The ω-3 polyunsaturated fatty acid, eicosapentaenoic acid, attenuates abdominal aortic aneurysm development via suppression of tissue remodeling

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Wang, Jack H ^a   Eguchi, Kosei ^a   Matsumoto, Sahohime ^a   Fujiu, Katsuhito ^a   Komuro, Issei ^a   Nagai, Ryozo ^b   Manabe, Ichiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHLORIDE; GELATINASE A; GELATINASE B; ICOSAPENTAENOIC ACID; OSTEOCLAST DIFFERENTIATION FACTOR; MMP2 PROTEIN, MOUSE; MMP9 PROTEIN, MOUSE; TNFSF11 PROTEIN, MOUSE;

ABDOMINAL AORTA; ABDOMINAL AORTA ANEURYSM; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTERY CALCIFICATION; ARTERY DIAMETER; ARTICLE; CELL STIMULATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DIET SUPPLEMENTATION; HISTOPATHOLOGY; MACROPHAGE; MALE; MEDICAL PARAMETERS; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; RAW264.7 CELL LINE; REAL TIME POLYMERASE CHAIN REACTION; TISSUE LEVEL; TISSUE REMODELING; ANIMAL; AORTA; AORTIC ANEURYSM, ABDOMINAL; BAGG ALBINO MOUSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; METABOLISM; PATHOLOGY; VASCULAR REMODELING;

ANIMALS; AORTA; AORTIC ANEURYSM, ABDOMINAL; EICOSAPENTAENOIC ACID; GENE EXPRESSION REGULATION; MACROPHAGES; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED BALB C; RANK LIGAND; VASCULAR REMODELING;

EID: 84900451710     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096286     Document Type: Article

References (54)

1. Siegel CL, Cohan RH, Korobkin M, Alpern MB, Courneya DL, et al. (1994) Abdominal aortic aneurysm morphology: CT features in patients with ruptured and nonruptured aneurysms. Am J Roentgenol 163: 1123-1129. (Pubitemid 24355705)
2. Force USPST (2005) Screening for abdominal aortic aneurysm: recommendation statement. Ann Intern Med 142: 198-202.
3. Norman PE, Spilsbury K, Semmens JB (2011) Falling rates of hospitalization and mortality from abdominal aortic aneurysms in Australia. J Vasc Surg 53: 274-277.
4. Weintraub NL (2009) Understanding abdominal aortic aneurysm. N Engl J Med 361: 1114-1116.
5. Sakalihasan N, Limet R, Defawe OD (2005) Abdominal aortic aneurysm. Lancet 365: 1577-1589. (Pubitemid 40615407)
6. Longo GM, Xiong W, Greiner TC, Zhao Y, Fiotti N, et al. (2002) Matrix metalloproteinases 2 and 9 work in concert to produce aortic aneurysms. J Clin Invest 110: 625-632. (Pubitemid 34988786)
7. Xiong W, Zhao Y, Prall A, Greiner TC, Baxter BT (2004) Key roles of CD4+ T cells and IFN-c in the development of abdominal aortic aneurysms in a murine model. J Immunol 172: 2607-2612. (Pubitemid 38182412)
8. Eliason JL, Hannawa KK, Ailawadi G, Sinha I, Ford JW, et al. (2005) Neutrophil depletion inhibits experimental abdominal aortic aneurysm formation. Circulation 112: 232-240. (Pubitemid 40982306)
9. Yoshimura K, Aoki H, Ikeda Y, Fujii K, Akiyama N, et al. (2005) Regression of abdominal aortic aneurysm by inhibition of c-Jun N-terminal kinase. Nat Med 11: 1330-1338. (Pubitemid 41752914)
10. Xiong W, MacTaggart J, Knispel R, Worth J, Persidsky Y, et al. (2009) Blocking TNF-α Attenuates Aneurysm Formation in a Murine Model. J Immunol 183: 2741-2746.
11. Kris-Etherton PM, Harris WS, Appel LJ, Nutrition Committee (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106: 2747-2757. (Pubitemid 35364932)
12. Schwab JM, Chiang N, Arita M, Serhan CN (2007) Resolvin E1 and protectin D1 activate inflammation-resolution programmes. Nature 447: 869-874. (Pubitemid 46920139)
13. Oh DY, Talukdar S, Bae EJ, Imamura T, Morinaga H, et al. (2010) GPR120 is an omega-3 fatty acid receptor mediating potent anti-inflammatory and insulinsensitizing effects. Cell 142: 687-698.
14. Tull SP, Yates CM, Maskrey BH, O'Donnell VB, Madden J, et al. (2009) Omega-3 fatty acids and inflammation: novel interactions reveal a new step in neutrophil recruitment. PLoS Biol 7: e1000177.
15. Chen J, Shearer GC, Chen Q, Healy CL, Beyer AJ, et al. (2011) Omega-3 fatty acids prevent pressure overload-induced cardiac fibrosis through activation of cyclic GMP/protein kinase G signaling in cardiac fibroblasts. Circulation 123: 584-593.
16. An WS, Kim HJ, Cho K-H, Vaziri ND (2009) Omega-3 fatty acid supplementation attenuates oxidative stress, inflammation, and tubulointerstitial fibrosis in the remnant kidney. Am J Physiol Renal Physiol 297: F895-903.
17. Yokoyama M, Origasa H, Matsuzaki M, Matsuzawa Y, Saito Y, et al. (2007) Effects of eicosapentaenoic acid on major coronary events in hypercholesterolaemic patients (JELIS): a randomised open-label, blinded endpoint analysis. Lancet 369: 1090-1098. (Pubitemid 46483662)
18. Saravanan P, Davidson NC, Schmidt EB, Calder PC (2010) Cardiovascular effects of marine omega-3 fatty acids. Lancet 376: 540-550.
19. Matsumoto M, Sata M, Fukuda D, Tanaka K, Soma M, et al. (2008) Orally administered eicosapentaenoic acid reduces and stabilizes atherosclerotic lesions in ApoE-deficient mice. Atherosclerosis 197: 524-533. (Pubitemid 351417875)
20. Serhan CN, Chiang N, Van Dyke TE (2008) Resolving inflammation: dual antiinflammatory and pro-resolution lipid mediators. Nat Rev Immunol 8: 349-361. (Pubitemid 351595216)
21. Wang Y, Krishna S, Golledge J (2013) The calcium chloride-induced rodent model of abdominal aortic aneurysm. Atherosclerosis 226: 29-39.
22. Shimizu K, Mitchell RN, Libby P (2006) Inflammation and cellular immune responses in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 26: 987-994. (Pubitemid 43732102)
23. Collin-Osdoby P (2004) Regulation of vascular calcification by osteoclast regulatory factors RANKL and osteoprotegerin. Circ Res 95: 1046-1057.
24. Panizo S, Cardus A, Encinas M, Parisi E, Valcheva P, et al. (2009) RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4-dependent pathway. Circ Res 104: 1041-1048.
25. Pyo R, Lee JK, Shipley JM, Curci JA, Mao D, et al. (2000) Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J Clin Invest 105: 1641-1649. (Pubitemid 30390315)
26. Davis V, Persidskaia R, Baca-Regen L, Itoh Y, Nagase H, et al. (1998) Matrix metalloproteinase-2 production and its binding to the matrix are increased in abdominal aortic aneurysms. Arterioscler Thromb Vasc Biol 18: 1625-1633. (Pubitemid 28465416)
27. Thompson RW, Holmes DR, Mertens RA, Liao S, Botney MD, et al. (1995) Production and localization of 92-kilodalton gelatinase in abdominal aortic aneurysms. An elastolytic metalloproteinase expressed by aneurysm-infiltrating macrophages. J Clin Invest 96: 318-326.
28. Fujiu K, Manabe I, Nagai R (2011) Renal collecting duct epithelial cells regulate inflammation in tubulointerstitial damage in mice. J Clin Invest 121: 3425-3441.
29. Gissi-HF Investigators (2008) 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 372: 1223-1230.
30. Bønaa KH, Bjerve KS, Straume B, Gram IT, Thelle D (1990) Effect of eicosapentaenoic and docosahexaenoic acids on blood pressure in hypertension. N Engl J Med 322: 795-801.
31. Pradelli L, Mayer K, Muscaritoli M, Heller A (2012) n-3 fatty acid-enriched parenteral nutrition regimens in elective surgical and ICU patients: a metaanalysis. Crit Care 16: R184.
32. Donadio JV, Bergstralh EJ, Offord KP, Spencer DC, Holley KE (1994) A controlled trial of fish oil in IgA nephropathy. N Engl J Med 331: 1194-1199. (Pubitemid 24331337)
33. Visse R, Nagase H (2003) Matrix metalloproteinases and tissue inhibitors of metalloproteinases: structure, function, and biochemistry. Circ Res 92: 827-839. (Pubitemid 36542523)
34. Allaire E, Forough R, Clowes M, Starcher B, Clowes AW (1998) Local overexpression of TIMP-1 prevents aortic aneurysm degeneration and rupture in a rat model. J Clin Invest 102: 1413-1420. (Pubitemid 28467570)
35. Defawe OD, Colige A, Lambert CA, Munaut C, Delvenne P, et al. (2003) TIMP-2 and PAI-1 mRNA levels are lower in aneurysmal as compared to athero-occlusive abdominal aortas. Cardiovasc Res 60: 205-213. (Pubitemid 38373493)
36. Wang S, Zhang C, Zhang M, Liang B, Zhu H, et al. (2012) Activation of AMPactivated protein kinase alpha2 by nicotine instigates formation of abdominal aortic aneurysms in mice in vivo. Nat Med 18: 902-910.
37. Abedin M, Lim J, Tang TB, Park D, Demer LL, et al. (2006) N-3 fatty acids inhibit vascular calcification via the p38-mitogen-activated protein kinase and peroxisome proliferator-activated receptor-gamma pathways. Circ Res 98: 727-729.
38. Byon CH, Sun Y, Chen J, Yuan K, Mao X, et al. (2011) Runx2-upregulated receptor activator of nuclear factor kb ligand in calcifying smooth muscle cells promotes migration and osteoclastic differentiation of macrophages. Arterioscler Thromb Vasc Biol 31: 1387-1396.
39. Daugherty A, Manning MW, Cassis LA (2000) Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest 105: 1605-1612. (Pubitemid 30390311)
40. Miyake T, Morishita R (2009) Pharmacological treatment of abdominal aortic aneurysm. Cardiovasc Res 83: 436-443.
41. Lindeman JHN, Abdul-Hussien H, van Bockel JH, Wolterbeek R, Kleemann R (2009) Clinical trial of doxycycline for matrix metalloproteinase-9 inhibition in patients with an abdominal aneurysm: doxycycline selectively depletes aortic wall neutrophils and cytotoxic T cells. Circulation 119: 2209-2216.
42. Mosorin M, Juvonen J, Biancari F, Satta J, Surcel H-M, et al. (2001) Use of doxycycline to decrease the growth rate of abdominal aortic aneurysms: A randomized, double-blind, placebo-controlled pilot study. J Vasc Surg 34: 606-610. (Pubitemid 33664907)
43. Vammen S, Lindholt JS, Østergaard L, Fasting H, Henneberg EW (2001) Randomized double-blind controlled trial of roxithromycin for prevention of abdominal aortic aneurysm expansion. Br J Surg 88: 1066-1072. (Pubitemid 32868660)
44. Rughani G, Robertson L, Clarke M (2012) Medical treatment for small abdominal aortic aneurysms. Cochrane Database Syst Rev 9.
45. van der Meij E, Koning GG, Vriens PW, Peeters MF, Meijer CA, et al. (2013) A clinical evaluation of statin pleiotropy: statins selectively and dose-dependently reduce vascular inflammation. PLoS ONE 8: e53882.
46. Itoh M, Suganami T, Satoh N, Tanimoto-Koyama K, Yuan X, et al. (2007) Increased adiponectin secretion by highly purified eicosapentaenoic acid in rodent models of obesity and human obese subjects. Arterioscler Thromb Vasc Biol 27: 1918-1925. (Pubitemid 47315642)
47. Connor KM, SanGiovanni JP, Lofqvist C, Aderman CM, Chen J, et al. (2007) Increased dietary intake of [omega]-3-polyunsaturated fatty acids reduces pathological retinal angiogenesis. Nat Med 13: 868-873. (Pubitemid 47038185)
48. Chiou AC, Chiu B, Pearce WH (2001) Murine aortic aneurysm produced by periarterial application of calcium chloride. J Surg Res 99: 371-376. (Pubitemid 32703462)
49. Aikawa E, Aikawa M, Libby P, Figueiredo J-L, Rusanescu G, et al. (2009) Arterial and aortic valve calcification abolished by elastolytic cathepsin s deficiency in chronic renal disease. Circulation 119: 1785-1794.
50. Yuan L-Q, Zhu J-H, Wang H-W, Liang Q-H, Xie H, et al. (2011) RANKL is a downstream mediator for insulin-induced osteoblastic differentiation of vascular smooth muscle cells. PLoS ONE 6: e29037.
51. Hu X, Beeton C (2010) Detection of functional matrix metalloproteinases by zymography. J Vis Exp: e2445.
52. Eguchi K, Manabe I, Oishi-Tanaka Y, Ohsugi M, Kono N, et al. (2012) Saturated fatty acid and TLR signaling link b cell dysfunction and islet inflammation. Cell Metab 15: 518-533.
53. Shen H, Eguchi K, Kono N, Fujiu K, Matsumoto S, et al. (2013) Saturated fatty acid palmitate aggravates neointima formation by promoting smooth muscle phenotypic modulation. Arterioscler Thromb Vasc Biol 33: 2596-2607.
54. Wylie-Sears J, Aikawa E, Levine RA, Yang J-H, Bischoff J (2011) Mitral valve endothelial cells with osteogenic differentiation potential. Arterioscler Thromb Vasc Biol 31: 598-607. Technology