Toll-like receptor 4 immunohistochemical expression is enhanced in macrophages of symptomatic carotid atherosclerotic plaques

Cerebrovascular Diseases

Volumn 31, Issue 1, 2010, Pages 29-36

  Katsargyris, Athanasios ^a   Tsiodras, Sotirios ^c   Theocharis, Stamatios ^b   Giaginis, Konstantinos ^b   Vasileiou, Ioanna ^a   Bakoyiannis, Christos ^a   Georgopoulos, Sotiris ^a   Bastounis, Elias ^a   Klonaris, Chris ^a  

^a IASO GENERAL HOSPITAL   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

^c UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

Carotid artery disease; Immunohistochemistry; Stroke; Symptomatic carotid stenosis; Toll like receptor; Transient ischemic attack; Unstable carotid plaque; Vulnerable plaque

Indexed keywords

C REACTIVE PROTEIN; HOMOCYSTEINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; TOLL LIKE RECEPTOR 4; TRIACYLGLYCEROL;

AGED; ARTICLE; BODY MASS; CAROTID ATHEROSCLEROSIS; CAROTID ENDARTERECTOMY; CHOLESTEROL BLOOD LEVEL; DISEASE ASSOCIATION; FEMALE; HUMAN; HUMAN TISSUE; HYPERLIPIDEMIA; IMMUNOHISTOCHEMISTRY; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOKING; SMOOTH MUSCLE FIBER; SYMPTOMATOLOGY; TRANSIENT ISCHEMIC ATTACK; TRIACYLGLYCEROL BLOOD LEVEL;

AGED; ANGIOGRAPHY, DIGITAL SUBTRACTION; ASYMPTOMATIC DISEASES; CAROTID STENOSIS; ENDARTERECTOMY, CAROTID; FEMALE; GREECE; HUMANS; IMMUNOHISTOCHEMISTRY; ISCHEMIC ATTACK, TRANSIENT; LOGISTIC MODELS; MACROPHAGES; MALE; MUSCLE, SMOOTH, VASCULAR; ODDS RATIO; RISK ASSESSMENT; RISK FACTORS; TOLL-LIKE RECEPTOR 4; ULTRASONOGRAPHY, DOPPLER, DUPLEX; UP-REGULATION;

EID: 77958507145     PISSN: 10159770     EISSN: None     Source Type: Journal    
DOI: 10.1159/000320259     Document Type: Article

References (41)

1. Redgrave JN, Lovett JK, Gallagher PJ, Rothwell PM: Histological assessment of 526 symptomatic carotid plaques in relation to the nature and timing of ischemic symptoms: the Oxford Plaque Study. Circulation 2006;113:2320-2328.
2. Ross R: Atherosclerosis - an inflammatory disease. N Engl J Med 1999;340:115-126.
3. Rothwell PM, Gibson R, Warlow CP: Interrelation between plaque surface morphology and degree of stenosis on carotid angiograms and the risk of ischemic stroke in patients with symptomatic carotid stenosis. On behalf of the European Carotid Surgery Trialists' Collaborative Group. Stroke 2000;31:615-621.
4. Wahlgren CM, Zheng W, Shaalan W, Tang J, Bassiouny HS: Human carotid plaque calcification and vulnerability: relationship between degree of plaque calcification, fibrous cap inflammatory gene expression and symptomatology. Cerebrovasc Dis 2009;27:193-200.
5. Ross R: Atherosclerosis is an inflammatory disease. Am Heart J 1999;138: S419-420.
6. Libby P, Ridker PM, Maseri A: Inflammation and atherosclerosis. Circulation 2002;105:1135-1143.
7. Ridker PM, Buring JE, Cook NR, Rifai N: Creactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14, 719 initially healthy American women. Circulation 2003;107:391-397.
8. Okazaki S, Furukado S, Abe Y, Tanaka M, Miwa K, Yamagami H, Sakaguchi M, Sakoda S, Kitagawa K: Association of inflammatory markers and carotid intima-media thickness with the risk of cardiovascular events in high-risk patients. Cerebrovasc Dis 2010;30:180-187.
9. Spagnoli LG, Mauriello A, Sangiorgi G, Fratoni S, Bonanno E, Schwartz RS, Piepgras DG, Pistolese R, Ippoliti A, Holmes DR Jr: Extracranial thrombotically active carotid plaque as a risk factor for ischemic stroke. JAMA 2004;292:1845-1852.
10. Spagnoli LG, Bonanno E, Sangiorgi G, Mauriello A: Role of inflammation in atherosclerosis. J Nucl Med 2007;48:1800-1815.
11. Kaperonis EA, Liapis CD, Kakisis JD, Dimitroulis D, Papavassiliou VG: Inflammation and atherosclerosis. Eur J Vasc Endovasc Surg 2006;31:386-393.
12. Redgrave JN, Lovett JK, Syed AB, Rothwell PM: Histological features of symptomatic carotid plaques in patients with impaired glucose tolerance and diabetes (Oxford Plaque Study). Cerebrovasc Dis 2008;26:79-86.
13. Chalela JA: Evaluating the carotid plaque: going beyond stenosis. Cerebrovasc Dis 2009;27(suppl 1):19-24.
14. Saba L, Mallarini G: Fissured fibrous cap of vulnerable carotid plaques and symptomaticity: are they correlated? Preliminary results by using multi-detector-row CT angiography. Cerebrovasc Dis 2009;27:322-327.
15. Pasterkamp G, Van Keulen JK, De Kleijn DP: Role of Toll-like receptor 4 in the initiation and progression of atherosclerotic disease. Eur J Clin Invest 2004;34:328-334.
16. Tobias P, Curtiss LK: Thematic review series: the immune system and atherogenesis. Paying the price for pathogen protection: Toll receptors in atherogenesis. J Lipid Res 2005;46:404-411.
17. Curtiss LK, Tobias PS: The toll of Toll-like receptors, especially Toll-like receptor 2, on murine atherosclerosis. Curr Drug Targets 2007;8:1230-1238.
18. Hommels MJ, Kroon AA, Netea MG, de Leeuw PW, Bruggeman CA, Leiner T, Koster DA, Stalenhoef AF, van der Ven AJ: The Asp-299Gly Toll-like receptor 4 polymorphism in advanced aortic atherosclerosis. Neth J Med 2007;65:203-207.
19. Li H, Sun B: Toll-like receptor 4 in atherosclerosis. J Cell Mol Med 2007;11:88-95.
20. Liu X, Ukai T, Yumoto H, Davey M, Goswami S, Gibson FC 3rd, Genco CA: Toll-like receptor 2 plays a critical role in the progression of atherosclerosis that is independent of dietary lipids. Atherosclerosis 2008;196:146-154.
21. Katsargyris A, Klonaris C, Bastounis E, Theocharis S: Toll-like receptor modulation: a novel therapeutic strategy in cardiovascular disease? Expert Opin Ther Targets 2008;12:1329-1346.
22. Edfeldt K, Swedenborg J, Hansson GK, Yan ZQ: Expression of Toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation. Circulation 2002;105:1158-1161.
23. Xu XH, Shah PK, Faure E, Equils O, Thomas L, Fishbein MC, Luthringer D, Xu XP, Rajavashisth TB, Yano J, Kaul S, Arditi M: Tolllike receptor-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL. Circulation 2001;104:3103-3108.
24. Labrum R, Bevan S, Sitzer M, Lorenz M, Markus HS: Toll receptor polymorphisms and carotid artery intima-media thickness. Stroke 2007;38:1179-1184. (Pubitemid 351664263)
25. Liapis CD, Bell PR, Mikhailidis D, Sivenius J, Nicolaides A, Fernandes e Fernandes J, Biasi G, Norgren L: ESVS guidelines. Invasive treatment for carotid stenosis: indications, techniques. Eur J Vasc Endovasc Surg 2009;37:1-19.
26. Katsargyris A, Theocharis SE, Tsiodras S, Giaginis K, Bastounis E, Klonaris C: Enhanced TLR4 endothelial cell immunohistochemical expression in symptomatic carotid atherosclerotic plaques. Expert Opin Ther Targets 2010;14:1-10.
27. Davies MJ, Thomas AC: Plaque fissuring - the cause of acute myocardial infarction, sudden ischaemic death, and crescendo angina. Br Heart J 1985;53:363-373.
28. Fuster V, Moreno PR, Fayad ZA, Corti R, Badimon JJ: Atherothrombosis and highrisk plaque. I. Evolving concepts. J Am Coll Cardiol 2005;46:937-954.
29. Tureyen K, Vemuganti R, Salamat MS, Dempsey RJ: Increased angiogenesis and angiogenic gene expression in carotid artery plaques from symptomatic stroke patients. Neurosurgery 2006;58:971-977, discussion 971-977.
30. Pelisek J, Rudelius M, Zepper P, Poppert H, Reeps C, Schuster T, Eckstein HH: Multiple biological predictors for vulnerable carotid lesions. Cerebrovasc Dis 2009;28:601-610.
31. Gough PJ, Gomez IG, Wille PT, Raines EW: Macrophage expression of active MMP-9 induces acute plaque disruption in ApoE-deficient mice. J Clin Invest 2006;116:59-69.
32. Moreno PR, Purushothaman KR, Fuster V, Echeverri D, Truszczynska H, Sharma SK, Badimon JJ, O'Connor WN: Plaque neovascularization is increased in ruptured atherosclerotic lesions of human aorta: implications for plaque vulnerability. Circulation 2004;110:2032-2038.
33. McCarthy MJ, Loftus IM, Thompson MM, Jones L, London NJ, Bell PR, Naylor AR, Brindle NP: Angiogenesis and the atherosclerotic carotid plaque: an association between symptomatology and plaque morphology. J Vasc Surg 1999;30:261-268.
34. Mofidi R, Crotty TB, McCarthy P, Sheehan SJ, Mehigan D, Keaveny TV: Association between plaque instability, angiogenesis and symptomatic carotid occlusive disease. Br J Surg 2001;88:945-950.
35. Vicenzini E, Giannoni MF, Benedetti-Valentini F, Lenzi GL: Imaging of carotid plaque angiogenesis. Cerebrovasc Dis 2009;27(suppl 2):48-54.
36. Polverini PJ, Cotran PS, Gimbrone MA Jr, Unanue ER: Activated macrophages induce vascular proliferation. Nature 1977;269:804-806.
37. Lee WS, Jain MK, Arkonac BM, Zhang D, Shaw SY, Kashiki S, Maemura K, Lee SL, Hollenberg NK, Lee ME, Haber E: Thy-1, a novel marker for angiogenesis upregulated by inflammatory cytokines. Circ Res 1998;82:845-851.
38. Pinhal-Enfield G, Ramanathan M, Hasko G, Vogel SN, Salzman AL, Boons GJ, Leibovich SJ: An angiogenic switch in macrophages involving synergy between Toll-like receptors 2, 4, 7, and 9 and adenosine A (2A) receptors. Am J Pathol 2003;163:711-721.
39. Methe H, Kim JO, Kofler S, Nabauer M, Weis M: Statins decrease Toll-like receptor 4 expression and downstream signaling in human CD14+ monocytes. Arterioscler Thromb Vasc Biol 2005;25:1439-1445.
40. Niessner A, Steiner S, Speidl WS, Pleiner J, Seidinger D, Maurer G, Goronzy JJ, Weyand CM, Kopp CW, Huber K, Wolzt M, Wojta J: Simvastatin suppresses endotoxin-induced upregulation of Toll-like receptors 4 and 2 in vivo. Atherosclerosis 2006;189:408-413.
41. Den Dekker WK, Cheng C, Pasterkamp G, Duckers HJ: Toll like receptor 4 in atherosclerosis and plaque destabilization. Atherosclerosis 2010;209:314-320.