Hyperhomocysteinemia exaggerates adventitial inflammation and angiotensin II-induced abdominal aortic aneurysm in mice

Circulation Research

Volumn 111, Issue 10, 2012, Pages 1261-1273

  Liu, Ziyi ^a   Luo, Hongzhi ^a   Zhang, Lu ^a   Huang, Yaqian ^a   Liu, Bo ^a   Ma, Kongyang ^a   Feng, Juan ^a   Xie, Jinsheng ^b   Zheng, Jingang ^c   Hu, Jing ^a   Zhan, Siyan ^a   Zhu, Yi ^a   Xu, Qingbo ^d   Kong, Wei ^a   Wang, Xian ^a  

^a PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c CHINA JAPAN FRIENDSHIP HOSPITAL   (China)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

abdominal aortic aneurysm; adventitial fibroblast; hyperhomocysteinemia; NADPH oxidase 4

Indexed keywords

ANGIOTENSIN II; APOLIPOPROTEIN E; DIPHENYLIODONIUM SALT; DRINKING WATER; FOLIC ACID; HOMOCYSTEINE; INTERLEUKIN 6; MONOCYTE CHEMOTACTIC PROTEIN 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SMALL INTERFERING RNA;

ABDOMINAL AORTA ANEURYSM; ADVENTITIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA DISSECTION; ARTICLE; CELL ACTIVATION; CELL TRANSFORMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; FIBROBLAST; GENE SILENCING; HISTOLOGY; HUMAN; HUMAN TISSUE; HYPERLIPOPROTEINEMIA TYPE 3; INCIDENCE; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; META ANALYSIS (TOPIC); MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; VASCULITIS;

ADVENTITIA; ANGIOTENSIN II; ANIMALS; AORTIC ANEURYSM, ABDOMINAL; APOLIPOPROTEINS E; CHEMOKINE CCL2; DISEASE MODELS, ANIMAL; FEMALE; FIBROBLASTS; HUMANS; HYPERHOMOCYSTEINEMIA; INCIDENCE; INTERLEUKIN-6; MALE; MICE; MICE, MUTANT STRAINS; MIDDLE AGED; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RISK FACTORS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; VASCULITIS; VASOCONSTRICTOR AGENTS;

EID: 84868693888     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.270520     Document Type: Article

References (48)

1. Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8:92-102.
2. Choke E, Cockerill G, Wilson WR, Sayed S, Dawson J, Loftus I, Thompson MM. A review of biological factors implicated in abdominal aortic aneurysm rupture. Eur J Vasc Endovasc Surg. 2005;30:227-244. (Pubitemid 41086292)
3. Michel JB, Martin-Ventura JL, Egido J, Sakalihasan N, Treska V, Lindholt J, Allaire E, Thorsteinsdottir U, Cockerill G, Swedenborg J; FAD EU consortium. Novel aspects of the pathogenesis of aneurysms of the abdominal aorta in humans. Cardiovasc Res. 2011;90:18-27.
4. Boushey CJ, Beresford SA, Omenn GS, Motulsky AG. A quantitative assessment of plasma homocysteine as a risk factor for vascular disease. Probable benefts of increasing folic acid intakes. JAMA. 1995;274:1049-1057.
5. Nygård O, Nordrehaug JE, Refsum H, Ueland PM, Farstad M, Vollset SE. Plasma homocysteine levels and mortality in patients with coronary artery disease. N Engl J Med. 1997;337:230-236. (Pubitemid 27310438)
6. Giusti B, Marcucci R, Lapini I, Sestini I, Lenti M, Yacoub M, Pepe G. Role of hyperhomocysteinemia in aortic disease. Cell Mol Biol (Noisy-le-grand). 2004;50:945-952.
7. Warsi AA, Davies B, Morris-Stiff G, Hullin D, Lewis MH. Abdominal aortic aneurysm and its correlation to plasma homocysteine, and vitamins. Eur J Vasc Endovasc Surg. 2004;27:75-79. (Pubitemid 38008997)
8. Sof F, Marcucci R, Giusti B, Pratesi G, Lari B, Sestini I, Lo Sapio P, Pulli R, Pratesi C, Abbate R, Gensini GF. High levels of homocyste-ine, lipoprotein (a) and plasminogen activator inhibitor-1 are present in patients with abdominal aortic aneurysm. Thromb Haemost. 2005;94:1094-1098. (Pubitemid 41645954)
9. Spark JI, Laws P, Fitridge R. The incidence of hyperhomocysteinaemia in vascular patients. Eur J Vasc Endovasc Surg. 2003;26:558-561. (Pubitemid 37362100)
10. Brunelli T, Prisco D, Fedi S, Rogolino A, Farsi A, Marcucci R, Giusti B, Pratesi C, Pulli R, Gensini GF, Abbate R, Pepe G. High prevalence of mild hyperhomocysteinemia in patients with abdominal aortic aneu-rysm. J Vasc Surg. 2000;32:531-536.
11. Peeters AC, van Landeghem BA, Graafsma SJ, Kranendonk SE, Hermus AR, Blom HJ, den Heijer M. Low vitamin B6, and not plasma homo-cysteine concentration, as risk factor for abdominal aortic aneurysm: a retrospective case-control study. J Vasc Surg. 2007;45:701-705. (Pubitemid 46483942)
12. Jones GT, Harris EL, Phillips LV, van Rij AM. The methylenetetrahy- drofolate reductase C677T polymorphism does not associate with susceptibility to abdominal aortic aneurysm. Eur J Vasc Endovasc Surg. 2005;30:137-142. (Pubitemid 40932011)
13. Strauss E, Waliszewski K, Gabriel M, Zapalski S, Pawlak AL. Increased risk of the abdominal aortic aneurysm in carriers of the MTHFR 677T allele. J Appl Genet. 2003;44:85-93. (Pubitemid 37138579)
14. Giusti B, Saracini C, Bolli P, Magi A, Sestini I, Sticchi E, Pratesi G, Pulli R, Pratesi C, Abbate R. Genetic analysis of 56 polymorphisms in 17 genes involved in methionine metabolism in patients with abdominal aortic aneurysm. J Med Genet. 2008;45:721-730.
15. Nordon IM, Hinchliffe RJ, Loftus IM, Thompson MM. Pathophysiology and epidemiology of abdominal aortic aneurysms. Nat Rev Cardiol. 2011;8:92-102.
16. Enzerink A, Vaheri A. Fibroblast activation in vascular infammation. J Thromb Haemost. 2011;9:619-626.
17. Forte A, Della Corte A, De Feo M, Cerasuolo F, Cipollaro M. Role of myofbroblasts in vascular remodelling: focus on restenosis and aneu-rysm. Cardiovasc Res. 2010;88:395-405.
18. Kuivaniemi H, Platsoucas CD, Tilson MD 3rd. Aortic aneurysms: an immune disease with a strong genetic component. Circulation. 2008;117:242-252.
19. Koch AE, Haines GK, Rizzo RJ, Radosevich JA, Pope RM, Robinson PG, Pearce WH. Human abdominal aortic aneurysms. Immunophenotypic analysis suggesting an immune-mediated response. Am J Pathol. 1990;137:1199-1213.
20. Tieu BC, Lee C, Sun H, Lejeune W, Recinos A 3rd, Ju X, Spratt H, Guo DC, Milewicz D, Tilton RG, Brasier AR. An adventitial IL-6/MCP1 am-plifcation loop accelerates macrophage-mediated vascular infammation leading to aortic dissection in mice. J Clin Invest. 2009;119:3637-3651.
21. Tieu BC, Ju X, Lee C, Sun H, Lejeune W, Recinos A 3rd, Brasier AR, Tilton RG. Aortic adventitial fbroblasts participate in angioten-sin-induced vascular wall infammation and remodeling. J Vasc Res. 2011;48:261-272.
22. Deguchi JO, Huang H, Libby P, Aikawa E, Whittaker P, Sylvan J, Lee RT, Aikawa M. Genetically engineered resistance for MMP collagenases promotes abdominal aortic aneurysm formation in mice infused with an-giotensin II. Lab Invest. 2009;89:315-326.
23. Clarke R, Daly L, Robinson K, Naughten E, Cahalane S, Fowler B, Graham I. Hyperhomocysteinemia: an independent risk factor for vascular disease. N Engl J Med. 1991;324:1149-1155.
24. Armitage JM, Bowman L, Clarke RJ, Wallendszus K, Bulbulia R, Rahimi K, Haynes R, Parish S, Sleight P, Peto R, Collins R; Study of the Effectiveness of Additional Reductions in Cholesterol and Homocysteine (SEARCH) Collaborative Group. Effects of homocysteine-lowering with folic acid plus vitamin B12 vs placebo on mortality and major morbidity in myocardial infarction survivors: a randomized trial. JAMA. 2010;303:2486-2494.
25. Bostom AG, Carpenter MA, Kusek JW, et al. Homocysteine-lowering and cardiovascular disease outcomes in kidney transplant recipients: primary results from the Folic Acid for Vascular Outcome Reduction in Transplantation trial. Circulation. 2011;123:1763-1770.
26. Spence JD, Stampfer MJ. Understanding the complexity of homocys-teine lowering with vitamins: the potential role of subgroup analyses. JAMA. 2012;306:2610-2611.
27. Rolland PH, Friggi A, Barlatier A, Piquet P, Latrille V, Faye MM, Guillou J, Charpiot P, Bodard H, Ghiringhelli O. Hyperhomocysteinemia-induced vascular damage in the minipig. Captopril-hydrochlorothiazide combination prevents elastic alterations. Circulation. 1995;91:1161-1174.
28. Charpiot P, Bescond A, Augier T, Chareyre C, Fraterno M, Rolland PH, Garçon D. Hyperhomocysteinemia induces elastolysis in minipig arteries: structural consequences, arterial site specifcity and effect of captopril-hydrochlorothiazide. Matrix Biol. 1998;17:559-574. (Pubitemid 29017224)
29. Refsum H, Smith AD, Ueland PM, Nexo E, Clarke R, McPartlin J, Johnston C, Engbaek F, Schneede J, McPartlin C, Scott JM. Facts and recommendations about total homocysteine determinations: an expert opinion. Clin Chem. 2004;50:3-32. (Pubitemid 38125696)
30. Recinos A 3rd, LeJeune WS, Sun H, Lee CY, Tieu BC, Lu M, Hou T, Boldogh I, Tilton RG, Brasier AR. Angiotensin II induces IL-6 expression and the Jak-STAT3 pathway in aortic adventitia of LDL receptor-defcient mice. Atherosclerosis. 2007;194:125-133. (Pubitemid 47464314)
31. Feng J, Zhang Z, Kong W, Liu B, Xu Q, Wang X. Regulatory T cells ameliorate hyperhomocysteinaemia-accelerated atherosclerosis in apoE-/-mice. Cardiovasc Res. 2009;84:155-163.
32. Zeng X, Dai J, Remick DG, Wang X. Homocysteine mediated expression and secretion of monocyte chemoattractant protein-1 and interleu-kin-8 in human monocytes. Circ Res. 2003;93:311-320. (Pubitemid 37048243)
33. Jagadesham VP, Scott DJ, Carding SR. Abdominal aortic aneurysms: an autoimmune disease? Trends Mol Med. 2008;14:522-529.
34. Herrmann W, Herrmann M, Obeid R. Hyperhomocysteinaemia: a critical review of old and new aspects. Curr Drug Metab. 2007;8:17-31. (Pubitemid 46043889)
35. Werstuck GH, Lentz SR, Dayal S, Hossain GS, Sood SK, Shi YY, Zhou J, Maeda N, Krisans SK, Malinow MR, Austin RC. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest. 2001;107:1263-1273. (Pubitemid 32494543)
36. Sakata N, Nabeshima K, Iwasaki H, Tashiro T, Uesugi N, Nakashima O, Ito H, Kawanami T, Furuya K, Kojima M. Possible involvement of myo-fbroblast in the development of infammatory aortic aneurysm. Pathol Res Pract. 2007;203:21-29. (Pubitemid 46118076)
37. Maiellaro K, Taylor WR. The role of the adventitia in vascular infamma-tion. Cardiovasc Res. 2007;75:640-648.
38. Sartore S, Chiavegato A, Faggin E, Franch R, Puato M, Ausoni S, Pauletto P. Contribution of adventitial fbroblasts to neointima formation and vascular remodeling: from innocent bystander to active participant. Circ Res. 2001;89:1111-1121. (Pubitemid 34627868)
39. Siow RC, Churchman AT. Adventitial growth factor signalling and vascular remodelling: potential of perivascular gene transfer from the outside-in. Cardiovasc Res. 2007;75:659-668. (Pubitemid 47238743)
40. Haurani MJ, Pagano PJ. Adventitial fbroblast reactive oxygen species as autacrine and paracrine mediators of remodeling: bellwether for vascular disease? Cardiovasc Res. 2007;75:679-689. (Pubitemid 47238744)
41. Shen WL, Gao PJ, Che ZQ, Ji KD, Yin M, Yan C, Berk BC, Zhu DL. NAD(P)H oxidase-derived reactive oxygen species regulate angioten-sin-II induced adventitial fbroblast phenotypic differentiation. Biochem Biophys Res Commun. 2006;339:337-343. (Pubitemid 41697555)
42. Csányi G, Taylor WR, Pagano PJ. NOX and infammation in the vascular adventitia. Free Radic Biol Med. 2009;47:1254-1266.
43. Pagano PJ, Clark JK, Cifuentes-Pagano ME, Clark SM, Callis GM, Quinn MT. Localization of a constitutively active, phagocyte-like NADPH oxidase in rabbit aortic adventitia: enhancement by angiotensin II. Proc Natl Acad Sci USA. 1997;94:14483-14488. (Pubitemid 28041400)
44. Thakur S, Du J, Hourani S, Ledent C, Li JM. Inactivation of adenos-ine A2A receptor attenuates basal and angiotensin II-induced ROS production by Nox2 in endothelial cells. J Biol Chem. 2010;285: 40104-40113.
45. Papatheodorou L, Weiss N. Vascular oxidant stress and infammation in hyperhomocysteinemia. Antioxid Redox Signal. 2007;9:1941-1958. (Pubitemid 47628602)
46. Barnes JL, Gorin Y. Myofbroblast differentiation during fbrosis: role of NAD(P)H oxidases. Kidney Int. 2011;79:944-956.
47. van de Laar IM, Oldenburg RA, Pals G, et al. Mutations in SMAD3 cause a syndromic form of aortic aneurysms and dissections with early-onset osteoarthritis. Nat Genet. 2011;43:121-126.
48. Bondi CD, Manickam N, Lee DY, Block K, Gorin Y, Abboud HE, Barnes JL. NAD(P)H oxidase mediates TGF-beta1-induced activation of kidney myofbroblasts. J Am Soc Nephrol. 2010;21:93-102.