Omega-3 fatty acids and their lipid mediators: Towards an understanding of resolvin and protectin formation. Omega-3 fatty acids and their resolvin/protectin mediators

Prostaglandins and Other Lipid Mediators

Volumn 97, Issue 3-4, 2012, Pages 73-82

  Weylandt, Karsten H ^a,b   Chiu, Cheng Ying ^a,b   Gomolka, Beate ^a   Waechter, Simon F ^a,b   Wiedenmann, Bertram ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

17 HDHA; 18 HEPE; n 3 PUFA; Omega 3; Protectins; Resolvins

Indexed keywords

17 HYDROPEROXYDOCOSAHEXAENOIC ACID; 18 HYDROPEROXYEICOSAPENTAENOIC ACID; CD59 ANTIGEN; DOCOSAHEXAENOIC ACID; HYDROXYL GROUP; ICOSAPENTAENOIC ACID; LIPID; OMEGA 3 FATTY ACID; POLYUNSATURATED FATTY ACID; PROTECTIN D1; PROTECTIN D2; RESOLVIN; RESOLVIN E1; RESOLVIN E2; UNCLASSIFIED DRUG;

BIOSYNTHESIS; BLOOD ANALYSIS; CHEMICAL STRUCTURE; CHIRALITY; CONCENTRATION (PARAMETERS); HUMAN; INFLAMMATION; NONHUMAN; PATHOPHYSIOLOGY; REVIEW;

ANIMALS; ANTIGENS, CD59; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FATTY ACIDS, OMEGA-3; HUMANS; INFLAMMATION;

EID: 84858700052     PISSN: 10988823     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.prostaglandins.2012.01.005     Document Type: Review

References (115)

1. Von Euler US. Further studies of prostaglandin, the physically active substance of certain genital glands. Skand Arch Physiol 1939;81:65-80.
2. Borgeat P, Hamberg M, Samuelsson B. Transformation of arachidonic acid and homo-gamma-linolenic acid by rabbit polymorphonuclear leukocytes. Monohydroxy acids from novel lipoxygenases. J Biol Chem 1976;251(24):7816-20. (Pubitemid 8015793)
3. Samuelsson B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation. Science 1983;220(4597):568-75. (Pubitemid 13130140)
4. Samuelsson B, Granstrom E, Green K, Hamberg M, Hammarstrom S. Prostaglandins. Annu Rev Biochem 1975;44:669-95.
5. Bang HO, Dyerberg J, Hjoorne N. The composition of food consumed by Greenland Eskimos. Acta Med Scand 1976;200(1-2):69-73.
6. Dyerberg J, Bang HO, Stoffersen E, Moncada S, Vane JR. Eicosapentaenoic acid and prevention of thrombosis and atherosclerosis? Lancet 1978;2(8081):117-9. (Pubitemid 8373454)
7. Leaf A. Historical overview of n-3 fatty acids and coronary heart disease. Am J Clin Nutr 2008;87(6):1978S-80S. (Pubitemid 351872678)
8. Marchioli R. Dietary supplementation with n-3 polyunsaturated fatty acids and vitamin E after myocardial infarction: results of the GISSI-Prevenzione trial. Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto miocardico. Lancet 1999;354(9177):447-55. (Pubitemid 29368922)
9. Kromann N, Green A. Epidemiological studies in the Upernavik district Greenland. Incidence of some chronic diseases 1950-1974. Acta Med Scand 1980;208(5):401-6. (Pubitemid 11162992)
10. Belluzzi A, Boschi S, Brignola C, Munarini A, Cariani G, Miglio F. Polyunsaturated fatty acids and inflammatory bowel disease. Am J Clin Nutr 2000;71(1 Suppl.):339S-42S. (Pubitemid 30046138)
11. Gilbert JA, Sartor VE. Regional enteritis: disease patterens and medical management. Can Med Assoc J 1964;91:23-7.
12. Horrobin DF. Low prevalences of coronary heart disease (CHD), psoriasis, asthma and rheumatoid arthritis in Eskimos: are they caused by high dietary intake of eicosapentaenoic acid (EPA), a genetic variation of essential fatty acid (EFA) metabolism or a combination of both? Med Hypotheses 1987;22(4):421-8. (Pubitemid 17140104)
13. Bilal S, Haworth O, Wu L, Weylandt KH, Levy BD, Kang JX. Fat-1 transgenic mice with elevated omega-3 fatty acids are protected from allergic airway responses. Biochim Biophys Acta 2011;1812(9):1164-9.
14. Hudert CA, Weylandt KH, Lu Y, et al. Transgenic mice rich in endogenous omega-3 fatty acids are protected from colitis. Proc Natl Acad Sci USA 2006;103(30):11276-81. (Pubitemid 44156509)
15. Schmocker C, Weylandt KH, Kahlke L, et al. Omega-3 fatty acids alleviate chemically induced acute hepatitis by suppression of cytokines. Hepatology 2007;45(4):864-9. (Pubitemid 46631554)
16. Weylandt KH, Krause LF, Gomolka B, et al. Suppressed liver tumorigenesis in fat-1 mice with elevated omega-3 fatty acids is associated with increased omega-3 derived lipid mediators and reduced TNF-{alpha}. Carcinogenesis 2011;32(6):897-903.
17. Nowak J, Weylandt KH, Habbel P, et al. Colitis-associated colon tumorigenesis is suppressed in transgenic mice rich in endogenous n-3 fatty acids. Carcinogenesis 2007;28(9):1991-5. (Pubitemid 47500613)
18. Weylandt KH, Nadolny A, Kahlke L, et al. Reduction of inflammation and chronic tissue damage by omega-3 fatty acids in fat-1 transgenic mice with pancreatitis. Biochim Biophys Acta 2008;1782(11):634-41.
19. Myhrstad MC, Retterstol K, Telle-Hansen VH, et al. Effect of marine n-3 fatty acids on circulating inflammatory markers in healthy subjects and subjects with cardiovascular risk factors. Inflamm Res 2011;60(4):309-19.
20. Weylandt KH, Kang JX. Rethinking lipid mediators. Lancet 2005;366(9486):618-20. (Pubitemid 41176007)
21. 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(8):1197-204.
22. 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(17):14677-87. (Pubitemid 36799790)
23. Marcheselli VL, Hong S, Lukiw WJ, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem 2003;278(44):43807-17. (Pubitemid 37346009)
24. Mukherjee PK, Marcheselli VL, Serhan CN, Bazan NG. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc Natl Acad Sci USA 2004;101(22):8491-6. (Pubitemid 38736602)
25. Serhan CN, Brain SD, Buckley CD, et al. Resolution of inflammation: state of the art, definitions and terms. FASEB J 2007;21(2):325-32. (Pubitemid 46213480)
26. Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxins are the first lipid mediators of endogenous anti-inflammation and resolution. Prostaglandins Leukot Essent Fatty Acids 2005;73(3-4):141-62. (Pubitemid 41253472)
27. Claria J, Serhan CN. Aspirin triggers previously undescribed bioactive eicosanoids by human endothelial cell-leukocyte interactions. Proc Natl Acad Sci USA 1995;92(21):9475-9.
28. Parkinson JF. Lipoxin and synthetic lipoxin analogs: an overview of antiinflammatory functions and new concepts in immunomodulation. Inflamm Allergy Drug Targets 2006;5(2):91-106. (Pubitemid 43796671)
29. Sun YP, Oh SF, Uddin J, et al. Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 2007;282(13):9323-34. (Pubitemid 47104612)
30. Serhan CN, Gotlinger K, Hong S, et al. Anti-inflammatory actions of neuroprotectin D1/protectin D1 and its natural stereoisomers: assignments of dihydroxy-containing docosatrienes. J Immunol 2006;176(3):1848-59. (Pubitemid 43134330)
31. Serhan CN, Fredman G, Yang R, et al. Novel proresolving aspirin-triggered DHA pathway. Chem Biol 2011;18(8):976-87.
32. Duffield JS, Hong S, Vaidya VS, et al. Resolvin D series and protectin D1 mitigate acute kidney injury. J Immunol 2006;177(9):5902-11. (Pubitemid 44628803)
33. Gonzalez-Periz A, Planaguma A, Gronert K, et al. Docosahexaenoic acid (DHA) blunts liver injury by conversion to protective lipid mediators: protectin D1 and 17S-hydroxy-DHA. FASEB J 2006;20(14):2537-9.
34. Lima-Garcia J, Dutra R, da Silva K, Motta E, Campos M, Calixto J. The precursor of resolvin D series and aspirin-triggered resolvin D1 display antihyperalgesic properties in adjuvant-induced arthritis in rats. Br J Pharmacol 2011;164(2):278-93.
35. Bento AF, Claudino RF, Dutra RC, Marcon R, Calixto JB. {omega}-3 Fatty acidderived mediators 17(R)-hydroxy docosahexaenoic acid aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J Immunol 2011;187(4):1957-69.
36. 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(7):2399-407.
37. 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(10):5543-7.
38. Recchiuti A, Krishnamoorthy S, Fredman G, Chiang N, Serhan CN. MicroRNAs in resolution of acute inflammation: identification of novel resolvin D1-miRNA circuits. FASEB J 2010;25(2):544-60.
39. Schif-Zuck S, Gross N, Assi S, Rostoker R, Serhan CN, Ariel A. Saturatedefferocytosis generates pro-resolving CD11b low macrophages: modulation by resolvins and glucocorticoids. Eur J Immunol 2011;41(2):366-79.
40. Kasuga K, Yang R, Porter TF, et al. Rapid appearance of resolvin precursors in inflammatory exudates: novel mechanisms in resolution. J Immunol 2008;181(12):8677-87.
41. 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(10):3595-606.
42. Krishnamoorthy S, Recchiuti A, Chiang N, et al. Resolvin D1 binds human phagocytes with evidence for proresolving receptors. Proc Natl Acad Sci USA 2010;107(4):1660-5.
43. Spite M, Norling LV, Summers L, et al. Resolvin D2 is a potent regulator of leukocytes and controls microbial sepsis. Nature 2009;461(7268): 1287-91.
44. Park CK, Xu ZZ, Liu T, Lu N, Serhan CN, Ji RR. Resolvin d2 is a potent endogenous inhibitor for transient receptor potential subtype v1/a1, inflammatory pain, and spinal cord synaptic plasticity in mice: distinct roles of resolvin d1, d2, and e1. J Neurosci 2011;31(50):18433-8.
45. Levy BD, Kohli P, Gotlinger K, et al. Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness. J Immunol 2007;178(1):496-502. (Pubitemid 46039663)
46. Lukiw WJ, Cui JG, Marcheselli VL, et al. A role for docosahexaenoic acidderived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest 2005;115(10):2774-83. (Pubitemid 41434404)
47. Ariel A, Fredman G, Sun YP, et al. Apoptotic neutrophils and T cells sequester chemokines during immune response resolution through modulation of CCR5 expression. Nat Immunol 2006;7(11):1209-16. (Pubitemid 44594317)
48. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007;447(7146): 869-74. (Pubitemid 46920139)
49. Hassan IR, Gronert K. 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 2009;182(5):3223-32.
50. Gonzalez-Periz A, Horrillo R, Ferre N, et al. Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins. FASEB J 2009;23(6):1946-57.
51. White PJ, Arita M, Taguchi R, Kang JX, Marette A. Transgenic restoration of long-chain n-3 fatty acids in insulin target tissues improves resolution capacity and alleviates obesity-linked inflammation and insulin resistance in high-fat-fed mice. Diabetes 2010;59(12):3066-73.
52. Yamada T, Tani Y, Nakanishi H, Taguchi R, Arita M, Arai H. Eosinophils promote resolution of acute peritonitis by producing proresolving mediators in mice. FASEB J 2010;25(2):561-8.
53. Connor KM, SanGiovanni JP, Lofqvist C, et al. Increased dietary intake of omega-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 2007;13(7):868-73. (Pubitemid 47038185)
54. Zhao Y, Calon F, Julien C, et al. Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARgamma-mediated mechanisms in Alzheimer's disease models. PLoS One 2011;6(1):e15816.
55. Marcheselli VL, Mukherjee PK, Arita M, et al. Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils. Prostaglandins Leukot Essent Fatty Acids 2009;82(1):27-34.
56. Serhan CN, Hong S, Gronert K, et al. 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(8):1025-37. (Pubitemid 35231761)
57. Ariel A, Li PL, Wang W, et al. The docosatriene protectin D1 is produced by TH2 skewing and promotes human T cell apoptosis via lipid raft clustering. J Biol Chem 2005;280(52):43079-86. (Pubitemid 43049274)
58. 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(2):569-81.
59. Krishnamurthy VR, Dougherty A, Haller CA, Chaikof EL. Total synthesis and bioactivity of 18(R)-hydroxyeicosapentaenoic acid. J Org Chem 2011;76(13):5433-7.
60. Hasturk H, Kantarci A, Goguet-Surmenian E, et al. Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 2007;179(10):7021-9.
61. Hasturk H, Kantarci A, Ohira T, et al. RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J 2006;20(2):401-3. (Pubitemid 46671185)
62. Bannenberg GL, Chiang N, Ariel A, et al. Molecular circuits of resolution: formation and actions of resolvins and protectins. J Immunol 2005;174(7):4345-55. (Pubitemid 40396017)
63. Arita M, Bianchini F, Aliberti J, et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 2005;201(5):713-22. (Pubitemid 40395117)
64. Li N, He J, Schwartz CE, Gjorstrup P, Bazan HE. Resolvin E1 improves tear production and decreases inflammation in a dry eye mouse model. J Ocul Pharmacol Ther 2010;26(5):431-9.
65. 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(6):3912-7. (Pubitemid 46417661)
66. Tjonahen E, Oh SF, Siegelman J, et al. Resolvin E2: identification and antiinflammatory actions: pivotal role of human 5-lipoxygenase in resolvin E series biosynthesis. Chem Biol 2006;13(11):1193-202. (Pubitemid 44750731)
67. Ogawa S, Urabe D, Yokokura Y, Arai H, Arita M, Inoue M. Total synthesis and bioactivity of resolvin E2. Org Lett 2009;11(16):3602-5.
68. Gomolka B, Siegert E, Blossey K, Schunck WH, Rothe M, Weylandt KH. Analysis of omega-3 and omega-6 fatty acid-derived lipid metabolite formation in human and mouse blood samples. Prostaglandins Other Lipid Mediat 2011;94(3-4):81-7.
69. Sapieha P, Stahl A, Chen J, et al. 5-Lipoxygenase metabolite 4-HDHA is a mediator of the antiangiogenic effect of omega-3 polyunsaturated fatty acids. Sci Transl Med 2011;3(69), 69ra12.
70. Kang JX, Wang J, Wu L, Kang ZB. Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature 2004;427(6974):504. (Pubitemid 38209102)
71. Jin Y, Arita M, Zhang Q, et al. Anti-angiogenesis effect of the novel antiinflammatory and pro-resolving lipid mediators. Invest Ophthalmol Vis Sci 2009;50(10):4743-52.
72. 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(8):3613-20.
73. Dartt DA, Hodges RR, Li D, Shatos MA, Lashkari K, Serhan CN. Conjunctival goblet cell secretion stimulated by leukotrienes is reduced by resolvins D1 and E1 to promote resolution of inflammation. J Immunol 2011;186(7):4455-66.
74. Xu ZZ, Zhang L, Liu T, et al. Resolvins RvE1 and RvD1 attenuate inflammatory pain via central and peripheral actions. Nat Med 2010;16(5):592-7 [1 p following 7].
75. Bang S, Yoo S, Yang T, Cho H, Hwang S. 17(R)-resolvin D1 specifically inhibits TRPV3 leading to peripheral antinociception. Br J Pharmacol 2012;165(3):683-92.
76. Bang S, Yoo S, Yang TJ, Cho H, Kim YG, Hwang SW. Resolvin D1 attenuates activation of sensory transient receptor potential channels leading to multiple anti-nociception. Br J Pharmacol 2010;161(3):707-20.
77. Huang L, Wang CF, Serhan CN, Strichartz G. Enduring prevention and transient reduction of postoperative pain by intrathecal resolvin D1. Pain 2011;152(3):557-65.
78. Spite M, Summers L, Porter TF, Srivastava S, Bhatnagar A, Serhan CN. Resolvin D1 controls inflammation initiated by glutathione-lipid conjugates formed during oxidative stress. Br J Pharmacol 2009;158(4):1062-73.
79. Wang B, Gong X, Wan JY, et al. Resolvin D1 protects mice from LPS-induced acute lung injury. Pulm Pharmacol Ther 2011;24(4):434-41.
80. Yuan J, Akiyama M, Nakahama K, Sato T, Uematsu H, Morita I. The effects of polyunsaturated fatty acids and their metabolites on osteoclastogenesis in vitro. Prostaglandins Other Lipid Mediat 2010;92(1-4):85-90.
81. Titos E, Rius B, Gonzalez-Periz A, et al. 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(10):5408-18.
82. Belayev L, Khoutorova L, Atkins KD, et al. Docosahexaenoic acid therapy of experimental ischemic stroke. Transl Stroke Res 2011;2(1):33-41.
83. Musto AE, Gjorstrup P, Bazan NG. The omega-3 fatty acid-derived neuroprotectin D1 limits hippocampal hyperexcitability and seizure susceptibility in kindling epileptogenesis. Epilepsia 2011;52(9):1601-8.
84. Mukherjee PK, Marcheselli VL, Barreiro S, Hu J, Bok D, Bazan NG. Neurotrophins enhance retinal pigment epithelial cell survival through neuroprotectin D1 signaling. Proc Natl Acad Sci USA 2007;104(32):13152-7. (Pubitemid 351737608)
85. Reinoso MA, Mukherjee P, Marcheselli V, Bergsma D, Hesse R, Bazan N. PEDF promotes biosynthesis of a novel anti-inflammatory and anti-apoptotic mediator NPD1 in retinal pigment epithelial cells. Ochsner J 2008;8(1): 39-43. (Pubitemid 351731904)
86. Qin Q, Patil KA, Gronert K, Sharma SC. Neuroprotectin D1 inhibits retinal ganglion cell death following axotomy. Prostaglandins Leukot Essent Fatty Acids 2008;79(6):201-7.
87. Calandria JM, Marcheselli VL, Mukherjee PK, et al. Selective survival rescue in 15-lipoxygenase-1-deficient retinal pigment epithelial cells by the novel docosahexaenoic acid-derived mediator, neuroprotectin D1. J Biol Chem 2009;284(26):17877-82.
88. Marcheselli VL, Mukherjee PK, Arita M, et al. Neuroprotectin D1/protectin D1 stereoselective and specific binding with human retinal pigment epithelial cells and neutrophils. Prostaglandins Leukot Essent Fatty Acids 2010;82(1):27-34.
89. Faghiri Z, Bazan NG. PI3K/Akt and mTOR/p70S6K pathways mediate neuroprotectin D1-induced retinal pigment epithelial cell survival during oxidative stress-induced apoptosis. Exp Eye Res 2010;90(6):718-25.
90. Sheets KG, Zhou Y, Ertel MK, et al. Neuroprotectin D1 attenuates laser-induced choroidal neovascularization in mouse. Mol Vis 2010;16:320-9.
91. Halapin NA, Bazan NG. NPD1 induction of retinal pigment epithelial cell survival involves PI3K/Akt phosphorylation signaling. Neurochem Res 2010;35(12):1944-7.
92. Antony R, Lukiw WJ, Bazan NG. 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 2010;285(24):18301-8.
93. Gronert K, Maheshwari N, Khan N, Hassan IR, Dunn M, Laniado Schwartzman M. A role for the mouse 12/15-lipoxygenase pathway in promoting epithelial wound healing and host defense. J Biol Chem 2005;280(15): 15267-78. (Pubitemid 40562883)
94. Rajasagi NK, Reddy PB, Suryawanshi A, Mulik S, Gjorstrup P, Rouse BT. Controlling herpes simplex virus-induced ocular inflammatory lesions with the lipid-derived mediator resolvin E1. J Immunol 2010;186(3):1735-46.
95. Zhang F, Yang H, Pan Z, et al. Dependence of resolvin-induced increases in corneal epithelial cell migration on EGF receptor transactivation. Invest Ophthalmol Vis Sci 2010;51(11):5601-9.
96. Ho KJ, Spite M, Owens CD, et al. Aspirin-triggered lipoxin and resolvin E1 modulate vascular smooth muscle phenotype and correlate with peripheral atherosclerosis. Am J Pathol 2010;177(4):2116-23.
97. Dona M, Fredman G, Schwab JM, et al. Resolvin E1, an EPA-derived mediator in whole blood, selectively counterregulates leukocytes and platelets. Blood 2008;112(3):848-55.
98. Fredman G, Van Dyke TE, Serhan CN. Resolvin E1 regulates adenosine diphosphate activation of human platelets. Arterioscler Thromb Vasc Biol 2010;30(10):2005-13.
99. Haas-Stapleton EJ, Lu Y, Hong S, et al. Candida albicans modulates host defense by biosynthesizing the pro-resolving mediator resolvin E1. PLoS One 2007;2(12):e1316.
100. Haworth O, Cernadas M, Levy BD. NK cells are effectors for resolvin e1 in the timely resolution of allergic airway inflammation. J Immunol 2011;186(11):6129-35.
101. Haworth O, Cernadas M, Yang R, Serhan CN, Levy BD. Resolvin E1 regulates interleukin 23, interferon-gamma and lipoxin A4 to promote the resolution of allergic airway inflammation. Nat Immunol 2008;9(8):873-9.
102. Aoki H, Hisada T, Ishizuka T, et al. Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem Biophys Res Commun 2008;367(2):509-15.
103. Aoki H, Hisada T, Ishizuka T, et al. Protective effect of resolvin E1 on the development of asthmatic airway inflammation. Biochem Biophys Res Commun 2010;400(1):128-33.
104. Seki H, Fukunaga K, Arita M, et al. The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J Immunol 2009;184(2):836-43.
105. Keyes KT, Ye Y, Lin Y, et al. Resolvin E1 protects the rat heart against reperfusion injury. Am J Physiol Heart Circ Physiol 2010;299(1):H153-64.
106. Campbell EL, Louis NA, Tomassetti SE, et al. Resolvin E1 promotes mucosal surface clearance of neutrophils: a new paradigm for inflammatory resolution. FASEB J 2007;21(12):3162-70. (Pubitemid 47565535)
107. Hong S, Porter TF, Lu Y, Oh SF, Pillai PS, Serhan CN. Resolvin E1 metabolome in local inactivation during inflammation-resolution. J Immunol 2008;180(5):3512-9.
108. 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(5):3451-61.
109. Levy BD, Zhang QY, Bonnans C, et al. The endogenous pro-resolving mediators lipoxin A4 and resolvin E1 preserve organ function in allograft rejection. Prostaglandins Leukot Essent Fatty Acids 2011;84(1-2): 43-50.
110. Lund T, Mangsbo SM, Scholz H, et al. Resolvin E1 reduces proinflammatory markers in human pancreatic islets in vitro. Exp Clin Endocrinol Diabetes 2010;118(4):237-44.
111. Fredman G, Oh SF, Ayilavarapu S, Hasturk H, Serhan CN, Van Dyke TE. Impaired phagocytosis in localized aggressive periodontitis: rescue by Resolvin E1. PloS one 2011;6(9):e24422.
112. Campbell EL, MacManus CF, Kominsky DJ, et al. Resolvin E1-induced intestinal alkaline phosphatase promotes resolution of inflammation through LPS detoxification. Proc Natl Acad Sci USA 2010;107(32):14298-303.
113. Ishida T, Yoshida M, Arita M, et al. Resolvin E1, an endogenous lipid mediator derived from eicosapentaenoic acid, prevents dextran sulfate sodium-induced colitis. Inflamm Bowel Dis 2009;16(1):87-95.
114. Arita M, Yoshida M, Hong S, et al. Resolvin E1, an endogenous lipid mediator derived from omega-3 eicosapentaenoic acid, protects against 2,4,6-trinitrobenzene sulfonic acid-induced colitis. Proc Natl Acad Sci USA 2005;102(21):7671-6. (Pubitemid 40741029)
115. Herrera BS, Ohira T, Gao L, et al. An endogenous regulator of inflammation, resolvin E1, modulates osteoclast differentiation and bone resorption. Br J Pharmacol 2008;155(8):1214-23.