Acute lung injury is reduced in fat-1 mice endogenously synthesizing n-3 fatty acids

American Journal of Respiratory and Critical Care Medicine

Volumn 179, Issue 6, 2009, Pages 474-483

  Mayer, Konstantin ^a   Kiessling, Almuth ^a   Ott, Juliane ^a   Schaefer, Martina Barbara ^a   Hecker, Matthias ^a   Henneke, Ingrid ^a   Schulz, Richard ^a   Gunther, Andreas ^a   Wang, Jingdong ^c   Wu, Lijun ^d   Roth, Joachim ^b   Seeger, Werner ^a   Kang, Jing X ^c  

^a JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d Resolvyx Pharmaceuticals Inc   (United States)

Author keywords

Acute lung injury; Eicosapentaenoic acid; Fat 1 mice; Inflammation; Sickness behavior

Indexed keywords

CYTOKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE INFLAMMATORY PROTEIN 2; MYELOPEROXIDASE; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROSTAGLANDIN; THROMBOXANE B2; TUMOR NECROSIS FACTOR ALPHA; ACYL COENZYME A DESATURASE; ARACHIDONIC ACID; CAENORHABDITIS ELEGANS PROTEIN; CXCL2 CHEMOKINE; CXCL2 PROTEIN, RAT; DOCOSAHEXAENOIC ACID; FAT 1 PROTEIN, C ELEGANS; FAT-1 PROTEIN, C ELEGANS; FISH OIL; ICOSAPENTAENOIC ACID; LIPID EMULSION;

ACUTE LUNG INJURY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; CELL INVASION; CONTROLLED STUDY; CRITICAL ILLNESS; FATTY ACID SYNTHESIS; INFLAMMATION; LEUKOCYTE; LUNG COMPLIANCE; LUNG LAVAGE; MOTOR ACTIVITY; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; VENTILATOR; ANIMAL; ANIMAL BEHAVIOR; ARTIFICIAL VENTILATION; CHEMISTRY; DISEASE MODEL; GENETICS; LEUKOCYTE COUNT; LUNG; METABOLISM; PATHOLOGY; TRANSGENIC MOUSE;

ACUTE LUNG INJURY; ANIMALS; ARACHIDONIC ACID; BEHAVIOR, ANIMAL; BODY TEMPERATURE; BRONCHOALVEOLAR LAVAGE FLUID; CAENORHABDITIS ELEGANS PROTEINS; CHEMOKINE CXCL2; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; EICOSAPENTAENOIC ACID; FAT EMULSIONS, INTRAVENOUS; FATTY ACID DESATURASES; FISH OILS; LEUKOCYTE COUNT; LEUKOCYTES; LUNG; MICE; MICE, TRANSGENIC; MOTOR ACTIVITY; NF-KAPPA B; RESPIRATION, ARTIFICIAL; THROMBOXANE B2; TUMOR NECROSIS FACTOR-ALPHA;

EID: 63249102365     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200807-1064OC     Document Type: Article

References (65)

1. Wheeler AP, Bernard GR. Acute lung injury and the acute respiratory distress syndrome: a clinical review. Lancet 2007;369:1553-1564.
2. Hecker M, Walmrath HD, Seeger W, Mayer K. Clinical aspects of acute lung insufficiency (ALI/TRALI). Transfus Med Hemother 2008;35: 80-88.
3. Brun-Buisson C, Minelli C, Bertolini G, Brazzi L, Pimentel J, Lewandowski K, Bion J, Romand JA, Villar J, Thorsteinsson A, et al. Epidemiology and outcome of acute lung injury in European intensive care units: results from the ALIVE study. Intensive Care Med 2004;30:51-61.
4. Esteban A, Anzueto A, Frutos F, Alia I, Brochard L, Stewart TE, Benito S, Epstein SK, Apezteguia C, Nightingale P, et al. Characteristics and outcomes in adult patients receiving mechanical ventilation: a 28-day international study. JAMA 2002;287:345-355.
5. Cepkova M, Matthay MA. Pharmacotherapy of acute lung injury and the acute respiratory distress syndrome. J Intensive Care Med 2006;21:119-143.
6. Calfee CS, Matthay MA. Nonventilatory treatments for acute lung injury and ARDS. Chest 2007;131:913-920.
7. Matthay MA, Zimmerman GA. Acute lung injury and the acute respiratory distress syndrome: four decades of inquiry into pathogen- esis and rational management. Am J Respir Cell Mol Biol 2005;33:319-327.
8. Sijben JW, Calder PC. Differential immunomodulation with long-chain n-3 PUFA in health and chronic disease. Proc Nutr Soc 2007;66:237-259.
9. Mayer K, Schaefer MB, Seeger W. Fish oil in the critically ill: from experimental to clinical data. Curr Opin Clin Nutr Metab Care 2006;9:140-148.
10. Heller A, Koch T, Schmeck J, van Ackern K. Lipid mediators in inflammatory disorders. Drugs 1998;55:487-196.
11. Mayer K, Seeger W. Fish oil in critical illness. Curr Opin Clin Nutr Metab Care 2008;11:121-127.
12. Calder PC. Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 2007;77:327-335.
13. Yaqoob P, Calder PC. Fatty acids and immune function: new insights into mechanisms. Br J Nutr 2007;98:S41-S45.
14. Kang JX, Wang J, Wu L, Kang ZB. Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature 2004;427:504.
15. Simopoulos AP. Evolutionary aspects of omega-3 fatty acids in the food supply. Prostaglandins Leukot Essent Fatty Acids 1999;60:421-429.
16. Gadek JE, DeMichele SJ, Karlstad MD, Pacht ER, Donahoe M, Albertson TE, Van Hoozen C, Wennberg AK, Nelson JL, Noursalehi M. Effect of enteral feeding with eicosapentaenoic acid, gamma- linolenic acid, and antioxidants in patients with acute respiratory distress syndrome. Enteral Nutrition in ARDS Study Group. Crit Care Med 1999;27:1409-1420.
17. Singer P, Theilla M, Fisher H, Gibstein L, Grozovski E, Cohen J. Benefit of an enteral diet enriched with eicosapentaenoic acid and gamma- linolenic acid in ventilated patients with acute lung injury. Crit Care Med 2006;34:1033-1038.
18. Pontes-Arruda A, Aragao AM, Albuquerque JD. Effects of enteral feeding with eicosapentaenoic acid, gamma-linolenic acid, and anti- oxidants in mechanically ventilated patients with severe sepsis and septic shock. Crit Care Med 2006;34:2325-2333.
19. Wichmann MW, Thul P, Czarnetzki HD, Morlion BJ, Kemen M, Jauch KW. Evaluation of clinical safety and beneficial effects of a fish oil containing lipid emulsion (Lipoplus, MLF541): data from a prospective, randomized, multicenter trial. Crit Care Med 2007;35:700-706.
20. Tsekos E, Reuter C, Stehle P, Boeden G. Perioperative administration of parenteral fish oil supplements in a routine clinical setting improves patient outcome after major abdominal surgery. Clin Nutr 2004;23:325-330.
21. Berger MM, Tappy L, Revelly JP, Koletzko BV, Gepert J, Corpataux JM, Cayeux MC, Chiolero RL. Fish oil after abdominal aorta aneurysm surgery. Eur J Clin Nutr 2008;62:1116-1122.
22. Mayer K, Kang JX. fat-1 Mice are protected from acute lung injury. J Nutrigenet Nutrigenomics 2008;1:271.
23. Schaefer MB, Ott J, Mohr A, Bi MH, Grosz A, Weissmann N, Ishii S, Grimminger F, Seeger W, Mayer K. Immunomodulation by n-3- versus n-6-rich lipid emulsions in murine acute lung injury-role of platelet-activating factor receptor. Crit Care Med 2007;35:544-554.
24. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951;193:265-275.
25. Gunther A, Lubke N, Ermert M, Schermuly RT, Weissmann N, Breithecker A, Markart P, Ruppert C, Quanz K, Ermert L, et al.Pre- vention of bleomycin-induced lung fibrosis by aerosolization of heparin or urokinase in rabbits. AmJRespirCritCareMed2003;168:1358-1365.
26. Rosseau S, Wiechmann K, Moderer S, Selhorst J, Mayer K, Krull M, Hocke A, Slevogt H, Seeger W, Suttorp N, et al. Moraxella catarrhalis- infected alveolar epithelium induced monocyte recruitment and oxidative burst. Am J Respir Cell Mol Biol 2005;32:157-166.
27. Wygrecka M, Markart P, Ruppert C, Petri K, Preissner KT, Seeger W, Guenther A. Cellular origin of pro-coagulant and (anti)-fibrinolytic factors in bleomycin-injured lungs. Eur Respir J 2007;29:1105-1114.
28. Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, Yang R, Petasis NA, Serhan CN. Stereochemical assignment, antiinflamma- tory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med 2005;201:713-722.
29. Hubschle T, Mutze J, Muhlradt PF, Korte S, Gerstberger R, Roth J. Pyrexia, anorexia, adipsia, and depressed motor activity in rats during systemic inflammation induced by the Toll-like receptors-2 and -6 agonists MALP-2 and FSL-1. Am J Physiol Regul Integr Comp Physiol 2006;290:R180-R187.
30. Mayer K, Gokorsch S, Fegbeutel C, Hattar K, Rosseau S, Walmrath D, Seeger W, Grimminger F. Parenteral nutrition with fish oil modulates cytokine response in patients with sepsis. Am J Respir Crit Care Med 2003;167:1321-1328.
31. Mayer K, Meyer S, Reinholz-Muhly M, Maus U, Merfels M, Lohmeyer J, Grimminger F, Seeger W. Short-time infusion of fish oil-based lipid emulsions, approved for parenteral nutrition, reduces monocyte proinflammatory cytokine generation and adhesive interaction with endothelium in humans. J Immunol 2003;171:4837-4843.
32. Sperling RI, Benincaso AI, Knoell CT, Larkin JK, Austen KF, Robinson DR. Dietary omega-3 polyunsaturated fatty acids inhibit phosphoi- nositide formation and chemotaxis in neutrophils. J Clin Invest 1993;91:651-660.
33. Schaefer MB, Wenzel A, Fischer T, Braun-Dullaeus RC, Renner F, Dietrich H, Schaefer CA, Seeger W, Mayer K. Fatty acids differentially influence phosphatidylinositol 3-kinase signal transduction in endothelial cells: impact on adhesion and apoptosis. Atherosclerosis 2008;197:630-637.
34. Denys A, Hichami A, Khan NA. n-3 PUFAs modulate T-cell activation via protein kinase C-alpha and -epsilon and the NF-kappaB signaling pathway. J Lipid Res 2005;46:752-758.
35. Camandola S, Leonarduzzi G, Musso T, Varesio L, Carini R, Scavazza A, Chiarpotto E, Baeuerle PA, Poli G. Nuclear factor KB is activated by arachidonic acid but not by eicosapentaenoic acid. Biochem Biophys Res Commun 1996;229:643-647.
36. Weber C, Erl W, Pietsch A, Danesch U, Weber PC. Docosahexaenoic acid selectively attenuates induction of vascular cell adhesion molecule- 1 and subsequent monocytic cell adhesion to human endothelial cells stimulated by tumor necrosis factor-alpha. Arterioscler Thromb Vasc Biol 1995;15:622-628.
37. Pluess TT, Hayoz D, Berger MM, Tappy L, Revelly JP, Michaeli B, Carpentier YA, Chiolero RL. Intravenous fish oil blunts the physiological response to endotoxin in healthy subjects. Intensive Care Med 2007;33:789-797.
38. Michaeli B, Berger MM, Revelly JP, Tappy L, Chiolero R. Effects of fish oil on the neuro-endocrine responses to an endotoxin challenge in healthy volunteers. Clin Nutr 2007;26:70-77.
39. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007;7:678-689.
40. Zimmerman GA, Mclntyre TM, Mehra M, Prescott SM. Endothelial cell-associated platelet-activating factor: a novel mechanism for signaling intercellular adhesion. J Cell Biol 1990;110:529-540.
41. Smith DF, Deem TL, Bruce AC, Reutershan J, Wu D, Ley K. Leukocyte phosphoinositide-3 kinase {gamma} is required for chemokine- induced, sustained adhesion under flow in vivo. J Leukoc Biol 2006;80:1491-1499.
42. Mayer K, Merfels M, Muhly-Reinholz M, Gokorsch S, Rosseau S, Lohmeyer J, Schwarzer N, Krull M, Suttorp N, Grimminger F, et al. Omega-3 fatty acids suppress monocyte adhesion to human endothe- lial cells: role of endothelial PAF generation. Am J Physiol Heart Circ Physiol 2002;283:H811-H818.
43. Parker JC, Townsley MI. Evaluation of lung injury in rats and mice. Am J Physiol Lung Cell Mol Physiol 2004;286:L231-L246.
44. Esper AM, Martin GS. Evolution of treatments for patients with acute lung injury. Expert Opin Investig Drugs 2005;14:633-645.
45. Weissman C. The metabolic response to stress: an overview and update. Anesthesiology 1990;73:308-327.
46. Mayer K, Fegbeutel C, Hattar K, Sibelius U, Kramer HJ, Heuer KU, Temmesfeld-Wollbruck B, Gokorsch S, Grimminger F, Seeger W. Omega-3 vs. omega-6 lipid emulsions exert differential influence on neutrophils in septic shock patients: impact on plasma fatty acids and lipid mediator generation. Intensive Care Med 2003;29:1472-1481.
47. Stoner HB, Little RA, Frayn KN, Elebute AE, Tresadern J, Gross E. The effect of sepsis on the oxidation of carbohydrate and fat. Br J Surg 1983;70:32-35.
48. Forse RA, Leibel R, Askanazi J, Hirsch J, Kinney JM. Adrenergic control of adipocyte lipolysis in trauma and sepsis. Ann Surg 1987;206:744-751.
49. Spitzer JA, Leach GJ, Palmer MA. Some metabolic and hormonal alterations in adipocytes isolated from septic dogs. Adv Shock Res 1980;4:55-62.
50. Grimminger F, Wahn H, Mayer K, Kiss L, Walmrath D, Seeger W. Impact of arachidonic versus eicosapentaenoic acid on exotonin- induced lung vascular leakage: relation to 4-series versus 5-series leukotriene generation. Am J Respir Crit Care Med 1997;155:513-519.
51. Grimminger F, Durr U, Seeger W. Ligand-operated synthesis of 4-series and 5-series leukotrienes in human neutrophils: critical dependence on exogenous free fatty acid supply. Mol Pharmacol 1992;41:757-766.
52. Grimminger F, Mayer K, Kiss L, Walmrath D, Seeger W. PAF-induced synthesis of tetraenoic and pentaenoic leukotrienes in the isolated rabbit lung. Am J Physiol Lung Cell Mol Physiol 2000;278:L268-L275.
53. Grimminger F, Wahn H, Kramer HJ, Stevens J, Mayer K, Walmrath D, Seeger W. Differential influence of arachidonic vs. eicosapentaenoic acid on experimental pulmonary hypertension. Am J Physiol 1995;268:H2252-H2259.
54. Bernard GR, Wheeler AP, Russell JA, Schein R, Summer WR, Steinberg KP, Fulkerson WJ, Wright PE, Christman BW, Dupont WD, et al. The effects of ibuprofen on the physiology and survival of patients with sepsis: the Ibuprofen in Sepsis Study Group. N Engl J Med 1997;336:912-918.
55. Romanovsky AA, Almeida MC, Aronoff DM, Ivanov AI, Konsman JP, Steiner AA, Turek VF. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front Biosci 2005;10:2193-2216.
56. Clemmer TP, Fisher CJ Jr, Bone RC, Slotman GJ, Metz CA, Thomas FO. Hypothermia in the sepsis syndrome and clinical outcome: the Methylprednisolone Severe Sepsis Study Group. Crit Care Med 1992;20:1395-1401.
57. Dantzer R. Cytokine-induced sickness behavior: mechanisms and implications. Ann N Y Acad Sci 2001;933:222-234.
58. 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 USA 2006;103:11276-11281.
59. 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.
60. Arita M, Yoshida M, Hong S, Tjonahen E, Glickman JN, Petasis NA, Blumberg RS, Serhan CN. 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;102:7671-7676.
61. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007;447:869-874.
62. 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;9:873-879.
63. Levy BD, Kohli P, Gotlinger K, Haworth O, Hong S, Kazani S, Israel E, Haley KJ, Serhan CN. Protectin D1 is generated in asthma and dampens airway inflammation and hyperresponsiveness. J Immunol 2007;178:496-502.
64. Pacht ER, DeMichele SJ, Nelson JL, Hart J, Wennberg AK, Gadek JE. Enteral nutrition with eicosapentaenoic acid, gamma-linolenic acid, and antioxidants reduces alveolar inflammatory mediators and protein influx in patients with acute respiratory distress syndrome. Crit Care Med 2003;31:491-500.
65. Luyer MD, Greve JW, Hadfoune M, Jacobs JA, Dejong CH, Buurman WA. Nutritional stimulation of cholecystokinin receptors inhibits inflammation via the vagus nerve. J Exp Med 2005;202:1023-1029.