Resolution of acute inflammation and the role of resolvins in immunity, thrombosis, and vascular biology

Circulation Research

Volumn 119, Issue 1, 2016, Pages 113-130

  Sansbury, Brian E ^a   Spite, Matthew ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

cardiovascular diseases; fatty acids, omega 3; homeostasis; inflammation; lipids

Indexed keywords

AGENTS AFFECTING LIPID METABOLISM; C REACTIVE PROTEIN; CHEMOKINE; CYCLOOXYGENASE 2; ICOSAPENTAENOIC ACID; LEUKOTRIENE B4; MONOCYTE CHEMOTACTIC PROTEIN; NITRIC OXIDE; OMEGA 3 FATTY ACID; PEPTIDOLEUKOTRIENE; PROSTACYCLIN; PROSTAGLANDIN; RESOLVIN; RESOLVIN E1; THROMBOXANE; UNCLASSIFIED DRUG; ANTIINFLAMMATORY AGENT; CARDIOVASCULAR AGENT; DOCOSAHEXAENOIC ACID;

APOPTOSIS; ATHEROSCLEROSIS; BLOOD VESSEL INJURY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR INFLAMMATION; CHRONIC DISEASE; ENDOTHELIUM CELL; HOMEOSTASIS; HOST RESISTANCE; HUMAN; IMMUNITY; INFLAMMATION; LEUKOCYTE MIGRATION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; REVIEW; THROMBOSIS; TISSUE REPAIR; TRANSENDOTHELIAL AND TRANSEPITHELIAL MIGRATION; VASCULAR BIOLOGY; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CARDIOVASCULAR DISEASES; LIPID METABOLISM; METABOLISM;

ANIMALS; ANTI-INFLAMMATORY AGENTS; CARDIOVASCULAR AGENTS; CARDIOVASCULAR DISEASES; DOCOSAHEXAENOIC ACIDS; HUMANS; LIPID METABOLISM; THROMBOSIS;

EID: 84975796992     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.116.307308     Document Type: Review

References (181)

1. Libby P, Nahrendorf M, Swirski FK, Leukocytes link local and systemic inflammation in ischemic cardiovascular disease: An expanded "cardiovascular continuum". J Am Coll Cardiol 2016 67 1091 1103. doi: 10.1016/j.jacc.2015.12.048
2. Libby P, Bornfeldt KE, Tall AR, Atherosclerosis: successes, surprises, and future challenges. Circ Res 2016 118 531 534. doi: 10.1161/CIRCRESAHA.116.308334
3. Libby P, Tabas I, Fredman G, Fisher EA, Inflammation and its resolution as determinants of acute coronary syndromes. Circ Res 2014 114 1867 1879. doi: 10.1161/CIRCRESAHA.114.302699
4. Shapiro MD, Fazio S, From lipids to inflammation: new approaches to reducing atherosclerotic risk. Circ Res 2016 118 732 749. doi: 10.1161/CIRCRESAHA.115.306471
5. Ridker PM, From C-reactive protein to interleukin-6 to interleukin-1: moving upstream to identify novel targets for atheroprotection. Circ Res 2016 118 145 156. doi: 10.1161/CIRCRESAHA.115.306656
6. Ridker PM, Testing the inflammatory hypothesis of atherothrombosis: scientific rationale for the cardiovascular inflammation reduction trial (CIRT). J Thromb Haemost 2009 7 suppl 1 332 339. doi: 10.1111/j.1538-7836.2009.03404.x
7. Everett BM, Pradhan AD, Solomon DH, Paynter N, Macfadyen J, Zaharris E, Gupta M, Clearfield M, Libby P, Hasan AA, Glynn RJ, Ridker PM, Rationale and design of the Cardiovascular Inflammation Reduction Trial: A test of the inflammatory hypothesis of atherothrombosis. Am Heart J 2013 166 199 207.e15. doi: 10.1016/j.ahj.2013.03.018
8. Ridker PM, Howard CP, Walter V, Everett B, Libby P, Hensen J, Thuren T, CANTOS Pilot Investigative Group Effects of interleukin-1β inhibition with canakinumab on hemoglobin A1c, lipids, C-reactive protein, interleukin-6, and fibrinogen: A phase IIb randomized, placebo-controlled trial. Circulation 2012 126 2739 2748. doi: 10.1161/CIRCULATIONAHA.112.122556
9. Serhan CN, Pro-resolving lipid mediators are leads for resolution physiology. Nature 2014 510 92 101. doi: 10.1038/nature13479
10. Serhan CN, Brain SD, Buckley CD, Gilroy DW, Haslett C, O'Neill LA, Perretti M, Rossi AG, Wallace JL, Resolution of inflammation: state of the art, definitions and terms. FASEB J 2007 21 325 332. doi: 10.1096/fj.06-7227rev
11. Gimbrone MA Jr, García-Cardeña G, Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ Res 2016 118 620 636. doi: 10.1161/CIRCRESAHA.115.306301
12. Kolaczkowska E, Kubes P, Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 2013 13 159 175. doi: 10.1038/nri3399
13. Granger DN, Rodrigues SF, Yildirim A, Senchenkova EY, Microvascular responses to cardiovascular risk factors. Microcirculation 2010 17 192 205. doi: 10.1111/j.1549-8719.2009.00015.x
14. Buckley CD, Gilroy DW, Serhan CN, Proresolving lipid mediators and mechanisms in the resolution of acute inflammation. Immunity 2014 40 315 327. doi: 10.1016/j.immuni.2014.02.009
15. Poon IK, Lucas CD, Rossi AG, Ravichandran KS, Apoptotic cell clearance: basic biology and therapeutic potential. Nat Rev Immunol 2014 14 166 180. doi: 10.1038/nri3607
16. Murray PJ, Allen JE, Biswas SK, Macrophage activation and polarization: nomenclature and experimental guidelines. Immunity 2014 41 14 20. doi: 10.1016/j.immuni.2014.06.008
17. Frangogiannis NG, Inflammation in cardiac injury, repair and regeneration. Curr Opin Cardiol 2015 30 240 245. doi: 10.1097/HCO.0000000000000158
18. Cohen HB, Mosser DM, Extrinsic and intrinsic control of macrophage inflammatory responses. J Leukoc Biol 2013 94 913 919. doi: 10.1189/jlb.0413236
19. Fullerton JN, Gilroy DW, Resolution of inflammation: A new therapeutic frontier [published online March 29, 2016]. Nat Rev Drug Discov. doi: 10.1038/nrd.2016.39. http://www.nature.com/nrd/journal/vaop/ncurrent/full/nrd.2016.39.html
20. Kupper TS, Fuhlbrigge RC, Immune surveillance in the skin: mechanisms and clinical consequences. Nat Rev Immunol 2004 4 211 222. doi: 10.1038/nri1310
21. Li S, Sun Y, Liang CP, Defective phagocytosis of apoptotic cells by macrophages in atherosclerotic lesions of ob/ob mice and reversal by a fish oil diet. Circ Res 2009 105 1072 1082. doi: 10.1161/CIRCRESAHA.109.199570
22. Tabas I, Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 2010 10 36 46. doi: 10.1038/nri2675
23. Hansson GK, Libby P, The immune response in atherosclerosis: A double-edged sword. Nat Rev Immunol 2006 6 508 519. doi: 10.1038/nri1882
24. Perretti M, The resolution of inflammation: new mechanisms in patho-physiology open opportunities for pharmacology. Semin Immunol 2015 27 145 148. doi: 10.1016/j.smim.2015.06.001
25. Serhan CN, Chiang N, Dalli J, The resolution code of acute inflammation: Novel pro-resolving lipid mediators in resolution. Semin Immunol 2015 27 200 215. doi: 10.1016/j.smim.2015.03.004
26. Headland SE, Norling LV, The resolution of inflammation: principles and challenges. Semin Immunol 2015 27 149 160. doi: 10.1016/j.smim.2015.03.014
27. Gilroy D, De Maeyer R, New insights into the resolution of inflammation. Semin Immunol 2015 27 161 168. doi: 10.1016/j.smim.2015.05.003
28. Crean D, Godson C, Specialised lipid mediators and their targets. Semin Immunol 2015 27 169 176. doi: 10.1016/j.smim.2015.05.002
29. Colgan SP, Neutrophils and inflammatory resolution in the mucosa. Semin Immunol 2015 27 177 183. doi: 10.1016/j.smim.2015.03.007
30. Viola J, Soehnlein O, Atherosclerosis-A matter of unresolved inflammation. Semin Immunol 2015 27 184 193. doi: 10.1016/j.smim.2015.03.013
31. Haworth O, Buckley CD, Pathways involved in the resolution of inflammatory joint disease. Semin Immunol 2015 27 194 199. doi: 10.1016/j.smim.2015.04.002
32. Montero-Melendez T, ACTH: the forgotten therapy. Semin Immunol 2015 27 216 226. doi: 10.1016/j.smim.2015.02.003
33. Wallace JL, Ianaro A, Flannigan KL, Cirino G, Gaseous mediators in resolution of inflammation. Semin Immunol 2015 27 227 233. doi: 10.1016/j.smim.2015.05.004
34. Nathan C, Ding A, Nonresolving inflammation. Cell 2010 140 871 882. doi: 10.1016/j.cell.2010.02.029
35. Serhan CN, Savill J, Resolution of inflammation: the beginning programs the end. Nat Immunol 2005 6 1191 1197. doi: 10.1038/ni1276
36. Ariel A, Fredman G, Sun YP, Kantarci A, Van Dyke TE, Luster AD, Serhan CN, Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol 2006 7 1209 1216. doi: 10.1038/ni1392
37. Chiang N, Fredman G, Bäckhed F, Oh SF, Vickery T, Schmidt BA, Serhan CN, Infection regulates pro-resolving mediators that lower antibiotic requirements. Nature 2012 484 524 528. doi: 10.1038/nature11042
38. Dalli J, Ramon S, Norris PC, Colas RA, Serhan CN, Novel proresolving and tissue-regenerative resolvin and protectin sulfido-conjugated pathways. FASEB J 2015 29 2120 2136. doi: 10.1096/fj.14-268441
39. Schwab JM, Chiang N, Arita M, Serhan CN, Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007 447 869 874. doi: 10.1038/nature05877
40. Spite M, Norling LV, Summers L, Yang R, Cooper D, Petasis NA, Flower RJ, Perretti M, Serhan CN, Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 2009 461 1287 1291. doi: 10.1038/nature08541
41. El Kebir D, Gjorstrup P, Filep JG, Resolvin E1 promotes phagocytosis-induced neutrophil apoptosis and accelerates resolution of pulmonary inflammation. Proc Natl Acad Sci U S A 2012 109 14983 14988. doi: 10.1073/pnas.1206641109
42. Levy BD, Clish CB, Schmidt B, Gronert K, Serhan CN, Lipid mediator class switching during acute inflammation: signals in resolution. Nat Immunol 2001 2 612 619. doi: 10.1038/89759
43. Serhan CN, Hamberg M, Samuelsson B, Lipoxins: novel series of biologically active compounds formed from arachidonic acid in human leukocytes. Proc Natl Acad Sci U S A 1984 81 5335 5339
44. Serhan CN, Clish CB, Brannon J, Colgan SP, Chiang N, Gronert K, 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 2000 192 1197 1204
45. Serhan CN, Hong S, Gronert K, Colgan SP, Devchand PR, Mirick G, Moussignac RL, Resolvins: A family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J Exp Med 2002 196 1025 1037
46. Serhan CN, Yang R, Martinod K, Kasuga K, Pillai PS, Porter TF, Oh SF, Spite M, Maresins: novel macrophage mediators with potent antiinflammatory and proresolving actions. J Exp Med 2009 206 15 23. doi: 10.1084/jem.20081880
47. Hong S, Gronert K, Devchand PR, Moussignac RL, Serhan CN, Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem 2003 278 14677 14687. doi: 10.1074/jbc.M300218200
48. Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, Yang R, Petasis NA, Serhan CN, Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 2005 201 713 722. doi: 10.1084/jem.20042031
49. Oh SF, Pillai PS, Recchiuti A, Yang R, Serhan CN, Pro-resolving actions and stereoselective biosynthesis of 18S E-series resolvins in human leukocytes and murine inflammation. J Clin Invest 2011 121 569 581. doi: 10.1172/JCI42545
50. Tjonahen E, Oh SF, Siegelman J, Elangovan S, Percarpio KB, Hong S, Arita M, Serhan CN, Resolvin E2: identification and anti-inflammatory actions: pivotal role of human 5-lipoxygenase in resolvin E series biosynthesis. Chem Biol 2006 13 1193 1202. doi: 10.1016/j.chembiol.2006.09.011
51. Oh SF, Dona M, Fredman G, Krishnamoorthy S, Irimia D, Serhan CN, Resolvin E2 formation and impact in inflammation resolution. J Immunol 2012 188 4527 4534. doi: 10.4049/jimmunol.1103652
52. Isobe Y, Arita M, Matsueda S, Iwamoto R, Fujihara T, Nakanishi H, Taguchi R, Masuda K, Sasaki K, Urabe D, Inoue M, Arai H, Identification and structure determination of novel anti-inflammatory mediator resolvin E3, 17,18-dihydroxyeicosapentaenoic acid. J Biol Chem 2012 287 10525 10534. doi: 10.1074/jbc.M112.340612
53. Sun YP, Oh SF, Uddin J, Yang R, Gotlinger K, Campbell E, Colgan SP, Petasis NA, Serhan CN, Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 2007 282 9323 9334. doi: 10.1074/jbc.M609212200
54. Dalli J, Winkler JW, Colas RA, Arnardottir H, Cheng CY, Chiang N, Petasis NA, Serhan CN, Resolvin D3 and aspirin-triggered resolvin D3 are potent immunoresolvents. Chem Biol 2013 20 188 201. doi: 10.1016/j.chembiol.2012.11.010
55. Winkler JW, Orr SK, Dalli J, Cheng CY, Sanger JM, Chiang N, Petasis NA, Serhan CN, Resolvin D4 stereoassignment and its novel actions in host protection and bacterial clearance. Sci Rep 2016 6 18972. doi: 10.1038/srep18972
56. Fredman G, Ozcan L, Spolitu S, Hellmann J, Spite M, Backs J, Tabas I, Resolvin D1 limits 5-lipoxygenase nuclear localization and leukotriene B4 synthesis by inhibiting a calcium-Activated kinase pathway. Proc Natl Acad Sci U S A 2014 111 14530 14535. doi: 10.1073/pnas.1410851111
57. Dalli J, Chiang N, Serhan CN, Identification of 14-series sulfido-conjugated mediators that promote resolution of infection and organ protection. Proc Natl Acad Sci U S A 2014 111 E4753 E4761. doi: 10.1073/pnas.1415006111
58. Krishnamoorthy S, Recchiuti A, Chiang N, Yacoubian S, Lee CH, Yang R, Petasis NA, Serhan CN, Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci U S A 2010 107 1660 1665. doi: 10.1073/pnas.0907342107
59. Norling LV, Dalli J, Flower RJ, Serhan CN, Perretti M, Resolvin D1 limits polymorphonuclear leukocyte recruitment to inflammatory loci: receptor-dependent actions. Arterioscler Thromb Vasc Biol 2012 32 1970 1978. doi: 10.1161/ATVBAHA.112.249508
60. Devchand PR, Arita M, Hong S, Bannenberg G, Moussignac RL, Gronert K, Serhan CN, Human ALX receptor regulates neutrophil recruitment in transgenic mice: roles in inflammation and host defense. FASEB J 2003 17 652 659. doi: 10.1096/fj.02-0770com
61. Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, Parmentier M, Serhan CN, Murphy PM, International union of basic and clinical pharmacology. LXXIII. Nomenclature for the formyl peptide receptor (FPR) family. Pharmacol Rev 2009 61 119 161. doi: 10.1124/pr.109.001578
62. Cooray SN, Gobbetti T, Montero-Melendez T, McArthur S, Thompson D, Clark AJ, Flower RJ, Perretti M, Ligand-specific conformational change of the G-protein-coupled receptor ALX/FPR2 determines proresolving functional responses. Proc Natl Acad Sci U S A 2013 110 18232 18237. doi: 10.1073/pnas.1308253110
63. El Kebir D, József L, Khreiss T, Pan W, Petasis NA, Serhan CN, Filep JG, Aspirin-triggered lipoxins override the apoptosis-delaying action of serum amyloid A in human neutrophils: A novel mechanism for resolution of inflammation. J Immunol 2007 179 616 622
64. Cash JL, Hart R, Russ A, Dixon JP, Colledge WH, Doran J, Hendrick AG, Carlton MB, Greaves DR, Synthetic chemerin-derived peptides suppress inflammation through ChemR23. J Exp Med 2008 205 767 775. doi: 10.1084/jem.20071601
65. Ohira T, Arita M, Omori K, Recchiuti A, Van Dyke TE, Serhan CN, Resolvin E1 receptor activation signals phosphorylation and phagocytosis. J Biol Chem 2010 285 3451 3461. doi: 10.1074/jbc.M109.044131
66. Arita M, Ohira T, Sun YP, Elangovan S, Chiang N, Serhan CN, Resolvin E1 selectively interacts with leukotriene B4 receptor BLT1 and ChemR23 to regulate inflammation. J Immunol 2007 178 3912 3917
67. Chiang N, Dalli J, Colas RA, Serhan CN, Identification of resolvin D2 receptor mediating resolution of infections and organ protection. J Exp Med 2015 212 1203 1217. doi: 10.1084/jem.20150225
68. Hudert CA, Weylandt KH, Lu Y, Wang J, Hong S, Dignass A, Serhan CN, Kang JX, Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc Natl Acad Sci U S A 2006 103 11276 11281. doi: 10.1073/pnas.0601280103
69. Connor KM, SanGiovanni JP, Lofqvist C, Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 2007 13 868 873. doi: 10.1038/nm1591
70. Calder PC, Marine omega-3 fatty acids and inflammatory processes: Effects, mechanisms and clinical relevance. Biochim Biophys Acta 2015 1851 469 484. doi: 10.1016/j.bbalip.2014.08.010
71. De Caterina R, n-3 fatty acids in cardiovascular disease. N Engl J Med 2011 364 2439 2450. doi: 10.1056/NEJMra1008153
72. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. GISSI-Prevenzione Investigators (Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico). Lancet 1999 354 447 455
73. Tavazzi L, Maggioni AP, Marchioli R, Barlera S, Franzosi MG, Latini R, Lucci D, Nicolosi GL, Porcu M, Tognoni G, Gissi-HF Investigators Effect of n-3 polyunsaturated fatty acids in patients with chronic heart failure (the GISSI-HF trial): A randomised, double-blind, placebo-controlled trial. Lancet 2008 372 1223 1230. doi: 10.1016/S0140-6736(08)61239-8
74. Colas RA, Shinohara M, Dalli J, Chiang N, Serhan CN, Identification and signature profiles for pro-resolving and inflammatory lipid mediators in human tissue. Am J Physiol Cell Physiol 2014 307 C39 C54. doi: 10.1152/ajpcell.00024.2014
75. Barden A, Mas E, Croft KD, Phillips M, Mori TA, Short-term n-3 fatty acid supplementation but not aspirin increases plasma proresolving mediators of inflammation. J Lipid Res 2014 55 2401 2407. doi: 10.1194/jlr.M045583
76. Mas E, Croft KD, Zahra P, Barden A, Mori TA, Resolvins D1, D2, and other mediators of self-limited resolution of inflammation in human blood following n-3 fatty acid supplementation. Clin Chem 2012 58 1476 1484. doi: 10.1373/clinchem.2012.190199
77. Barden AE, Mas E, Mori TA, n-3 Fatty acid supplementation and proresolving mediators of inflammation. Curr Opin Lipidol 2016 27 26 32. doi: 10.1097/MOL.0000000000000262
78. Grenon SM, Owens CD, Nosova EV, Hughes-Fulford M, Alley HF, Chong K, Perez S, Yen PK, Boscardin J, Hellmann J, Spite M, Conte MS, Short-term, high-dose fish oil supplementation increases the production of Omega-3 Fatty Acid-Derived Mediators in Patients With Peripheral Artery Disease (the OMEGA-PAD I Trial). J Am Heart Assoc 2015 4 e002034. doi: 10.1161/JAHA.115.002034
79. Barden AE, Moghaddami M, Mas E, Phillips M, Cleland LG, Mori TA, Specialised pro-resolving mediators of inflammation in inflammatory arthritis. Prostaglandins Leukot Essent Fatty Acids 2016 107 24 29. doi: 10.1016/j.plefa.2016.03.004
80. Elajami TK, Colas RA, Dalli J, Chiang N, Serhan CN, Welty FK, Specialized proresolving lipid mediators in patients with coronary artery disease and their potential for clot remodeling [published online ahead of print April 27, 2016]. FASEB J. doi: 10.1096/fj.201500155R. http://www.fasebj.org/content/early/2016/04/27/fj.201500155R.long
81. Spite M, Clària J, Serhan CN, Resolvins, specialized proresolving lipid mediators, and their potential roles in metabolic diseases. Cell Metab 2014 19 21 36. doi: 10.1016/j.cmet.2013.10.006
82. Roberts LJ 2nd, Montine TJ, Markesbery WR, Tapper AR, Hardy P, Chemtob S, Dettbarn WD, Morrow JD, Formation of isoprostane-like compounds (neuroprostanes) in vivo from docosahexaenoic acid. J Biol Chem 1998 273 13605 13612
83. Arnardottir H, Orr SK, Dalli J, Serhan CN, Human milk proresolving mediators stimulate resolution of acute inflammation. Mucosal Immunol 2016 9 757 766. doi: 10.1038/mi.2015.99
84. Sasaki A, Fukuda H, Shiida N, Tanaka N, Furugen A, Ogura J, Shuto S, Mano N, Yamaguchi H, Determination of ω-6 and ω-3 PUFA metabolites in human urine samples using UPLC/MS/MS. Anal Bioanal Chem 2015 407 1625 1639. doi: 10.1007/s00216-014-8412-5
85. Murphy RC, Specialized pro-resolving mediators: do they circulate in plasma? J Lipid Res 2015 56 1641 1642. doi: 10.1194/jlr.C062356
86. Marchioli R, Schweiger C, Tavazzi L, Valagussa F, Efficacy of n-3 polyunsaturated fatty acids after myocardial infarction: results of GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico. Lipids 2001 36 Suppl S119 S126
87. Vane JR, Botting RM, The mechanism of action of aspirin. Thromb Res 2003 110 255 258
88. Clària J, Serhan CN, Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci U S A 1995 92 9475 9479
89. Demetz E, Schroll A, Auer K, The arachidonic acid metabolome serves as a conserved regulator of cholesterol metabolism. Cell Metab 2014 20 787 798. doi: 10.1016/j.cmet.2014.09.004
90. Ridker PM, Danielson E, Fonseca FA, Genest J, Gotto AM Jr, Kastelein JJ, Koenig W, Libby P, Lorenzatti AJ, MacFadyen JG, Nordestgaard BG, Shepherd J, Willerson JT, Glynn RJ, JUPITER Study Group Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med 2008 359 2195 2207. doi: 10.1056/NEJMoa0807646
91. Birnbaum Y, Ye Y, Lin Y, Freeberg SY, Nishi SP, Martinez JD, Huang MH, Uretsky BF, Perez-Polo JR, Augmentation of myocardial production of 15-epi-lipoxin-A4 by pioglitazone and atorvastatin in the rat. Circulation 2006 114 929 935. doi: 10.1161/CIRCULATIONAHA.106.629907
92. Planagumà A, Pfeffer MA, Rubin G, Croze R, Uddin M, Serhan CN, Levy BD, Lovastatin decreases acute mucosal inflammation via 15-epi-lipoxin A4. Mucosal Immunol 2010 3 270 279. doi: 10.1038/mi.2009.141
93. Dalli J, Chiang N, Serhan CN, Elucidation of novel 13-series resolvins that increase with atorvastatin and clear infections. Nat Med 2015 21 1071 1075. doi: 10.1038/nm.3911
94. Gilroy DW, Colville-Nash PR, Willis D, Chivers J, Paul-Clark MJ, Willoughby DA, Inducible cyclooxygenase may have anti-inflammatory properties. Nat Med 1999 5 698 701. doi: 10.1038/9550
95. Scapini P, Cassatella MA, Social networking of human neutrophils within the immune system. Blood 2014 124 710 719. doi: 10.1182/blood-2014-03-453217
96. Jones HR, Robb CT, Perretti M, Rossi AG, The role of neutrophils in inflammation resolution. Semin Immunol 2016 28 137 145. doi: 10.1016/j.smim.2016.03.007
97. Fierro IM, Colgan SP, Bernasconi G, Petasis NA, Clish CB, Arita M, Serhan CN, Lipoxin A4 and aspirin-triggered 15-epi-lipoxin A4 inhibit human neutrophil migration: comparisons between synthetic 15 epimers in chemotaxis and transmigration with microvessel endothelial cells and epithelial cells. J Immunol 2003 170 2688 2694
98. Godson C, Mitchell S, Harvey K, Petasis NA, Hogg N, Brady HR, Cutting edge: lipoxins rapidly stimulate nonphlogistic phagocytosis of apoptotic neutrophils by monocyte-derived macrophages. J Immunol 2000 164 1663 1667
99. Dalli J, Serhan CN, Specific lipid mediator signatures of human phagocytes: microparticles stimulate macrophage efferocytosis and pro-resolving mediators. Blood 2012 120 e60 e72. doi: 10.1182/blood-2012-04-423525
100. Dona M, Fredman G, Schwab JM, Chiang N, Arita M, Goodarzi A, Cheng G, von Andrian UH, Serhan CN, Resolvin E1, an EPA-derived mediator in whole blood, selectively counterregulates leukocytes and platelets. Blood 2008 112 848 855. doi: 10.1182/blood-2007-11-122598
101. Swirski FK, Nahrendorf M, Leukocyte behavior in atherosclerosis, myocardial infarction, and heart failure. Science 2013 339 161 166. doi: 10.1126/science.1230719
102. Kain V, Ingle KA, Colas RA, Dalli J, Prabhu SD, Serhan CN, Joshi M, Halade GV, Resolvin D1 activates the inflammation resolving response at splenic and ventricular site following myocardial infarction leading to improved ventricular function. J Mol Cell Cardiol 2015 84 24 35. doi: 10.1016/j.yjmcc.2015.04.003
103. Keyes KT, Ye Y, Lin Y, Zhang C, Perez-Polo JR, Gjorstrup P, Birnbaum Y, Resolvin E1 protects the rat heart against reperfusion injury. Am J Physiol Heart Circ Physiol 2010 299 H153 H164. doi: 10.1152/ajpheart.01057.2009
104. Duffield JS, Hong S, Vaidya VS, Lu Y, Fredman G, Serhan CN, Bonventre JV, Resolvin D series and protectin D1 mitigate acute kidney injury. J Immunol 2006 177 5902 5911
105. Kasuga K, Yang R, Porter TF, Agrawal N, Petasis NA, Irimia D, Toner M, Serhan CN, Rapid appearance of resolvin precursors in inflammatory exudates: novel mechanisms in resolution. J Immunol 2008 181 8677 8687
106. Dufton N, Hannon R, Brancaleone V, Dalli J, Patel HB, Gray M, D'Acquisto F, Buckingham JC, Perretti M, Flower RJ, Anti-inflammatory role of the murine formyl-peptide receptor 2: ligand-specific effects on leukocyte responses and experimental inflammation. J Immunol 2010 184 2611 2619. doi: 10.4049/jimmunol.0903526
107. Horckmans M, Ring L, Duchene J, Santovito D, Schloss MJ, Drechsler M, Weber C, Soehnlein O, Steffens S, Neutrophils orchestrate post-myocardial infarction healing by polarizing macrophages towards a reparative phenotype [published online ahead of print February 2, 2016]. Eur Heart J. doi:10.1093/eurheartj/ehw002. http://eurheartj.oxfordjournals.org/content/early/2016/02/01/eurheartj.ehw002
108. Gao Y, Min K, Zhang Y, Su J, Greenwood M, Gronert K, Female-specific downregulation of tissue polymorphonuclear neutrophils drives impaired regulatory T cell and amplified effector T cell responses in autoimmune dry eye disease. J Immunol 2015 195 3086 3099. doi: 10.4049/jimmunol.1500610
109. Döring Y, Drechsler M, Soehnlein O, Weber C, Neutrophils in atherosclerosis: from mice to man. Arterioscler Thromb Vasc Biol 2015 35 288 295. doi: 10.1161/ATVBAHA.114.303564
110. Weber C, Zernecke A, Libby P, The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Immunol 2008 8 802 815. doi: 10.1038/nri2415
111. Drechsler M, Megens RT, Van Zandvoort M, Weber C, Soehnlein O, Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation 2010 122 1837 1845. doi: 10.1161/CIRCULATIONAHA.110.961714
112. Döring Y, Drechsler M, Wantha S, Kemmerich K, Lievens D, Vijayan S, Gallo RL, Weber C, Soehnlein O, Lack of neutrophil-derived CRAMP reduces atherosclerosis in mice. Circ Res 2012 110 1052 1056. doi: 10.1161/CIRCRESAHA.112.265868
113. Nagareddy PR, Murphy AJ, Stirzaker RA, Hu Y, Yu S, Miller RG, Ramkhelawon B, Distel E, Westerterp M, Huang LS, Schmidt AM, Orchard TJ, Fisher EA, Tall AR, Goldberg IJ, Hyperglycemia promotes myelopoiesis and impairs the resolution of atherosclerosis. Cell Metab 2013 17 695 708. doi: 10.1016/j.cmet.2013.04.001
114. Warnatsch A, Ioannou M, Wang Q, Papayannopoulos V, Inflammation. Neutrophil extracellular traps license macrophages for cytokine production in atherosclerosis. Science 2015 349 316 320. doi: 10.1126/science.aaa8064
115. Subbarao K, Jala VR, Mathis S, Suttles J, Zacharias W, Ahamed J, Ali H, Tseng MT, Haribabu B, Role of leukotriene B4 receptors in the development of atherosclerosis: potential mechanisms. Arterioscler Thromb Vasc Biol 2004 24 369 375. doi: 10.1161/01.ATV.0000110503.16605.15
116. Mehrabian M, Allayee H, Wong J, Shi W, Wang XP, Shaposhnik Z, Funk CD, Lusis AJ, Shih W, Identification of 5-lipoxygenase as a major gene contributing to atherosclerosis susceptibility in mice. Circ Res 2002 91 120 126
117. Davé S, Van Dyke T, The link between periodontal disease and cardiovascular disease is probably inflammation. Oral Dis 2008 14 95 101. doi: 10.1111/j.1601-0825.2007.01438.x
118. Hasturk H, Abdallah R, Kantarci A, Nguyen D, Giordano N, Hamilton J, Van Dyke TE, Resolvin E1 (RvE1) attenuates atherosclerotic plaque formation in diet and inflammation-induced atherogenesis. Arterioscler Thromb Vasc Biol 2015 35 1123 1133. doi: 10.1161/ATVBAHA.115.305324
119. Abdulnour RE, Dalli J, Colby JK, Krishnamoorthy N, Timmons JY, Tan SH, Colas RA, Petasis NA, Serhan CN, Levy BD, Maresin 1 biosynthesis during platelet-neutrophil interactions is organ-protective. Proc Natl Acad Sci U S A 2014 111 16526 16531. doi: 10.1073/pnas.1407123111
120. Norris PC, Arnardottir H, Sanger JM, Fichtner D, Keyes GS, Serhan CN, Resolvin D3 multi-level proresolving actions are host protective during infection [published online ahead of print January 21, 2016]. Prostaglandins Leukot Essent Fatty Acids. doi: 10.1016/j.plefa.2016.01.001. http://www.plefa.com/article/S0952-3278(15)30052-1/abstract
121. Gerdes N, Seijkens T, Lievens D, Kuijpers MJ, Winkels H, Projahn D, Hartwig H, Beckers L, Megens RT, Boon L, Noelle RJ, Soehnlein O, Heemskerk JW, Weber C, Lutgens E, Platelet CD40 exacerbates atherosclerosis by transcellular activation of endothelial cells and leukocytes. Arterioscler Thromb Vasc Biol 2016 36 482 490. doi: 10.1161/ATVBAHA.115.307074
122. Maderna P, Cottell DC, Toivonen T, Dufton N, Dalli J, Perretti M, Godson C, FPR2/ALX receptor expression and internalization are critical for lipoxin A4 and annexin-derived peptide-stimulated phagocytosis. FASEB J 2010 24 4240 4249. doi: 10.1096/fj.10-159913
123. Maderna P, Cottell DC, Berlasconi G, Petasis NA, Brady HR, Godson C, Lipoxins induce actin reorganization in monocytes and macrophages but not in neutrophils: differential involvement of rho GTPases. Am J Pathol 2002 160 2275 2283. doi: 10.1016/S0002-9440(10)61175-3
124. Reville K, Crean JK, Vivers S, Dransfield I, Godson C, Lipoxin A4 redistributes myosin IIA and Cdc42 in macrophages: implications for phagocytosis of apoptotic leukocytes. J Immunol 2006 176 1878 1888
125. Tang Y, Zhang MJ, Hellmann J, Kosuri M, Bhatnagar A, Spite M, Proresolution therapy for the treatment of delayed healing of diabetic wounds. Diabetes 2013 62 618 627. doi: 10.2337/db12-0684
126. Khanna S, Biswas S, Shang Y, Collard E, Azad A, Kauh C, Bhasker V, Gordillo GM, Sen CK, Roy S, Macrophage dysfunction impairs resolution of inflammation in the wounds of diabetic mice. PLoS One 2010 5 e9539. doi: 10.1371/journal.pone.0009539
127. Cai B, Thorp EB, Doran AC, Subramanian M, Sansbury BE, Lin C, Spite M, Fredman G, Tabas I, MerTK cleavage limits pro-resolving mediator biosynthesis and exacerbates tissue inflammation [published online ahead of print May 19, 2016]. Proc Natl Acad Sci U S A. doi: 10.1073/pnas.1524292113. http://www.pnas.org/content/early/2016/05/18/1524292113.abstract
128. Wan E, Yeap XY, Dehn S, Enhanced efferocytosis of apoptotic cardiomyocytes through myeloid-epithelial-reproductive tyrosine kinase links acute inflammation resolution to cardiac repair after infarction. Circ Res 2013 113 1004 1012. doi: 10.1161/CIRCRESAHA.113.301198
129. Howangyin KY, Zlatanova I, Pinto C, Ngkelo A, Cochain C, Rouanet M, Vilar J, Lemitre M, Stockmann C, Fleischmann BK, Mallat Z, Silvestre JS, Myeloid-epithelial-reproductive receptor tyrosine kinase and milk fat globule epidermal growth factor 8 coordinately improve remodeling after myocardial infarction via local delivery of vascular endothelial growth factor. Circulation 2016 133 826 839. doi: 10.1161/CIRCULATIONAHA.115.020857
130. Tabas I, Bornfeldt KE, Macrophage phenotype and function in different stages of atherosclerosis. Circ Res 2016 118 653 667. doi: 10.1161/CIRCRESAHA.115.306256
131. Lee HN, Surh YJ, Resolvin D1-mediated NOX2 inactivation rescues macrophages undertaking efferocytosis from oxidative stress-induced apoptosis. Biochem Pharmacol 2013 86 759 769. doi: 10.1016/j.bcp.2013.07.002
132. Merched AJ, Ko K, Gotlinger KH, Serhan CN, Chan L, Atherosclerosis: evidence for impairment of resolution of vascular inflammation governed by specific lipid mediators. FASEB J 2008 22 3595 3606. doi: 10.1096/fj.08-112201
133. Shen J, Herderick E, Cornhill JF, Zsigmond E, Kim HS, Kühn H, Guevara NV, Chan L, Macrophage-mediated 15-lipoxygenase expression protects against atherosclerosis development. J Clin Invest 1996 98 2201 2208. doi: 10.1172/JCI119029
134. Wittwer J, Hersberger M, The two faces of the 15-lipoxygenase in atherosclerosis. Prostaglandins Leukot Essent Fatty Acids 2007 77 67 77. doi: 10.1016/j.plefa.2007.08.001
135. Drechsler M, De Jong R, Rossaint J, Viola JR, Leoni G, Wang JM, Grommes J, Hinkel R, Kupatt C, Weber C, Döring Y, Zarbock A, Soehnlein O, Annexin A1 counteracts chemokine-induced arterial myeloid cell recruitment. Circ Res 2015 116 827 835. doi: 10.1161/CIRCRESAHA.116.305825
136. Fredman G, Kamaly N, Spolitu S, Milton J, Ghorpade D, Chiasson R, Kuriakose G, Perretti M, Farokhzad O, Farokzhad O, Tabas I, Targeted nanoparticles containing the proresolving peptide Ac2-26 protect against advanced atherosclerosis in hypercholesterolemic mice. Sci Transl Med 2015 7 275ra20. doi: 10.1126/scitranslmed.aaa1065
137. Hilgendorf I, Gerhardt LM, Tan TC, Winter C, Holderried TA, Chousterman BG, Iwamoto Y, Liao R, Zirlik A, Scherer-Crosbie M, Hedrick CC, Libby P, Nahrendorf M, Weissleder R, Swirski FK, Ly-6Chigh monocytes depend on Nr4a1 to balance both inflammatory and reparative phases in the infarcted myocardium. Circ Res 2014 114 1611 1622. doi: 10.1161/CIRCRESAHA.114.303204
138. Varga T, Mounier R, Horvath A, Cuvellier S, Dumont F, Poliska S, Ardjoune H, Juban G, Nagy L, Chazaud B, Highly dynamic transcriptional signature of distinct macrophage subsets during sterile inflammation, resolution, and tissue repair. J Immunol 2016 196 4771 4782. doi: 10.4049/jimmunol.1502490
139. Sager HB, Heidt T, Hulsmans M, Dutta P, Courties G, Sebas M, Wojtkiewicz GR, Tricot B, Iwamoto Y, Sun Y, Weissleder R, Libby P, Swirski FK, Nahrendorf M, Targeting interleukin-1β reduces leukocyte production after acute myocardial infarction. Circulation 2015 132 1880 1890. doi: 10.1161/CIRCULATIONAHA.115.016160
140. Panizzi P, Swirski FK, Figueiredo JL, Waterman P, Sosnovik DE, Aikawa E, Libby P, Pittet M, Weissleder R, Nahrendorf M, Impaired infarct healing in atherosclerotic mice with Ly-6C(hi) monocytosis. J Am Coll Cardiol 2010 55 1629 1638. doi: 10.1016/j.jacc.2009.08.089
141. Epelman S, Lavine KJ, Beaudin AE, Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 2014 40 91 104. doi: 10.1016/j.immuni.2013.11.019
142. Schmid M, Gemperle C, Rimann N, Hersberger M, Resolvin D1 polarizes primary human macrophages toward a proresolution phenotype through GPR32. J Immunol 2016 196 3429 3437. doi: 10.4049/jimmunol.1501701
143. Titos E, Rius B, González-Périz A, López-Vicario C, Morán-Salvador E, Martínez-Clemente M, Arroyo V, Clària J, Resolvin D1 and its precursor docosahexaenoic acid promote resolution of adipose tissue inflammation by eliciting macrophage polarization toward an M2-like phenotype. J Immunol 2011 187 5408 5418. doi: 10.4049/jimmunol.1100225
144. Hellmann J, Tang Y, Kosuri M, Bhatnagar A, Spite M, Resolvin D1 decreases adipose tissue macrophage accumulation and improves insulin sensitivity in obese-diabetic mice. FASEB J 2011 25 2399 2407. doi: 10.1096/fj.10-178657
145. Schif-Zuck S, Gross N, Assi S, Rostoker R, Serhan CN, Ariel A, Saturated-efferocytosis generates pro-resolving CD11b low macrophages: modulation by resolvins and glucocorticoids. Eur J Immunol 2011 41 366 379. doi: 10.1002/eji.201040801
146. Bystrom J, Evans I, Newson J, Stables M, Toor I, Van Rooijen N, Crawford M, Colville-Nash P, Farrow S, Gilroy DW, Resolution-phase macrophages possess a unique inflammatory phenotype that is controlled by cAMP. Blood 2008 112 4117 4127. doi: 10.1182/blood-2007-12-129767
147. Tian H, Lu Y, Sherwood AM, Hongqian D, Hong S, Resolvins E1 and D1 in choroid-retinal endothelial cells and leukocytes: biosynthesis and mechanisms of anti-inflammatory actions. Invest Ophthalmol Vis Sci 2009 50 3613 3620. doi: 10.1167/iovs.08-3146
148. Chiang N, Arita M, Serhan CN, Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX. Prostaglandins Leukot Essent Fatty Acids 2005 73 163 177. doi: 10.1016/j.plefa.2005.05.003
149. Offertáler L, Mo FM, Bátkai S, Liu J, Begg M, Razdan RK, Martin BR, Bukoski RD, Kunos G, Selective ligands and cellular effectors of a G protein-coupled endothelial cannabinoid receptor. Mol Pharmacol 2003 63 699 705
150. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, Villela CG, Fierro IM, Novel lipid mediator aspirin-triggered lipoxin A4 induces heme oxygenase-1 in endothelial cells. Am J Physiol Cell Physiol 2005 289 C557 C563. doi: 10.1152/ajpcell.00045.2005
151. Souza MC, Pádua TA, Torres ND, Lipoxin A4 attenuates endothelial dysfunction during experimental cerebral malaria. Int Immunopharmacol 2015 24 400 407. doi: 10.1016/j.intimp.2014.12.033
152. Baker N, O'Meara SJ, Scannell M, Maderna P, Godson C, Lipoxin A4: Anti-inflammatory and anti-Angiogenic impact on endothelial cells. J Immunol 2009 182 3819 3826. doi: 10.4049/jimmunol.0803175
153. Brezinski ME, Gimbrone MA Jr, Nicolaou KC, Serhan CN, Lipoxins stimulate prostacyclin generation by human endothelial cells. FEBS Lett 1989 245 167 172
154. Paul-Clark MJ, Van Cao T, Moradi-Bidhendi N, Cooper D, Gilroy DW, 15-epi-lipoxin A4-mediated induction of nitric oxide explains how aspirin inhibits acute inflammation. J Exp Med 2004 200 69 78. doi: 10.1084/jem.20040566
155. Nascimento-Silva V, Arruda MA, Barja-Fidalgo C, Fierro IM, Aspirin-triggered lipoxin A4 blocks reactive oxygen species generation in endothelial cells: A novel antioxidative mechanism. Thromb Haemost 2007 97 88 98
156. Maekawa T, Hosur K, Abe T, Kantarci A, Ziogas A, Wang B, Van Dyke TE, Chavakis T, Hajishengallis G, Antagonistic effects of IL-17 and D-resolvins on endothelial Del-1 expression through a GSK-3β-C/EBPβ pathway. Nat Commun 2015 6 8272. doi: 10.1038/ncomms9272
157. Zhang X, Wang T, Gui P, Yao C, Sun W, Wang L, Wang H, Xie W, Yao S, Lin Y, Wu Q, Resolvin D1 reverts lipopolysaccharide-induced TJ proteins disruption and the increase of cellular permeability by regulating IκBα signaling in human vascular endothelial cells. Oxid Med Cell Longev 2013 2013 185715. doi: 10.1155/2013/185715
158. Eickmeier O, Seki H, Haworth O, Hilberath JN, Gao F, Uddin M, Croze RH, Carlo T, Pfeffer MA, Levy BD, Aspirin-triggered resolvin D1 reduces mucosal inflammation and promotes resolution in a murine model of acute lung injury. Mucosal Immunol 2013 6 256 266. doi: 10.1038/mi.2012.66
159. Takano T, Clish CB, Gronert K, Petasis N, Serhan CN, Neutrophil-mediated changes in vascular permeability are inhibited by topical application of aspirin-triggered 15-epi-lipoxin A4 and novel lipoxin B4 stable analogues. J Clin Invest 1998 101 819 826. doi: 10.1172/JCI1578
160. Jin Y, Arita M, Zhang Q, Saban DR, Chauhan SK, Chiang N, Serhan CN, Dana R, Anti-Angiogenesis effect of the novel anti-inflammatory and pro-resolving lipid mediators. Invest Ophthalmol Vis Sci 2009 50 4743 4752. doi: 10.1167/iovs.08-2462
161. Leedom AJ, Sullivan AB, Dong B, Lau D, Gronert K, Endogenous LXA4 circuits are determinants of pathological angiogenesis in response to chronic injury. Am J Pathol 2010 176 74 84. doi: 10.2353/ajpath.2010.090678
162. Nie D, Tang K, Diglio C, Honn KV, Eicosanoid regulation of angiogenesis: role of endothelial arachidonate 12-lipoxygenase. Blood 2000 95 2304 2311
163. Finetti F, Donnini S, Giachetti A, Morbidelli L, Ziche M, Prostaglandin E(2) primes the angiogenic switch via a synergic interaction with the fibroblast growth factor-2 pathway. Circ Res 2009 105 657 666. doi: 10.1161/CIRCRESAHA.109.203760
164. Bennett MR, Sinha S, Owens GK, Vascular smooth muscle cells in atherosclerosis. Circ Res 2016 118 692 702. doi: 10.1161/CIRCRESAHA.115.306361
165. Ho KJ, Spite M, Owens CD, Lancero H, Kroemer AH, Pande R, Creager MA, Serhan CN, Conte MS, Aspirin-triggered lipoxin and resolvin E1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am J Pathol 2010 177 2116 2123. doi: 10.2353/ajpath.2010.091082
166. 4 signals through FPR2/ALX in vascular smooth muscle cells and protects against intimal hyperplasia after carotid ligation. Int J Cardiol 2015 179 370 372. doi: 10.1016/j.ijcard.2014.11.010
167. Petri MH, Laguna-Fernández A, Gonzalez-Diez M, Paulsson-Berne G, Hansson GK, Bäck M, The role of the FPR2/ALX receptor in atherosclerosis development and plaque stability. Cardiovasc Res 2015 105 65 74. doi: 10.1093/cvr/cvu224
168. Miyahara T, Runge S, Chatterjee A, Chen M, Mottola G, Fitzgerald JM, Serhan CN, Conte MS, D-series resolvin attenuates vascular smooth muscle cell activation and neointimal hyperplasia following vascular injury. FASEB J 2013 27 2220 2232. doi: 10.1096/fj.12-225615
169. Wu B, Mottola G, Chatterjee A, Lance KD, Chen M, Siguenza IO, Desai TA, Conte MS, Perivascular delivery of resolvin D1 inhibits neointimal hyperplasia in a rat model of arterial injury [published online ahead of print March 29, 2016]. J Vasc Surg. doi: 10.1016/j.jvs.2016.01.030. http://www.jvascsurg.org/article/S0741-5214(16)00158-0/abstract
170. Akagi D, Chen M, Toy R, Chatterjee A, Conte MS, Systemic delivery of proresolving lipid mediators resolvin D2 and maresin 1 attenuates intimal hyperplasia in mice. FASEB J 2015 29 2504 2513. doi: 10.1096/fj.14-265363
171. Chatterjee A, Sharma A, Chen M, Toy R, Mottola G, Conte MS, The pro-resolving lipid mediator maresin 1 (MaR1) attenuates inflammatory signaling pathways in vascular smooth muscle and endothelial cells. PLoS One 2014 9 e113480. doi: 10.1371/journal.pone.0113480
172. Hiram R, Rizcallah E, Sirois C, Sirois M, Morin C, Fortin S, Rousseau E, Resolvin D1 reverses reactivity and Ca2+ sensitivity induced by ET-1, TNF-α and IL-6 in the human pulmonary artery. Am J Physiol Heart Circ Physiol 2014 307 H1547 H1558. doi: 10.1152/ajpheart.00452.2014
173. Hiram R, Rizcallah E, Marouan S, Sirois C, Sirois M, Morin C, Fortin S, Rousseau E, Resolvin E1 normalizes contractility, Ca2+ sensitivity and smooth muscle cell migration rate in TNF-α- and IL-6-pretreated human pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 2015 309 L776 L788. doi: 10.1152/ajplung.00177.2015
174. Foley JH, Conway EM, Cross talk pathways between coagulation and inflammation. Circ Res 2016 118 1392 1408. doi: 10.1161/CIRCRESAHA.116.306853
175. Chiang N, Bermudez EA, Ridker PM, Hurwitz S, Serhan CN, Aspirin triggers antiinflammatory 15-epi-lipoxin A4 and inhibits thromboxane in a randomized human trial. Proc Natl Acad Sci U S A 2004 101 15178 15183. doi: 10.1073/pnas.0405445101
176. Chiang N, Hurwitz S, Ridker PM, Serhan CN, Aspirin has a gender-dependent impact on antiinflammatory 15-epi-lipoxin A4 formation: A randomized human trial. Arterioscler Thromb Vasc Biol 2006 26 e14 e17. doi: 10.1161/01.ATV.0000196729.98651.bf
177. Fredman G, Van Dyke TE, Serhan CN, Resolvin E1 regulates adenosine diphosphate activation of human platelets. Arterioscler Thromb Vasc Biol 2010 30 2005 2013. doi: 10.1161/ATVBAHA.110.209908
178. Bohr S, Patel SJ, Sarin D, Irimia D, Yarmush ML, Berthiaume F, Resolvin D2 prevents secondary thrombosis and necrosis in a mouse burn wound model. Wound Repair Regen 2013 21 35 43. doi: 10.1111/j.1524-475X.2012.00853.x
179. Morita M, Kuba K, Ichikawa A, The lipid mediator protectin D1 inhibits influenza virus replication and improves severe influenza. Cell 2013 153 112 125. doi: 10.1016/j.cell.2013.02.027
180. Auven Therapeutics. http://www.auventherapeutics.com/auven/products/RX10045.php
181. Norling LV, Spite M, Yang R, Flower RJ, Perretti M, Serhan CN, Cutting edge: Humanized nano-proresolving medicines mimic inflammation-resolution and enhance wound healing. J Immunol 2011 186 5543 5547. doi: 10.4049/jimmunol.1003865