapy in a nonhuman primate model of lung inflammation. Am. J. Physiol. Lung Cell. Mol. Physiol. 299: L891-L897.
28. Recchiuti, A., S. Krishnamoorthy, G. Fredman, N. Chiang, and C. N. Serhan. 2011. MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits. FASEB J. 25: 544-560.
29. Haworth, O., M. Cernadas, R. Yang, C. N. Serhan, and B. D. Levy. 2008. Resolvin E1 regulates interleukin 23, interferon-g and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat. Immunol. 9: 873-879.
30. Xu, Y. N., Z. Zhang, P. Ma, and S. H. Zhang. 2011. Adenovirus-delivered angiopoietin 1 accelerates the resolution of inflammation of acute endotoxic lung injury in mice. Anesth. Analg. 112: 1403-1410.
31. Chiang, N., J. M. Schwab, G. Fredman, K. Kasuga, S. Gelman, and C. N. Serhan. 2008. Anesthetics impact the resolution of inflammation. PLoS One 3: e1879.
32. Chiang, N., G. Fredman, F. Bäckhed, S. F. Oh, T. W. Vickery, B. A. Schmidt, and C. N. Serhan. 2012. Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 484: 524-528.
33. Mansouri, A., and C. A. Perry. 1982. Alteration of platelet aggregation by cigarette smoke and carbon monoxide. Thromb. Haemost. 48: 286-288. (Pubitemid 13209595)
34. Brüne, B., and V. Ullrich. 1987. Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32: 497-504. (Pubitemid 18006150)
35. Shak, S., and I. M. Goldstein. 1984. v-oxidation is the major pathway for the catabolism of leukotriene B4 in human polymorphonuclear leukocytes. J. Biol. Chem. 259: 10181-10187. (Pubitemid 14067694)
36. Kikuta, Y., E. Kusunose, K. Endo, S. Yamamoto, K. Sogawa, Y. Fujii-Kuriyama, and M. Kusunose. 1993. A novel form of cytochrome P-450 family 4 in human polymorphonuclear leukocytes: cDNA cloning and expression of leukotriene B4 v-hydroxylase. J. Biol. Chem. 268: 9376-9380. (Pubitemid 23145985)
37. Hong, S., K. Gronert, P. R. Devchand, R.-L. Moussignac, and C. N. Serhan. 2003. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells: autacoids in anti-inflammation. J. Biol. Chem. 278: 14677-14687. (Pubitemid 36799790)
38. Arita, M., S. F. Oh, T. Chonan, S. Hong, S. Elangovan, Y.-P. Sun, J. Uddin, N. A. Petasis, and C. N. Serhan. 2006. Metabolic inactivation of resolvin E1 and stabilization of its anti-inflammatory actions. J. Biol. Chem. 281: 22847-22854.
39. Hong, S., T. F. Porter, Y. Lu, S. F. Oh, P. S. Pillai, and C. N. Serhan. 2008. Resolvin E1 metabolome in local inactivation during inflammation- resolution. J. Immunol. 180: 3512-3519.
40. 4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction. J. Exp. Med. 183: 137-146.