Drug-induced immunomodulation to affect the development and progression of atherosclerosis: A new opportunity?

Expert Review of Cardiovascular Therapy

Volumn 5, Issue 2, 2007, Pages 345-364

  Heeneman, Sylvia ^a   Donners, Marjo M P C ^a   Bai, Lili ^a   Daemen, Mat J A P ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Atherosclerosis; Coronary artery disease; COX 1 COX 2 inhibition; Cyclosporine A; Inflammation; Mycophenolate mofetil; Sirolimus; Tacrolimus

Indexed keywords

4 [5 (4 CHLOROPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOL 1 YL]BENZENESULFONAMIDE; 5 (4 CHLOROPHENYL) 1 (4 METHOXYPHENYL) 3 TRIFLUOROMETHYL 1H PYRAZOLE; ACETYLSALICYLIC ACID; CELECOXIB; CYCLOOXYGENASE 2 INHIBITOR; CYCLOSPORIN A; DICLOFENAC; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; EVEROLIMUS; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; IBUPROFEN; IMMUNOMODULATING AGENT; IMMUNOSUPPRESSIVE AGENT; INDOMETACIN; LICOFELONE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; N (2 CYCLOHEXYLOXY 4 NITROPHENYL)METHANESULFONAMIDE; NAPROXEN; NIMESULIDE; NONSTEROID ANTIINFLAMMATORY AGENT; PHENYLBUTAZONE; PROSTAGLANDIN SYNTHASE INHIBITOR; RAMIPRIL; RAPAMYCIN; ROFECOXIB; SULINDAC; TACROLIMUS; UNINDEXED DRUG; VALDECOXIB;

ACUTE GRAFT REJECTION; ANTIINFLAMMATORY ACTIVITY; ARTERY THROMBOSIS; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOIMMUNE DISEASE; CARDIAC ALLOGRAFT VASCULOPATHY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CLINICAL TRIAL; CORONARY ARTERY DISEASE; COST EFFECTIVENESS ANALYSIS; DIABETES MELLITUS; DIARRHEA; DRUG BLOOD LEVEL; DRUG COST; DRUG MEGADOSE; DRUG TOLERABILITY; ENDOTHELIAL DYSFUNCTION; GASTROINTESTINAL DISEASE; GASTROINTESTINAL HEMORRHAGE; GASTROINTESTINAL SYMPTOM; GRAFT REJECTION; HEART INFARCTION; HEART TRANSPLANTATION; HUMAN; HYPERLIPIDEMIA; HYPERTENSION; IMMUNOMODULATION; IMMUNOREGULATION; IN-STENT RESTENOSIS; INTRAVASCULAR ULTRASOUND; KIDNEY DYSFUNCTION; LIPID METABOLISM; LONG TERM CARE; LOW DRUG DOSE; META ANALYSIS; MULTIPLE SCLEROSIS; NAUSEA; NONHUMAN; OPPORTUNISTIC INFECTION; OSTEOARTHRITIS; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; RHEUMATOID ARTHRITIS; RISK REDUCTION; SECONDARY PREVENTION; SIDE EFFECT; SYSTEMATIC REVIEW; THROMBOCYTE ACTIVATION; VOMITING;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ATHEROSCLEROSIS; CORONARY ARTERIOSCLEROSIS; CYCLOOXYGENASE INHIBITORS; DISEASE PROGRESSION; FEMALE; FOLLOW-UP STUDIES; FORECASTING; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; IMMUNOSUPPRESSIVE AGENTS; MALE; PRIMARY PREVENTION; RISK ASSESSMENT; SEVERITY OF ILLNESS INDEX; TREATMENT OUTCOME;

EID: 33947637637     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1586/14779072.5.2.345     Document Type: Review

References (137)

1. Mallat Z, Tedgui A. Immunomodulation to combat atherosclerosis: the potential role of immune regulatory cells. Expert Opin. Biol. Ther. 4, 1387-1393 (2004).
2. Nilsson J, Hansson GK, Shah PK. Immunomodulation of atherosclerosis: implications for vaccine development. Arteriosder. Thromb. Vasc. Biol. 25, 18-28 (2005).
3. Lusis AJ. Atherosclerosis. Nature 407, 233-241 (2000).
4. Libby P. Inflammation in atherosclerosis. Nature 420, 868-874 (2002).
5. Colotta F, Borre A, Wang JM et al. Expression of a monocyte chemotactic cytokine by human mononuclear phagocytes. J. Immunol. 148, 760-765 (1992).
6. Wang JM, Sica A, Peri G et al. Expression of monocyte chemotactic protein and interleukin-8 by cytokine-activated human vascular smooth muscle cells. Arterioscler. Thromb. 11, 1166-1174 (1991).
7. Wang DL, Wung BS, Shyy YJ et al. Mechanical strain induces monocyte chemotactic protein-1 gene expression in endothelial cells. Effects of mechanical strain on monocyte adhesion to endothelial cells. Circ. Res. 77, 294-302 (1995).
8. Terkeltaub R, Boisvert WA, Curtiss LK. Chemokines and atherosclerosis. Curr. Opin. Lipidol. 9, 397-405 (1998).
9. Charo IF, Ransohoff RM. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 354, 610-621 (2006).
10. Liao HS, Matsumoto A, Itakura H et al. Transcriptional inhibition by interleukin-6 of the class A macrophage scavenger receptor in macrophages derived from human peripheral monocytes and the THP-1 monocytic cell line. Arterioscler. Thromb. Vasc. Biol, 19, 1872-1880 (1999).
11. Hsu HY, Nicholson AC, Hajjar DP. Inhibition of macrophage scavenger receptor activity by tumor necrosis factor-α is transcriptionally and post-transcriptionally regulated. J. Biol. Chem. 271, 7767-7773 (1996).
12. Geng YJ, Holm J, Nygren S, Bruzelius M, Stemme S, Hansson GK. Expression of the macrophage scavenger receptor in atheroma. Relationship to immune activation and the T-cell cytokine interferon-γ. Arterioscler. Thromb. Vasc. Biol. 15, 1995-2002 (1995).
13. Janabi M, Yamashita S, Hirano K et al. Oxidized LDL-induced NF-κ B activation and subsequent expression of proinflammatory genes are defective in monocyte-derived macrophages from CD36-deficient patients. Arterioscler. Thromb. Vasc. Biol. 20, 1953-1960 (2000).
14. Feng J, Han J, Pearce SF et al. Induction of CD36 expression by oxidized LDL and IL-4 by a common signaling pathway dependent on protein kinase C and PPAR-γ. J. Lipid Res. 41, 688-696 (2000).
15. Kume N, Moriwaki H, Kataoka H et al. Inducible expression of LOX-1, a novel receptor for oxidized LDL, in macrophages and vascular smooth muscle cells. Ann. NY Acad. Sci. 902, 323-327 (2000).
16. Minami M, Kume N, Kataoka H et al. Transforming growth factor-β(1) increases the expression of lectin-like oxidized low-density lipoprotein receptor-1. Biochem. Biophys. Res. Commun. 272, 357-361 (2000).
17. Li PF, Maasch C, Haller H, Dietz R, von Harsdorf R. Requirement for protein kinase C in reactive oxygen species-induced apoptosis of vascular smooth muscle cells. Circulation 100, 967-973 (1999).
18. Geng YJ, Henderson LE, Levesque EB, Muszynski M, Libby P. Fas is expressed in human atherosclerotic intima and promotes apoptosis of cytokine-primed human vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 17, 2200-2208 (1997).
19. Chinetti G, Griglio S, Antonucci M et al. Activation of proliferator-activated receptors α and γ induces apoptosis of human monocyte-derived macrophages. J. Biol. Chem. 273, 25573-25580 (1998).
20. Lee YW, Kuhn H, Hennig B, Toborek M. IL-4 induces apoptosis of endothelial cells through the caspase-3-dependent pathway. FEBS Lett. 485, 122-126 (2000).
21. Lindner H, Holler E, Ertl B et al. Peripheral blood mononuclear cells induce programmed cell death in human endothelial cells and may prevent repair: role of cytokines. Blood 89, 1931-1938 (1997).
22. Oshima K, Sen L, Cui G et al. Localized interleukin-10 gene transfer induces apoptosis of alloreactive T cells via FAS/FASL pathway, improves function, and prolongs survival of cardiac allograft. Transplantation 73, 1019-1026 (2002).
23. Heldin CH, Westermark B. Mechanism of action and in vivo role of platelet-derived growth factor. Physiol. Rev. 79, 1283-1316 (1999).
24. Hansson GK, Jonasson L, Holm J, Clowes MM, Clowes AW. γ-interferon regulates vascular smooth muscle proliferation and la antigen expression in vivo and in vitro. Circ. Res. 63, 712-719 (1988).
25. Harrop AR, Ghahary A, Scott PG, Forsyth N, Uji-Friedland A, Tredget EE. Regulation of collagen synthesis and mRNA expression in normal and hypertrophic scar fibroblasts in vitro by interferon-γ. J. Surg. Res. 58, 471-477 (1995).
26. Galis ZS, Khatri JJ. Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res. 90, 251-262 (2002).
27. Amento EP, Ehsani N, Palmer H, Libby P. Cytokines and growth factors positively and negatively regulate interstitial collagen gene expression in human vascular smooth muscle cells. Arterioscler. Thromb. 11, 1223-1230 (1991).
28. Schonbeck U, Mach F, Sukhova GK et al. Regulation of matrix metalloproteinase expression in human vascular smooth muscle cells by T lymphocytes: a role for CD40 signaling in plaque rupture? Circ. Res. 81, 448-454 (1997).
29. Galis ZS' Muszynski M, Sukhova GK, Simon-Morrissey E, Libby P. Enhanced expression of vascular matrix metalloproteinases induced in vitro by cytokines and in regions of human atherosclerotic lesions. Ann. NY Acad. Sci. 748, 501-507 (1995).
30. Galis ZS, Muszynski M, Sukhova GK et al. Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of enzymes required for extracellular matrix digestion. Circ. Res. 75, 181-189 (1994).
31. Taubman MB, Fallon JT, Schecter AD et al. Tissue factor in the pathogenesis of atherosclerosis. Thromb. Haemost. 78, 200-204 (1997).
32. Taubman MB. Tissue factor regulation in vascular smooth muscle: a summary of studies performed using in vivo and in vitro models. Am. J. Cardiol. 72, 55C-60C (1993).
33. Osnes LT, Westvik AB, Joo GB, Okkenhaug C, Kierulf P. Inhibition of IL-1 induced tissue factor (TF) synthesis and procoagulant activity (PCA) in purified human monocytes by ILA-4, IL-10 and IL-13. Cytokine 8, 822-827 (1996).
34. Wojta J, Gallicchio M, Zoellner H et al. Thrombin stimulates expression of tissue-type plasminogen activator and plasminogen activator inhibitor type 1 in cultured human vascular smooth muscle cells. Thromb. Haemost. 70, 469-474 (1993).
35. Gallicchio M, Hufnagl P. Wojta J, Tipping P. IFN-γ inhibits thrombin- and endotoxin-induced plasminogen activator inhibitor type 1 in human endothelial cells. J. Immunol. 157, 2610-2617 (1996).
36. Krakauer T. IL-10 inhibits the adhesion of leukocytic cells to IL-1-activated human endothelial cells. Immunol, Lett. 45, 61-65 (1995).
37. Van Der Meeren A, Squiban C, Gourmelon P, Lafont H, Gaugler MH. Differential regulation by IL-4 and IL-10 of radiation-induced IL-6 and IL-8 production and ICAM-1 expression by human endothelial cells. Cytokine 11, 831-838 (1999).
38. Mostafa Mtairag E, Chollet-Martin S, Oudghiri M et al. Effects of interleukin-10 on monocyte/endothelial cell adhesion and MMP-9/TIMP-1 secretion. Cardiovasc. Res. 49, 882-890 (2001).
39. Lacraz S, Nicod L, Galve-de Rochemonteix B, Baumberger C, Dayer JM, Welgus HG. Suppression of metalloproteinase biosynthesis in human alveolar macrophages by interleukin-4. J. Clin. Invest. 90, 382-388 (1992).
40. Brasier AR, Recinos A 3rd, Eledrisi MS. Vascular inflammation and the rennin-angiotensin system. Arterioscler. Thromb. Vasc. Biol. 22, 1257-1266 (2002).
41. + T cells. Annu. Rev. Immunol 12, 635-673 (1994).
42. Frostegard J, Ulfgren AK, Nyberg P et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Thl) and macrophagestimulating cytokines. Atherosclerosis 145, 33-43 (1999).
43. Armstrong EJ, Morrow DA, Sabatine MS. Inflammatory biomarkers in acute coronary syndromes: part I: introduction and cytokines. Circulation 113, e72-e75 (2006).
44. Armstrong EJ, Morrow DA, Sabatine MS. Inflammatory biomarkers in acute coronary syndromes: part II: acute-phase reactants and biomarkers of endothelial cell activation. Circulation 113, e152-e155 (2006).
45. Yusuf S, Sleight P, Pogue J, Bosch J, Davies R, Dagenais G. Effects of an angiotensin-converting-enzyme inhibitor, ramipril, on cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342, 145-153 (2000).
46. Schmeisser A, Soehnlein O, Illmer T et al. ACE inhibition lowers angiotensin II-induced chemokine expression by reduction of NF-κB activity and AT1 receptor expression. Biochem. Biophys. Res. Commun. 325, 532-540 (2004).
47. da Cunha V, Tham DM, Martin-McNulty B et al. Enalapril attenuates angiotensin II-induced atherosclerosis and vascular inflammation. Atherosclerosis 178, 9-17 (2005).
48. Schieffer B, Bunte C, Witte J et al. Comparative effects of AT1-antagonism and angiotensin-converting enzyme inhibition on markers of inflammation and platelet aggregation in patients with coronary artery disease. J. Am. Coll. Cardiol. 44, 362-368 (2004).
49. Lutgens E, Daemen M. HMG-coA reductase inhibitors: lipid-lowering and beyond. Drug Discovery Today 1, 189-194 (2004).
50. Kleemann R, Princen HM, Emeis JJ et al. Rosuvastatin reduces atherosclerosis development beyond and independent of its plasma cholesterol-lowering effect in APOE*3-Leiden transgenic mice: evidence for anti-inflammatory effects of rosuvastatin. Circulation 108, 1368-1374 (2003).
51. Sparrow CP. Burton CA, Hernandez M et al. Simvastatin has anti-inflammatory and antiatherosclerotic activities independent of plasma cholesterol lowering. Arterioscler. Thromb. Vasc. Biol. 21, 115-121 (2001).
52. Bea F, Blessing E, Bennett B, Levitz M, Wallace EP, Rosenfeld ME. Simvastatin promotes atherosclerotic plaque stability in apoE-deficient mice independently of lipid lowering. Arterioscler. Thromb. Vasc. Biol. 22, 1832-1837 (2002).
53. Fukumoto Y, Libby P, Rabkin E et al. Statins alter smooth muscle cell accumulation and collagen content in established atheroma of watanabe heritable hyperlipidemic rabbits. Circulation 103, 993-999 (2001).
54. Crisby M, Nordin-Fredriksson G, Shah PK, Yano J, Zhu J, Nilsson J. Pravastatin treatment increases collagen content and decreases lipid content, inflammation, metalloproteinases, and cell death in human carotid plaques: implications for plaque stabilization. Circulation 103, 926-933 (2001).
55. Molloy KJ, Thompson MM, Schwalbe EC, Bell PR, Naylor AR, Loftus IM. Comparison of levels of matrix metalloproteinases, tissue inhibitor of metalloproteinases, interleukins, and tissue necrosis factor in carotid endarterectomy specimens from patients on versus not on statins preoperatively. Am. J. Cardiol. 94, 144-146 (2004).
56. Verhoeven BA, Moll FL, Koekkoek JA et al. Statin treatment is not associated with consistent alterations in inflammatory status of carotid atherosclerotic plaques: a retrospective study in 378 patients undergoing carotid endarterectomy. Stroke 37, 2054-2060 (2006).
57. Robinson JG, Smith B, Maheshwari N, Schrott H. Pleiotropic effects of statins: benefit beyond cholesterol reduction? A meta-regression analysis. J. Am. Coll. Cardiol. 46, 1855-1862 (2005).
58. Steffens S, Mach F. Drug insight: immunomodulatory effects of statins - potential benefits for renal patients? Nat. Clin. Pract. Nephrol. 2, 378-387 (2006).
59. LaRosa JC, He J, Vupputuri S. Effect of statins on risk of coronary disease: a meta- analysis of randomized controlled trials. J. Am. Coll. Cardiol. 282, 2340-2346 (1999).
60. Patrono C, Garcia Rodriguez LA, Landolfi R, Baigent C. Low-dose aspirin for the prevention of atherothrombosis. N. Engl. J. Med. 353, 2373-2383 (2005).
61. Henn V, Slupsky JR, Grafe M et al. CD40 ligand on activated platelets triggers an inflammatory reaction of endothelial cells. Nature 391, 591-594 (1998).
62. Massberg S, Brand K, Gruner S et al. A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation. J. Exp. Med. 196, 887-896 (2002).
63. Massberg S, Vogt F, Dickfeld T, Brand K, Page S, Gawaz M. Activated platelets trigger an inflammatory response and enhance migration of aortic smooth muscle cells. Thromb. Res. 110, 187-194 (2003).
64. Huo Y, Schober A, Forlow SB et al. Circulating activated platelets exacerbate atherosclerosis in mice deficient in apolipoprotein E. Nat. Med. 9, 61-67 (2003).
65. Cyrus T, Yao Y, Tung LX, Pratico D. Stabilization of advanced atherosclerosis in low-density lipoprotein receptor-deficient mice by aspirin. Atherosclerosis 184, 8-14 (2006).
66. Tous M, Ferre N, Vilella E, Riu F, Camps J, Joven J. Aspirin attenuates the initiation but not the progression of atherosclerosis in apolipoprotein Edeficient mice fed a high-fat, high-cholesterol diet. Basic Clin. Pharmacol Toxicol. 95, 15-19 (2004).
67. Paul A, Calleja L, Camps J. et al. The continuous administration of aspirin attenuates atherosclerosis in apolipoprotein E-deficient mice. Life Sci. 68, 457-465 (2000).
68. Cyrus T, Sung S, Zhao L, Funk CD, Tang S, Pratico D. Effect of low-dose aspirin on vascular inflammation, plaque stability, and atherogenesis in low-dcnsity lipoprotein receptor-deficient mice. Circulation 106, 1282-1287 (2002).
69. Pratico D, Tillmann C, Zhang ZB, Li H, FitzGerald GA. Acceleration of atherogenesis by COX-1-dependent prostanoid formation in low density lipoprotein receptor knockout mice. Proc. Natl Acad. Sci, USA 98, 3358-3363 (2001).
70. Belton OA, Duffy A, Toomey S, Fitzgerald DJ. Cyclooxygenase isoforms and platelet vessel wall interactions in the apolipoprotein E knockout mouse model of atherosclerosis. Circulation 108, 3017-3023 (2003).
71. Stoller DK, Grorud CB, Michalek V, Buchwald H. Reduction of atherosclerosis with nonsteroidal anti-inflammatory drugs. J. Surg. Res. 54, 7-11 (1993).
72. Dhawan V, Ganguly NK, Majumdar S, Chakravarti RN. Effect of indomethacin on serum lipids, lipoproteins, prostaglandins and the extent and severity of atherosclerosis in rhesus monkeys. Can. J. Cardiol. 8, 306-312 (1992).
73. Egan KM, Wang M, Fries S et al. Cyclooxygenases, thromboxane, and atherosclerosis: plaque destabilization by cyclooxygenase-2 inhibition combined with thromboxane receptor antagonism. Circulation 111, 334-342 (2005).
74. Cayatte AJ, Du Y, Oliver-Krasinski J, Lavielle G, Verbeuren TJ, Cohen RA. The thromboxane receptor antagonist S18886 but not aspirin inhibits atherogenesis in apo E-deficient mice: evidence that eicosanoids other than thromboxane contribute to atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 20, 1724-1728 2000).
75. Pratico D, Cheng Y. FitzGerald GA. TP or not TP: primary mediators in a close runoff? Arterioscler. Thromb. Vasc. Biol. 20, 1695-1698 (2000).
76. Rogowski O, Shapira I, Assayag EB et al. Lack of significant effect of low doses of aspirin on the concentrations of C-reactive protein in a group of individuals with atherothrombotic risk factors and vascular events. Blood Coagul. Fibrinolysis 17, 19-22 (2006).
77. Olesen M, Kwong E, Maztli A et al. No effect of cyclooxygenase inhibition on plaque size in atherosclerosis-prone mice. Scand Cardiovasc. J. 36, 362-367 (2002).
78. Burleigh ME, Babaev VR, Yancey PG et al. Cyclooxygenase-2 promotes early atherosclerotic lesion formation in ApoE-deficient and C57BL/6 mice. J. Mol. Cell. Cardiol. 39, 443-452 (2005).
79. Rott D, Zhu J, Burnett MS et al. Effects of MF-tricyclic, a selective cyclooxygenase-2 inhibitor, on atherosclerosis progression and susceptibility to cytomegalovirus replication in apolipoprotein-E knockout mice. J. Am. Coll. Cardiol. 41, 1812-1819 (2003).
80. Burleigh ME, Babaev VR, Patel MB et al. Inhibition of cyclooxygenase with indomethacin phenethylamide reduces atherosclerosis in apoE-null mice. Biochem. Pharmacol, 70, 334-342 (2005).
81. Burleigh ME, Babaev VR, Oates JA et al. Cyclooxygenase-2 promotes early atherosclerotic lesion formation in LDL receptor-deficient mice. Circulation 105, 1816-1823 (2002).
82. Bea F, Blessing E, Bennett BJ et al. Chronic inhibition of cyclooxygenase-2 does not alter plaque composition in a mouse model of advanced unstable atherosclerosis. Cardiovasc. Res. 60, 198-204 (2003).
83. Mukherjee D, Nissen SE, Topol EJ. Risk of cardiovascular events associated with selective COX-2 inhibitors. JAMA 286, 954-959 (2001).
84. Konstam MA, Weir MR, Reicin A et al. Cardiovascular thrombotic events in controlled, clinical trials of rofecoxib. Circulation 104, 2280-2288 (2001).
85. Bolten WW. Problem of the atherothrombotic potential of non-steroidal anti-inflammatory drugs. Ann. Rheum. Dis. 65, 7-13 (2006).
86. Kearney PM, Baigent C, Godwin J, Halls H, Emberson JR, Patrono C. Do selective cyclo-oxygenase-2 inhibitors and traditional non-steroidal anti-inflammatory drugs increase the risk of atherothrombosis? Meta-analysis of randomised trials. Br. Med. J. 332, 1302-1308 (2006).
87. Spektor G, Fuster V. Drug insight: cyclo- oxygenase 2 inhibitors and cardiovascular risk - where are we now? Nat. Clin. Pract. Cardiovasc. Med. 2, 290-300 (2005).
88. Title LM, Giddens K, McInerney MM, McQueen MJ, Nassar BA. Effect of cyclooxygenase-2 inhibition with rofecoxib on endothelial dysfunction and inflammatory markers in patients with coronary artery disease. J. Am. Coll. Cardiol. 42, 1747-1753 (2003).
89. Charlier C, Michaux C. Dual inhibition of cyclooxygenase-2 (COX-2) and 5-lipoxygenase (5-LOX) as a new strategy to provide safer non-steroidal anti-inflammatory drugs. Eur. J. Med. Chem. 38, 645-659 (2003).
90. Frishman WH. Effects of nonsteroidal anti-inflammatory drug therapy on blood pressure and peripheral edema. Am. J. Cardiol. 89, 18D-25D (2002).
91. Huang ZH, Bates EJ, Ferrante JV et al. Inhibition of stimulus-induced endothelial cell intercellular adhesion molecule-1, E-selectin, and vascular cellular adhesion molecule-1 expression by arachidonic acid and its hydroxy and hydroperoxy derivatives. Circ. Res. 80, 149-158 (1997).
92. Zuccollo A, Shi C, Mastroianni R et al. The thromboxane A2 receptor antagonist S18886 prevents enhanced atherogenesis caused by diabetes mellitus. Circulation 112, 3001-3008 (2005).
93. Viles-Gonzalez JF, Fuster V, Corti R et al. Atherosclerosis regression and TP receptor inhibition: effect of S18886 on plaque size and composition - a magnetic resonance imaging study. Eur. Heart J. 26, 1557-1561 (2005).
94. Belhassen L, Pelle G, Dubois-Rande JL, Adnot S. Improved endothelial function by the thromboxane A2 receptor antagonist S 18886 in patients with coronary artery disease treated with aspirin. J. Am. Coll. Cardiol. 41, 1198-1204 (2003).
95. Ulbrich H, Soehnlein O, Xie X et al. Licofelone, a novel 5-LOX/COX- inhibitor, attenuates leukocyte rolling and adhesion on endothelium under flow. Biochem. Pharmacol. 70, 30-36 (2005).
96. Alvaro-Gracia JM. Licofelone-clinical update on a novel LOX/COX inhibitor for the treatment of osteoarthritis. Rheumatology (Oxf.) 43(Suppl. 1), i2l-i25 (2004).
97. Ranke C, Hecker H, Creutzig A, Alexander K. Dose-dependent effect of aspirin on carotid atherosclerosis. Circulation 87, 1873-1879 (1993).
98. Mirshafiey A, Matsuo H, Nakane S, Rehm BH, Koh CS, Miyoshi S. Novel immunosuppressive therapy by M2000 in experimental multiple sclerosis. Immunopharmacol. Immunotoxicol. 27, 255-265 (2005).
99. Mirshafiey A, Cuzzocrea S, Rehm B, Mazzon E, Saadat F, Sotoude. M. Treatment of experimental arthritis with M2000, a novel designed non-steroidal anti-inflammatory drug. Scand. J. Immunol 61, 435-441 (2005).
100. van Leuven SI, Kastelein JJ, Allison AC, Hayden MR, Stroes ES. Mycophenolate mofetil (MMF): firing at the atherosclerotic plaque from different angles? Cardiovasc. Res. 69, 341-347 (2006).
101. Allison AC, Eugui EM. Mechanisms of action of mycophenolate mofetil in preventing acute and chronic allograft rejection. Transplantation 80, S181-190 (2005).
102. Kobashigawa JA, Meiser BM. Review of major clinical trials with mycophenolate mofetil in cardiac transplantation. Transplantation 80, S235-S243 (2005).
103. Pethig K, Heublein B, Wahlers T, Dannenberg O, Oppelt P, Haverich A. Mycophenolate mofetil for secondary prevention of cardiac allograft vasculopathy: influence on inflammation and progression of intimal hyperplasia. J. Heart Lung Transplant. 23, 61-66 (2004).
104. Romero F, Rodriguez-Iturbe B, Pons H et al. Mycophenolate mofetil treatment reduces cholesterol-induced atherosclerosis in the rabbit. Atherosclerosis 152, 127-133 (2000).
105. Greenstein SM, Sun S, Calderon TM et al. Mycophenolate mofetil treatment reduces atherosclerosis in the cholesterol-fed rabbit. J. Surg. Res. 91, 123-129 (2000).
106. Schreiber TC, Greenstein SM, Kim DY et al. Effect of mycophenolate mofetil on atherosclerosis in a rabbit model: initial histologic and immunohistochemical analyses. Transplant. Proc. 30, 961-962 (1998).
107. Law BK. Rapamycin: an anti-cancer immunosuppressant? Crit. Rev. Oncol. Hematol. 56, 47-60 (2005).
108. Lindenfeld J, Miller GG, Shakar SF et al. Drug therapy in the heart transplant recipient: part II: immunosuppressive drugs. Circulation 110, 3858-3865 (2004).
109. Serruys PW, Kutryk MJ, Ong AT. Coronary-artery stents. N. Engl. J. Med. 354, 483-495 (2006).
110. Mancini D, Pinney S, Burkhoff D et al. Use of rapamycin slows progression of cardiac transplantation vasculopathy. Circulation 108, 48-53 (2003).
111. Waksman R, Pakala R, Burnett MS et al. Oral rapamycin inhibits growth of atherosclerotic plaque in apoE knock-out mice. Cardiovasc. Radiat. Med. 4, 34-38 (2003).
112. Naoum JJ, Woodside KJ, Zhang S, Rychahou PG, Hunter GC. Effects of rapamycin on the arterial inflammatory response in atherosclerotic plaques in Apo-E knockout mice. Transplant. Proc. 37, 1880-1884 (2005).
113. Pakala R, Stabile E, Jang GJ, Clavijo L, Waksman R. Rapamycin attenuates atherosclerotic plaque progression in apolipoprotein E knockout mice: inhibitory effect on monocyte chemotaxis. J. Cardiovasc. Pharmacol. 46, 481-486 (2005).
114. Castro C, Campistol JM, Sancho D, Sanchez-Madrid F, Casals E, Andres V. Rapamycin attenuates atherosclerosis induced by dietary cholesterol in apolipoprotein-deficient mice through a p27 Kip1-independent pathway. Atherosclerosis 172, 31-38 (2004).
115. Elloso MM, Azrolan N, Sehgal SN et al. Protective effect of the immunosuppressant sirolimus against aortic atherosclerosis in apoE-deficient mice. Am. J. Transplant. 3, 562-569 (2003).
116. Basso MD, Nambi P, Adelman SJ. Effect of sirolimus on the cholesterol content of aortic arch in ApoE knockout mice. Transplant. Proc. 35, 3136-3138 (2003).
117. Farb A, John M, Acampado E, Kolodgie FD, Prescott MF, Virmani R. Oral everolimus inhibits in-stent neointimal growth. Circulation 106, 2379-2384 (2002).
118. Shibasaki F, Hallin U, Uchino H. Calcineurin as a multifunctional regulator. J. Biochem. (Tokyo) 131, 1-15 (2002).
119. Horsley V, Pavlath GK. NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell. Biol. 156, 771-774 (2002).
120. Pinney SP, Mancini D. Cardiac allograft vasculopathy: advances in understanding its pathophysiology, prevention, and treatment. Curr. Opin. Cardiol. 19, 170-176 (2004).
121. Miller LW. Cardiovascular toxicities of immunosuppressive agents. Am. J. Transplant. 2, 807-818 (2002).
122. Emeson EE, Shen ML. Accelerated atherosclerosis in hyperlipidemic C57BL/ 6 mice treated with cyclosporin A. Am. J. Pathol. 142, 1906-1915 (1993).
123. Drew AF, Tipping PG. Cyclosporine treatment reduces early atherosclerosis in the cholesterol-fed rabbit. Atherosclerosis 116, 181-189 (1995).
124. Roselaar SE, Schonfeld G, Daugherty A. Enhanced development of atherosclerosis in cholesterol-fed rabbits by suppression of cell-mediated immunity. J. Clin. Invest. 96, 1389-1394 (1995).
125. Andersen HO, Hansen BF, Holm P, Stender S, Nordestgaard BG. Effect of cyclosporine on arterial balloon injury lesions in cholesterol-clamped rabbits: T lymphocyte-mediated immune responses not involved in balloon injury-induced neointimal proliferation. Arterioscler. Thromb. Vasc. Biol. 19, 1687-1694 (1999).
126. Andersen HO, Holm P, Stender S, Hansen BF, Nordestgaard BG. Dose-dependent suppression of transplant arteriosclerosis in aorta-allografted, cholesterol-clamped rabbits. Suppression not eliminated by the cholesterol-raising effect of cyclosporine. Arterioscler. Thromb. Vasc. Biol. 17, 2515-2523 (1997).
127. Matsumoto T, Saito E, Watanabe H et al. Influence of FK506 on experimental atherosclerosis in cholesterol-fed rabbits. Atherosclerosis 139, 95-106 (1998).
128. Wu GD, Cramer DV, Chapman FA et al. FK 506 inhibits the development of transplant arteriosclerosis. Transplant. Proc. 23, 3272-3274 (1991).
129. -/- mice. Am. J. Transplant. 5, 1204-1215 (2005).
130. Pirsch JD, Miller J, Deierhoi MH, Vincenti F, Filo RS. A comparison of tacrolimus (FK506) and cyclosporine for immunosuppression after cadaveric renal transplantation. FK506 Kidney Transplant Study Group. Transplantation 63, 977-983 (1997).
131. Kung L, Halloran PF. Immunophilins may limit calcineurin inhibition by cyclosporine and tacrolimus at high drug concentrations. Transplantation 70, 327-335 (2000).
132. Zohlnhofer D, Klein CA, Richter T et al. Gene expression profiling of human stent-induced neointima by cDNA array analysis of microscopic specimens retrieved by helix cutter atherectomy: Detection of FK506-binding protein 12 upregulation. Circulation 103, 1396-1402 (2001).
133. Madjid M, Zarrabi A, Litovsky S, Willerson JT, Casscells W. Finding vulnerable atherosclerotic plaques: is it worth the effort? Arterioscler. Thromb. Vasc. Biol. 24, 1775-1782 (2004).
134. Mauriello A, Sangiorgi G, Fratoni S et al. Diffuse and active inflammation occurs in both vulnerable and stable plaques of the entire coronary tree: a histopathologic study of patients dying of acute myocardial infarction. J. Am. Coll. Cardiol. 45, 1585-1593 (2005).
135. Buffon A, Biasucci LM, Liuzzo G, D'Onofrio G, Crea F, Maseri A. Widespread coronary inflammation in unstable angina. N. Engl. J. Med. 347, 5-12 (2002).
136. Rioufol G, Gilard M, Finer G, Ginon I, Boschat J, Andre-Fouet X. Evolution of spontaneous atherosclerotic plaque rupture with medical therapy: long-term follow-up with intravascular ultrasound. Circulation 110, 2875-2880 (2004).
137. Humar A, Michaels M. American Society of Transplantation recommendations for screening, monitoring and reporting of infectious complications in immunosuppression trials in recipients of organ transplantation. Am. J. Transplant. 6, 262-274 (2006).