Pulmonary delivery of docosahexaenoic acid mitigates bleomycin-induced pulmonary fibrosis

BMC Pulmonary Medicine

Volumn 14, Issue 1, 2014, Pages

  Zhao, Hongyun ^a,b   Chan Li, Yee ^a   Collins, Samuel L ^a   Zhang, Yuan ^c   Hallowell, Robert W ^a   Mitzner, Wayne ^b   Horton, Maureen R ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c SHANGHAI PULMONARY HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; DOCOSAHEXAENOIC ACID; ICOSANOID; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 33; INTERLEUKIN 6; OMEGA 3 FATTY ACID; PROSTAGLANDIN E; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; BODY WEIGHT; CELL INFILTRATION; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATORY CELL; LEUKOCYTE DIFFERENTIAL COUNT; LUNG FUNCTION; LUNG LAVAGE; LUNG MECHANICS; LUNG PARENCHYMA; MORTALITY; MOUSE; NONHUMAN; PNEUMONIA; RESPIRATORY TRACT PARAMETERS; SURVIVAL; WEIGHT REDUCTION;

ANIMALS; BLEOMYCIN; DOCOSAHEXAENOIC ACIDS; FEMALE; MICE; MICE, INBRED C57BL; PULMONARY FIBROSIS; TRACHEA;

EID: 84899487891     PISSN: None     EISSN: 14712466     Source Type: Journal    
DOI: 10.1186/1471-2466-14-64     Document Type: Article

References (67)

1. Katzenstein AL, Myers JL. Idiopathic pulmonary fibrosis: clinical relevance of pathologic classification. Am J Respir Crit Care Med 1998, 157:1301-1315. 10.1164/ajrccm.157.4.9707039, 9563754.
2. Raghu G, Weycker D, Edelsberg J, Bradford WZ, Oster G. Incidence and prevalence of idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2006, 174:810-816. 10.1164/rccm.200602-163OC, 16809633.
3. Kuhn C. The pathogenesis of pulmonary fibrosis. Churg A and Katzenstein A-LA (Eds.), The Lung Current Concepts (Series: Monographs in Pathology; no. 36) 1993, 78-92. Baltimore: Williams & Wilkins.
4. Martinet Y, Menard O, Vaillant P, Vignaud JM, Martinet N. Cytokines in human lung fibrosis. Arch Toxicol Suppl 1996, 18:127-139. 10.1007/978-3-642-61105-6_14, 8678788.
5. Agostini C, Gurrieri C. Chemokine/cytokine cocktail in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 2006, 3:357-363. 10.1513/pats.200601-010TK, 16738201.
6. Charbeneau RP, Peters-Golden M. Eicosanoids: mediators and therapeutic targets in fibrotic lung disease. Clin Sci (Lond) 2005, 108:479-491. 10.1042/CS20050012, 15896193.
7. Izumo T, Kondo M, Nagai A. Effects of a leukotriene B4 receptor antagonist on bleomycin-induced pulmonary fibrosis. Eur Respir J 2009, 34:1444-1451. 10.1183/09031936.00143708, 19460787.
8. Stratton R, Shiwen X. Role of prostaglandins in fibroblast activation and fibrosis. J Cell Commun Signal 2010, 4:75-77. 10.1007/s12079-010-0089-8, 2876240, 20531982.
9. Dackor RT, Cheng J, Voltz JW, Card JW, Ferguson CD, Garrett RC, Bradbury JA, DeGraff LM, Lih FB, Tomer KB, Flake GP, Travlos GS, Ramsey RW, Edin ML, Morgan DL, Zeldin DC. Prostaglandin E(2) protects murine lungs from bleomycin-induced pulmonary fibrosis and lung dysfunction. Am J Physiol Lung Cell Mol Physiol 2011, 301:L645-L655. 10.1152/ajplung.00176.2011, 3213994, 21856819.
10. Lovgren AK, Jania LA, Hartney JM, Parsons KK, Audoly LP, Fitzgerald GA, Tilley SL, Koller BH. COX-2-derived prostacyclin protects against bleomycin-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2006, 291:L144-L156. 10.1152/ajplung.00492.2005, 16473862.
11. Cleland LG, James MJ. Fish oil and rheumatoid arthritis: antiinflammatory and collateral health benefits. J Rheumatol 2000, 27:2305-2307.
12. Broughton KS, Johnson CS, Pace BK, Liebman M, Kleppinger KM. Reduced asthma symptoms with n-3 fatty acid ingestion are related to 5-series leukotriene production. Am J Clin Nutr 1997, 65:1011-1017.
13. Belluzzi A, Brignola C, Campieri M, Pera A, Boschi S, Miglioli M. Effect of an enteric-coated fish-oil preparation on relapses in Crohn's disease. N Engl J Med 1996, 334:1557-1560. 10.1056/NEJM199606133342401, 8628335.
14. Calder PC. N-3 polyunsaturated fatty acids and inflammation: from molecular biology to the clinic. Lipids 2003, 38:343-352. 10.1007/s11745-003-1068-y, 12848278.
15. Thies F, Garry JM, Yaqoob P, Rerkasem K, Williams J, Shearman CP, Gallagher PJ, Calder PC, Grimble RF. Association of n-3 polyunsaturated fatty acids with stability of atherosclerotic plaques: a randomised controlled trial. Lancet 2003, 361:477-485. 10.1016/S0140-6736(03)12468-3, 12583947.
16. Baggio B, Musacchio E, Priante G. Polyunsaturated fatty acids and renal fibrosis: pathophysiologic link and potential clinical implications. J Nephrol 2005, 18:362-367.
17. Thien FCK, De Luca S, Woods RK, Thien FC, Abramson MJ. Dietary marine fatty acids (fish oil) for asthma in adults and children. Cochrane Database Syst Rev 2002, (2):CD001283. doi:10.1002/14651858.CD001283.
18. Rauch B, Schiele R, Schneider S, Diller F, Victor N, Gohlke H, Gottwik M, Steinbeck G, del Castillo U, Sack R, Worth H, Katus H, Spitzer W, Sabin G, Senges J, OMEGA Study Group OMEGA, a randomized, placebo-controlled trial to test the effect of highly purified omega-3 fatty acids on top of modern guideline-adjusted therapy after myocardial infarction. Circulation 2010, 122:2152-2159. 10.1161/CIRCULATIONAHA.110.948562, 21060071, OMEGA Study Group.
19. Galan P, Kesse-Guyot E, Czernichow S, Briancon S, Blacher J, Hercberg S. Effects of B vitamins and omega 3 fatty acids on cardiovascular diseases: a randomised placebo controlled trial. BMJ 2010, 341:c6273. 10.1136/bmj.c6273, 2993045, 21115589.
20. Hooper L, Thompson RL, Harrison RA, Summerbell CD, Ness AR, Moore HJ, Worthington HV, Durrington PN, Higgins JP, Capps NE, Riemersma RA, Ebrahim SB, Davey Smith G. Risks and benefits of omega 3 fats for mortality, cardiovascular disease, and cancer: systematic review. BMJ 2006, 332:752-760. 10.1136/bmj.38755.366331.2F, 1420708, 16565093.
21. Root M, Collier SR, Zwetsloot KA, West KL, McGinn MC. A randomized trial of fish oil omega-3 fatty acids on arterial health, inflammation, and metabolic syndrome in a young healthy population. Nutr J 2013, 12:40. 10.1186/1475-2891-12-40, 3655855, 23565815.
22. Bosco N, Brahmbhatt V, Oliveira M, Martin FP, Lichti P, Raymond F, Mansourian R, Metairon S, Pace-Asciak C, Bastic Schmid V, Rezzi S, Haller D, Benyacoub J. Effects of increase in fish oil intake on intestinal eicosanoids and inflammation in a mouse model of colitis. Lipids Health Dis 2013, 12:81. 10.1186/1476-511X-12-81, 3691874, 23725086.
23. Mercer DF, Hobson BD, Fischer RT, Talmon GA, Perry DA, Gerhardt BK, Grant WJ, Botha JF, Langnas AN, Quiros-Tejeira RE. Hepatic fibrosis persists and progresses despite biochemical improvement in children treated with intravenous fish oil emulsion. J Pediatr Gastroenterol Nutr 2013, 56:364-369. 10.1097/MPG.0b013e31827e208c, 23201707.
24. Pot GK, Brouwer IA, Enneman A, Rijkers GT, Kampman E, Geelen A. No effect of fish oil supplementation on serum inflammatory markers and their interrelationships: a randomized controlled trial in healthy, middle-aged individuals. Eur J Clin Nutr 2009, 63:1353-1359. 10.1038/ejcn.2009.63, 19623203.
25. Kirkhus B, Lamglait A, Eilertsen KE, Falch E, Haider T, Vik H, Hoem N, Hagve TA, Basu S, Olsen E, Seljeflot I, Nyberg L, Elind E, Ulven SM. Effects of similar intakes of marine n-3 fatty acids from enriched food products and fish oil on cardiovascular risk markers in healthy human subjects. Br J Nutr 2011, 107:1339-1349.
26. Rizos EC, Ntzani EE, Bika E, Kostapanos MS, Elisaf MS. Association between omega-3 fatty acid supplementation and risk of major cardiovascular disease events: a systematic review and meta-analysis. JAMA 2012, 308:1024-1033. 10.1001/2012.jama.11374, 22968891.
27. Correia M, Michel V, Matos AA, Carvalho P, Oliveira MJ, Ferreira RM, Dillies MA, Huerre M, Seruca R, Figueiredo C, Machado JC, Touati E. Docosahexaenoic acid inhibits Helicobacter pylori growth in vitro and mice gastric mucosa colonization. PLoS One 2012, 7:e35072. 10.1371/journal.pone.0035072, 3328494, 22529974.
28. Titos E, Rius B, Gonzalez-Periz A, Lopez-Vicario C, Moran-Salvador E, Martinez-Clemente M, Arroyo V, Claria 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. 10.4049/jimmunol.1100225, 22013115.
29. Schwab JM, Chiang N, Arita M, Serhan CN. Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 2007, 447:869-874. 10.1038/nature05877, 2757086, 17568749.
30. 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. 10.1016/j.bbrc.2008.01.012, 18190790.
31. Weldon SM, Mullen AC, Loscher CE, Hurley LA, Roche HM. Docosahexaenoic acid induces an anti-inflammatory profile in lipopolysaccharide-stimulated human THP-1 macrophages more effectively than eicosapentaenoic acid. J Nutr Biochem 2007, 18:250-258. 10.1016/j.jnutbio.2006.04.003, 16781858.
32. Denkins Y, Kempf D, Ferniz M, Nileshwar S, Marchetti D. Role of omega-3 polyunsaturated fatty acids on cyclooxygenase-2 metabolism in brain-metastatic melanoma. J Lipid Res 2005, 46:1278-1284. 10.1194/jlr.M400474-JLR200, 15772428.
33. Kirkup SE, Cheng Z, Elmes M, Wathes DC, Abayasekara DR. Polyunsaturated fatty acids modulate prostaglandin synthesis by ovine amnion cells in vitro. Reproduction 2010, 140:943-951. 10.1530/REP-09-0575, 20826537.
34. Oliver E, McGillicuddy FC, Harford KA, Reynolds CM, Phillips CM, Ferguson JF, Roche HM. Docosahexaenoic acid attenuates macrophage-induced inflammation and improves insulin sensitivity in adipocytes-specific differential effects between LC n-3 PUFA. J Nutr Biochem 2012, 23:1192-1200. 10.1016/j.jnutbio.2011.06.014, 22137266.
35. Li X, Yu Y, Funk CD. Cyclooxygenase-2 induction in macrophages is modulated by docosahexaenoic acid via interactions with free fatty acid receptor 4 (FFA4). FASEB J 2013, 27:4987-4997. 10.1096/fj.13-235333, 24005906.
36. Calder PC. Immunomodulation by omega-3 fatty acids. Prostaglandins Leukot Essent Fatty Acids 2007, 77:327-335. 10.1016/j.plefa.2007.10.015, 18032006.
37. Stulnig TM. Immunomodulation by polyunsaturated fatty acids: mechanisms and effects. Int Arch Allergy Immunol 2003, 132:310-321. 10.1159/000074898, 14707462.
38. Manali ED, Moschos C, Triantafillidou C, Kotanidou A, Psallidas I, Karabela SP, Roussos C, Papiris S, Armaganidis A, Stathopoulos GT, Maniatis NA. Static and dynamic mechanics of the murine lung after intratracheal bleomycin. BMC Pulm Med 2011, 11:33. 10.1186/1471-2466-11-33, 3128859, 21627835.
39. Ashcroft T, Simpson JM, Timbrell V. Simple method of estimating severity of pulmonary fibrosis on a numerical scale. J Clin Pathol 1988, 41:467-470. 10.1136/jcp.41.4.467, 1141479, 3366935.
40. Awada M, Soulage CO, Meynier A, Debard C, Plaisancie P, Benoit B, Picard G, Loizon E, Chauvin MA, Estienne M, Peretti N, Guichardant M, Lagarde M, Genot C, Michalski MC. Dietary oxidized n-3 PUFA induce oxidative stress and inflammation: role of intestinal absorption of 4-HHE and reactivity in intestinal cells. J Lipid Res 2012, 53:2069-2080. 10.1194/jlr.M026179, 3435540, 22865918.
41. 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, 52:1601-1608. 10.1111/j.1528-1167.2011.03081.x, 21569016.
42. Hantos Z, Daroczy B, Suki B, Nagy S, Fredberg JJ. Input impedance and peripheral inhomogeneity of dog lungs. J Appl Physiol 1992, 72:168-178. 10.1063/1.352153, 1537711.
43. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, Lynch DA, Ryu JH, Swigris JJ, Wells AU, Ancochea J, Bouros D, Carvalho C, Costabel U, Ebina M, Hansell DM, Johkoh T, Kim DS, King TE, Kondoh Y, Myers J, Müller NL, Nicholson AG, Richeldi L, Selman M, Dudden RF, et al. An official ATS/ERS/JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011, 183:788-824. 10.1164/rccm.2009-040GL, 21471066.
44. Silva LP, Lemos AP, Curi R, Azevedo RB. Effects of fish oil treatment on bleomycin-induced pulmonary fibrosis in mice. Cell Biochem Funct 2006, 24:387-396. 10.1002/cbf.1237, 15952187.
45. Baybutt RC, Rosales C, Brady H, Molteni A. Dietary fish oil protects against lung and liver inflammation and fibrosis in monocrotaline treated rats. Toxicology 2002, 175:1-13. 10.1016/S0300-483X(02)00063-X, 12049831.
46. Rees D, Miles EA, Banerjee T, Wells SJ, Roynette CE, Wahle KW, Calder PC. Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men. Am J Clin Nutr 2006, 83:331-342.
47. Healy DA, Wallace FA, Miles EA, Calder PC, Newsholm P. Effect of low-to-moderate amounts of dietary fish oil on neutrophil lipid composition and function. Lipids 2000, 35:763-768. 10.1007/s11745-000-0583-1, 10941877.
48. Chua F, Gauldie J, Laurent GJ. Pulmonary fibrosis: searching for model answers. Am J Respir Cell Mol Biol 2005, 33:9-13. 10.1165/rcmb.2005-0062TR, 15964990.
49. Moore BB, Hogaboam CM. Murine models of pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008, 294:L152-L160.
50. Wilson KS, Worth A, Richards AG, Ford HS. Low-dose bleomycin lung. Med Pediatr Oncol 1982, 10:283-288. 10.1002/mpo.2950100309, 6178008.
51. Moeller A, Ask K, Warburton D, Gauldie J, Kolb M. The bleomycin animal model: a useful tool to investigate treatment options for idiopathic pulmonary fibrosis?. Int J Biochem Cell Biol 2008, 40:362-382. 10.1016/j.biocel.2007.08.011, 2323681, 17936056.
52. Saito F, Tasaka S, Inoue K, Miyamoto K, Nakano Y, Ogawa Y, Yamada W, Shiraishi Y, Hasegawa N, Fujishima S, Takano H, Ishizaka A. Role of interleukin-6 in bleomycin-induced lung inflammatory changes in mice. Am J Respir Cell Mol Biol 2008, 38:566-571. 10.1165/rcmb.2007-0299OC, 18096870.
53. Melendez GC, McLarty JL, Levick SP, Du Y, Janicki JS, Brower GL. Interleukin 6 mediates myocardial fibrosis, concentric hypertrophy, and diastolic dysfunction in rats. Hypertension 2010, 56:225-231. 10.1161/HYPERTENSIONAHA.109.148635, 2921860, 20606113.
54. Phan SH. The myofibroblast in pulmonary fibrosis. Chest 2002, 122:286S-289S. 10.1378/chest.122.6_suppl.286S, 12475801.
55. Kuhn C, McDonald JA. The roles of the myofibroblast in idiopathic pulmonary fibrosis. Ultrastructural and immunohistochemical features of sites of active extracellular matrix synthesis. Am J Pathol 1991, 138:1257-1265. 1886011, 2024710.
56. Wynn TA. Cellular and molecular mechanisms of fibrosis. J Pathol 2008, 214:199-210. 10.1002/path.2277, 2693329, 18161745.
57. Kitaba S, Murota H, Terao M, Azukizawa H, Terabe F, Shima Y, Fujimoto M, Tanaka T, Naka T, Kishimoto T, Katayama I. Blockade of interleukin-6 receptor alleviates disease in mouse model of scleroderma. Am J Pathol 2012, 180:165-176. 10.1016/j.ajpath.2011.09.013, 22062222.
58. Nakagome K, Dohi M, Okunishi K, Tanaka R, Miyazaki J, Yamamoto K. In vivo IL-10 gene delivery attenuates bleomycin induced pulmonary fibrosis by inhibiting the production and activation of TGF-beta in the lung. Thorax 2006, 61:886-894. 10.1136/thx.2005.056317, 2104751, 16809410.
59. Kradin RL, Sakamoto H, Jain F, Zhao LH, Hymowitz G, Preffer F. IL-10 inhibits inflammation but does not affect fibrosis in the pulmonary response to bleomycin. Exp Mol Pathol 2004, 76:205-211. 10.1016/j.yexmp.2003.12.010, 15126102.
60. Peters-Golden M, Bailie M, Marshall T, Wilke C, Phan SH, Toews GB, Moore BB. Protection from pulmonary fibrosis in leukotriene-deficient mice. Am J Respir Crit Care Med 2002, 165:229-235. 10.1164/ajrccm.165.2.2104050, 11790660.
61. Kelley DS, Taylor PC, Nelson GJ, Schmidt PC, Ferretti A, Erickson KL, Yu R, Chandra RK, Mackey BE. Docosahexaenoic acid ingestion inhibits natural killer cell activity and production of inflammatory mediators in young healthy men. Lipids 1999, 34:317-324. 10.1007/s11745-999-0369-5, 10443964.
62. Stratton R, Shiwen X, Martini G, Holmes A, Leask A, Haberberger T, Martin GR, Black CM, Abraham D. Iloprost suppresses connective tissue growth factor production in fibroblasts and in the skin of scleroderma patients. J Clin Invest 2001, 108:241-250. 10.1172/JCI12020, 203022, 11457877.
63. Failla M, Genovese T, Mazzon E, Fruciano M, Fagone E, Gili E, Barera A, la Rosa C, Conte E, Crimi N, Cuzzocrea S, Vancheri C. 16,16-Dimethyl prostaglandin E2 efficacy on prevention and protection from bleomycin-induced lung injury and fibrosis. Am J Respir Cell Mol Biol 2009, 41:50-58. 10.1165/rcmb.2007-0438OC, 19059888.
64. Kowal-Bielecka O, Kowal K, Distler O, Rojewska J, Bodzenta-Lukaszyk A, Michel BA, Gay RE, Gay S, Sierakowski S. Cyclooxygenase- and lipoxygenase-derived eicosanoids in bronchoalveolar lavage fluid from patients with scleroderma lung disease: an imbalance between proinflammatory and antiinflammatory lipid mediators. Arthritis Rheum 2005, 52:3783-3791. 10.1002/art.21432, 16320329.
65. Wilborn J, Crofford LJ, Burdick MD, Kunkel SL, Strieter RM, Peters-Golden M. Cultured lung fibroblasts isolated from patients with idiopathic pulmonary fibrosis have a diminished capacity to synthesize prostaglandin E2 and to express cyclooxygenase-2. J Clin Invest 1995, 95:1861-1868. 10.1172/JCI117866, 295728, 7706493.
66. Ivanova V, Garbuzenko OB, Reuhl KR, Reimer DC, Pozharov VP, Minko T. Inhalation treatment of pulmonary fibrosis by liposomal prostaglandin E2. Eur J Pharm Biopharm 2012, 84:335-344.
67. McCann MR, Monemdjou R, Ghassemi-Kakroodi P, Fahmi H, Perez G, Liu S, Shi-Wen X, Parapuram SK, Kojima F, Denton CP, Abraham DJ, Martel-Pelletier J, Crofford LJ, Leask A, Kapoor M. mPGES-1 null mice are resistant to bleomycin-induced skin fibrosis. Arthritis Res Ther 2011, 13:R6. 10.1186/ar3226, 3546456, 21266028.