Cyclosporin A and atherosclerosis - Cellular pathways in atherogenesis

Pharmacology and Therapeutics

Volumn 128, Issue 1, 2010, Pages 106-118

  Kockx, Maaike ^a   Jessup, Wendy ^a   Kritharides, Leonard ^a,b  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Atherosclerosis; Calcineurin; Cardiovascular disease; Cyclosporin A; Hyperlipidemia; Immunosuppression

Indexed keywords

CHAPERONE; CYCLOPHILIN; CYCLOSPORIN A; LOW DENSITY LIPOPROTEIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PEPTIDYLPROLYL ISOMERASE; RAPAMYCIN; TACROLIMUS; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT; TRIACYLGLYCEROL;

ANTIINFLAMMATORY ACTIVITY; ATHEROGENESIS; ATHEROSCLEROSIS; BILE ACID SYNTHESIS; CARDIOVASCULAR EFFECT; CELL SECRETION; CELL STIMULATION; DISEASE ASSOCIATION; DRUG ABSORPTION; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG MECHANISM; DRUG METABOLISM; DRUG PROTEIN BINDING; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HYPERLIPIDEMIA; IMMUNOSUPPRESSIVE TREATMENT; LIPID METABOLISM; MACROPHAGE; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; CYCLOSPORINE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; NFATC TRANSCRIPTION FACTORS; SIGNAL TRANSDUCTION;

EID: 77956616337     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pharmthera.2010.06.001     Document Type: Review

References (150)

1. al Rayyes O., Wallmark A., Floren C.H. Reversal of cyclosporine-inhibited low-density lipoprotein receptor activity in HepG2 cells by 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors. Hepatology 1997, 25(4):991-994.
2. Allan L.L., Hoefl K., Zheng D.J., Chung B.K., Kozak F.K., Tan R., et al. Apolipoprotein-mediated lipid antigen presentation in B cells provides a pathway for innate help by NKT cells. Blood 2009, 114(12):2411-2416.
3. Andersen H.O., Hansen B.F., Holm P., Stender S., Nordestgaard B.G. 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 1999, 19(7):1687-1694.
4. Andersen H.O., Qvortrup K., Rostgaard J., Nordestgaard B.G. Effect of cyclosporine during initiation of transplant arteriosclerosis. An ultrastructural study in the aorta-transplanted rabbit. Atherosclerosis 1997, 133(2):171-181.
5. Andersson J., Libby P., Hansson G.K. Adaptive immunity and atherosclerosis. Clin Immunol 2010, 134(1):33-46.
6. Apanay D.C., Neylan J.F., Ragab M.S., Sgoutas D.S. Cyclosporine increases the oxidizability of low-density lipoproteins in renal transplant recipients. Transplantation 1994, 58(6):663-669.
7. Atger V., Leclerc T., Cambillau M., Guillemain R., Marti C., Moatti N., et al. Elevated high density lipoprotein concentrations in heart transplant recipients are related to impaired plasma cholesteryl ester transfer and hepatic lipase activity. Atherosclerosis 1993, 103(1):29-41.
8. Attur M.G., Patel R., Thakker G., Vyas P., Levartovsky D., Patel P., et al. Differential anti-inflammatory effects of immunosuppressive drugs: cyclosporin, rapamycin and FK-506 on inducible nitric oxide synthase, nitric oxide, cyclooxygenase-2 and PGE2 production. Inflamm Res 2000, 49(1):20-26.
9. Avdonin P.V., Cottet-Maire F., Afanasjeva G.V., Loktionova S.A., Lhote P., Ruegg U.T. Cyclosporine A up-regulates angiotensin II receptors and calcium responses in human vascular smooth muscle cells. Kidney Int 1999, 55(6):2407-2414.
10. Babiker A., Andersson O., Lund E., Xiu R.J., Deeb S., Reshef A., et al. Elimination of cholesterol in macrophages and endothelial cells by the sterol 27-hydroxylase mechanism. Comparison with high density lipoprotein-mediated reverse cholesterol transport. J Biol Chem 1997, 272(42):26253-26261.
11. Barik S. Immunophilins: for the love of proteins. Cell Mol Life Sci 2006, 63(24):2889-2900.
12. Bellosta S., Mahley R.W., Sanan D.A., Murata J., Newland D.L., Taylor J.M., et al. Macrophage-specific expression of human apolipoprotein E reduces atherosclerosis in hypercholesterolemic apolipoprotein E-null mice. J Clin Invest 1995, 96(5):2170-2179.
13. Bianchi G., Marchesini G., Marzocchi R., Pinna A.D., Zoli M. Metabolic syndrome in liver transplantation: relation to etiology and immunosuppression. Liver Transpl 2008, 14(11):1648-1654.
14. Bjorkhem I., Andersson O., Diczfalusy U., Sevastik B., Xiu R.J., Duan C., et al. Atherosclerosis and sterol 27-hydroxylase: evidence for a role of this enzyme in elimination of cholesterol from human macrophages. Proc Natl Acad Sci U S A 1994, 91(18):8592-8596.
15. Bohme M., Jedlitschky G., Leier I., Buchler M., Keppler D. ATP-dependent export pumps and their inhibition by cyclosporins. Adv Enzyme Regul 1994, 34:371-380.
16. Bohmer A.E., Souza D.G., Hansel G., Brum L.M., Portela L.V., Souza D.O. Long-term cyclosporine treatment in non-transplanted rats and metabolic risk factors of vascular diseases. Chem Biol Interact 2010, 185:53-58.
17. Borel J.F., Di Padova F., Mason J., Quesniaux V., Ryffel B., Wenger R. Pharmacology of cyclosporine (sandimmune). I. Introduction. Pharmacol Rev 1990, 41(3):239-242.
18. Bunjes D., Hardt C., Rollinghoff M., Wagner H. Cyclosporin A mediates immunosuppression of primary cytotoxic T cell responses by impairing the release of interleukin 1 and interleukin 2. Eur J Immunol 1981, 11(8):657-661.
19. Chan F.K., Shaffer E.A. Cholestatic effects of cyclosporine in the rat. Transplantation 1997, 63(11):1574-1578.
20. Chiara M.D., Sobrino F. Modulation of the inhibition of respiratory burst in mouse macrophages by cyclosporin A: effect of in vivo treatment, glucocorticoids and the state of activation of cells. Immunology 1991, 72(1):133-137.
21. Cofan F., Zambon D., Rodriguez C., Laguna J.C., Vazquez M., Casals E., et al. Fatty acid composition in low-density lipoproteins from renal transplant recipients. Transplant Proc 1999, 31(6):2330-2332.
22. Conde M., Andrade J., Bedoya F.J., Santa Maria C., Sobrino F. Inhibitory effect of cyclosporin A and FK506 on nitric oxide production by cultured macrophages. Evidence of a direct effect on nitric oxide synthase activity. Immunology 1995, 84(3):476-481.
23. Coppinger J.A., Cagney G., Toomey S., Kislinger T., Belton O., McRedmond J.P., et al. Characterization of the proteins released from activated platelets leads to localization of novel platelet proteins in human atherosclerotic lesions. Blood 2004, 103(6):2096-2104.
24. Cottet-Maire F., Avdonin P.V., Roulet E., Buetler T.M., Mermod N., Ruegg U.T. Upregulation of vasopressin V1A receptor mRNA and protein in vascular smooth muscle cells following cyclosporin A treatment. Br J Pharmacol 2001, 132(4):909-917.
25. Crompton M., Ellinger H., Costi A. Inhibition by cyclosporin A of a Ca2+-dependent pore in heart mitochondria activated by inorganic phosphate and oxidative stress. Biochem J 1988, 255(1):357-360.
26. Deters M., Kirchner G., Koal T., Resch K., Kaever V. Everolimus/cyclosporine interactions on bile flow and biliary excretion of bile salts and cholesterol in rats. Dig Dis Sci 2004, 49(1):30-37.
27. Devaraj S., Li D.J., Vazquez M., Jialal I. Cyclosporin A does not increase the oxidative susceptibility of low density lipoprotein in vitro. Free Radic Biol Med 1999, 26(7-8):1064-1068.
28. Drath D.B., Kahan B.D. Alterations in rat pulmonary macrophage function by the immunosuppressive agents cyclosporine, azathioprine, and prednisolone. Transplantation 1983, 35(6):588-592.
29. Drew A.F., Tipping P.G. Cyclosporine treatment reduces early atherosclerosis in the cholesterol-fed rabbit. Atherosclerosis 1995, 116(2):181-189.
30. Du M.R., Zhou W.H., Dong L., Zhu X.Y., He Y.Y., Yang J.Y., et al. Cyclosporin A promotes growth and invasiveness in vitro of human first-trimester trophoblast cells via MAPK3/MAPK1-mediated AP1 and Ca2+/calcineurin/NFAT signaling pathways. Biol Reprod 2008, 78(6):1102-1110.
31. Du S., Hiramatsu N., Hayakawa K., Kasai A., Okamura M., Huang T., et al. Suppression of NF-kappaB by cyclosporin a and tacrolimus (FK506) via induction of the C/EBP family: implication for unfolded protein response. J Immunol 2009, 182(11):7201-7211.
32. Emeson E.E., Shen M.L. Accelerated atherosclerosis in hyperlipidemic C57BL/6 mice treated with cyclosporin A. Am J Pathol 1993, 142(6):1906-1915.
33. Emmel E.A., Verweij C.L., Durand D.B., Higgins K.M., Lacy E., Crabtree G.R. Cyclosporin A specifically inhibits function of nuclear proteins involved in T cell activation. Science 1989, 246(4937):1617-1620.
34. Farmer J.A., Ballantyne C.M., Frazier O.H., Radovancevic B., Payton-Ross C., Patsch W., et al. Lipoprotein(a) and apolipoprotein changes after cardiac transplantation. J Am Coll Cardiol 1991, 18(4):926-930.
35. Fernandez-Miranda C., Guijarro C., de la Calle A., Loinaz C., Gonzalez-Pinto I., Gomez-Izquierdo T., et al. Lipid abnormalities in stable liver transplant recipients-effects of cyclosporin, tacrolimus, and steroids. Transpl Int 1998, 11(2):137-142.
36. Ferns G., Reidy M., Ross R. Vascular effects of cyclosporine A in vivo and in vitro. Am J Pathol 1990, 137(2):403-413.
37. Fliri H., Baumann G., Enz A., Kallen J., Luyten M., Mikol V., et al. Cyclosporins. Structure-activity relationships. Ann N Y Acad Sci 1993, 696:47-53.
38. Frantz B., Nordby E.C., Bren G., Steffan N., Paya C.V., Kincaid R.L., et al. Calcineurin acts in synergy with PMA to inactivate I kappa B/MAD3, an inhibitor of NF-kappa B. EMBO J 1994, 13(4):861-870.
39. Galan A.I., Roman I.D., Munoz M.E., Cava F., Gonzalez-Buitrago J.M., Esteller A., et al. Inhibition of biliary lipid and protein secretion by cyclosporine A in the rat. Biochem Pharmacol 1992, 44(6):1105-1113.
40. Galkina E., Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol 2009, 27:165-197.
41. Garcia J.E., de Cabo M.R., Rodriguez F.M., Losada J.P., Lopez A.J., Arellano J.L. Effect of cyclosporin A on inflammatory cytokine production by U937 monocyte-like cells. Mediators Inflamm 2000, 9(3-4):169-174.
42. Garvey S.M., Sinden D.S., Schoppee Bortz P.D., Wamhoff B.R. Cyclosporine up-regulates Kruppel-like factor-4 (KLF4) in vascular smooth muscle cells and drives phenotypic modulation in vivo. J Pharmacol Exp Ther 2010, 333(1):34-42.
43. Ghanem H., van den Dorpel M.A., Weimar W., Man in T.V.A.J., El-Kannishy M.H., Jansen H. Increased low density lipoprotein oxidation in stable kidney transplant recipients. Kidney Int 1996, 49(2):488-493.
44. Gomez L., Li B., Mewton N., Sanchez I., Piot C., Elbaz M., et al. Inhibition of mitochondrial permeability transition pore opening: translation to patients. Cardiovasc Res 2009, 83(2):226-233.
45. Gueguen Y., Ferrari L., Souidi M., Batt A.M., Lutton C., Siest G., et al. Compared effect of immunosuppressive drugs cyclosporine A and rapamycin on cholesterol homeostasis key enzymes CYP27A1 and HMG-CoA reductase. Basic Clin Pharmacol Toxicol 2007, 100(6):392-397.
46. Hamalainen M., Korhonen R., Moilanen E. Calcineurin inhibitors down-regulate iNOS expression by destabilizing mRNA. Int Immunopharmacol 2009, 9(2):159-167.
47. Hamalainen M., Lahti A., Moilanen E. Calcineurin inhibitors, cyclosporin A and tacrolimus inhibit expression of inducible nitric oxide synthase in colon epithelial and macrophage cell lines. Eur J Pharmacol 2002, 448(2-3):239-244.
48. Hansson G.K., Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006, 6(7):508-519.
49. Hirozane T., Matsumori A., Furukawa Y., Sasayama S. Experimental graft coronary artery disease in a murine heterotopic cardiac transplant model. Circulation 1995, 91(2):386-392.
50. Ho S., Clipstone N., Timmermann L., Northrop J., Graef I., Fiorentino D., et al. The mechanism of action of cyclosporin A and FK506. Clin Immunol Immunopathol 1996, 80(3 Pt 2):S40-S45.
51. Holdaas H., Fellstrom B., Jardine A.G., Holme I., Nyberg G., Fauchald P., et al. Effect of fluvastatin on cardiac outcomes in renal transplant recipients: a multicentre, randomised, placebo-controlled trial. Lancet 2003, 361(9374):2024-2031.
52. Husi H., Zurini M.G. Comparative binding studies of cyclophilins to cyclosporin A and derivatives by fluorescence measurements. Anal Biochem 1994, 222(1):251-255.
53. Ichiki T. Role of cAMP response element binding protein in cardiovascular remodeling: good, bad, or both?. Arterioscler Thromb Vasc Biol 2006, 26(3):449-455.
54. Ichimaru N., Takahara S., Kokado Y., Wang J.D., Hatori M., Kameoka H., et al. Changes in lipid metabolism and effect of simvastatin in renal transplant recipients induced by cyclosporine or tacrolimus. Atherosclerosis 2001, 158(2):417-423.
55. Ishikawa Y., Vranka J., Wirz J., Nagata K., Bachinger H.P. The rough endoplasmic reticulum-resident FK506-binding protein FKBP65 is a molecular chaperone that interacts with collagens. J Biol Chem 2008, 283(46):31584-31590.
56. Ito J., Nagayasu Y., Kato K., Sato R., Yokoyama S. Apolipoprotein A-I induces translocation of cholesterol, phospholipid, and caveolin-1 to cytosol in rat astrocytes. J Biol Chem 2002, 277(10):7929-7935.
57. Ivery M.T. Immunophilins: switched on protein binding domains?. Med Res Rev 2000, 20(6):452-484.
58. Jang G.H., Park I.S., Yang J.H., Bischoff J., Lee Y.M. Differential functions of genes regulated by VEGF-NFATc1 signaling pathway in the migration of pulmonary valve endothelial cells. FEBS Lett 2010, 584(1):141-146.
59. Jardine A.G., Holdaas H., Fellstrom B., Cole E., Nyberg G., Gronhagen-Riska C., et al. fluvastatin prevents cardiac death and myocardial infarction in renal transplant recipients: post-hoc subgroup analyses of the ALERT Study. Am J Transplant 2004, 4(6):988-995.
60. Javadov S., Karmazyn M., Escobales N. Mitochondrial permeability transition pore opening as a promising therapeutic target in cardiac diseases. J Pharmacol Exp Ther 2009, 330(3):670-678.
61. Javitt N.B. 25R, 26-Hydroxycholesterol revisited: synthesis, metabolism, and biologic roles. J Lipid Res 2002, 43(5):665-670.
62. Jin Z.G., Lungu A.O., Xie L., Wang M., Wong C., Berk B.C. Cyclophilin A is a proinflammatory cytokine that activates endothelial cells. Arterioscler Thromb Vasc Biol 2004, 24(7):1186-1191.
63. Jonasson L., Holm J., Hansson G.K. Cyclosporin A inhibits smooth muscle proliferation in the vascular response to injury. Proc Natl Acad Sci U S A 1988, 85(7):2303-2306.
64. Kang Y.J., Kusler B., Otsuka M., Hughes M., Suzuki N., Suzuki S., et al. Calcineurin negatively regulates TLR-mediated activation pathways. J Immunol 2007, 179(7):4598-4607.
65. Kaptein A., de Wit E.C., Princen H.M. Cotranslational inhibition of apoB-100 synthesis by cyclosporin A in the human hepatoma cell line HepG2. Arterioscler Thromb 1994, 14(5):780-789.
66. Karwatsky J., Ma L., Dong F., Zha X. Cholesterol efflux to apoA-I in ABCA1-expressing cells is regulated by Ca2+ dependent-calcineurin signaling. J Lipid Res 2010, 51:1144-1156.
67. Kasiske B.L. Cardiovascular disease after renal transplantation. Semin Nephrol 2000, 20(2):176-187.
68. Kheirollah A., Ito J., Nagayasu Y., Lu R., Yokoyama S. Cyclosporin A inhibits apolipoprotein A-I-induced early events in cellular cholesterol homeostasis in rat astrocytes. Neuropharmacology 2006, 51(4):693-700.
69. Kim S.H., Lessner S.M., Sakurai Y., Galis Z.S. Cyclophilin A as a novel biphasic mediator of endothelial activation and dysfunction. Am J Pathol 2004, 164(5):1567-1574.
70. Kimak E., Solski J., Baranowicz-Gaszczyk I., Ksiazek A. A long-term study of dyslipidemia and dyslipoproteinemia in stable post-renal transplant patients. Ren Fail 2006, 28(6):483-486.
71. Kockx M., Guo D.L., Traini M., Gaus K., Kay J., Wimmer-Kleikamp S., et al. Cyclosporin A decreases apolipoprotein E secretion from human macrophages via a protein phosphatase 2B-dependent and ATP-binding cassette transporter A1 (ABCA1)-independent pathway. J Biol Chem 2009, 284(36):24144-24154.
72. Kou R., Greif D., Michel T. Dephosphorylation of endothelial nitric-oxide synthase by vascular endothelial growth factor. Implications for the vascular responses to cyclosporin A. J Biol Chem 2002, 277(33):29669-29673.
73. Krauskopf A., Lhote P., Petermann O., Ruegg U.T., Buetler T.M. Cyclosporin A generates superoxide in smooth muscle cells. Free Radic Res 2005, 39(9):913-919.
74. Kritharides L., Stocker R. The use of antioxidant supplements in coronary heart disease. Atherosclerosis 2002, 164(2):211-219.
75. Kruger M., Schwaninger M., Blume R., Oetjen E., Knepel W. Inhibition of CREB- and cAMP response element-mediated gene transcription by the immunosuppressive drugs cyclosporin A and FK506 in T cells. Naunyn Schmiedebergs Arch Pharmacol 1997, 356(4):433-440.
76. Kunz D., Walker G., Eberhardt W., Nitsch D., Pfeilschifter J. Interleukin 1 beta-induced expression of nitric oxide synthase in rat renal mesangial cells is suppressed by cyclosporin A. Biochem Biophys Res Commun 1995, 216(2):438-446.
77. Kuster G.M., Drexel H., Bleisch J.A., Rentsch K., Pei P., Binswanger U., et al. Relation of cyclosporine blood levels to adverse effects on lipoproteins. Transplantation 1994, 57(10):1479-1483.
78. Le Goff W., Peng D.Q., Settle M., Brubaker G., Morton R.E., Smith J.D. Cyclosporin A traps ABCA1 at the plasma membrane and inhibits ABCA1-mediated lipid efflux to apolipoprotein A-I. Arterioscler Thromb Vasc Biol 2004, 24(11):2155-2161.
79. Lehmann J.M., Kliewer S.A., Moore L.B., Smith-Oliver T.A., Oliver B.B., Su J.L., et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem 1997, 272(6):3137-3140.
80. Li X., Stark G.R. NFkappaB-dependent signaling pathways. Exp Hematol 2002, 30(4):285-296.
81. Libby P. Inflammation in atherosclerosis. Nature 2002, 420(6917):868-874.
82. Liu Z., Zhang C., Dronadula N., Li Q., Rao G.N. Blockade of nuclear factor of activated T cells activation signaling suppresses balloon injury-induced neointima formation in a rat carotid artery model. J Biol Chem 2005, 280(15):14700-14708.
83. Lo Russo A., Passaquin A.C., Andre P., Skutella M., Ruegg U.T. Effect of cyclosporin A and analogues on cytosolic calcium and vasoconstriction: possible lack of relationship to immunosuppressive activity. Br J Pharmacol 1996, 118(4):885-892.
84. Lodish H.F., Kong N. Cyclosporin A inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J Biol Chem 1991, 266(23):14835-14838.
85. Lopez-Miranda J., Vilella E., Perez-Jimenez F., Espino A., Jimenez-Pereperez J.A., Masana L., et al. Low-density lipoprotein metabolism in rats treated with cyclosporine. Metabolism 1993, 42(6):678-683.
86. Lorenzi I., von Eckardstein A., Cavelier C., Radosavljevic S., Rohrer L. Apolipoprotein A-I but not high-density lipoproteins are internalised by RAW macrophages: roles of ATP-binding cassette transporter A1 and scavenger receptor BI. J Mol Med 2008, 86(2):171-183.
87. Lundberg A.M., Hansson G.K. Innate immune signals in atherosclerosis. Clin Immunol 2010, 134(1):5-24.
88. Lungu A.O., Jin Z.G., Yamawaki H., Tanimoto T., Wong C., Berk B.C. Cyclosporin A inhibits flow-mediated activation of endothelial nitric-oxide synthase by altering cholesterol content in caveolae. J Biol Chem 2004, 279(47):48794-48800.
89. Ma W., Mishra S., Gee K., Mishra J.P., Nandan D., Reiner N.E., et al. Cyclosporin A and FK506 inhibit IL-12p40 production through the calmodulin/calmodulin-dependent protein kinase-activated phosphoinositide 3-kinase in lipopolysaccharide-stimulated human monocytic cells. J Biol Chem 2007, 282(18):13351-13362.
90. Macri J., Adeli K. Studies on intracellular translocation of apolipoprotein B in a permeabilized HepG2 system. J Biol Chem 1997, 272(11):7328-7337.
91. Maitra U., Parks J.S., Li L. An innate immunity signaling process suppresses macrophage ABCA1 expression through IRAK-1-mediated downregulation of retinoic acid receptor alpha and NFATc2. Mol Cell Biol 2009, 29(22):5989-5997.
92. Malesevic M., Kuhling J., Erdmann F., Balsley M.A., Bukrinsky M.I., Constant S.L., et al. A cyclosporin derivative discriminates between extracellular and intracellular cyclophilins. Angew Chem Int Ed Engl 2010, 49(1):213-215.
93. Marks A.R. Cellular functions of immunophilins. Physiol Rev 1996, 76(3):631-649.
94. Matsuda S., Shibasaki F., Takehana K., Mori H., Nishida E., Koyasu S. Two distinct action mechanisms of immunophilin-ligand complexes for the blockade of T-cell activation. EMBO Rep 2000, 1(5):428-434.
95. Matsumoto Y., Hof A., Baumlin Y., Hof R.P. Differential effect of cyclosporine A and SDZ RAD on neointima formation of carotid allografts in apolipoprotein E-deficient mice. Transplantation 2003, 76(8):1166-1170.
96. Mercanoglu F., Turkmen A., Kocaman O., Pinarbasi B., Dursun M., Selcukbiricik F., et al. Endothelial dysfunction in renal transplant patients is closely related to serum cyclosporine levels. Transplant Proc 2004, 36(5):1357-1360.
97. Meurs I., Van Eck M., Van Berkel T.J. HDL: key molecule in cholesterol efflux and the prevention of atherosclerosis. Curr Pharm Des 2010, 16(13):1445-1467.
98. Miller L.W. Cardiovascular toxicities of immunosuppressive agents. Am J Transplant 2002, 2(9):807-818.
99. Moghadasian M.H. Dietary phytosterols reduce cyclosporine-induced hypercholesterolemia in apolipoprotein E-knockout mice. Transplantation 2006, 81(2):207-213.
100. Mok D., Allan R.K., Carrello A., Wangoo K., Walkinshaw M.D., Ratajczak T. The chaperone function of cyclophilin 40 maps to a cleft between the prolyl isomerase and tetratricopeptide repeat domains. FEBS Lett 2006, 580(11):2761-2768.
101. Monaco C., Paleolog E. Nuclear factor kappaB: a potential therapeutic target in atherosclerosis and thrombosis. Cardiovasc Res 2004, 61(4):671-682.
102. Montori V.M., Basu A., Erwin P.J., Velosa J.A., Gabriel S.E., Kudva Y.C. Posttransplantation diabetes: a systematic review of the literature. Diabetes Care 2002, 25(3):583-592.
103. Moran D., De Buitrago J.M., Fernandez E., Galan A.I., Munoz M.E., Jimenez R. Inhibition of biliary glutathione secretion by cyclosporine A in the rat: possible mechanisms and role in the cholestasis induced by the drug. J Hepatol 1998, 29(1):68-77.
104. Murakami R., Kambe F., Mitsuyama H., Okumura K., Murohara T., Niwata S., et al. Cyclosporin A enhances interleukin-8 expression by inducing activator protein-1 in human aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 2003, 23(11):2034-2040.
105. Naseem K.M. The role of nitric oxide in cardiovascular diseases. Mol Aspects Med 2005, 26(1-2):33-65.
106. Navarro-Antolin J., Rey-Campos J., Lamas S. Transcriptional induction of endothelial nitric oxide gene by cyclosporine A. A role for activator protein-1. J Biol Chem 2000, 275(5):3075-3080.
107. Ojo A.O. Cardiovascular complications after renal transplantation and their prevention. Transplantation 2006, 82(5):603-611.
108. Olyaei A.J., de Mattos A.M., Bennett W.M. Nephrotoxicity of immunosuppressive drugs: new insight and preventive strategies. Curr Opin Crit Care 2001, 7(6):384-389.
109. Palay D.A., Cluff C.W., Wentworth P.A., Ziegler H.K. Cyclosporine inhibits macrophage-mediated antigen presentation. J Immunol 1986, 136(12):4348-4353.
110. Parthasarathy S., Raghavamenon A., Garelnabi M.O., Santanam N. Oxidized low-density lipoprotein. Methods Mol Biol 2010, 610:403-417.
111. Payeli S.K., Schiene-Fischer C., Steffel J., Camici G.G., Rozenberg I., Luscher T.F., et al. Cyclophilin A differentially activates monocytes and endothelial cells: role of purity, activity, and endotoxin contamination in commercial preparations. Atherosclerosis 2008, 197(2):564-571.
112. Piot C., Croisille P., Staat P., Thibault H., Rioufol G., Mewton N., et al. Effect of cyclosporine on reperfusion injury in acute myocardial infarction. N Engl J Med 2008, 359(5):473-481.
113. Princen H.M., Meijer P., Wolthers B.G., Vonk R.J., Kuipers F. Cyclosporin A blocks bile acid synthesis in cultured hepatocytes by specific inhibition of chenodeoxycholic acid synthesis. Biochem J 1991, 275(Pt 2):501-505.
114. Rafiee P., Johnson C.P., Li M.S., Ogawa H., Heidemann J., Fisher P.J., et al. Cyclosporine A enhances leukocyte binding by human intestinal microvascular endothelial cells through inhibition of p38 MAPK and iNOS. Paradoxical proinflammatory effect on the microvascular endothelium. J Biol Chem 2002, 277(38):35605-35615.
115. Ragheb A., Attia A., Elbarbry F., Prasad K., Shoker A. Attenuated combined action of cyclosporine A and hyperlipidemia on atherogenesis in rabbits by thymoquinone. Evid Based Complement Alternat Med 2009, [Electronic publication ahead of print, Dec 29].
116. Ramezani M., Einollahi B., Ahmadzad-Asl M., Nafar M., Pourfarziani V., Samadpour A., et al. Hyperlipidemia after renal transplantation and its relation to graft and patient survival. Transplant Proc 2007, 39(4):1044-1047.
117. Rasola A., Sciacovelli M., Pantic B., Bernardi P. Signal transduction to the permeability transition pore. FEBS Lett 2010, 584:1989-1996.
118. Rayyes O.A., Wallmark A., Floren C.H. Cyclosporine inhibits catabolism of low-density lipoproteins in HepG2 cells by about 25%. Hepatology 1996, 24(3):613-619.
119. Reymond J.P., Steimer J.L., Niederberger W. On the dose dependency of cyclosporin A absorption and disposition in healthy volunteers. J Pharmacokinet Biopharm 1988, 16(4):331-353.
120. Robert N., Wong G.W., Wright J.M. Effect of cyclosporine on blood pressure. Cochrane Database Syst Rev 2010, 1. CD007893.
121. Rodriguez A., Roy J., Martinez-Martinez S., Lopez-Maderuelo M.D., Nino-Moreno P., Orti L., et al. A conserved docking surface on calcineurin mediates interaction with substrates and immunosuppressants. Mol Cell 2009, 33(5):616-626.
122. Roselaar S.E., Schonfeld G., Daugherty A. Enhanced development of atherosclerosis in cholesterol-fed rabbits by suppression of cell-mediated immunity. J Clin Invest 1995, 96(3):1389-1394.
123. Satoh K., Nigro P., Matoba T., O'Dell M.R., Cui Z., Shi X., et al. Cyclophilin A enhances vascular oxidative stress and the development of angiotensin II-induced aortic aneurysms. Nat Med 2009, 15(6):649-656.
124. Satonaka H., Suzuki E., Nishimatsu H., Oba S., Takeda R., Goto A., et al. Calcineurin promotes the expression of monocyte chemoattractant protein-1 in vascular myocytes and mediates vascular inflammation. Circ Res 2004, 94(5):693-700.
125. Schweighofer B., Testori J., Sturtzel C., Sattler S., Mayer H., Wagner O., et al. The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation. Thromb Haemost 2009, 102(3):544-554.
126. Segev H., Honigman A., Rosen H., Leitersdorf E. Transcriptional regulation of the human sterol 27-hydroxylase gene (CYP27) and promoter mapping. Atherosclerosis 2001, 156(2):339-347.
127. Seizer P., Schonberger T., Schott M., M.R.L., Langer H.F., Bigalke B., et al. EMMPRIN and its ligand cyclophilin A regulate MT1-MMP, MMP-9 and M-CSF during foam cell formation. Atherosclerosis 2010, 209:51-57.
128. Sherry B., Yarlett N., Strupp A., Cerami A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc Natl Acad Sci U S A 1992, 89(8):3511-3515.
129. Souidi M., Parquet M., Ferezou J., Lutton C. Modulation of cholesterol 7alpha-hydroxylase and sterol 27-hydroxylase activities by steroids and physiological conditions in hamster. Life Sci 1999, 64(17):1585-1593.
130. Spady D.K. Regulatory effects of individual n-6 and n-3 polyunsaturated fatty acids on LDL transport in the rat. J Lipid Res 1993, 34(8):1337-1346.
131. Steinmann B., Bruckner P., Superti-Furga A. Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cis-trans-isomerase. J Biol Chem 1991, 266(2):1299-1303.
132. Stieger B., Fattinger K., Madon J., Kullak-Ublick G.A., Meier P.J. Drug- and estrogen-induced cholestasis through inhibition of the hepatocellular bile salt export pump (Bsep) of rat liver. Gastroenterology 2000, 118(2):422-430.
133. Sutherland W.H., Walker R.J., Ball M.J., Stapley S.A., Corboy J., Robertson M.C. Cholesterol precursor concentration in plasma from patients with chronic renal failure or kidney grafts. Clin Nephrol 1995, 43(6):392-398.
134. Tanaka H., Sukhova G.K., Libby P. Interaction of the allogeneic state and hypercholesterolemia in arterial lesion formation in experimental cardiac allografts. Arterioscler Thromb 1994, 14(5):734-745.
135. Tedgui A., Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 2006, 86(2):515-581.
136. Thomas S.R., Witting P.K., Drummond G.R. Redox control of endothelial function and dysfunction: molecular mechanisms and therapeutic opportunities. Antioxid Redox Signal 2008, 10(10):1713-1765.
137. Tory R., Sachs-Barrable K., Hill J.S., Wasan K.M. Cyclosporine A and Rapamycin induce in vitro cholesteryl ester transfer protein activity, and suppress lipoprotein lipase activity in human plasma. Int J Pharm 2008, 358(1-2):219-223.
138. Uittenbogaard A., Everson W.V., Matveev S.V., Smart E.J. Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J Biol Chem 2002, 277(7):4925-4931.
139. Uittenbogaard A., Ying Y., Smart E.J. Characterization of a cytosolic heat-shock protein-caveolin chaperone complex. Involvement in cholesterol trafficking. J Biol Chem 1998, 273(11):6525-6532.
140. van den Dorpel M.A., Ghanem H., Rischen-Vos J., Man in't Veld A.J., Jansen H., Weimar W. Conversion from cyclosporine A to azathioprine treatment improves LDL oxidation in kidney transplant recipients. Kidney Int 1997, 51(5):1608-1612.
141. van den Elzen P., Garg S., Leon L., Brigl M., Leadbetter E.A., Gumperz J.E., et al. Apolipoprotein-mediated pathways of lipid antigen presentation. Nature 2005, 437(7060):906-910.
142. Vaziri N.D., Liang K., Azad H. Effect of cyclosporine on HMG-CoA reductase, cholesterol 7alpha-hydroxylase, LDL receptor, HDL receptor, VLDL receptor, and lipoprotein lipase expressions. J Pharmacol Exp Ther 2000, 294(2):778-783.
143. Wehr S., Rudin M., Joergensen J., Hof A., Hof R.P. Allo- and autotransplantation of carotid artery-a new model of chronic graft vessel disease: evaluation by magnetic resonance imaging and histology. Transplantation 1997, 64(1):20-27.
144. Wenger R.M., Payne T. Cyclosporine: intrinsic binding energies to interpret structure-activity relationships. Prog Clin Biol Res 1989, 291:301-305.
145. Whisler R.L., Lindsey J.A., Proctor K.V., Newhouse Y.G., Cornwell D.G. The impaired ability of human monocytes to stimulate autologous and allogeneic mixed lymphocyte reactions after exposure to cyclosporine. Associated alterations of HLA-DR expression and physical characteristics of monocytes. Transplantation 1985, 40(1):57-61.
146. Winegar D.A., Salisbury J.A., Sundseth S.S., Hawke R.L. Effects of cyclosporin on cholesterol 27-hydroxylation and LDL receptor activity in HepG2 cells. J Lipid Res 1996, 37(1):179-191.
147. Woodfield K., Ruck A., Brdiczka D., Halestrap A.P. Direct demonstration of a specific interaction between cyclophilin-D and the adenine nucleotide translocase confirms their role in the mitochondrial permeability transition. Biochem J 1998, 336(Pt 2):287-290.
148. Wu J., Zhu Y.H., Patel S.B. Cyclosporin-induced dyslipoproteinemia is associated with selective activation of SREBP-2. Am J Physiol 1999, 277(6 Pt 1):E1087-E1094.
149. Yu H., van Berkel T.J., Biessen E.A. Therapeutic potential of VIVIT, a selective peptide inhibitor of nuclear factor of activated T cells, in cardiovascular disorders. Cardiovasc Drug Rev 2007, 25(2):175-187.
150. Zheng X.L., Wong N.C. Cyclosporin A inhibits apolipoprotein AI gene expression. J Mol Endocrinol 2006, 37(2):367-373.