Everolimus triggers cytokine release by macrophages: Rationale for stents eluting everolimus and a glucocorticoid

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 5, 2012, Pages 1228-1235

  Martinet, Wim ^a   Verheye, Stefan ^b   De Meyer, Inge ^a   Timmermans, Jean Pierre ^a   Schrijvers, Dorien M ^a   Van Brussel, Ilse ^a   Bult, Hidde ^a   De Meyer, Guido R Y ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b MIDDELHEIM HOSPITAL   (Belgium)

Author keywords

Atherosclerosis; Autophagy; Everolimus; Inflammation; Macrophages

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CLOBETASOL; CYTOKINE; EVEROLIMUS; INTERLEUKIN 6; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PEPTIDES AND PROTEINS; PROTEIN ATG7; RANTES; RAPAMYCIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; AUTOPHAGY; CONTROLLED STUDY; CORONARY ARTERY DISEASE; CYTOKINE RELEASE; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; DRUG ELUTING STENT; ENZYME ACTIVATION; ENZYME INHIBITION; EXPERIMENTAL RABBIT; HUMAN; HUMAN CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN SYNTHESIS;

ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CELL SURVIVAL; CELLS, CULTURED; CORONARY ARTERY DISEASE; CYTOKINES; DISEASE MODELS, ANIMAL; DRUG-ELUTING STENTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLUCOCORTICOIDS; HUMANS; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; PROSTHESIS DESIGN; RABBITS; SIROLIMUS;

EID: 84860224468     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.245381     Document Type: Article

References (44)

1. Kapur NK, Musunuru K. Clinical efficacy and safety of statins in managing cardiovascular risk. Vasc Health Risk Manag. 2008;4:341-353. (Pubitemid 351711963)
2. Ambrose JA, Martinez EE. A new paradigm for plaque stabilization. Circulation. 2002;105:2000-2004. (Pubitemid 34437631)
3. Beltowski J, Wojcicka G, Jamroz-Wisniewska A. Adverse effects of statins: mechanisms and consequences. Curr Drug Saf. 2009;4:209-228.
4. Moubayed SP, Heinonen TM, Tardif JC. Anti-inflammatory drugs and atherosclerosis. Curr Opin Lipidol. 2007;18:638-644. (Pubitemid 350103399)
5. Jia L, Hui RT. Everolimus, a promising medical therapy for coronary heart disease? Med Hypotheses. 2009;73:153-155.
6. Marx SO, Jayaraman T, Go LO, Marks AR. Rapamycin-FKBP inhibits cell cycle regulators of proliferation in vascular smooth muscle cells. Circ Res. 1995;76:412-417.
7. Easton JB, Houghton PJ. Therapeutic potential of target of rapamycin inhibitors. Exp Opin Ther Targets. 2004;8:551-564. (Pubitemid 40028366)
8. Baetta R, Granata A, Canavesi M, Ferri N, Arnaboldi L, Bellosta S, Pfister P, Corsini A. Everolimus inhibits monocyte/macrophage migration in vitro and their accumulation in carotid lesions of cholesterol-fed rabbits. J Pharmacol Exp Ther. 2009;328:419-425.
9. Verheye S, Martinet W, Kockx MM, Knaapen MW, Salu K, Timmermans JP, Ellis JT, Kilpatrick DL, De Meyer GRY. Selective clearance of macrophages in atherosclerotic plaques by autophagy. J Am Coll Cardiol. 2007;49:706-715. (Pubitemid 46205042)
10. Martinet W, Verheye S, De Meyer GRY. Everolimus-induced mTOR inhibition selectively depletes macrophages in atherosclerotic plaques by autophagy. Autophagy. 2007;3:241-244. (Pubitemid 46752686)
11. Ma KL, Varghese Z, Ku Y, Powis SH, Chen Y, Moorhead JF, Ruan XZ. Sirolimus inhibits endogenous cholesterol synthesis induced by inflammatory stress in human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2010;298:H1646-H1651.
12. Ma KL, Ruan XZ, Powis SH, Moorhead JF, Varghese Z. Anti-atherosclerotic effects of sirolimus on human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2007;292:H2721-H2728. (Pubitemid 47084520)
13. Mathis AS, Jin S, Friedman GS, Peng F, Carl SM, Knipp GT. The pharmacodynamic effects of sirolimus and sirolimus-calcineurin inhibitor combinations on macrophage scavenger and nuclear hormone receptors. J Pharm Sci. 2007;96:209-222. (Pubitemid 46087351)
14. Cheng C, Tempel D, Oostlander A, Helderman F, Gijsen F, Wentzel J, van Haperen R, Haitsma DB, Serruys PW, van der Steen AF, de Crom R, Krams R. Rapamycin modulates the eNOS vs shear stress relationship. Cardiovasc Res. 2008;78:123-129. (Pubitemid 351430952)
15. Goueffic Y, Potter-Perigo S, Chan CK, Johnson PY, Braun K, Evanko SP, Wight TN. Sirolimus blocks the accumulation of hyaluronan (HA) by arterial smooth muscle cells and reduces monocyte adhesion to the ECM. Atherosclerosis. 2007;195:23-30. (Pubitemid 47561940)
16. 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. 2005;46:481-486. (Pubitemid 41407577)
17. Mueller MA, Beutner F, Teupser D, Ceglarek U, Thiery J. Prevention of atherosclerosis by the mTOR inhibitor everolimus in LDLR2/2 mice despite severe hypercholesterolemia. Atherosclerosis. 2008;198:39-48. (Pubitemid 351406366)
18. Johnson EM, Zimmerman J, Duderstadt K, Chambers J, Sorenson AL, Granger DK, Almond PS, Fryer J, Leventhal JR, Scarola J, Matas AJ, Canafax DM. A randomized, double-blind, placebo-controlled study of the safety, tolerance, and preliminary pharmacokinetics of ascending single doses of orally administered sirolimus (rapamycin) in stable renal transplant recipients. Transplant Proc. 1996;28:987. (Pubitemid 26138507)
19. Brattstrom C, Sawe J, Jansson B, Lonnebo A, Nordin J, Zimmerman JJ, Burke JT, Groth CG. Pharmacokinetics and safety of single oral doses of sirolimus (rapamycin) in healthy male volunteers. Ther Drug Monit. 2000;22:537-544.
20. Formica RN, Formica RN Jr, Lorber KM, Friedman AL, Bia MJ, Lakkis F, Smith JD, Lorber MI. The evolving experience using everolimus in clinical transplantation. Transplant Proc. 2004;36:495S-499S. (Pubitemid 38373918)
21. Cassese S, Piccolo R, Galasso G, De Rosa R, Piscione F. Twelve-month clinical outcomes of everolimus-eluting stent as compared to paclitaxel-and sirolimus-eluting stent in patients undergoing percutaneous coronary interventions: a meta-analysis of randomized clinical trials. Int J Cardiol. 2011;150:84-89.
22. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, Tanaka K, Kawai T, Tsujimura T, Takeuchi O, Yoshimori T, Akira S. Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature. 2008;456:264-268.
23. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011;469:221-225.
24. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, Fitzgerald KA, Ryter SW, Choi AM. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011;12:222-230.
25. Harris J, Hartman M, Roche C, Zeng SG, O'Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem. 2011;286:9587-9597.
26. Crisan TO, Plantinga TS, van de Veerdonk FL, Farcas MF, Stoffels M, Kullberg BJ, van der Meer JW, Joosten LA, Netea MG. Inflammasome-independent modulation of cytokine response by autophagy in human cells. PLoS One. 2011;6:e18666.
27. Davies JQ, Gordon S. Isolation and culture of murine macrophages. Methods Mol Biol. 2005;290:91-103.
28. Komatsu M, Waguri S, Ueno T, Iwata J, Murata S, Tanida I, Ezaki J, Mizushima N, Ohsumi Y, Uchiyama Y, Kominami E, Tanaka K, Chiba T. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005;169:425-434. (Pubitemid 40686693)
29. Vindelov LL, Christensen IJ. Detergent and proteolytic enzyme-based techniques for nuclear isolation and DNA content analysis. Methods Cell Biol. 1994;41:219-229.
30. Schieven GL. The biology of p38 kinase: a central role in inflammation. Curr Top Med Chem. 2005;5:921-928. (Pubitemid 41582124)
31. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GRY. Selective clearance of macrophages in atherosclerotic plaques by the protein synthesis inhibitor cycloheximide. J Pharmacol Exp Ther. 2007;320:986-993. (Pubitemid 46294043)
32. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GRY. The protein synthesis inhibitor anisomycin induces macrophage apoptosis in rabbit atherosclerotic plaques through p38 mitogen-activated protein kinase. J Pharmacol Exp Ther. 2009;329:856-864.
33. Abeliovich H. Regulation of autophagy by the target of rapamycin (Tor) proteins. In: Klionsky DJ, ed. Autophagy. Georgetown, TX: Landes Bioscience; 2004:60-69.
34. Leonard EJ, Skeel A, Yoshimura T, Rankin J. Secretion of monocyte chemoattractant protein-1 (MCP-1) by human mononuclear phagocytes. Adv Exp Med Biol. 1993;351:55-64. (Pubitemid 24222626)
35. Ueda A, Ishigatsubo Y, Okubo T, Yoshimura T. Transcriptional regulation of the human monocyte chemoattractant protein-1 gene: cooperation of two NF-kappaB sites and NF-kappaB/Rel subunit specificity. J Biol Chem. 1997;272:31092-31099. (Pubitemid 27527558)
36. Tanimoto A, Murata Y, Wang KY, Tsutsui M, Kohno K, Sasaguri Y. Monocyte chemoattractant protein-1 expression is enhanced by granulocyte-macrophage colony-stimulating factor via Jak2-Stat5 signaling and inhibited by atorvastatin in human monocytic U937 cells. J Biol Chem. 2008;283:4643-4651.
37. Pels R, Sterry W, Lademann J. Clobetasol propionate: where, when, why? Drugs Today (Barc). 2008;44:547-557.
38. Ning YM, Sanchez ER. Potentiation of glucocorticoid receptor-mediated gene expression by the immunophilin ligands FK506 and rapamycin. J Biol Chem. 1993;268:6073-6076. (Pubitemid 23099290)
39. Medh RD, Lay RH, Schmidt TJ. Agonist-specific modulation of glucocorticoid receptor-mediated transcription by immunosuppressants. Mol Cell Endocrinol. 1998;138:11-23. (Pubitemid 28302013)
40. Boumpas DT, Paliogianni F, Anastassiou ED, Balow JE. Glucocorticosteroid action on the immune system: molecular and cellular aspects. Clin Exp Rheumatol. 1991;9:413-423.
41. Boumpas DT. A novel action of glucocorticoids: NF-kappa B inhibition. Br J Rheumatol. 1996;35:709-710. (Pubitemid 26273190)
42. Yang Z, Klionsky DJ. Eaten alive: a history of macroautophagy. Nat Cell Biol. 2010;12:814-822.
43. Garg S, Serruys P, Onuma Y, Dorange C, Veldhof S, Miquel-Hebert K, Sudhir K, Boland J, Huber K, Garcia E, te Riele JA. Three-year clinical follow-up of the XIENCE V everolimus-eluting coronary stent system in the treatment of patients with de novo coronary artery lesions: the SPIRIT II trial. J Am Coll Cardiol Cardiovasc Interv. 2009;2:1190-1198.
44. Nakazawa G, Nakano M, Otsuka F, Wilcox JN, Melder R, Pruitt S, Kolodgie FD, Virmani R. Evaluation of polymer-based comparator drug-eluting stents using a rabbit model of iliac artery atherosclerosis. Circ Cardiovasc Interv. 2011;4:38-46.