Soluble E-selectin in cardiovascular disease and its risk factors

Vanessa Roldán; Francisco Marín; Gregory Y. H. Lip; Andrew D. Blann

doi:10.1160/TH02-09-0083

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2003; 90(06): 1007-1020
DOI: 10.1160/TH02-09-0083

Review Article

Schattauer GmbH

Soluble E-selectin in cardiovascular disease and its risk factors

A review of the literature

Vanessa Roldán

¹Haemostasis, Thrombosis and Vascular Biology Unit, University Department of Medicine, City Hospital, Birmingham, UK

²Hematology Unit, Hospital San Vicente, Spain

,

Francisco Marín

¹Haemostasis, Thrombosis and Vascular Biology Unit, University Department of Medicine, City Hospital, Birmingham, UK

³Cardiology Unit, Hospital General Alicante, Spain

,

Gregory Y. H. Lip

¹Haemostasis, Thrombosis and Vascular Biology Unit, University Department of Medicine, City Hospital, Birmingham, UK

,

Andrew D. Blann

¹Haemostasis, Thrombosis and Vascular Biology Unit, University Department of Medicine, City Hospital, Birmingham, UK

› Author Affiliations

Abstract

Summary

The initial steps in the pathogenesis of atherosclerosis involve changes to the vascular endothelium, which produces numerous substances involved in the regulation and maintenance of vascular integrity and the homeostasis of the coagulation/fibrinolysis system. A further change in endothelial physiology is an increase in the surface expression of cell adhesion molecules, such as E-selectin, which regulate adhesive interactions between certain blood cells and endothelium. As E-selectin is only expressed on activated endothelium, it therefore provides an opportunity to study pathophysiological aspects of this cell in cardiovascular and other disease. However, a soluble form of E selectin (i.e. sE-selectin) can be found in the plasma. This review will focus on sE-selectin, and its potential role in the pathogenesis of cardiovascular disease as raised levels have been found in hypertension, diabetes and hyperlipidemia, although its association in established atherosclerosis disease and its value as a prognostic factor is more controversial.

Search strategy: We performed a keyword search (listed above) using electronic databases (PUB-MED, MEDLINE, EMBASE, DARE), and additionally, abstracts from national and international cardiovascular meetings were studied to identify unpublished studies. Relevant authors of these studies were contacted to obtain further data.

Keywords

Soluble E selectin - atherosclerosis - diabetes - smoking - coronary artery disease - peripheral artery disease - hypertension - hyper-cholesterolaemia

Full Text

References

References
1 Ross R. Atherosclerosis – An inflammatory disease. N Eng J Med 1999; 340: 115-26.
2 Blann AD, Taberner DA. A reliable marker of endothelial cell dysfunction: does it exist?. Br J Hematol 1995; 90: 244-8.
3 Cines DB, Pollak ES, Buck CA. et al. Endothelial cells in physiology and in the pathophysiology of vascular disorders. Blood 1998; 91: 3527-61.
4 Kansas G. Selectins and their ligands: current concepts and controversies. Blood 1996; 347 88: 3259-87.
5 McEver RP, Moore KL, Cummings RD. Leukocyte trafficking mediated by selectins-carbohydrate interactions. J Biol Chem 1995; 270: 11025-8.
6 Eppihimer MJ, Wolitzky B, Anderson DC. et al. Heterogeneity of expression of E- and P-Selectins in vivo. Circ Res 1996; 79: 560-9.
7 Thiagarajan RR, Winn RK, Harlan JM. The role of leukocyte and endothelial adhesion molecules in ischaemia. Reper-fusion injury. Thromb Haemost 1997; 78: 310-4.
8 Wyble CW, Hynes KL, Kuchibhotla J. et al. TNF alpha and IL-1 upregulate membrane bound and soluble E selectin through a common pathway. J Surg Res 1997; 73: 107-12.
9 Vestwever D, Blanks JE. Mechanism that regulate the function of the selectins and their ligands. Phys Rev 1999; 79: 181-213.
10 McIntyre TM, Modur V, Prescott SM. et al. Molecular mechanisms of early inflammation. Thromb Haemost 1997; 78: 302-5.
11 Gearing AJH, Newman W. Circulating adhesion molecules in disease. Immunol Today 1993; 14: 506-12.
12 Pigott R, Dillon LP, Hemingway IH. et al. Soluble forms of E-selectin, ICAM-and VCAM-1 are present in the supernatants of cytokine activated cultured endothelial cells. Biochem Biophys Res Commun 1992; 187: 584-9.
13 Leeuwenberg JFM, Smeets EF, Neefjes JJ. et al. E-selectin and intercellular adhesion molecule-1 are released by activated human endothelial cells in vitro. Immunology 1992; 77: 543-9.
14 Smith CW. Potential significance of circulating E-selectin. Circulation 1997; 95: 1986-8.
15 Jilma B, Dirnberger E, Eichler HG. et al. Sex differences in circulating P-selectin, E-selec-tin and thrombomodulin. Br J Hematol 1996; 95: 575-6.
16 Jilma B, Eichler HG, Breiterneder H. et al. Effects of 17 beta-estradiol on circulating adhesion molecules. J Clin Endocrinol Metab 1994; 79: 1619-24.
17 Blann AD, Davis A, Miller JP. et al. Von Willebrand factor and soluble E-selectin in hyperlipidemia: relationship to lipids and vascular disease. Am J Hematol 1997; 55: 15-23.
18 Blann AD, Daly RJ, Amiral J. The influence of age, gender and ABO group on soluble endothelial-cell markers and adhesion molecules. Br J Hematol 1996; 92: 498-500.
19 Nash MC, Shah V, Dillon MJ. Soluble cell adhesion molecules and von Willebrand factor in children with Kawasaki disease. Clin Exp Immunol 1995; 101: 13-17.
20 Nash MC, Wade AM, Shah V. et al. Normal levels of soluble E-selectin, soluble intercellular adhesion molecule-1 (sICAM-1), and soluble vascular cell adhesion molecule-1 (sVCAM-1) decrease with age. Clin Exp Immunol 1996; 103: 167-70.
21 Maple C, Kirk G, Mclaren M. et al. A circadian variation exists for soluble levels of intercellular adhesion molecule-1 and E-selectin in healthy volunteers. Clin Sci 1998; 94: 537-40.
22 Kennedy G, McLaren M, Belch JJF. et al. Elevated levels of sE-selectin in post-menopausal females are decreased by hormone replacement therapy to levels observed in pre-menopausal females. Thromb Haemost 1999; 82: 1433-6.
23 Cushman M, Legault C, Barrett-Connor E. et al. Effect of postmenopausal hormones on inflammation-sensitive proteins: the Postmenopausal Estrogen/Progestin Interventions (PEPI) Study. Circulation 1999; 100: 717-22.
24 Herrington DM, Brosnihan B, Pusser BE. et al. Differential effects of E and Droloxifene on C-reactive protein and other markers of inflammation in healthy postmenopausal women. J Clin Endocrinol Metab 2001; 86: 4216-22.
25 Herrington DM, Howard TD, Brosnihan B. et al. Common estrogen receptor polymorphism augments effects of hormone replacement therapy on E-selectin but not C-reactive protein. Circulation 2002; 105: 1879-82.
26 Vehkavaara S, Silveira A, Hakala-Ala-Pietila T. et al. Effects of oral and transdermal estrogen replacement therapy on markers of coagulation, fibrinolysis, inflammation and serum lipids and lipoproteins in postmenopausal women. Thromb Haemost 2001; 85: 619-25.
27 Blann AD, Steele C. McCollum: The influence of smoking on soluble adhesion molecules and endothelial cell markers. Thromb Res 1997 85: 433-8.
28 Koundouros E, Odell E, Coward P. et al. Soluble adhesion molecules in serum of smokers and non-smokers, with and without periodontitis. J Periodontal Res 1996; 3: 596-9.
29 Adams MR, Jessup W, Celermajer DS. Cigarette smoking is associated with increased human monocyte adhesion to endothelial cells: reversibility with oral L-arginine but not vitamin C. J Am Coll Cardiol 1997; 29: 491-7.
30 Demerath E, Townet B, Blangero J. et al. The relationship of soluble ICAM-1, VCAM-1, P-selectin and E-selectin to cardiovascular disease risk factors in healthy men and women. Ann Hum Biol 2001; 28: 664-78.
31 Bermudez EA, Rifai N, Buring JE. et al. Relation between markers of systemic vascular inflammation and smoking in women. Am J Cardiol 2002; 89: 1117-9.
32 Stone PC, Fisher AC, Rainger GE. et al. Neutrophil capture by selectins on endothelial cells exposed to cgarette smoke. Biochem Biophys Res Commn 2002; 295: 1150-5.
33 Ferri C, Desideri G, Valenti M. et al. Early upregulation of endothelial adhesion molecules in obese hypertensive men. Hypertension 1999; 34: 568-73.
34 Ito H, Ohshima A, Inoue M. et al. Weight reduction decreases soluble cellular adhesion molecules in obese women. Clin Exp Pharmacol Physiol 2002; 29: 399-404.
35 Hwang SJ, Ballantyne CM, Sharret AR. et al. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease. Circulation 1997; 96: 4219-25.
36 Malik I, Danesh J, Whincup P.. et al. Soluble adhesion molecules and prediction of coronary heart disease: a prospective study and meta-analysis. Lancet 2001; 358: 971-5.
37 Hackman A, Abe Y, Insull W. et al. Levels of soluble cell adhesion molecules in patients with dyslipemia. Circulation 1996; 93: 1334-8.
38 Sampieto T, Tuoni M, Ferdeghini M. et al. Plasma cholesterol regulates soluble cell adhesion molecule expression in familial hypercholesterolemia. Circulation 1997; 96: 1381-5.
39 Steinberg D. Low density lipoprotein oxidation and its pathobiological significance. J Biol Chem 1997; 272: 20963-6.
40 Hulthe J, Fagerberg B. Circulating oxidized LDL is associated with increased levels of cell-adhesion molecules in clinically healthy 58-year men. Med Sci Monit 2002; 8: 148-52.
41 Sardo MA, Castaldo M, Cinquegrani M. et al. Effects of simvastatin treatment on sICAM-1 and sE-selectin levels in hypercholesterolemic patients. Atherosclerosis 2001; 155: 143-7.
42 Colome C, Martinez-Gonzalez J, Vidal F. et al. Small oxidative changes in atherogenic LDL concentrations irreversibly regulate adhesiveness of human endothelial cells: effect of the lazaroid U74500A. Atherosclerosis 2000; 149: 295-302.
43 Takei A, Huang Y, Lopes-Virella MF. Expression of adhesion molecules by human endothelial cells exposed to oxidized low-density lipoprotein. Influences of degree of oxidation and location of oxidized LDL. Atherosclerosis 2001; 154: 79-86.
44 Alonso R, Mata P, De Andres R. et al. Sustained long-term improvement of arterial endothelial function in heterozygous familial hypercholesterolemia patients treated with simvastatin. Atherosclerosis 2001; 157: 423-9.
45 Koh KK. Effects of statins on vascular wall: vasomotor function, inflammation, and plaque stability. Cardiovasc Res 2000; 47: 648-57.
46 Maron DJ, Fazio S, Linton MF. Current perspectives on statins. Circulation 2000; 101: 207-13.
47 Pascer V, Willerson JT, Yeh ETH. Direct pro-inflammatory effect of C-reactive protein on human endothelial cells. Circulation 2000; 102: 2165-8.
48 Ridker PM, Rifai N, Pfeffer MA. et al. Longterm effects of pravastatin on plasma concentration of C-reactive protein. Circulation 1999; 100: 230-5.
49 Calabresi L, Gomaraschi M, Villa B. et al. Elevated soluble cellular adhesion molecules in subjects with low HDL-cholesterol. Arterioscler Thromb Vasc Biol 2002; 22: 656-61.
50 Cockerill GW, Saklatvala J, Ridley SH. et al. High-density lipoproteins differentially modulate cytokine-induced expression of E-selec-tin and cyclooxygenase-2. Arterioscler Thromb Vasc Biol 1999; 19: 910-7.
51 Abe Y, El-Masri B, Kimball KT. et al. Soluble cell adhesion molecules in hypertriglyceridemia and potential significance on monocyte adhesion. Arterioscler Thromb Vasc Biol 1998; 18: 723-31.
52 Ferri C, Bellini C, Desideri G. et al. Clustering of endothelial markers of vascular damage in human salt-sensitive hypertension. Influence of dietary sodium load and depletion. Hypertension 1999; 32: 862-8.
53 Blann AD, Tse W, Maxwell JR S. et al. Increased levels of the soluble adhesion molecule E-selectin in essential hypertension. J Hypertension 1994; 12: 925-8.
54 Nomura S, Kanazawa S, Fukuhara S. Effect of efonidipine on platelet and monocytes activation markers in hypertensive patients with ands without type 2 diabetes mellitus. J Human Hypertens 2002; 16: 539-47.
55 Matsumoto K, Miyake S, Yano M. et al. High serum concentrations of soluble E-selectin in patients with impaired glucose tolerance with hyperinsulinemia. Atherosclerosis 2000; 152: 415-20.
56 Gearing AJH, Hemingway I, Pigott R. et al. Soluble forms of vascular adhesion molecules, E-Selectin, ICAM-1, and VCAM-1: pathological significance. Annals NY Acad Sci 1992; 667: 324-31.
57 DeSouza CA, Dengel DR, Macko RF. et al. Elevated levels of circulating cell adhesion molecules in uncomplicated essential hypertension. Am J Hypertens 1997; 10: 1335-41.
58 Dörffel Y, Franz S, Pruβ A. et al. Preactivated monocytes from hypertensive patients as a factor for atherosclerosis?. Atherosclerosis 2001; 157: 151-60.
59 Hlubocka Z, Umnerova V, Heller S. et al. Circulating intercellular adhesion molecule-1, endothelin-1 and von Willebrand factor – markers of endothelial dysfunction in uncomplicated essential hypertension: the effect of treatment with ACE inhibitors. J Human Hypertens 2002; 16: 557-62.
60 Kuroda YT, Komamura K, Tatsumi R. et al. Vascular cell adhesion molecule-1 as a biochemical marker of left ventricular mass in the patients with hypertension. Am J Hypertens 2001; 14: 868-72.
61 Malmqvist K, Wallen HN, Held C. et al. Soluble adhesion molecules in hypertensive concentric left ventricular hypertrophy. J Hypertens 2002; 20: 1563-9.
62 Buemi M, Allegra A, Aloisi C. et al. Cold pressor test raises serum concentrations of ICAM-1, VCAM-1, and E-selectin in normo-tensive and hypertensive patients. Hypertension 1997; 30: 845-7.
63 De Caterina R, Guiadoni L, Tadeei S. et al. Soluble E-selectin in essential hypertension: a correlate of vascular structural changes. Am J Hypertension 2001; 14: 259-66.
64 Cominacini L, Pasini AF, Garbin U. et al. Elevated levels of soluble E-selectin in patients with IDDM and NIDDM: relation to metabolic control. Diabetologia 1995; 38: 1122-4.
65 Fasching P, Waldhaus W, Wagner OF. Elevated circulating adhesion molecules in NIDDM -potential mediators in diabetic macroangiopathy. Diabetologia 1996; 39: 1242-4.
66 Smulders RA, Stehouwer CDA, Schalkwijk CG. et al. Distinct associations of HbA1c and the urinary excretion of pentosidine, and advanced glycosilation end-product, with markers of endothelial function in insulin-dependent diabetes mellitus. Thromb Haemost 1998; 80: 52-57.
67 Steiner M, Reinhardt K, Krammer B. et al. Increased levels of soluble adhesion molecules in type 2 (non-insulin dependent) diabetes mellitus are independent of glycaemic control. Thromb Haemost 1994; 72: 979-84.
68 Bannan S, Mansfield MW, Grant PJ. Soluble vascular cell adhesion molecule-1 and E-selectin levels in relation to vascular risk factors and to E-selectin genotype in the first degree relatives of NIDDM patients and in NIDDM patients. Diabetologia 1998; 41: 460-6.
69 Fasching P, Veitl M, Rohac M. et al. Elevated concentrations of circulating adhesion molecules and their association with microvascular complications in insulin-dependent diabetes mellitus. J Clin Endocrinol Metab 1996; 81: 4313-7.
70 Albertini JP, Valensi P, Lormeau B. et al. Elevated concentrations of soluble E-selectin and vascular cell adhesion molecule 1 in NIDDM. Diabetes Care 1998; 21: 1008-13.
71 Cominacini L, Garbin U, Pasini AF. et al. Troglitazone reduces LDL oxidation and lowers plasma E-selectin concentration in NIDDM patients. Diabetes 1998; 47: 130-3.
72 Matsumoto K, Sera Y, Abe Y. et al. Serum concentrations of soluble adhesion vascular molecule-1 and E-selectin are elevated in insulin resistant patients with type 2 diabetes. Diabetes Care 2001; 24: 1697-8.
73 Chen NG, Holmes M, Reaven GM. Relationship between insulin resistance, soluble adhesion molecules, and mononuclear cell binding in healthy volunteers. J Clin Endocrinol Metab 1999; 84: 3485-9.
74 Jilma B, Dallinger N, Eichler HG. et al. Effects of hyperinsulinemia on plasma levels of circulating adhesion molecules. J Clin Endocrinol Metab 2000; 85: 1748-51.
75 Bluher M, Unger R, Rassoul F. et al. Relation between glycaemic control, hyperinsulinaemia and plasma concentrations of soluble adhesion molecules in patients with impaired glucose tolerance or type II diabetes. Diabetologia 2002; 45: 210-6.
76 Ferri C, Desideri G, Baldoncini R. et al. Early activation of vascular endothelium in non-obese, non-diabetic essential hypertensive patients with multiple metabolic abnormalities. Diabetes 1998; 47: 660-7.
77 Matsumoto K, Sera Y, Abe Y. et al. High serum concentrations of soluble E selectin correlate with obesity but not fat distribution in patients with type 2 daibetes mellitus. Metabolism 2002; 51: 932-4.
78 Blann AD, Lip GYH. Endothelial integrity, soluble adhesion molecules and platelet markers in type 1 diabetes mellitus. Diabet Med 1998; 15: 634-42.
79 Matsumoto K, Sera Y, Nakamura H. et al. Serum concentration of soluble adhesion molecules are related to degree of hyperglycaemia and insulin resistance in patients with type 2 diabetes mellitus. Diab Res Clin Pract 2002; 55: 131-8.
80 Takeuchi N, Kawamura T, Kanai A. et al. The effect of cigarette smoking on soluble adhesion molecules in middle aged patients with type 2 diabetes mellitus. Diabetic Med 2002; 19: 57-64.
81 Davies MJ, Gordon JL, Gearing AJ. et al. The expression of the adhesion molecules ICAM-1, VCAM-1, PECAM, and E-selectin in human atherosclerosis. J Pathol 1993; 171: 223-9.
82 Blann AD, McCollum CN. Circulating endothelial cell/leukocyte adhesion molecules in atherosclerosis. Thromb Haemost 1994; 77: 151-4.
83 Blann AD, Morris J. McCollum. Soluble L-selectin in peripheral arterial disease: relationship with soluble E-selectin and soluble P-selectin. Atherosclerosis 1996; 126: 227-31.
84 Peter K, Nawroth P, Conradt C. et al. Circulating vascular cell adhesion molecule-1 correlates with the extent of human atherosclerosis in contrast to circulating intercellular adhesion molecule-1, E-selectin, P-selec-tin and thrombomodulin. Arterioscler Thromb Vasc Biol 1997; 17: 505-12.
85 De Caterina R, Basta G, Lazzerini G. et al. Soluble Vascular Cell Adhesion Molecule-1 as a biohumoral correlate for atherosclerosis. Arterioscler Thromb Vasc Biol 1997; 17: 2646-54.
86 Blann AD, Seigneur M, Steiner M. et al. Circulating endothelial cell markers in peripheral vascular disease: relationship to the location and extent of atherosclerotic disease. Eur J Clin Invest 1997; 27: 916-21.
87 Blann AD, Farrel A, Picton A. et al. Relationship between endothelial cell markers and arterial stenosis in peripheral and carotid artery disease. Thromb Res 2000; 97: 209-16.
88 Hulthe J, Wikstrand J, Mattsson-Hulten L. et al. Circulating ICAM-1 (intercellular adhesion molecule-1) is associated with early stages of atherosclerosis development and with inflammatory cytokines in healthy 58 year old men. Clin Sci 2002; 103: 123-9.
89 Matsumoto K, Sera Y, Ueki Y. et al. Comparison of serum concentrations of soluble adhesion molecules in diabetic microangiopathy and macroangiopathy. Diabetic Med 2002; 19: 822-6.
90 Fassbender K, Bertsch T, Mielke O. et al. Adhesion molecules in cerebrovascular disease. Evidence for an inflammatory endothelial activation in cerebral large- and small-vessel disease. Stroke 1999; 30: 1647-50.
91 Fassbender K, Mossner R, Motsch L. et al. Circulating selectin- and immunoglobulin-type adhesion molecules in acute ischemic stroke. Stroke 1995; 26: 1361-4.
92 Kozuka K, Kohriyama T, Nomura E. et al. Endothelial markers and adhesion molecules in acute ischemic stroke- sequential change and differences in stroke subtypes. Atherosclerosis 2002; 161: 161-8.
93 Frijns CJ, Kappelle LJ, van Gijn J. et al. Soluble adhesion molecules reflect endothelial cell activation in ischemic stroke and in carotid atherosclerosis. Stroke 1997; 28: 2214-8.
94 Shyu KG, Chang H, Lin CC. Serum levels of intercellular adhesion molecule-1 and E-selectin in patients with acute ischaemic stroke. J Neurol 1997; 244: 90-3.
95 Plutzky J. Inflammatory pathways in atherosclerosis and acute coronary syndromes. Am J Cardiol 2001; 88 (08) suppl 10K-15K.
96 Blann AD, Kumar P, Krupinski J. et al. Soluble intercellular adhesion molecule-1, E-selectin, vascular cell adhesion molecule-1 and von Willebrand factor in stroke. Blood Coagul Fibinolysis 1999; 10: 277-84.
97 Bitsch A, Klene W, Murtada L. et al. A longitudinal prospective study of soluble adhesion molecules in acute stroke. Stroke 1998; 29: 2129-35.
98 Skoog T, Dichtl W, Boquist S. et al. Plasma tumour necrosis factor-alpha and early carotid atherosclerosis in healthy middle-aged men. Eur Heart J 2002; 23: 376-83.
99 Blann AD, Amiral J, McCollum CN. Circulating endothelial cell/leucocyte adhesion molecules in ischaemic heart disease. Br J Haematol 1996; 95: 263-5.
100 Mulvihil NT, Foley JB, Murphy R. et al. Evidence of prolonged inflammation in unstable angina and non-Q wave myocardial infarction. J Am Coll Cardiol 2000; 36: 1210-6.
101 Miwa J, Igawa A, Inoue H. Soluble E-selec-tin, ICAM-1 and VCAM-1 levels in systemic and coronary circulation in patients with variant angina. Cardiovas Res 2001; 36: 37-44.
102 Suefuji H, Ogawa H, Yasue H. et al. Increased plasma levels of soluble E-selectin in acute myocardial infarction. Am Heart J 2000; 140: 243-8.
103 Ghaisas NK, Shahi ChN, Foley B. et al. Elevated levels of circulating soluble adhesion molecules in peripheral blood of patients with unstable angina. Am J Cardiol 1997; 80: 617-9.
104 Atalar E, Aytemir K, Haznedaroglu I. et al. Increased plasma levels of soluble selectins in patients with unstable angina. Int J Cardiol 2001; 78: 69-73.
105 Shyu KG, Chang H, Lin CC. et al. Circulating intercellular adhesion molecule-1 and E-selectin in patients with acute coronary syndrome. Chest 1996; 109: 1627-30.
106 Parker III C, Vita JA, Freedman JE. Soluble adhesion molecules and unstable coronary disease. Atherosclerosis 2001; 156: 417-24.
107 Tenaglia AN, Buda AJ, Wilkins RG. et al. Levels of expression of P-selectin, E-selectin, and intercellular adhesion molecule-1 in coronary atherectomy specimens from patients with stable and unstable angina pectoris. Am J Cardiol 1997; 79: 742-7.
108 Nasuno A, Matsubara T, Hori T. et al. Levels of soluble E-selectin and ICAM-1 in the coronary circulation of patients with stable CAD: association with the severity of coronary atherosclerosis. Jpn Heart J 2002; 43: 93-101.
109 Li YH, Teng JK, Tsai WC. et al. Elevation of soluble adhesion molecules is associated with the severity of myocardial damage in acute myocardial infarction. Am J Cardiol 1997; 80: 1218-21.
110 Atalar E, Haznedaroglu Y, Aytemir K. et al. Circulating adhesion molecules in patients with stable coronary artery disease. Int J Hematol 2000; 72: 507-11.
111 Mizia-Stec K, Zarhorska-Markiewicz Man-dechi T. et al. Serum levels of selected adhesion molecules in patients with coronary artery disease. Int J Cardiol 2002; 83: 143-50.
112 Newman W, Beall LD, Carson CW. et al. Soluble E-selectin is found in supernatants of activated endothelial cells and is elevated in the serum of patients with septic shock. J Immunol 1993; 150: 644-54.
113 Mulvihill NT, Foley JB, Murphy RT. et al. Enhanced endothelial activation in diabetic patients with unstable angina and non-Q-wave myocardial infarction. Diabetic Med 2001; 18: 979-83.
114 Kowalska I, Straczkowski M, Szelachowska M. et al. Circulating E-selectin, vascular cell adhesion molecule-1, and intercellular adhesion molecule-1 in men with coronary artery disease assessed by angiography and disturbances of carbohydrate metabolism. Metabolism 2002; 51: 733-6.
115 Cauli-Glaser T, Farrel WJ, Pfau SE. et al. Modulating of cellular adhesion molecules in postmenopausal women with coronary artery disease. J Am Coll Cardiol 1998; 31: 1555-60.
116 Zanger D, Yang BK, Ardans J. et al. Divergent effects of hormone therapy on serum markers of inflammation in postmenopausal women with coronary artery disease on appropriate medical management. J Am Coll Cardiol 2000; 36: 1797-802.
117 Seljeflot I, Arnesen H, Hofstad AE, Os I. Reduced expression of endothelial cell markers after long-term transdermal hormone replacement therapy in women with coronary artery disease. Thromb Haemost 2000; 83: 944-8.
118 Sbarouni E, Kroupis C, Kyriakides ZS. et al. Cell adhesion molecules in relation to simvastatin and hormone replacement therapy in coronary artery disease. Eur Heart J 2000; 21: 975-80.
119 Schumacher A, Seljeflot I, Sommervoll L. et al. Increased levels of markers of vascular inflammation in patents with coronary heart disease. Scand J Clin Lab Invest 2002; 62: 59-68.
120 Blann AD, Miller JP, McCollum CN. Von Willebrand factor and soluble E-selectin in the prediction of cardiovascular disease progression in hyperlipidaemia. Atherosclerosis 1997; 32: 151-6.
121 Blann AD, Waite MA. Von Willebrand factor and soluble E-selectin in hypertension: influence of treatment and value in predicting the progression of atherosclerosis. Coronary Art Dis 1996; 7: 143-7.
122 Galen FX. Cell adhesion molecules in hypertension: endothelial markers of vascular injury and predictors of target organ damage?. J Hypertens 2002; 20: 813-6.
123 Stehouwer CDA, Gall MA, Twisk JWR. et al. Increased urinary albumin excretion, endothelial dysfunction, and chronic low-grade inflammation in type 2 diabetes. Progressive, interrelated, and independently associated with risk of death. Diabetes 2002; 51: 1157-65.
124 Blann AD, Amiral J, McCollum CN. Prognostic value of increased soluble thrombomodulin and increased soluble E-selectin in ischaemic heart disease. Eur J Hematol 1997; 59: 115-20.
125 O’Malley T, Ludlam CA, Riemersa RA. et al. Early increase in levels of soluble inter-cellular adhesion molecule-1 (sICAM-1). Potential risk factor for the acute coronary syndromes. Eur Heart J 2001; 22: 1226-34.
126 Hillis GS, Terrgino C, Taggart P. et al. Elevated soluble P-selectin levels are associated with an increased risk of early adverse events in patients with presumed myocardial ischaemia. Am Heart J 2002; 143: 235-41.
127 Wallen NH, Held C, Rehnqvist N. et al. Elevated serum intercellular adhesion molecule-1 and vascular adhesion molecule-1 among patients with stable angina pectoris who suffer cardiovascular death or non-fatal myocardial infarction. Eur Heart J 1999; 20: 1039-43.
128 Mulvihill NT, Foley JB, Murphy RT. et al. Risk stratification in unstable angina and non-Q wave myocardial infarction using soluble cell adhesion molecules. Heart 2001; 85: 623-7.
129 Porsch-Oezcueruemez M, Kunz D, Kloer HU. et al. Evaluation of serum levels of solubilized adhesion molecules and cytokine receptors in coronary heart disease. J Am Coll Cardiol 1999; 34: 1995-2001.
130 Blankenberg S, Rupprecht HJ, Bickel C. et al. Circulating cell adhesion molecules and death in patients with coronary artery disease. Circulation 2001; 104: 1336-42.
131 Belch JJF, Shaw JW, McLaren M. et al. The white blood cell adhesion molecule E-selec-tin predicts restenosis in patients with intermittent claudication undergoing percutaneous transluminal angioplasty. Circulation 1997; 95: 2027-31.
132 Tsakiris DA, Tschopl M, Jager K. et al. Circulating cell adhesion molecules in peripheral arterial occlusive disease. Atherosclerosis 1999; 142: 193-2000.
133 Tsakiris DA, Tschopl M, Wolf F. et al. Platelets and cytokines in concert with endothelial activation in patients with peripheral arterial occlusive disease. Blood Coagul Fibrinolysis 2000; 11: 165-73.
134 Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis. The good, the bad and the ugly. Circ Res 2002; 90: 251-62.
135 Kurz RW, Graf B, Gremmel F. et al. Increased serum concentration of adhesion molecules after coronary angioplasty. Clin Sci 1994; 87: 627-33.
136 Siminiak T, Dye JF, Egdell RM. et al. The release of soluble adhesion molecules ICAM-1 and E-selectin after acute myocardial infarction and following coronary angioplasty. Int J Cardiol 1997; 61: 113-8.
137 Inoue T, Hoshi K, Yaguchi I. et al. Serum levels of circulating adhesion molecules after coronary angioplasty. Cardiology 1999; 9: 236-42.
138 Squadrito F, Saitta A, Altavilla D. et al. Thrombolytic therapy with urokinase reduces increased circulating endothelial adhesion molecules in acute myocardial infarction. Inflamm Res 1996; 45: 14-19.
139 Blann AD. Endothelial cell activation, injury, damage and dysfunction; separate entities or mutual terms?. Blood Coagul Fibrinolysis 2000; 11: 623-30.
140 Boneu B, Abbal M, Plante J, Bierme R. Factor VIII complex and endothelial damage. Lancet 1975; I: 1430
141 Jilma B, Blann A, Pernerstorfer T. et al. Regulation of adhesion molecules during human endotoxaemia: no acute effects of aspirin. Am J Respir Crit Care Med 1999; 159: 857-63.
142 Koch AE, Halloran MM, Haskell CJ. et al. Angiogenesis mediated by soluble forms of E-selectin and vascular cell adhesion molecule-1. Nature 1995; 376: 517-9.
143 Farzati A, Esposito K, Colacurci N. et al. Effects of transdermal hormone replacement therapy on levels of soluble P and E selectin in postmenopausal women. Fertil Steril 2002; 77: 476-80.
144 Ray KK, Camp NJ, Bennett CE. et al. Genetic variation at the interleukin-1 locus is a determinant of changes in soluble endothelial factors in patients with acute coronary syndromes. Clin Sci 2002; 103: 303-10.
145 Jilma B, Blann A, Stohlawetz P. et al. Dexamethasone lowers circulating E-selectin ands ICAM-1 in healthy men. J Lab Clin Med 2000; 135: 270-4.
146 Wenzel K, Ernst M, Rohde K. et al. DNA polymorphisms in adhesion molecule genes – a new risk factor for early atherosclerosis. Hum Genet 1996; 97: 15-20.
147 Wenzel K, Felix S, Kleber FX. et al. E-selec-tin polymorphism and atherosclerosis: an association study. Hum Mol Gen 1994; 3: 1935-7.
148 Wenzel K, Blackburn A, Ernst A. et al. Relationship of polymorphisms in the reninangiotensin system and in E-selectin of patients with early severe coronary heart disease. J Mol Med 1997; 75: 57-61.
149 Zheng F, Chevalier JA, Zhang LQ. et al. An HpnI polymorphism in the E-selectin gene is associated with premature coronary artery disease. Clin Genet 2001; 59: 58-64.
150 Ellsworth DL, Bielak LF, Turner ST. et al. Gender- and age-dependent relationships between the E-selectin S128R polymorphism and coronary artery calcification. J Mol Med 2001; 79: 390-8.
151 Rauchhaus M, Gross M, Schulz S. et al. The E-selectin SER128ARG gene polymorphism and restenosis after successful coronary angioplasty. Int J Cardiol 2002; 83: 249-57.
152 Yoshida M, Takano Y, Sasaoka T. et al. E-selectin polymorphism associated with myocardial infarction causes enhanced leukocyte-endothelial interactions under flow conditions. Arterioscl Thromb Vasc Biol 2003; 23: 783-8.
153 Manning AM, Bell FP, Rosenbloom CL. et al. NF-kappa B is activated during acute inflammation in vivo in association with elevated endothelial cell adhesion molecule gene expression and leukocyte recruitment. J Inflamm 1995; 45: 283-96.
154 Denk A, Goebeler M, Schmid S. et al. Activation of NF kappa B via the I kappa B kinase complex is both essential and sufficient for pro-inflammatory gene expression in primary endothelial cells. J Biol Chem 2001; 276: 28451-8.
155 Yaron A, Gonen H, Alkalay I. et al. Inhibition of NFkB cellular function via specific targeting of the UikB ubiquitin ligase. The EMBO J 1997; 16: 6486-94.
156 Kaur J, Woodman RC, Kubes P. P38 MAPK: critical molecule in thrombin induced NF kappa B dependent leukocyte recruitment. Am J Physiol Heart Circ Physiol 2003; 284: H1095-1103.
157 Cominacini L, Pasini A, Garbin U. et al. Zofenopril inhibits the expression of adhesion molecules on endothelial cells by reducing reactive oxygen species. Am J Hypertens 2002; 15: 891-5.
158 Jilma B, Li-Saw-Hee FL, Wagner OF. et al. Effects of enalapril and losartan on circulating adhesion molecules and monocyte chemotactic factor-1. Clin Sci 2003; 103: 131-6.
159 Mason JC, Yarwood H, Sugars K. et al. Human umbilical vein and dermal microvascular endothelial cells show heterogeneity in response to PKC activation. Am J Physiol. 1997: C1233-C1240.
160 Kluger MS, Johnson DR, Pober JS. Mechanism of sustained E-selectin expression in cultured human dermal microvascular endothelial cells. J Immunol 1997; 158: 887-96.
161 Murakami S, Morioka T, Nakagawa Y. et al. Expression of adhesion molecules by cultured human glomerular endothelial cells in response to cytokines: comparison to human umbilical vein endothelial cells and dermal microvascular endothelial cells. Microvasc Res 2001; 62: 383-91.
162 Vora M, Romero I L, Karasek MA. Interleukin-10 induces E-selectin on small and large blood vessel endothelial cells. J Exp Med 1996; 184: 821-9.
163 Thompson SG, Kienast J, Pyke SDM. et al. Hemostatic factors and the risk of myocardial infarction or sudden death in patients with angina pectoris. N Engl J Med 1995; 332: 635-41.
164 Salomaa V, Matei C, Aleksic N. et al. Soluble thrombomodulin as a predictor of incident coronary heart disease and symptomless carotid artery atherosclerosis in the Atherosclerosis Risks in Communities (ARIC) study. A case-cohort study. Lancet 1999; 353: 1729-34.
165 Pernerstorfer T, Eichler HG, Stohlawetz P. et al. Effects of heparin and aspirin on circulating P-selectin, E-selectin and von Willebrand factor levels in healthy men. Atherosclerosis 2001; 155: 389-93.
166 Seljeflot I, Tonstad S, Hjermann I. et al. Reduced expression of endothelial cell markers after 1 year treatment with simvastatin and atorvastatin in patients with coronary heart disease. Atherosclerosis 2002; 162: 179-85.
167 Jilma B, Joukhadar C, Derhaschnig U. et al. Levels of adhesion molecules do not decrease after 3 months of statin therapy in moderate hypercholesterolaemia. Clin Sci 2003; 104: 189-93.
168 Miller MA, Sagnella GA, Kerry SM. et al. Ethnic differences in circulating soluble adhesion molecules: the Wandsworth Heart and Stroke Study. Clin Sci 2003; 104: 591-8.
169 Signorelli SS, Mazzarino MC, Di Pino L. et al. High circulating levels of cytokines (IL-6 and TNFalpha), adhesion molecules (VCAM-1 and ICAM-1) and selectins in patients with peripheral arterial disease at rest and after a treadmill test. Vasc Med 2003; 8: 15-9.
170 Cherian P, Hankey GJ, Eikelboom JW. et al. Endothelial and platelet activation in acute ischemic stroke and its etiological subtypes. Stroke 2003; 34: 2132-7.
171 Papagianni A, Kalovoulos M, Kirmizis D. et al. Carotid atherosclerosis is associated with inflammation and endothelial cell adhesion molecules in chronic haemodialysis patients. Nephrol Dial Transplant 2003; 18: 113-9.
172 O’Neal DN, Dragicevic G, Rowley KG. et al. A cross-sectional study of the effects of type 2 diabetes and other cardiovascular risk factors on structure and function of nonstenotic arteries of the lower limb. Diabetes Care 2003; 26: 199-205.
173 Schram MT, Chaturvedi N, Schalkwijk C. et al. EURODIAB Prospective Complications Study. Vascular risk factors and markers of endothelial function as determinants of inflammatory markers in type 1 diabetes: the EURODIAB Prospective Complications Study. Diabetes Care 2003; 26: 2165-73.
174 Nomura S, Kanazawa S, Fukuhara S. Effects of eicosapentaenoic acid on platelet activation markers and cell adhesion molecules in hyperlipidemic patients with Type 2 diabetes mellitus. J Diabetes Complications 2003; 17: 153-9.
175 Vermeulen EG, Rauwerda JA, van den Berg M. et al. Homocysteine-lowering treatment with folic acid plus vitamin B6 lowers urinary albumin excretion but not plasma markers of endothelial function or C-reactive protein: further analysis of secondary endpoints of a randomized clinical trial. Eur J Clin Invest 2003; 33: 209-15.
176 Roldan V, Marin F, Blann AD. et al. Interleukin-6, endothelial activation and thrombogenesis in chronic atrial fibrillation. Eur Heart J 2003; 24: 1373-80.
177 Nawawi H, Osman NS, Annuar R. etal Soluble intercellular adhesion molecule-1 and interleukin-6 levels reflect endothelial dysfunction in patients with primary hyper-cholesterolaemia treated with atorvastatin. Atherosclerosis 2003; 169: 283-91.
178 van Haelst PL, van Doormaal JJ, Asselbergs FW. et al. Correlates of endothelial function and their relationship with inflammation in patients with familial hypercholesterolaemia. Clin Sci 2003; 104: 627-32.
179 Menown IB, Mathew TP, Gracey HM. et al. Prediction of Recurrent Events by D-Dimer and Inflammatory Markers in Patients with Normal Cardiac Troponin I Study. Prediction of Recurrent Events by D-Dimer and Inflammatory Markers in Patients with Normal Cardiac Troponin I (PREDICT) Study. Am Heart J 2003; 145: 986-92.
180 Reinhart K, Bayer O, Brunkhorst F. et al. Markers of endothelial damage in organ dysfunction and sepsis. Crit Care Med 2002; 30 (05) Suppl S302-12.