The omega-3 fatty acid docosahexaenoic acid attenuates organic dust-induced airway inflammation

Nutrients

Volumn 6, Issue 12, 2014, Pages 5434-5452

  Nordgren, Tara M ^a   Friemel, Taylor D ^a   Heires, Art J ^a   Poole, Jill A ^a   Wyatt, Todd A ^a,b   Romberger, Debra J ^a,b  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b VA NEBRASKA WESTERN IOWA HEALTH CARE SYSTEM   (United States)

Author keywords

Airway inflammation; Docosahexaenoic acid (DHA); Organic dust; Specialized pro resolving mediators (SPM)

Indexed keywords

CHEMOKINE; CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; CYTOKINE; DOCOSAHEXAENOIC ACID; INTERLEUKIN 6; INTERLEUKIN 8; PROSTAGLANDIN E2; PROTEIN; RESOLVIN D1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; AIR POLLUTANT; ANTIINFLAMMATORY AGENT; AUTACOID; DUST; INTERCELLULAR ADHESION MOLECULE 1;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME LINKED IMMUNOSORBENT ASSAY; EPITHELIUM CELL; FIBROBLAST; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOASSAY; LUNG LAVAGE; MONOCYTE; MOUSE; MURINAE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; ORGANIC DUST; RESPIRATORY TRACT INFLAMMATION; UPREGULATION; AIR POLLUTANT; ANIMAL; C57BL MOUSE; CELL LINE; CHEMICALLY INDUCED; DISEASE MODEL; DOSE RESPONSE; DRUG EFFECTS; DUST; EXPOSURE; IMMUNOLOGY; LUNG; MALE; METABOLISM; PIG; PNEUMONIA;

AIR POLLUTANTS; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELL LINE; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; DUST; EPITHELIAL CELLS; FIBROBLASTS; HUMANS; INFLAMMATION MEDIATORS; INHALATION EXPOSURE; INTERCELLULAR ADHESION MOLECULE-1; LUNG; MALE; MICE, INBRED C57BL; MONOCYTES; NEUTROPHIL INFILTRATION; PNEUMONIA; SWINE;

EID: 84912571940     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu6125434     Document Type: Article

References (57)

1. Kirkhorn, S.R.; Garry, V.F. Agricultural lung diseases. Environ. Health Perspect. 2000, 108, 705–712.
2. Langley, R.L. Consequences of respiratory exposures in the farm environment. N. C. Med. J. 2011, 72, 477–480.
3. American Thoracic Society; National Institute for Occupational Safety and Health. Respiratory Health Hazards in Agriculture. Am. J. Respir. Crit. Care Med. 1998, 158, S1–S76.
4. Von Essen, S.; Romberger, D. The respiratory inflammatory response to the swine confinement building environment: The adaptation to respiratory exposures in the chronically exposed worker. J. Agric. Saf. Health2003, 9, 185–196.
5. Wang, Z.; Larsson, K.; Palmberg, L.; Malmberg, P.; Larsson, P.; Larsson, L. Inhalation of swine dust induces cytokine release in the upper and lower airways. Eur. Respir. J. 1997, 10, 381–387.
6. Szczyrek, M.; Krawczyk, P.; Milanowski, J.; Jastrzebska, I.; Zwolak, A.; Daniluk, J. Chronic obstructive pulmonary disease in farmers and agricultural workers—An overview. Ann. Agric. Environ. Med. 2011, 18, 310–313.
7. De Lorgeril, M.; Salen, P. New insights into the health effects of dietary saturated and omega-6 and omega-3 polyunsaturated fatty acids. BMC Med.2012, doi:10.1186/1741-7015-10-50.
8. Deckelbaum, R.J.; Torrejon, C. The omega-3 fatty acid nutritional landscape: Health benefits and sources. J. Nutr. 2012, 142, 587S–591S.
9. Giudetti, A.M.; Cagnazzo, R. Beneficial effects of n-3 PUFA on chronic airway inflammatory diseases. Prostaglandins Other Lipid Mediat. 2012, 99, 57–67.
10. Ji, R.R.; Xu, Z.Z.; Strichartz, G.; Serhan, C.N. Emerging roles of resolvins in the resolution of inflammation and pain. Trends Neurosci. 2011, 34, 599–609.
11. Schwab, J.M.; Serhan, C.N. Lipoxins and new lipid mediators in the resolution of inflammation. Curr. Opin. Pharmacol. 2006, 6, 414–420.
12. Serhan, C.N. Controlling the resolution of acute inflammation: A new genus of dual anti-inflammatory and proresolving mediators. J. Periodontol. 2008, 79, 1520–1526.
13. Weylandt, K.H.; Chiu, C.Y.; Gomolka, B.; Waechter, S.F.; Wiedenmann, B. Omega-3 fatty acids and their lipid mediators: Towards an understanding of resolvin and protectin formation. Prostaglandins Other Lipid Mediat. 2012, 97, 73–82.
14. Serhan, C.N.; Dalli, J.; Karamnov, S.; Choi, A.; Park, C.K.; Xu, Z.Z.; Ji, R.R.; Zhu, M.; Petasis, N.A. Macrophage proresolving mediator maresin 1 stimulates tissue regeneration and controls pain. FASEB J.2012, 26, 1755–1765.
15. Hasturk, H.; Kantarci, A.; Goguet-Surmenian, E.; Blackwood, A.; Andry, C.; Serhan, C.N.; van Dyke, T.E. Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 2007, 179, 7021–7029.
16. Hsiao, H.M.; Sapinoro, R.E.; Thatcher, T.H.; Croasdell, A.; Levy, E.P.; Fulton, R.A.; Olsen, K.C.; Pollock, S.J.; Serhan, C.N.; Phipps, R.P.; et al. A novel anti-inflammatory and pro-resolving role for resolvin d1 in acute cigarette smoke-induced lung inflammation. PLoS One2013, doi:10.1371/journal.pone.0058258.
17. Seki, H.; Fukunaga, K.; Arita, M.; Arai, H.; Nakanishi, H.; Taguchi, R.; Miyasho, T.; Takamiya, R.; Asano, K.; Ishizaka, A.; et al. The anti-inflammatory and proresolving mediator resolvin E1 protects mice from bacterial pneumonia and acute lung injury. J. Immunol. 2010, 184, 836–843.
18. Serhan, C.N. Pro-resolving lipid mediators are leads for resolution physiology. Nature2014, 510, 92–101.
19. Aoki, H.; Hisada, T.; Ishizuka, T.; Utsugi, M.; Kawata, T.; Shimizu, Y.; Okajima, F.; Dobashi, K.; Mori, M. Resolvin E1 dampens airway inflammation and hyperresponsiveness in a murine model of asthma. Biochem. Biophys. Res. Commun. 2008, 367, 509–515.
20. Nordgren, T.M.; Heires, A.J.; Wyatt, T.A.; Poole, J.A.; LeVan, T.D.; Cerutis, D.R.; Romberger, D.J. Maresin-1 reduces the pro-inflammatory response of bronchial epithelial cells to organic dust. Respir. Res. 2013, doi:10.1186/1465-9921-14-51.
21. Poole, J.A.; Wyatt, T.A.; Oldenburg, P.J.; Elliott, M.K.; West, W.W.; Sisson, J.H.; Von Essen, S.G.; Romberger, D.J. Intranasal organic dust exposure-induced airway adaptation response marked by persistent lung inflammation and pathology in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2009, 296, L1085–L1095.
22. Romberger, D.J.; Bodlak, V.; von Essen, S.G.; Mathisen, T.; Wyatt, T.A. Hog barn dust extract stimulates IL-8 and IL-6 release in human bronchial epithelial cells via PKC activation. J. Appl. Physiol. 2002, 93, 289–296.
23. Poole, J.A.; Dooley, G.P.; Saito, R.; Burrell, A.M.; Bailey, K.L.; Romberger, D.J.; Mehaffy, J.; Reynolds, S.J. Muramic acid, endotoxin, 3-hydroxy fatty acids, and ergosterol content explain monocyte and epithelial cell inflammatory responses to agricultural dusts. J. Toxicol. Environ. Health2010, 73, 684–700.
24. Wyatt, T.A.; Kharbanda, K.K.; McCaskill, M.L.; Tuma, D.J.; Yanov, D.; DeVasure, J.; Sisson, J.H. Malondialdehyde-acetaldehyde-adducted protein inhalation causes lung injury. Alcohol2012, 46, 51–59.
25. Gurzell, E.A.; Wiesinger, J.A.; Morkam, C.; Hemmrich, S.; Harris, W.S.; Fenton, J.I. Is the omega-3 index a valid marker of intestinal membrane phospholipid EPA + DHA content? Prostaglandins Leukot. Essent. Fatty Acids2014, 91, 87–96.
26. Bachmanov, A.A.; Reed, D.R.; Beauchamp, G.K.; Tordoff, M.G. Food intake, water intake, and drinking spout side preference of 28 mouse strains. Behav. Genet. 2002, 32, 435–443.
27. Mathisen, T.; von Essen, S.G.; Wyatt, T.A.; Romberger, D.J. Hog barn dust extract augments lymphocyte adhesion to human airway epithelial cells. J. Appl. Physiol. 2004, 96, 1738–1744.
28. Poole, J.A.; Wyatt, T.A.; von Essen, S.G.; Hervert, J.; Parks, C.; Mathisen, T.; Romberger, D.J. Repeat organic dust exposure-induced monocyte inflammation is associated with protein kinase C activity. J. Allergy Clin. Immunol. 2007, 120, 366–373.
29. Laberge, S.; El Bassam, S. Cytokines, structural cells of the lungs and airway inflammation. Paediatr. Respir. Rev. 2004, 5, S41–S45.
30. Suzuki, T.; Chow, C.W.; Downey, G.P. Role of innate immune cells and their products in lung immunopathology. Int. J. Biochem. Cell Biol. 2008, 40, 1348–1361.
31. Tosi, M.F.; Stark, J.M.; Smith, C.W.; Hamedani, A.; Gruenert, D.C.; Infeld, M.D. Induction of ICAM-1 expression on human airway epithelial cells by inflammatory cytokines: Effects on neutrophil-epithelial cell adhesion. Am. J. Respir. Cell Mol. Biol. 1992, 7, 214–221.
32. Bloemen, P.G.; van den Tweel, M.C.; Henricks, P.A.; Engels, F.; Wagenaar, S.S.; Rutten, A.A.; Nijkamp, F.P. Expression and modulation of adhesion molecules on human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 1993, 9, 586–593.
33. Takizawa, H. Airway epithelial cells as regulators of airway inflammation (review). Int. J. Mol. Med. 1998, 1, 367–378.
34. Message, S.D.; Johnston, S.L. Host defense function of the airway epithelium in health and disease: Clinical background. J. Leukoc. Biol. 2004, 75, 5–17.
35. Wyatt, T.A.; Slager, R.E.; Heires, A.J.; Devasure, J.M.; Vonessen, S.G.; Poole, J.A.; Romberger, D.J. Sequential activation of protein kinase C isoforms by organic dust is mediated by tumor necrosis factor. Am. J. Respir. Cell. Mol. Biol. 2010, 42, 706–715.
36. Poole, J.A.; Gleason, A.M.; Bauer, C.; West, W.W.; Alexis, N.; van Rooijen, N.; Reynolds, S.J.; Romberger, D.J.; Kielian, T.L. CD11c+/CD11b+ cells are critical for organic dust—Elicited murine lung inflammation. Am. J. Respir. Cell. Mol. Biol. 2012, 47, 652–659.
37. Poole, J.A.; Romberger, D.J. Immunological and inflammatory responses to organic dust in agriculture. Curr. Opin. Allergy Clin. Immunol. 2012, 12, 126–132.
38. Gong, J.; Wu, Z.Y.; Qi, H.; Chen, L.; Li, H.B.; Li, B.; Yao, C.Y.; Wang, Y.X.; Wu, J.; Yuan, S.Y.; et al. Maresin 1 mitigates lipopolysaccharide-induced acute lung injury in mice. Br. J. Pharmacol. 2014, 171, 3539–3550.
39. Liao, Z.; Dong, J.; Wu, W.; Yang, T.; Wang, T.; Guo, L.; Chen, L.; Xu, D.; Wen, F. Resolvin D1 attenuates inflammation in lipopolysaccharide-induced acute lung injury through a process involving the PPARγ/NF-κB pathway. Respir. Res. 2012, 13, 110.
40. Pontes-Arruda, A.; Demichele, S.; Seth, A.; Singer, P. The use of an inflammation-modulating diet in patients with acute lung injury or acute respiratory distress syndrome: A meta-analysis of outcome data. JPEN J. Parenter. Enter. Nutr. 2008, 32, 596–605.
41. Oliver, C.; Jahnke, N. Omega-3 fatty acids for cystic fibrosis. Cochrane Database Syst. Rev. 2013, doi:10.1002/14651858.CD002201.pub3.
42. Strasser, T.; Fischer, S.; Weber, P.C. Leukotriene B5 is formed in human neutrophils after dietary supplementation with icosapentaenoic acid. Proc. Natl. Acad. Sci. USA1985, 82, 1540–1543.
43. Zhao, H.; Chan-Li, Y.; Collins, S.L.; Zhang, Y.; Hallowell, R.W.; Mitzner, W.; Horton, M.R. Pulmonary delivery of docosahexaenoic acid mitigates bleomycin-induced pulmonary fibrosis. BMC Pulm. Med. 2014, 14, 64.
44. Schuster, G.U.; Bratt, J.M.; Jiang, X.; Pedersen, T.L.; Grapov, D.; Adkins, Y.; Kelley, D.S.; Newman, J.W.; Kenyon, N.J.; Stephensen, C.B. Dietary long-chain omega-3 fatty acids do not diminish eosinophilic pulmonary inflammation in mice. Am. J. Respir. Cell. Mol. Biol. 2014, 50, 626–636.
45. Im, D.S. Omega-3 fatty acids in anti-inflammation (pro-resolution) and GPCRs. Prog. Lipid Res. 2012, 51, 232–237.
46. Norris, P.C.; Dennis, E.A. Omega-3 fatty acids cause dramatic changes in TLR4 and purinergic eicosanoid signaling. Proc. Natl. Acad. Sci. USA2012, 109, 8517–8522.
47. Mimoun, M.; Coste, T.C.; Lebacq, J.; Lebecque, P.; Wallemacq, P.; Leal, T.; Armand, M. Increased tissue arachidonic acid and reduced linoleic acid in a mouse model of cystic fibrosis are reversed by supplemental glycerophospholipids enriched in docosahexaenoic acid. J. Nutr. 2009, 139, 2358–2364.
48. Stillwell, W.; Wassall, S.R. Docosahexaenoic acid: Membrane properties of a unique fatty acid. Chem Phys. Lipids2003, 126, 1–27.
49. Shek, L.P.; Chong, M.F.; Lim, J.Y.; Soh, S.E.; Chong, Y.S. Role of dietary long-chain polyunsaturated fatty acids in infant allergies and respiratory diseases. Clin. Dev. Immunol. 2012, doi:10.1155/2012/730568.
50. Oh, D.Y.; Talukdar, S.; Bae, E.J.; Imamura, T.; Morinaga, H.; Fan, W.; Li, P.; Lu, W.J.; Watkins, S.M.; Olefsky, J.M. GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulin-sensitizing effects. Cell2010, 142, 687–698.
51. Bailey, K.L.; Poole, J.A.; Mathisen, T.L.; Wyatt, T.A.; von Essen, S.G.; Romberger, D.J. Toll-like receptor 2 is upregulated by hog confinement dust in an IL-6-dependent manner in the airway epithelium. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294, L1049–L1054.
52. Poole, J.A.; Wyatt, T.A.; Kielian, T.; Oldenburg, P.; Gleason, A.M.; Bauer, A.; Golden, G.; West, W.W.; Sisson, J.H.; Romberger, D.J. Toll-like receptor 2 regulates organic dust-induced airway inflammation. Am. J. Respir. Cell. Mol. Biol. 2011, 45, 711–719.
53. Martel, G.; Berube, J.; Rousseau, S. The protein kinase TPL2 is essential for ERK1/ERK2 activation and cytokine gene expression in airway epithelial cells exposed to pathogen-associated molecular patterns (PAMPs). PLoS One2013, doi:10.1371/journal.pone.0059116.
54. Gardner, A.; Fisher, A.J.; Richter, C.; Johnson, G.E.; Moisey, E.J.; Brodlie, M.; Ward, C.; Krippner-Heidenreich, A.; Mann, D.A.; Borthwick, L.A. The critical role of TAK1 in accentuated epithelial to mesenchymal transition in obliterative bronchiolitis after lung transplantation. Am. J. Pathol. 2012, 180, 2293–2308.
55. Huang, F.; Kao, C.Y.; Wachi, S.; Thai, P.; Ryu, J.; Wu, R. Requirement for both JAK-mediated PI3K signaling and ACT1/TRAF6/TAK1-dependent NF-κB activation by IL-17A in enhancing cytokine expression in human airway epithelial cells. J. Immunol. 2007, 179, 6504–6513.
56. Bannenberg, G.L. Therapeutic applicability of anti-inflammatory and proresolving polyunsaturated fatty acid-derived lipid mediators. Sci. World J. 2010, 10, 676–712.
57. Wendell, S.G.; Baffi, C.; Holguin, F. Fatty acids, inflammation, and asthma. J. Allergy Clin. Immunol. 2014, 33, 1255–1264.