Protectins and maresins: New pro-resolving families of mediators in acute inflammation and resolution bioactive metabolome

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1851, Issue 4, 2015, Pages 397-413

  Serhan, Charles N ^a   Dalli, Jesmond ^a   Colas, Romain A ^a   Winkler, Jeremy W ^a   Chiang, Nan ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Eicosanoid; LC MS MS based targeted lipid mediator; Leukocyte; Lipid mediator; metabolomics; Resolvin

Indexed keywords

ACETYLSALICYLIC ACID; ARACHIDONATE 12 LIPOXYGENASE; CD59 ANTIGEN; DOCOSAHEXAENOIC ACID; MARESIN; OXYGEN; POLYUNSATURATED FATTY ACID; PROTEIN; UNCLASSIFIED DRUG; 13,14-DIHYDROXYDOCOSAHEXAENOIC ACID; 7,14-DIHYDROXYDOCOSA-4,8,10,12,16,19-HEXAENOIC ACID; ANTIINFLAMMATORY AGENT; LIPOXYGENASE; PROTECTIN D1;

ARTHRITIS; ARTICLE; ATHEROSCLEROSIS; CORNEA INJURY; DEGENERATIVE DISEASE; ENDOMETRIOSIS; FATTY ACID METABOLISM; HUMAN; INFECTION; INFLAMMATION; LEUKOCYTE; MACROPHAGE; METABOLOME; NEUROPROTECTION; PERITONITIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STEREOCHEMISTRY; TISSUE REGENERATION; WOUND HEALING; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; METABOLISM; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

MUS;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ASPIRIN; DOCOSAHEXAENOIC ACIDS; HUMANS; INFLAMMATION; LIPOXYGENASES; METABOLOME; MOLECULAR STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84922571766     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2014.08.006     Document Type: Review

References (164)

1. N.G. Bazan Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors Trends Neurosci. 29 2006 263 271
2. M.A. Crawford, C.L. Broadhurst, M. Guest, A. Nagar, Y. Wang, K. Ghebremeskel, and W.F. Schmidt A quantum theory for the irreplaceable role of docosahexaenoic acid in neural cell signalling throughout evolution Prostaglandins Leukot. Essent. Fat. Acids 88 2013 5 13
3. W.E.M. Lands Fish, Omega-3 and Human Health 2nd ed 2005 AOCS Press Champaign, IL
4. N. Salem Jr., B. Litman, H.-Y. Kim, and K. Gawrisch Mechanisms of action of docosahexaenoic acid in the nervous system Lipids 36 2001 945 959
5. C.N. Serhan Novel resolution mechanisms in acute inflammation: to resolve or not? Am. J. Pathol. 177 2010 1576 1591
6. G. Majno, R.S. Cotran, and N. Kaufman Current topics in inflammation and infection N. Kaufman, International Academy of Pathology Monograph vol. 23 1982 Williams & Wilkins Baltimore 242
7. C.A. Dinarello Anti-inflammatory agents: present and future Cell 140 2010 935 950
8. C.N. Serhan, and J. Savill Resolution of inflammation: The beginning programs the end Nat. Immunol. 6 2005 1191 1197
9. 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 pro-inflammation signals J. Exp. Med. 196 2002 1025 1037
10. C.N. Serhan, 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 omega-3 fatty acids via cyclooxygenase 2-nonsteroidal antiinflammatory drugs and transcellular processing J. Exp. Med. 192 2000 1197 1204
11. B. Samuelsson Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation Science 220 1983 568 575
12. N.G. Bazan, J.M. Calandria, and C.N. Serhan Rescue and repair during photoreceptor cell renewal mediated by docosahexaenoic acid-derived neuroprotectin D1 J. Lipid Res. 51 2010 2018 2031
13. S. Hong, K. Gronert, P. Devchand, R.-L. Moussignac, and C.N. Serhan 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 2003 14677 14687
14. P.K. Mukherjee, V.L. Marcheselli, C.N. Serhan, and N.G. Bazan Neuroprotectin D1: A docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress Proc. Natl. Acad. Sci. U. S. A. 101 2004 8491 8496
15. G. Majno, and I. Joris Cells, Tissues, and Disease: Principles of General Pathology 2nd ed. 2004 Oxford University Press New York
16. L.M. Coussens, and Z. Werb Inflammation and cancer Nature 420 2002 860 867
17. P. Libby Inflammation in atherosclerosis Nature 420 2002 868 878
18. H.L. Weiner, and D.J. Selkoe Inflammation and therapeutic vaccination in CNS diseases Nature 420 2002 879 884
19. B. Samuelsson Role of basic science in the development of new medicines: examples from the eicosanoid field J. Biol. Chem. 287 2012 10070 10080
20. C. Nathan Points of control in inflammation Nature 420 2002 846 852
21. C.N. Serhan, and N. Chiang Novel endogenous small molecules as the checkpoint controllers in inflammation and resolution: entrée for resoleomics Rheum. Dis. Clin. N. Am. 30 2004 69 95
22. B.D. Levy, C.B. Clish, B. Schmidt, K. Gronert, and C.N. Serhan Lipid mediator class switching during acute inflammation: signals in resolution Nat. Immunol. 2 2001 612 619
23. B. Samuelsson, S.E. Dahlén, J.Å. Lindgren, C.A. Rouzer, and C.N. Serhan Leukotrienes and lipoxins: structures, biosynthesis, and biological effects Science 237 1987 1171 1176
24. B. McMahon, and C. Godson Lipoxins: endogenous regulators of inflammation Am. J. Physiol. Renal Physiol. 286 2004 F189 F201
25. C.N. Serhan Lipoxin biosynthesis and its impact in inflammatory and vascular events Biochim. Biophys. Acta 1212 1994 1 25
26. J.L. Wallace, and S. Fiorucci A magic bullet for mucosal protection... and aspirin is the trigger! Trends Pharmacol. Sci. 24 2003 323 326
27. C. Godson, S. Mitchell, K. Harvey, N.A. Petasis, N. Hogg, and H.R. Brady Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages J. Immunol. 164 2000 1663 1667
28. 4 are potent stimuli for human monocyte migration and adhesion: selective inactivation by dehydrogenation and reduction J. Exp. Med. 183 1996 137 146
29. D.W. Gilroy, T. Lawrence, M. Perretti, and A.G. Rossi Inflammatory resolution: new opportunities for drug discovery Nat. Rev. Drug Discov. 3 2004 401 416
30. C.N. Serhan A search for endogenous mechanisms of anti-inflammation uncovers novel chemical mediators: missing links to resolution Histochem. Cell Biol. 122 2004 305 321
31. C.N. Serhan, K. Gotlinger, S. Hong, and M. Arita Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their aspirin-triggered endogenous epimers: An overview of their protective roles in catabasis Prostaglandins Lipid Mediat. 73 2004 155 172
32. J. Dalli, R.A. Colas, and C.N. Serhan Novel n- 3 immunoresolvents: structures and actions Sci. Rep. 3 2013 1940
33. G.O. Burr, and M.M. Burr A new deficiency disease produced by the rigid exclusion of fat from the diet J. Biol. Chem. 82 1929 345 367
34. D. Camuesco, J. Galvez, A. Nieto, M. Comalada, M.E. Rodriguez-Cabezas, A. Concha, J. Xaus, and A. Zarzuelo Dietary olive oil supplemented with fish oil, rich in EPA and DHA (n - 3) polyunsaturated fatty acids, attenuates colonic inflammation in rats with DSS-induced colitis J. Nutr. 135 2005 687 694
35. G.E. Billman, J.X. Kang, and A. Leaf Prevention of sudden cardiac death by dietary pure w - 3 polyunsaturated fatty acids in dogs Circulation 99 1999 2452 2457
36. R. Marchioli, F. Barzi, E. Bomba, C. Chieffo, D. Di Gregorio, R. Di Mascio, M.G. Franzosi, E. Geraci, G. Levantesi, A.P. Maggioni, L. Mantini, R.M. Marfisi, G. Mastrogiuseppe, N. Mininni, G.L. Nicolosi, M. Santini, C. Schweiger, L. Tavazzi, G. Tognoni, C. Tucci, and F. Valagussa Early protection against sudden death by n - 3 polyunsaturated fatty acids after myocardial infarction: time-course analysis of the results of the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico (GISSI)-Prevenzione Circulation 105 2002 1897 1903
37. D.J. Holub, and B.J. Holub Omega-3 fatty acids from fish oils and cardiovascular disease Mol. Cell. Biochem. 263 2004 217 225
38. M.M. Engler, M.B. Engler, M. Malloy, E. Chiu, D. Besio, S. Paul, M. Stuehlinger, J.D. Morrow, P.M. Ridker, N. Rifai, and M. Mietus-Snyder Docosahexaenoic acid restores endothelial function in children with hyperlipidemia: results from the EARLY study Int. J. Clin. Pharmacol. Ther. 42 2004 672 679
39. G.P. Lim, F. Calon, T. Morihara, F. Yang, B. Teter, O. Ubeda, N. Salem Jr., S.A. Frautschy, and G.M. Cole A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model J. Neurosci. 25 2005 3032 3040
40. N.G. Bazan Supply of n - 3 polyunsaturated fatty acids and their significance in the central nervous system R.J. Wurtman, J.J. Wurtman, Nutrition and the Brain vol. 8 1990 Raven Press New York 1 22
41. N.G. Bazan, D.L. Birkle, and T.S. Reddy Docosahexaenoic acid (22:6, n - 3) is metabolized to lipoxygenase reaction products in the retina Biochem. Biophys. Res. Commun. 125 1984 741 747
42. S. Sawazaki, N. Salem Jr., and H.-Y. Kim Lipoxygenation of docosahexaenoic acid by the rat pineal body J. Neurochem. 62 1994 2437 2447
43. G.L. Bannenberg, N. Chiang, A. Ariel, M. Arita, E. Tjonahen, K.H. Gotlinger, S. Hong, and C.N. Serhan Molecular circuits of resolution: formation and actions of resolvins and protectins J. Immunol. 174 2005 4345 4355
44. V.L. Marcheselli, S. Hong, W.J. Lukiw, X. Hua Tian, K. Gronert, A. Musto, M. Hardy, J.M. Gimenez, N. Chiang, C.N. Serhan, and N.G. Bazan Novel docosanoids inhibit brain ischemia -reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression J. Biol. Chem. 278 2003 43807 43817
45. L. Belayev, V.L. Marcheselli, L. Khoutorova, E.B. Rodriguez de Turco, R. Busto, M.D. Ginsberg, and N.G. Bazan Docosahexaenoic acid complexed to albumin elicits high-grade ischemic neuroprotection Stroke 36 2005 118 123
46. K. Gronert, N. Maheshwari, N. Khan, I.R. Hassan, M. Dunn, and M.L. Schwartzman A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense J. Biol. Chem. 280 2005 15267 15278
47. S. Hong, E. Tjonahen, E.L. Morgan, L. Yu, C.N. Serhan, and A.F. Rowley Rainbow trout (Oncorhynchus mykiss) brain cells biosynthesize novel docosahexaenoic acid-derived resolvins and protectins - mediator lipidomic analysis Prostaglandins Lipid Mediat. 78 2005 107 116
48. H2 skewing and promotes human T cell apoptosis via lipid raft clustering J. Biol. Chem. 280 2005 43079 43086
49. C.N. Serhan, G. Fredman, R. Yang, S. Karamnov, L.S. Belayev, N.G. Bazan, M. Zhu, J.W. Winkler, and N.A. Petasis Novel proresolving aspirin-triggered DHA pathway Chem. Biol. 18 2011 976 987
50. C.N. Serhan, K. Gotlinger, S. Hong, Y. Lu, J. Siegelman, T. Baer, R. Yang, S.P. Colgan, and N.A. Petasis Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: Assignments of dihydroxy-containing docosatrienes J. Immunol. 176 2006 1848 1859
51. A. Sica, and A. Mantovani Macrophage plasticity and polarization: in vivo veritas J. Clin. Invest. 122 2012 787 795
52. S. Gordon Targeting a monocyte subset to reduce inflammation Circ. Res. 110 2012 1546 1548
53. M.J. Stables, S. Shah, E.B. Camon, R.C. Lovering, J. Newson, J. Bystrom, S. Farrow, and D.W. Gilroy Transcriptomic analyses of murine resolution-phase macrophages Blood 118 2011 e192 e208
54. C.N. Serhan, J. Dalli, S. Karamnov, A. Choi, C.K. Park, Z.Z. Xu, R.R. Ji, M. Zhu, and N.A. Petasis Macrophage pro-resolving mediator maresin 1 stimulates tissue regeneration and controls pain FASEB J. 26 2012 1755 1765
55. C.N. Serhan, R. Yang, K. Martinod, K. Kasuga, P.S. Pillai, T.F. Porter, S.F. Oh, and M. Spite Maresins: novel macrophage mediators with potent anti-inflammatory and pro-resolving actions J. Exp. Med. 206 2009 15 23
56. C.N. Serhan, Resolvins: biotemplates for novel therapeutic interventions, in: U.S. Patent 7,585,856 and Application Publication 2004/0116408 A1, Brigham and Women's Hospital, 2004.
57. N. Chiang, G. Fredman, F. Bäckhed, S.F. Oh, T.W. Vickery, B.A. Schmidt, and C.N. Serhan Infection regulates pro-resolving mediators that lower antibiotic requirements Nature 484 2012 524 528
58. R. Yang Synthetic study of lipid mediators; Doctoral thesis 2005 University of Southern California Los Angeles
59. N.A. Petasis, R. Yang, J.W. Winkler, M. Zhu, J. Uddin, N.G. Bazan, and C.N. Serhan Stereocontrolled total synthesis of neuroprotectin D1/protectin D1 and its aspirin-triggered stereoisomer Tetrahedron Lett. 53 2012 1695 1698
60. C.N. Serhan, and B. Samuelsson Lipoxins: A new series of eicosanoids (biosynthesis, stereochemistry, and biological activities) Adv. Exp. Med. Biol. 229 1988 1 14
61. C.N. Serhan, K.C. Nicolaou, S.E. Webber, C.A. Veale, S.E. Dahlen, T.J. Puustinen, and B. Samuelsson Lipoxin A J Biol Chem. 261 1986 16340 16345
62. H. Kuhn, A.R. Brash, R. Wiesner, and L. Alder Lipoxygenase catalyzed oxygenation of hydroxy fatty acids to lipoxins Adv. Exp. Med. Biol. 229 1988 39 49
63. K. Gronert, C.B. Clish, M. Romano, and C.N. Serhan Transcellular regulation of eicosanoid biosynthesis E.A. Lianos, Eicosanoid Protocols 1999 Humana Press Totowa, NJ 119 144
64. P. Chen, B. Fenet, S. Michaud, N. Tomczyk, E. Véricel, M. Lagarde, and M. Guichardant Full characterization of PDX, a neuroprotectin/protectin D1 isomer, which inhibits blood platelet aggregation FEBS Lett. 583 2009 3478 3484
65. R.L. Maas, J. Turk, J.A. Oates, and A.R. Brash Formation of a novel dihydroxy acid from arachidonic acid by lipoxygenase-catalyzed double oxygenation in rat mononuclear cells and human leukocytes J. Biol. Chem. 257 1982 7056 7067
66. C.N. Serhan On the relationship between leukotriene and lipoxin production by human neutrophils: evidence for differential metabolism of 15-HETE and 5-HETE Biochim. Biophys. Acta 1004 1989 158 168
67. P.J. White, P. St-Pierre, A. Charbonneau, P.L. Mitchell, E. St-Amand, B. Marcotte, and A. Marette Protectin DX alleviates insulin resistance by activating a myokine-liver glucoregulatory axis Nat. Med. 20 2014 664 669
68. I. Tabas, and C.K. Glass Anti-inflammatory therapy in chronic disease: challenges and opportunities Science 339 2013 166 172
69. A. Ariel, G. Fredman, Y.-P. Sun, A. Kantarci, T.E. Van Dyke, A.D. Luster, and C.N. Serhan Apoptotic neutrophils and T cells sequester chemokines during immune response resolution via modulation of CCR5 expression Nat. Immunol. 7 2006 1209 1216
70. C.K. Park, N. Lü, Z.Z. Xu, T. Liu, C.N. Serhan, and R.R. Ji Resolving TRPV1 and TNF-α-mediated spinal cord synaptic plasticity and inflammatory pain with neuroprotectin D1 J. Neurosci. 31 2011 15072 15085
71. K.M. Connor, J.P. SanGiovanni, C. Lofqvist, C.M. Aderman, J. Chen, A. Higuchi, S. Hong, E.A. Pravda, S. Majchrzak, D. Carper, A. Hellstrom, J.X. Kang, E.Y. Chew, N.N. Salem Jr., C.N. Serhan, and L.E.H. Smith Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis Nat. Med. 13 2007 868 873
72. D.T. Stark, and N.G. Bazan Neuroprotectin D1 induces neuronal survival and downregulation of amyloidogenic processing in Alzheimer's disease cellular models Mol. Neurobiol. 43 2011 131 138
73. I.R. Hassan, and K. Gronert Acute changes in dietary omega-3 and omega-6 polyunsaturated fatty acids have a pronounced impact on survival following ischemic renal injury and formation of renoprotective docosahexaenoic acid-derived protectin D1 J. Immunol. 182 2009 3223 3232
74. M.S. Cortina, J. He, N. Li, N.G. Bazan, and H.E. Bazan Neuroprotectin D1 synthesis and corneal nerve regeneration after experimental surgery and treatment with PEDF plus DHA Invest. Ophthalmol. Vis. Sci. 51 2010 804 810
75. O. Yanes, J. Clark, D.M. Wong, G.G. Patti, A. Sánchez-Ruiz, H.P. Benton, S.A. Trauger, C. Desponts, S. Ding, and G. Siuzdak Metabolic oxidation regulates embryonic stem cell differentiation Nat. Chem. Biol. 6 2010 411 417
76. J.M. Schwab, N. Chiang, M. Arita, and C.N. Serhan Resolvin E1 and protectin D1 activate inflammation-resolution programmes Nature 447 2007 869 874
77. V.L. Marcheselli, P.K. Mukherjee, M. Arita, S. Hong, R. Antony, K. Sheets, N. Petasis, C.N. Serhan, and N.G. Bazan Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils Prostaglandins Leukot. Essent. Fat. Acids 82 2010 27 34
78. C.N. Serhan, and N. Chiang Resolution phase lipid mediators of inflammation: Agonists of resolution Curr. Opin. Pharmacol. 13 2013 632 640
79. J. Whelan Arachidonic acid cascade: The 5-lipoxygenase pathway; Doctoral thesis, Department of Nutrition 1988 Pennsylvania State University University Park
80. J. Whelan, P. Reddanna, V. Nikolaev, G.R. Hildenbrandt, and T.S. Reddy The unique characteristics of the purified 5-lipoxygenase from potato tubers and the proposed mechanism of formation of leukotrienes and lipoxins Biological Oxidation Systems vol. 2 1990 Academic Press San Diego 765 778
81. I.A. Butovich, M. Hamberg, and O. Rådmark Novel oxylipins formed from docosahexaenoic acid by potato lipoxygenase-10(S)-hydroxydocosahexaenoic acid and 10,20-dihydroxydocosahexaenoic acid Lipids 40 2005 249 257
82. B.T. Kalish, H.D. Le, J.M. Fitzgerald, S. Wang, K. Seamon, K.M. Gura, K. Gronert, and M. Puder Intravenous fish oil lipid emulsion promotes a shift toward anti-inflammatory proresolving lipid mediators Am. J. Physiol. Gastrointest. Liver Physiol. 305 2013 G818 G828
83. D.W. Gilroy, P.R. Colville-Nash, D. Willis, J. Chivers, M.J. Paul-Clark, and D.A. Willoughby Inducible cycloxygenase may have anti-inflammatory properties Nat. Med. 5 1999 698 701
84. C.N. Serhan Resolution phases of inflammation: novel endogenous anti-inflammatory and pro-resolving lipid mediators and pathways Annu. Rev. Immunol. 25 2007 101 137
85. D.W. Gilroy, and M. Perretti Aspirin and steroids: new mechanistic findings and avenues for drug discovery Curr. Op. Pharmacol. 5 2005 405 411
86. J. Clària, and C.N. Serhan Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions Proc. Natl. Acad. Sci. U. S. A. 92 1995 9475 9479
87. B. Samuelsson From studies of biochemical mechanisms to novel biological mediators: prostaglandin endoperoxides, thromboxanes and leukotrienes Les Prix Nobel, Nobel Prizes, Presentations, Biographies and Lecture 1982 Almqvist & Wiksell Stockholm 153 174
88. J.R. Vane Adventures and excursions in bioassay: The stepping stones to prostacyclin Les Prix Nobel, Nobel Prizes, Presentations, Biographies and Lectures 1982 Almqvist & Wiksell Stockholm 181 206
89. S.W. Rowlinson, B.C. Crews, D.C. Goodwin, C. Schneider, J.K. Gierse, and L.J. Marnett Spatial requirements for 15-(R)-hydroxy-5Z,8Z,11Z,13E-eicosatetraenoic acid synthesis within the cyclooxygenase active site of murine COX-2 J. Biol. Chem. 2000 6586 6591
90. 4 and inhibits thromboxane in a randomized human trial Proc. Natl. Acad. Sci. U. S. A. 101 2004 15178 15183
91. 4 metabolism by differentiated HL-60 cells and human monocytes: conversion to novel 15-oxo and dihydro products Biochemistry (Mosc) 32 1993 6313 6319
92. T. Morris, M. Stables, A. Hobbs, P. de Souza, P. Colville-Nash, T. Warner, J. Newson, G. Bellingan, and D.W. Gilroy Effects of low-dose aspirin on acute inflammatory responses in humans J. Immunol. 183 2009 2089 2096
93. V.L. Tsikitis, N.A. Morin, E.O. Harrington, J.E. Albina, and J.S. Reichner The lectin-like domain of complement receptor 3 protects endothelial barrier function from activated neutrophils J. Immunol. 173 2004 1284 1291
94. Y.-P. Sun, S.F. Oh, J. Uddin, R. Yang, K. Gotlinger, E. Campbell, S.P. Colgan, N.A. Petasis, and C.N. Serhan Resolvin D1 and its aspirin-triggered 17R epimer: stereochemical assignments, anti-inflammatory properties and enzymatic inactivation J. Biol. Chem. 282 2007 9323 9334
95. M. Spite, L.V. Norling, L. Summers, R. Yang, D. Cooper, N.A. Petasis, R.J. Flower, M. Perretti, and C.N. Serhan Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis Nature 461 2009 1287 1291
96. C.N. Serhan, and N.A. Petasis Resolvins and protectins in inflammation-resolution Chem. Rev. 111 2011 5922 5943
97. P. Borgeat, and B. Samuelsson Arachidonic acid metabolism in polymorphonuclear leukocytes: effects of ionophore A23187 Proc. Natl. Acad. Sci. U. S. A. 76 1979 2148 2152
98. F.A. Carey, and R.J. Sundberg Advanced Organic Chemistry, Part A: Structure and Mechanisms 2007 Springer Science New York
99. R.A. Lewis, E.J. Goetzl, J.M. Drazen, N.A. Soter, K.F. Austen, and E.J. Corey Functional characterization of synthetic leukotriene B and its stereochemical isomers J. Exp. Med. 154 1981 1243 1248
100. C. Antoni, and J. Braun Side effects of anti-TNF therapy: current knowledge Clin. Exp. Rheumatol. 20 2002 S152 S157
101. J. Lin, D. Ziring, S. Desai, S. Kim, M. Wong, Y. Korin, J. Braun, E. Reed, D. Gjertson, and R.R. Singh TNFalpha blockade in human diseases: An overview of efficacy and safety Clin. Immunol. 126 2008 13 30
102. 4 synthesis from arachidonic acid Proc. Natl. Acad. Sci. U. S. A. 81 1984 689 693
103. 4 hydrolase: effects on purified enzyme and human polymorphonuclear leukocytes J. Pharmacol. Exp. Ther. 275 1995 31 37
104. P.M. Rothwell, M. Wilson, C.E. Elwin, B. Norrving, A. Algra, C.P. Warlow, and T.W. Meade Long-term effect of aspirin on colorectal cancer incidence and mortality: 20-year follow-up of five randomised trials Lancet 376 2010 1713 1714
105. A.C. Skulas-Ray, P.M. Kris-Etherton, W.S. Harris, J.P. Vanden Heuvel, P.R. Wagner, and S.G. West Dose-response effects of omega-3 fatty acids on triglycerides, inflammation, and endothelial function in healthy persons with moderate hypertriglyceridemia Am. J. Clin. Nutr. 93 2011 243 252
106. H. El-Sharkawy, N. Aboelsaad, M. Eliwa, M. Darweesh, M. Alshahat, A. Kantarci, H. Hasturk, and T.E. Van Dyke Adjunctive treatment of chronic periodontitis with daily dietary supplementation with omega-3 fatty acids and low-dose aspirin J. Periodontol. 81 2010 1635 1643
107. T.E. Van Dyke, and C.N. Serhan A novel approach to resolving inflammation Sci. Am. 2006 42 45
108. A. Ariel, and C.N. Serhan New lives given by cell death: macrophage differentiation following their encounter with apoptotic leukocytes during the resolution of inflammation Front. Immunol. 3 2012 4
109. M.J. Stables, S. Shah, E.B. Camon, R.C. Lovering, J. Newson, J. Bystrom, S. Farrow, and D.W. Gilroy Transcriptomic analyses of murine resolution-phase macrophages Blood 118 2011 e192 e208
110. M.J. Zhang, and M. Spite Resolvins: Anti-inflammatory and proresolving mediators derived from omega-3 polyunsaturated fatty acids Annu. Rev. Nutr. 32 2012 203 227
111. C.N. Serhan, R. Yang, K. Martinod, K. Kasuga, P.S. Pillai, T.F. Porter, S.F. Oh, and M. Spite Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions J. Exp. Med. 206 2009 15 23
112. J. Dalli, and C.N. Serhan Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators Blood 120 2012 e60 e72
113. M. Giera, A. Ioan-Facsinay, R. Toes, F. Gao, J. Dalli, A.M. Deelder, C.N. Serhan, and O.A. Mayboroda Lipid and lipid mediator profiling of human synovial fluid in rheumatoid arthritis patients by means of LC-MS/MS Biochim. Biophys. Acta 1821 2012 1415 1424
114. C.N. Serhan, J. Dalli, S. Karamnov, A. Choi, C.K. Park, Z.Z. Xu, R.R. Ji, M. Zhu, and N.A. Petasis Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain FASEB J. 26 2012 1755 1765
115. J. Dalli, M. Zhu, N.A. Vlasenko, B. Deng, J.Z. Haeggstrom, N.A. Petasis, and C.N. Serhan The novel 13S,14S-epoxy-maresin is converted by human macrophages to maresin1 (MaR1), inhibits leukotriene A4 hydrolase (LTA4H), and shifts macrophage phenotype FASEB J. 27 2013 2573 2583
116. B. Deng, C.W. Wang, H.H. Arnardottir, Y. Li, C.Y. Cheng, J. Dalli, and C.N. Serhan Maresin biosynthesis and identification of maresin 2, a new anti-inflammatory and pro-resolving mediator from human macrophages PLoS One 9 2014 e102362
117. M.A. Ingersoll, A.M. Platt, S. Potteaux, and G.J. Randolph Monocyte trafficking in acute and chronic inflammation Trends Immunol. 32 2011 470 477
118. J. Hellmann, Y. Tang, M. Kosuri, A. Bhatnagar, and M. Spite Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice FASEB J. 25 2011 2399 2407
119. E. Titos, B. Rius, A. Gonzalez-Periz, C. Lopez-Vicario, E. Moran-Salvador, M. Martinez-Clemente, V. Arroyo, and J. Claria Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype J. Immunol. 187 2011 5408 5418
120. 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
121. H. Tian, Y. Lu, S.P. Shah, Q. Wang, and S. Hong 14S,21R-dihydroxy-docosahexaenoic acid treatment enhances mesenchymal stem cell amelioration of renal ischemia/reperfusion injury Stem Cells Dev. 21 2012 1187 1199
122. H. Tian, Y. Lu, S.P. Shah, and S. Hong 14S,21R-dihydroxydocosahexaenoic acid remedies impaired healing and mesenchymal stem cell functions in diabetic wounds J. Biol. Chem. 286 2011 4443 4453
123. B. Samuelsson Role of basic science in the development of new medicines: examples from the eicosanoid field J. Biol. Chem. 287 2012 10070 10080
124. T. Shimizu Lipid mediators in health and disease: enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation Annu. Rev. Pharmacol. Toxicol. 49 2009 123 150
125. M. Spite, L.V. Norling, L. Summers, R. Yang, D. Cooper, N.A. Petasis, R.J. Flower, M. Perretti, and C.N. Serhan Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis Nature 461 2009 1287 1291
126. N. Chiang, G. Fredman, F. Backhed, S.F. Oh, T. Vickery, B.A. Schmidt, and C.N. Serhan Infection regulates pro-resolving mediators that lower antibiotic requirements Nature 484 2012 524 528
127. 4 hydrolase/aminopeptidase: glutamate 271 is a catalytic residue with specific roles in two distinct enzyme mechanisms J. Biol. Chem. 277 2002 1398 1404
128. S.F. Oh, P.S. Pillai, A. Recchiuti, R. Yang, and C.N. Serhan Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation J. Clin. Invest. 121 2011 569 581
129. C.N. Serhan, P.A. Ward, and D.W. Gilroy Fundamentals of Inflammation 2010 Cambridge University Press Cambridge
130. O. Yanes, J. Clark, D.M. Wong, G.J. Patti, A. Sanchez-Ruiz, H.P. Benton, S.A. Trauger, C. Desponts, S. Ding, and G. Siuzdak Metabolic oxidation regulates embryonic stem cell differentiation Nat. Chem. Biol. 6 2010 411 417
131. M.J. Mueller, A. Wetterholm, M. Blomster, H. Jornvall, B. Samuelsson, and J.Z. Haeggstrom Leukotriene A4 hydrolase: mapping of a henicosapeptide involved in mechanism-based inactivation Proc. Natl. Acad. Sci. U. S. A. 92 1995 8383 8387
132. C.N. Serhan, A. Jain, S. Marleau, C. Clish, A. Kantarci, B. Behbehani, S.P. Colgan, G.L. Stahl, A. Merched, N.A. Petasis, L. Chan, and T.E. Van Dyke Reduced inflammation and tissue damage in transgenic rabbits overexpressing 15-lipoxygenase and endogenous anti-inflammatory lipid mediators J. Immunol. 171 2003 6856 6865
133. A. Merched, K. Ko, K.H. Gotlinger, C.N. Serhan, and L. Chan Atherosclerosis: evidence for impairment of resolution of vascular inflammation governed by specific lipid mediators FASEB J. 22 2008 3595 3606
134. N. Chiang, M. Shinohara, J. Dalli, V. Mirakaj, M. Kibi, A.M.K. Choi, and C.N. Serhan Inhaled carbon monoxide accelerates resolution of inflammation via unique pro-resolving mediator-heme oxygenase-1 circuits J. Immunol. 190 2013 6378 6388
135. J.M. Calandria, V.L. Marcheselli, P.K. Mukherjee, J. Uddin, J.W. Winkler, N.A. Petasis, and N.G. Bazan Selective survival rescue in 15-lipoxygenase-1-deficient retinal pigment epithelial cells by the novel docosahexaenoic acid-derived mediator, neuroprotectin D1 J. Biol. Chem. 284 2009 17877 17882
136. P. Chen, E. Vericel, M. Lagarde, and M. Guichardant Poxytrins, a class of oxygenated products from polyunsaturated fatty acids, potently inhibit blood platelet aggregation FASEB J. 25 2011 382 388
137. B.D. Levy, P. Kohli, K. Gotlinger, O. Haworth, S. Hong, S. Kazani, E. Israel, K.J. Haley, and C.N. Serhan Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness J. Immunol. 178 2007 496 502
138. O. Koltsida, S. Karamnov, K. Pyrillou, T. Vickery, A.D. Chairakaki, C. Tamvakopoulos, P. Sideras, C.N. Serhan, and E. Andreakos Toll-like receptor 7 stimulates production of specialized pro-resolving lipid mediators and promotes resolution of airway inflammation Mol. Med. 5 2013 762 775
139. J. Miyata, K. Fukunaga, R. Iwamoto, Y. Isobe, K. Niimi, R. Takamiya, T. Takihara, K. Tomomatsu, Y. Suzuki, T. Oguma, K. Sayama, H. Arai, T. Betsuyaku, M. Arita, and K. Asano Dysregulated synthesis of protectin D1 in eosinophils from patients with severe asthma J. Allergy Clin. Immunol. 131 2013 353 360
140. T. Yamada, Y. Tani, H. Nakanishi, R. Taguchi, M. Arita, and H. Arai Eosinophils promote resolution of acute periotonitis by producing proresolving mediators in mice FASEB J. 25 2011 561 568
141. J.S. Duffield, S. Hong, V. Vaidya, Y. Lu, G. Fredman, C.N. Serhan, and J.V. Bonventre Resolvin D series and protectin D1 mitigate acute kidney injury J. Immunol. 177 2006 5902 5911
142. W.J. Lukiw, J.G. Cui, V.L. Marcheselli, M. Bodker, A. Botkjaer, K. Gotlinger, C.N. Serhan, and N.G. Bazan A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease J. Clin. Invest. 115 2005 2774 2783
143. A. González-Périz, A. Planagumà, K. Gronert, R. Miquel, M. López-Parra, E. Titos, R. Horrillo, N. Ferré, R. Deulofeu, V. Arroyo, J. Rodés, and J. Clària Docosahexanenoic acid (DHA) blunts liver injury by conversion to protective lipid mediators: protectin D1 and 17S-hydroxy-DHA FASEB J. 20 2006 2537 2539
144. M.S. Cortina, J. He, T. Russ, N.G. Bazan, and H.E. Bazan Neuroprotectin D1 restores corneal nerve integrity and function after damage from experimental surgery Invest. Ophthalmol. Vis. Sci. 54 2013 4109 4116
145. V.A. Blaho, M.W. Buczynski, C.R. Brown, and E.A. Dennis Lipidomic analysis of dynamic eicosanoid responses during the induction and resolution of Lyme arthritis J. Biol. Chem. 284 2009 21599 21612
146. Q. Qin, K.A. Patil, K. Gronert, and S.C. Sharma Neuroprotectin D1 inhibits retinal ganglion cell death following axotomy Prostaglandins Leukot. Essent. Fat. Acids 79 2008 201 207
147. A. González-Périz, R. Horrillo, N. Ferré, K. Gronert, B. Dong, E. Morán-Salvador, E. Titos, M. Martínez-Clemente, M. López-Parra, V. Arroyo, and J. Clària Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: A role for resolvins and protectins FASEB J. 23 2009 1946 1957
148. Z.Z. Xu, X.J. Liu, T. Berta, C.K. Park, N. Lu, C.N. Serhan, and R.R. Ji Neuroprotectin/protectin D1 protects against neuropathic pain in mice after nerve trauma Ann. Neurol. 74 2013 490 495
149. N.K. Rajasagi, P.B. Reddy, S. Mulik, P. Gjorstrup, and B.T. Rouse Neuroprotectin D1 reduces the severity of herpes simplex virus-induced corneal immunopathology Invest. Ophthalmol. Vis. Sci. 54 2013 6269 6279
150. A.E. Musto, P. Gjorstrup, and N.G. Bazan The omega-3 fatty acid-derived neuroprotectin D1 limits hippocampal hyperexcitability and seizure susceptibility in kindling epileptogenesis Epilepsia 52 2011 1601 1608
151. C.A. Hudert, K.H. Weylandt, J. Wang, Y. Lu, S. Hong, A. Dignass, C.N. Serhan, and J.X. Kang Transgenic mice rich in endogenous n- 3 fatty acids are protected from colitis Proc. Natl. Acad. Sci. U. S. A. 103 2006 11276 11281
152. R. Antony, W.J. Lukiw, and N.G. Bazan Neuroprotectin D1 induces dephosphorylation of Bcl-xL in a PP2A-dependent manner during oxidative stress and promotes retinal pigment epithelial cell survival J. Biol. Chem. 285 2010 18301 18308
153. M. Morita, K. Kuba, A. Ichikawa, M. Nakayama, J. Katahira, R. Iwamoto, T. Watanebe, S. Sakabe, T. Daidoji, S. Nakamura, A. Kadowaki, T. Ohto, H. Nakanishi, R. Taguchi, T. Nakaya, M. Murakami, Y. Yoneda, H. Arai, Y. Kawaoka, J.M. Penninger, M. Arita, and Y. Imai The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza Cell 153 2013 112 125
154. X. Li, C. Li, W. Liang, Y. Bi, M. Chen, and S. Dong Protectin D1 promotes resolution of inflammation in a murine model of lipopolysaccharide-induced acute lung injury via enhancing neutrophil apoptosis Chin. Med. J. 127 2014 810 814
155. N.G. Bazan, T.N. Eady, L. Khoutorova, K.D. Atkins, S. Hong, Y. Lu, C. Zhang, B. Jun, A. Obenaus, G. Fredman, M. Zhu, J.W. Winkler, N.A. Petasis, C.N. Serhan, and L. Belayev Novel aspirin-triggered neuroprotectin D1 attenuates cerebral ischemic injury after experimental stroke Exp. Neurol. 236 2012 122 130
156. R. Marcon, A.F. Bento, R.C. Dutra, M.A. Bicca, D.F. Leite, and J.B. Calixto Maresin 1, a proresolving lipid mediator derived from omega-3 polyunsaturated fatty acids, exerts protective actions in murine models of colitis J. Immunol. 191 2013 4288 4298
157. Y. Li, J. Dalli, N. Chiang, R.M. Baron, C. Quintana, and C.N. Serhan Plasticity of leukocytic exudates in resolving acute inflammation is regulated by microRNA and proresolving mediators Immunity 39 2013 885 898
158. T.M. Nordgren, A.J. Heires, T.A. Wyatt, J.A. Poole, T.D. Levan, D.R. Cerutis, and D.J. Romberger Maresin-1 reduces the pro-inflammatory response of bronchial epithelial cells to organic dust Respir. Res. 14 2013 51
159. B. Biteman, I.R. Hassan, E. Walker, A.J. Leedom, M. Dunn, F. Seta, M. Laniado-Schwartzman, and K. Gronert Interdependence of lipoxin A4 and heme-oxygenase in counter-regulating inflammation during corneal wound healing FASEB J. 21 2007 2257 2266
160. G. Kronke, J. Katzenbeisser, S. Uderhardt, M.M. Zaiss, C. Scholtysek, G. Schabbauer, A. Zarbock, M.I. Koenders, R. Axmann, J. Zwerina, H.W. Baenckler, W. van den Berg, R.E. Voll, H. Kuhn, L.A. Joosten, and G. Schett 12/15-lipoxygenase counteracts inflammation and tissue damage in arthritis J. Immunol. 183 2009 3383 3389
161. M.M.-Y. Chan, and A.R. Moore Resolution of inflammation in murine autoimmune arthritis is disrupted by cyclooxygenase-2 inhibition and restored by prostaglandin E2-mediated lipoxin A4 production J. Immunol. 184 2010 6418 6426
162. A.J. Leedom, A.B. Sullivan, B. Dong, D. Lau, and K. Gronert Endogenous LXA4 circuits are determinants of pathological angiogenesis in response to chronic injury Am. J. Pathol. 176 2010 74-84
163. G. Kronke, N. Reich, C. Scholtysek, A. Akhmetshina, S. Uderhardt, P. Zerr, K. Palumbo, V. Lang, C. Dees, O. Distler, G. Schett, and J.H. Distler The 12/15-lipoxygenase pathway counteracts fibroblast activation and experimental fibrosis Ann. Rheum. Dis. 71 2012 1081 1087
164. K. Tomio, K. Kawana, A. Taguchi, Y. Isobe, R. Iwamoto, A. Yamashita, S. Kojima, M. Mori, T. Nagamatsu, T. Arimoto, K. Oda, Y. Osuga, Y. Taketani, J.X. Kang, H. Arai, M. Arita, S. Kozuma, and T. Fujii Omega-3 polyunsaturated fatty acids suppress the cystic lesion formation of peritoneal endometriosis in transgenic mouse models PLoS One 8 2013 e73085