Angiogenesis and oxidative stress: Common mechanisms linking psoriasis with atherosclerosis

Journal of Dermatological Science

Volumn 63, Issue 1, 2011, Pages 1-9

  Armstrong, April W ^a   Voyles, Stephanie V ^a   Armstrong, Ehrin J ^b   Fuller, Erin N ^c   Rutledge, John C ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF HAWAII   (United States)

Author keywords

Angiogenesis; Atherosclerosis; Oxidative stress; Psoriasis

Indexed keywords

CYTOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 17; INTERLEUKIN 8; PHOSPHOLIPID; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

ANGIOGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; GENETIC POLYMORPHISM; HUMAN; INFLAMMATION; NEOVASCULARIZATION (PATHOLOGY); OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PSORIASIS; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; VASCULAR DISEASE;

ANGIOGENIC PROTEINS; ANIMALS; ATHEROSCLEROSIS; HUMANS; INFLAMMATION MEDIATORS; NEOVASCULARIZATION, PATHOLOGIC; OXIDATIVE STRESS; PSORIASIS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 79957551340     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2011.04.007     Document Type: Review

References (106)

1. Griffiths C.E., Barker J.N. Pathogenesis and clinical features of psoriasis. Lancet 2007, 370:263-271.
2. Libby P. The molecular mechanisms of the thrombotic complications of atherosclerosis. J Intern Med 2008, 263:517-527.
3. Armstrong E.J., Morrow D.A., Sabatine M.S. Inflammatory biomarkers in acute coronary syndromes: Part I. Introduction and cytokines. Circulation 2006, 113:e72-e75.
4. Alexanderoff ABea: more than skin deep: atherosclerosis as a systemic manifestation of psoriasis. Br J Dermatol 2009, 161:1-7.
5. Friedewald V.E., Cather J.C., Gelfand J.M., Gordon K.B., Gibbons G.H., Grundy S.M., et al. AJC editor's consensus: psoriasis and coronary artery disease. Am J Cardiol 2008, 102:1631-1643.
6. Ludwig R.J., Herzog C., Rostock A., Ochsendorf F.R., Zollner T.M., Thaci D., et al. Psoriasis: a possible risk factor for development of coronary artery calcification. Br J Dermatol 2007, 156:271-276.
7. Gelfand J.M., Neimann A.L., Shin D.B., Wang X., Margolis D.J., Troxel A.B. Risk of myocardial infarction in patients with psoriasis. JAMA 2006, 296:1735-1741.
8. Mallbris L., Akre O., Granath F., Yin L., Lindelof B., Ekbom A., et al. Increased risk for cardiovascular mortality in psoriasis inpatients but not in outpatients. Eur J Epidemiol 2004, 19:225-230.
9. Stern R.S. Psoriasis is not a useful independent risk factor for cardiovascular disease. J Invest Dermatol 2010, 130:917-919.
10. Gelfand J.M., Azfar R.S., Mehta N.N. Psoriasis and cardiovascular risk: strength in numbers. J Invest Dermatol 2010, 130:919-922.
11. Boehncke W.H., Boehncke S., Schon M.P. Managing comorbid disease in patients with psoriasis. BMJ 2010, 340:b5666.
12. Prodanovich S., Ma F., Taylor J.R., Pezon C., Fasihi T., Kirsner R.S. Methotrexate reduces incidence of vascular diseases in veterans with psoriasis or rheumatoid arthritis. J Am Acad Dermatol 2005, 52:262-267.
13. Kimball A.B., Gladman D., Gelfand J.M., Gordon K., Horn E.J., Korman N.J., et al. National Psoriasis Foundation clinical consensus on psoriasis comorbidities and recommendations for screening. J Am Acad Dermatol 2008, 58:1031-1042.
14. Bettman S. Kapillarmikroskopische untersuchungen bei psoriasis. Dermat Wchnschr 1926, 83.
15. Braverman I.M. Electron microscopic studies of the microcirculation in psoriasis. J Invest Dermatol 1972, 59:91-98.
16. De Angelis R., Bugatti L., Del Medico P., Nicolini M., Filosa G. Videocapillaroscopic findings in the microcirculation of the psoriatic plaque. Dermatology 2002, 204:236-239.
17. Elias P.M., Arbiser J., Brown B.E., Rossiter H., Man M.Q., Cerimele F., et al. Epidermal vascular endothelial growth factor production is required for permeability barrier homeostasis, dermal angiogenesis, and the development of epidermal hyperplasia: implications for the pathogenesis of psoriasis. Am J Pathol 2008, 173:689-699.
18. Heidenreich R., Rocken M., Ghoreschi K. Angiogenesis drives psoriasis pathogenesis. Int J Exp Pathol 2009, 90:232-248.
19. Takahashi H., Tsuji H., Hashimoto Y., Ishida-Yamamoto A., Iizuka H. Serum cytokines and growth factor levels in Japanese patients with psoriasis. Clin Exp Dermatol 2009.
20. Tuschil A., Lam C., Haslberger A., Lindley I. Interleukin-8 stimulates calcium transients and promotes epidermal cell proliferation. J Invest Dermatol 1992, 99:294-298.
21. Bhushan M., McLaughlin B., Weiss J.B., Griffiths C.E. Levels of endothelial cell stimulating angiogenesis factor and vascular endothelial growth factor are elevated in psoriasis. Br J Dermatol 1999, 141:1054-1060.
22. Young C.N., Koepke J.I., Terlecky L.J., Borkin M.S., Boyd Savoy L., Terlecky S.R. Reactive oxygen species in tumor necrosis factor-alpha-activated primary human keratinocytes: implications for psoriasis and inflammatory skin disease. J Invest Dermatol 2008, 128:2606-2614.
23. Markham T., Mullan R., Golden-Mason L., Rogers S., Bresnihan B., Fitzgerald O., et al. Resolution of endothelial activation and down-regulation of Tie2 receptor in psoriatic skin after infliximab therapy. J Am Acad Dermatol 2006, 54:1003-1012.
24. Szekanecz Z., Szanto S., Szabo Z., Vancsa A., Szamosi S., Bodnar N., et al. Biologics - beyond the joints. Autoimmun Rev 2010, 9:820-824.
25. Hurlimann D., Forster A., Noll G., Enseleit F., Chenevard R., Distler O., et al. Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation 2002, 106:2184-2187.
26. Campanati A., Goteri G., Simonetti O., Ganzetti G., Giuliodori K., Giuliano A., et al. Angiogenesis in psoriatic skin and its modifications after administration of etanercept: videocapillaroscopic, histological and immunohistochemical evaluation. Int J Immunopathol Pharmacol 2009, 22:371-377.
27. Nofal A., Al-Makhzangy I., Attwa E., Nassar A., Abdalmoati A. Vascular endothelial growth factor in psoriasis: an indicator of disease severity and control. J Eur Acad Dermatol Venereol 2009, 23:803-806.
28. Simonetti O., Lucarini G., Campanati A., Goteri G., Zizzi A., Marconi B., et al. VEGF, survivin and NOS overexpression in psoriatic skin: critical role of nitric oxide synthases. J Dermatol Sci 2009, 54:205-208.
29. Detmar M., Brown L.F., Schon M.P., Elicker B.M., Velasco P., Richard L., et al. Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 1998, 111:1-6.
30. Detmar M., Brown L.F., Claffey K.P., Yeo K.T., Kocher O., Jackman R.W., et al. Overexpression of vascular permeability factor/vascular endothelial growth factor and its receptors in psoriasis. J Exp Med 1994, 180:1141-1146.
31. Xia Y.P., Li B., Hylton D., Detmar M., Yancopoulos G.D., Rudge J.S. Transgenic delivery of VEGF to mouse skin leads to an inflammatory condition resembling human psoriasis. Blood 2003, 102:161-168.
32. Wang Z., Liang W., Zhang B., Lv M., Wang J., Zhang L. Single nucleotide polymorphisms of VEGF gene and Psoriasis risk. J Dermatol Sci 2008, 49:263-265.
33. Young H.S., Summers A.M., Bhushan M., Brenchley P.E., Griffiths C.E. Single-nucleotide polymorphisms of vascular endothelial growth factor in psoriasis of early onset. J Invest Dermatol 2004, 122:209-215.
34. Young H.S., Summers A.M., Read I.R., Fairhurst D.A., Plant D.J., Campalani E., et al. Interaction between genetic control of vascular endothelial growth factor production and retinoid responsiveness in psoriasis. J Invest Dermatol 2006, 126:453-459.
35. Celletti F.L., Waugh J.M., Amabile P.G., Brendolan A., Hilfiker P.R., Dake M.D. Vascular endothelial growth factor enhances atherosclerotic plaque progression. Nat Med 2001, 7:425-429.
36. Stannard A.K., Khurana R., Evans I.M., Sofra V., Holmes D.I., Zachary I. Vascular endothelial growth factor synergistically enhances induction of E-selectin by tumor necrosis factor-alpha. Arterioscler Thromb Vasc Biol 2007, 27:494-502.
37. Hoffman F., McGlave, Silberstein, Shattil, Benz, Heslop Hematology: basic principles and practice 2008, Churchill Livingstone. 5th ed.
38. Heeschen C., Dimmeler S., Hamm C.W., Boersma E., Zeiher A.M., Simoons M.L. Prognostic significance of angiogenic growth factor serum levels in patients with acute coronary syndromes. Circulation 2003, 107:524-530.
39. Holm P.W., Slart R.H., Zeebregts C.J., Hillebrands J.L., Tio R.A. Atherosclerotic plaque development and instability: a dual role for VEGF. Ann Med 2009, 41:257-264.
40. Higashida T., Kanno H., Nakano M., Funakoshi K., Yamamoto I. Expression of hypoxia-inducible angiogenic proteins (hypoxia-inducible factor-1alpha, vascular endothelial growth factor, and E26 transformation-specific-1) and plaque hemorrhage in human carotid atherosclerosis. J Neurosurg 2008, 109:83-91.
41. Kolodgie F.D., Gold H.K., Burke A.P., Fowler D.R., Kruth H.S., Weber D.K., et al. Intraplaque hemorrhage and progression of coronary atheroma. N Engl J Med 2003, 349:2316-2325.
42. Takaya N., Yuan C., Chu B., Saam T., Polissar N.L., Jarvik G.P., et al. Presence of intraplaque hemorrhage stimulates progression of carotid atherosclerotic plaques: a high-resolution magnetic resonance imaging study. Circulation 2005, 111:2768-2775.
43. Hashmi S., Zeng Q.T. Role of interleukin-17 and interleukin-17-induced cytokines interleukin-6 and interleukin-8 in unstable coronary artery disease. Coron Artery Dis 2006, 17:699-706.
44. Numasaki M., Fukushi J., Ono M., Narula S.K., Zavodny P.J., Kudo T., et al. Interleukin-17 promotes angiogenesis and tumor growth. Blood 2003, 101:2620-2627.
45. Numasaki M., Lotze M.T., Sasaki H. Interleukin-17 augments tumor necrosis factor-alpha-induced elaboration of proangiogenic factors from fibroblasts. Immunol Lett 2004, 93:39-43.
46. Salomonsson L., Pettersson S., Englund M.C., Wiklund O., Ohlsson B.G. Post-transcriptional regulation of VEGF expression by oxidised LDL in human macrophages. Eur J Clin Invest 2002, 32:767-774.
47. Bochkov V.N., Philippova M., Oskolkova O., Kadl A., Furnkranz A., Karabeg E., et al. Oxidized phospholipids stimulate angiogenesis via autocrine mechanisms, implicating a novel role for lipid oxidation in the evolution of atherosclerotic lesions. Circ Res 2006, 99:900-908.
48. Bu S., Yamanaka M., Pei H., Bielawska A., Bielawski J., Hannun Y.A., et al. Dihydrosphingosine 1-phosphate stimulates MMP1 gene expression via activation of ERK1/2-Ets1 pathway in human fibroblasts. FASEB J 2006, 20:184-186.
49. Rosenberger C., Solovan C., Rosenberger A.D., Jinping L., Treudler R., Frei U., et al. Upregulation of hypoxia-inducible factors in normal and psoriatic skin. J Invest Dermatol 2007, 127:2445-2452.
50. Kulka J.P. Microcirculatory impairment as a factor in inflammatory tissue damage. Ann N Y Acad Sci 1964, 116:1018-1044.
51. Lawler J.C., Vineyard W.R. The effect of treatment on the vascular component of the psoriatic lesion. Arch Dermatol 1960, 82:190-193.
52. Sluimer J.C., Kolodgie F.D., Bijnens A.P., Maxfield K., Pacheco E., Kutys B., et al. Thin-walled microvessels in human coronary atherosclerotic plaques show incomplete endothelial junctions relevance of compromised structural integrity for intraplaque microvascular leakage. J Am Coll Cardiol 2009, 53:1517-1527.
53. Hedman M., Hartikainen J., Syvanne M., Stjernvall J., Hedman A., Kivela A., et al. Safety and feasibility of catheter-based local intracoronary vascular endothelial growth factor gene transfer in the prevention of postangioplasty and in-stent restenosis and in the treatment of chronic myocardial ischemia: phase II results of the Kuopio Angiogenesis Trial (KAT). Circulation 2003, 107:2677-2683.
54. Henry T.D., Grines C.L., Watkins M.W., Dib N., Barbeau G., Moreadith R., et al. Effects of Ad5FGF-4 in patients with angina: an analysis of pooled data from the AGENT-3 and AGENT-4 trials. J Am Coll Cardiol 2007, 50:1038-1046.
55. Kastrup J., Jorgensen E., Ruck A., Tagil K., Glogar D., Ruzyllo W., et al. Direct intramyocardial plasmid vascular endothelial growth factor-A165 gene therapy in patients with stable severe angina pectoris A randomized double-blind placebo-controlled study: the Euroinject One trial. J Am Coll Cardiol 2005, 45:982-988.
56. Scappaticci F.A., Skillings J.R., Holden S.N., Gerber H.P., Miller K., Kabbinavar F., et al. Arterial thromboembolic events in patients with metastatic carcinoma treated with chemotherapy and bevacizumab. J Natl Cancer Inst 2007, 99:1232-1239.
57. Briganti S., Picardo M. Antioxidant activity, lipid peroxidation and skin diseases. What's new. J Eur Acad Dermatol Venereol 2003, 17:663-669.
58. Bickers D.R., Athar M. Oxidative stress in the pathogenesis of skin disease. J Invest Dermatol 2006, 126:2565-2575.
59. Trouba K.J., Hamadeh H.K., Amin R.P., Germolec D.R. Oxidative stress and its role in skin disease. Antioxid Redox Signal 2002, 4:665-673.
60. Hampton M.B., Kettle A.J., Winterbourn C.C. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 1998, 92:3007-3017.
61. Kuehl F.A., Egan R.W. Prostaglandins, arachidonic acid, and inflammation. Science 1980, 210:978-984.
62. Kuhn H., Thiele B.J. The diversity of the lipoxygenase family. Many sequence data but little information on biological significance. FEBS Lett 1999, 449:7-11.
63. Babior B.M. NADPH oxidase: an update. Blood 1999, 93:1464-1476.
64. Van Heerebeek L., Meischl C., Stooker W., Meijer C.J., Niessen H.W., Roos D. NADPH oxidase(s): new source(s) of reactive oxygen species in the vascular system?. J Clin Pathol 2002, 55:561-568.
65. Buder-Hoffmann S., Palmer C., Vacek P., Taatjes D., Mossman B. Different accumulation of activated extracellular signal-regulated kinases (ERK 1/2) and role in cell-cycle alterations by epidermal growth factor, hydrogen peroxide, or asbestos in pulmonary epithelial cells. Am J Respir Cell Mol Biol 2001, 24:405-413.
66. Usatyuk P.V., Vepa S., Watkins T., He D., Parinandi N.L., Natarajan V. Redox regulation of reactive oxygen species-induced p38 MAP kinase activation and barrier dysfunction in lung microvascular endothelial cells. Antioxid Redox Signal 2003, 5:723-730.
67. Xiao L., Pimentel D.R., Wang J., Singh K., Colucci W.S., Sawyer D.B. Role of reactive oxygen species and NAD(P)H oxidase in alpha(1)-adrenoceptor signaling in adult rat cardiac myocytes. Am J Physiol Cell Physiol 2002, 282:C926-C934.
68. Conde de la Rosa L., Schoemaker M.H., Vrenken T.E., Buist-Homan M., Havinga R., Jansen P.L., et al. Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms: involvement of JNK and ERK MAP kinases. J Hepatol 2006, 44:918-929.
69. Griffith C.E., Zhang W., Wange R.L. ZAP-70-dependent and -independent activation of Erk in Jurkat T cells. Differences in signaling induced by H2o2 and Cd3 cross-linking. J Biol Chem 1998, 273:10771-10776.
70. Takahashi H., Ibe M., Nakamura S., Ishida-Yamamoto A., Hashimoto Y., Iizuka H. Extracellular regulated kinase and c-Jun N-terminal kinase are activated in psoriatic involved epidermis. J Dermatol Sci 2002, 30:94-99.
71. Johansen C., Kragballe K., Westergaard M., Henningsen J., Kristiansen K., Iversen L. The mitogen-activated protein kinases p38 and ERK1/2 are increased in lesional psoriatic skin. Br J Dermatol 2005, 152:37-42.
72. Yu X.J., Li C.Y., Dai H.Y., Cai D.X., Wang K.Y., Xu Y.H., et al. Expression and localization of the activated mitogen-activated protein kinase in lesional psoriatic skin. Exp Mol Pathol 2007, 83:413-418.
73. Abdou A.G., Hanout H.M. Evaluation of survivin and NF-kappaB in psoriasis, an immunohistochemical study. J Cutan Pathol 2008, 35:445-451.
74. Treumer F., Zhu K., Glaser R., Mrowietz U. Dimethylfumarate is a potent inducer of apoptosis in human T cells. J Invest Dermatol 2003, 121:1383-1388.
75. Amigo M., Paya M., De Rosa S., Terencio M.C. Antipsoriatic effects of avarol-3'-thiosalicylate are mediated by inhibition of TNF-alpha generation and NF-kappaB activation in mouse skin. Br J Pharmacol 2007, 152:353-365.
76. Lizzul P.F., Aphale A., Malaviya R., Sun Y., Masud S., Dombrovskiy V., et al. Differential expression of phosphorylated NF-kappaB/RelA in normal and psoriatic epidermis and downregulation of NF-kappaB in response to treatment with etanercept. J Invest Dermatol 2005, 124:1275-1283.
77. Jozsef L., Filep J.G. Selenium-containing compounds attenuate peroxynitrite-mediated NF-kappaB and AP-1 activation and interleukin-8 gene and protein expression in human leukocytes. Free Radic Biol Med 2003, 35:1018-1027.
78. Kishimoto T., Taga T., Akira S. Cytokine signal transduction. Cell 1994, 76:253-262.
79. Wolk K., Kunz S., Witte E., Friedrich M., Asadullah K., Sabat R. IL-22 increases the innate immunity of tissues. Immunity 2004, 21:241-254.
80. Wang F., Lee E., Lowes M.A., Haider A.S., Fuentes-Duculan J., Abello M.V., et al. Prominent production of IL-20 by CD68+/CD11c+ myeloid-derived cells in psoriasis: gene regulation and cellular effects. J Invest Dermatol 2006, 126:1590-1599.
81. Ross R., Glomset J.A. Atherosclerosis and the arterial smooth muscle cell: proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 1973, 180:1332-1339.
82. Steinberg D., Parthasarathy S., Carew T.E., Khoo J.C., Witztum J.L. Beyond cholesterol. Modifications of low-density lipoprotein that increase its atherogenicity. N Engl J Med 1989, 320:915-924.
83. Gozin A., Franzini E., Andrieu V., Da Costa L., Rollet-Labelle E., Pasquier C. Reactive oxygen species activate focal adhesion kinase, paxillin and p130cas tyrosine phosphorylation in endothelial cells. Free Radic Biol Med 1998, 25:1021-1032.
84. Antoniades C., Tousoulis D., Stefanadis C. Effects of endothelial nitric oxide synthase gene polymorphisms on oxidative stress, inflammatory status, and coronary atherosclerosis: an example of a transient phenotype. J Am Coll Cardiol 2007, 49:1226. [author reply 1226-7].
85. Griendling K.K., Sorescu D., Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000, 86:494-501.
86. Griendling K.K., FitzGerald G.A. Oxidative stress and cardiovascular injury: Part I. Basic mechanisms and in vivo monitoring of ROS. Circulation 2003, 108:1912-1916.
87. Moller D.E., Kaufman K.D. Metabolic syndrome: a clinical and molecular perspective. Annu Rev Med 2005, 56:45-62.
88. Chinen I., Shimabukuro M., Yamakawa K., Higa N., Matsuzaki T., Noguchi K., et al. Vascular lipotoxicity: endothelial dysfunction via fatty-acid-induced reactive oxygen species overproduction in obese Zucker diabetic fatty rats. Endocrinology 2007, 148:160-165.
89. Inoguchi T., Li P., Umeda F., Yu H.Y., Kakimoto M., Imamura M., et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000, 49:1939-1945.
90. Bellin C., de Wiza D.H., Wiernsperger N.F., Rosen P. Generation of reactive oxygen species by endothelial and smooth muscle cells: influence of hyperglycemia and metformin. Horm Metab Res 2006, 38:732-739.
91. Horani M.H., Haas M.J., Mooradian A.D. Saturated, unsaturated, and trans-fatty acids modulate oxidative burst induced by high dextrose in human umbilical vein endothelial cells. Nutrition 2006, 22:123-127.
92. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol 1996, 16:4604-4613.
93. Oikawa M., Abe M., Kurosawa H., Hida W., Shirato K., Sato Y. Hypoxia induces transcription factor ETS-1 via the activity of hypoxia-inducible factor-1. Biochem Biophys Res Commun 2001, 289:39-43.
94. Kumamoto M., Nakashima Y., Sueishi K. Intimal neovascularization in human coronary atherosclerosis: its origin and pathophysiological significance. Hum Pathol 1995, 26:450-456.
95. Kuwahara F., Kai H., Tokuda K., Shibata R., Kusaba K., Tahara N., et al. Hypoxia-inducible factor-1alpha/vascular endothelial growth factor pathway for adventitial vasa vasorum formation in hypertensive rat aorta. Hypertension 2002, 39:46-50.
96. Bourcier T., Sukhova G., Libby P. The nuclear factor kappa-B signaling pathway participates in dysregulation of vascular smooth muscle cells in vitro and in human atherosclerosis. J Biol Chem 1997, 272:15817-15824.
97. Yoshida S., Ono M., Shono T., Izumi H., Ishibashi T., Suzuki H., et al. Involvement of interleukin-8, vascular endothelial growth factor, and basic fibroblast growth factor in tumor necrosis factor alpha-dependent angiogenesis. Mol Cell Biol 1997, 17:4015-4023.
98. Ettehadi P., Greaves M.W., Wallach D., Aderka D., Camp R.D. Elevated tumour necrosis factor-alpha (TNF-alpha) biological activity in psoriatic skin lesions. Clin Exp Immunol 1994, 96:146-151.
99. Gotsman I., Stabholz A., Planer D., Pugatsch T., Lapidus L., Novikov Y., et al. Serum cytokine tumor necrosis factor-alpha and interleukin-6 associated with the severity of coronary artery disease: indicators of an active inflammatory burden?. Isr Med Assoc J 2008, 10:494-498.
100. Ridker P.M., Rifai N., Pfeffer M., Sacks F., Lepage S., Braunwald E. Elevation of tumor necrosis factor-alpha and increased risk of recurrent coronary events after myocardial infarction. Circulation 2000, 101:2149-2153.
101. Jovanovic D.V., Di Battista J.A., Martel-Pelletier J., Jolicoeur F.C., He Y., Zhang M., et al. IL-17 stimulates the production and expression of proinflammatory cytokines, IL-beta and TNF-alpha, by human macrophages. J Immunol 1998, 160:3513-3521.
102. Eid R.E., Rao D.A., Zhou J., Lo S.F., Ranjbaran H., Gallo A., et al. Interleukin-17 and interferon-gamma are produced concomitantly by human coronary artery-infiltrating T cells and act synergistically on vascular smooth muscle cells. Circulation 2009, 119:1424-1432.
103. Armstrong E.J., Morrow D.A., Sabatine M.S. Inflammatory biomarkers in acute coronary syndromes: Part II. Acute-phase reactants and biomarkers of endothelial cell activation. Circulation 2006, 113:e152-e155.
104. Soedamah-Muthu S.S., Chaturvedi N., Schalkwijk C.G., Stehouwer C.D., Ebeling P., Fuller J.H. Soluble vascular cell adhesion molecule-1 and soluble E-selectin are associated with micro- and macrovascular complications in type 1 diabetic patients. J Diabetes Complications 2006, 20:188-195.
105. Rallidis L.S., Gika H.I., Zolindaki M.G., Xydas T.A., Paravolidakis K.E., Velissaridou A.H. Usefulness of elevated levels of soluble vascular cell adhesion molecule-1 in predicting in-hospital prognosis in patients with unstable angina pectoris. Am J Cardiol 2003, 92:1195-1197.
106. Mulvihill N.T., Foley J.B., Murphy R.T., Curtin R., Crean P.A., Walsh M. Risk stratification in unstable angina and non-Q wave myocardial infarction using soluble cell adhesion molecules. Heart 2001, 85:623-627.