Drug-induced macrophage autophagy in atherosclerosis: For better or worse?

Basic Research in Cardiology

Volumn 108, Issue 1, 2013, Pages

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

^a UNIVERSITY OF ANTWERP   (Belgium)

^b ZNA Middelheim   (Belgium)

Author keywords

Atherosclerosis; Autophagy; Everolimus; Imiquimod; Macrophage

Indexed keywords

CLOBETASOL; EVEROLIMUS; IMIQUIMOD; INFLAMMASOME; LIGAND; MAMMALIAN TARGET OF RAPAMYCIN INHIBITOR; RAPAMYCIN; RIDAFOROLIMUS; TEMSIROLIMUS; TOLL LIKE RECEPTOR 7; ZOTAROLIMUS;

APOPTOSIS; ATG5 GENE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPHAGY; CYTOKINE RELEASE; DRUG MECHANISM; GENE; GENE DELETION; HUMAN; MACROPHAGE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; REVIEW;

EID: 84870584445     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-012-0321-1     Document Type: Review

References (83)

1. Alinari L, Baiocchi RA, Praetorius-Ibba M (2012) FTY720-induced blockage of autophagy enhances anticancer efficacy of milatuzumab in mantle cell lymphoma: is FTY720 the next autophagy-blocking agent in lymphoma treatment? Autophagy 8:416-417. doi: 10.4161/auto.19050
2. Alinari L, Mahoney E, Patton J, Zhang X, Huynh L, Earl CT, Mani R, Mao Y, Yu B, Quinion C, Towns WH, Chen CS, Goldenberg DM, Blum KA, Byrd JC, Muthusamy N, Praetorius-Ibba M, Baiocchi RA (2011) FTY720 increases CD74 expression and sensitizes mantle cell lymphoma cells to milatuzumab-mediated cell death. Blood 118:6893-6903. doi: 10.1182/blood-2011-06-363879
3. Andersson U, Wang H, Palmblad K, Aveberger AC, Bloom O, Erlandsson-Harris H, Janson A, Kokkola R, Zhang M, Yang H, Tracey KJ (2000) High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J Exp Med 192:565-570. doi: 10.1084/jem.192.4.565 (Pubitemid 30666257)
4. Baetta R, Granata A, Canavesi M, Ferri N, Arnaboldi L, Bellosta S, Pfister P, Corsini A (2009) Everolimus inhibits monocyte/macrophage migration in vitro and their accumulation in carotid lesions of cholesterol-fed rabbits. J Pharmacol Exp Ther 328:419-425. doi: 10.1124/jpet.108.144147
5. Baldo P, Cecco S, Giacomin E, Lazzarini R, Ros B, Marastoni S (2008) mTOR pathway and mTOR inhibitors as agents for cancer therapy. Curr Cancer Drug Targets 8:647-665
6. Basso MD, Nambi P, Adelman SJ (2003) Effect of sirolimus on the cholesterol content of aortic arch in ApoE knockout mice. Transplant Proc 35:3136-3138. doi: 10.1016/j.transproceed.2003.10.050 (Pubitemid 38102149)
7. Bjornheden T, Bondjers G (1987) Oxygen consumption in aortic tissue from rabbits with diet-induced atherosclerosis. Arteriosclerosis 7:238-247 (Pubitemid 17090952)
8. Clarke PG, Puyal J (2012) Autophagic cell death exists. Autophagy 8:867-869. doi: 10.4161/auto.20380
9. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GRY (2007) Selective clearance of macrophages in atherosclerotic plaques by the protein synthesis inhibitor cycloheximide. J Pharmacol Exp Ther 320:986-993. doi: 10.1124/jpet.106.113944 (Pubitemid 46294043)
10. Croons V, Martinet W, Herman AG, Timmermans JP, De Meyer GRY (2009) The protein synthesis inhibitor anisomycin induces macrophage apoptosis in rabbit atherosclerotic plaques through p38 mitogen-activated protein kinase. J Pharmacol Exp Ther 329:856-864. doi: 10.1124/jpet.108.149948
11. De Meyer I, Martinet W, Van Hove CE, Schrijvers DM, Hoymans VY, Van VL, Fransen P, Bult H, De Meyer GRY (2011) Inhibition of inositol monophosphatase by lithium chloride induces selective macrophage apoptosis in atherosclerotic plaques. Br J Pharmacol 162:1410-1423. doi: 10.1111/j.1476-5381.2010.01152.x
12. De Meyer I, Martinet W, Schrijvers DM, Timmermans J-P, Bult H, De Meyer GRY (2012) Toll-like receptor 7 stimulation by imiquimod induces macrophage autophagy and inflammation in atherosclerotic plaques. Basic Res Cardiol 107:269. doi: 10.1007/s00395-012-0269-1
13. Decuypere JP, Bultynck G, Parys JB (2011) A dual role for Ca(2+) in autophagy regulation. Cell Calcium 50:242-250. doi: 10.1016/j.ceca.2011.04.001
14. Delgado MA, Elmaoued RA, Davis AS, Kyei G, Deretic V (2008) Toll-like receptors control autophagy. EMBO J 27:1110-1121. doi: 10.1038/emboj.2008.31 (Pubitemid 351508141)
15. Denton D, Nicolson S, Kumar S (2012) Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 19:87-95. doi: 10.1038/cdd.2011.146
16. Eisenberg T, Knauer H, Schauer A, Buttner S, Ruckenstuhl C, Carmona-Gutierrez D, Ring J, Schroeder S, Magnes C, Antonacci L, Fussi H, Deszcz L, Hartl R, Schraml E, Criollo A, Megalou E, Weiskopf D, Laun P, Heeren G, Breitenbach M, Grubeck-Loebenstein B, Herker E, Fahrenkrog B, Frohlich KU, Sinner F, Tavernarakis N, Minois N, Kroemer G, Madeo F (2009) Induction of autophagy by spermidine promotes longevity. Nat Cell Biol 11:1305-1314. doi: 10.1038/ncb1975
17. Feingold KR, Kazemi MR, Magra AL, McDonald CM, Chui LG, Shigenaga JK, Patzek SM, Chan ZW, Londos C, Grunfeld C (2010) ADRP/ADFP and Mal1 expression are increased in macrophages treated with TLR agonists. Atherosclerosis 209:81-88. doi: 10.1016/j.atherosclerosis.2009.08.042
18. Fiuza C, Bustin M, Talwar S, Tropea M, Gerstenberger E, Shelhamer JH, Suffredini AF (2003) Inflammation-promoting activity of HMGB1 on human microvascular endothelial cells. Blood 101:2652-2660. doi: 10.1182/blood-2002- 05-1300 (Pubitemid 36857626)
19. Giordano A, Romano A (2011) Inhibition of human in-stent restenosis: a molecular view. Curr Opin Pharmacol 11:372-377. doi: 10.1016/j.coph.2011.03.006
20. Hill BG, Haberzettl P, Ahmed Y, Srivastava S, Bhatnagar A (2008) Unsaturated lipid peroxidation-derived aldehydes activate autophagy in vascular smooth-muscle cells. Biochem J 410:525-534 (Pubitemid 351429023)
21. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jaattela M (2007) Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25:193-205. doi: 10.1016/j.molcel.2006.12.009 (Pubitemid 46109606)
22. Huang J, Lam GY, Brumell JH (2011) Autophagy signaling through reactive oxygen species. Antioxid Redox Signal 14:2215-2231. doi: 10.1089/ars.2010.3554
23. Jia L, Hui RT (2009) Everolimus, a promising medical therapy for coronary heart disease? Med Hypotheses 73:153-155. doi: 10.1016/j.mehy.2009.03.011
24. Jung CH, Ro SH, Cao J, Otto NM, Kim DH (2010) mTOR regulation of autophagy. FEBS Lett 584:1287-1295. doi: 10.1016/j.febslet.2010.01.017
25. Kalinina N, Agrotis A, Antropova Y, DiVitto G, Kanellakis P, Kostolias G, Ilyinskaya O, Tararak E, Bobik A (2004) Increased expression of the DNA-binding cytokine HMGB1 in human atherosclerotic lesions: role of activated macrophages and cytokines. Arterioscler Thromb Vasc Biol 24:2320-2325. doi: 10.1161/01.ATV.0000145573.36113.8a (Pubitemid 39658036)
26. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S, White E (2007) Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 21:1621-1635. doi: 10.1101/quad.1565707 (Pubitemid 47026367)
27. Keul P, Lucke S, von Wnuck LK, Bode C, Graler M, Heusch G, Levkau B (2011) Sphingosine-1-phosphate receptor 3 promotes recruitment of monocyte/macrophages in inflammation and atherosclerosis. Circ Res 108:314-323. doi: 10.1161/CIRCRESAHA.110.235028
28. Keul P, Tolle M, Lucke S, von Wnuck LK, Heusch G, Schuchardt M, van der Giet M, Levkau B (2007) The sphingosine-1-phosphate analogue FTY720 reduces atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 27:607-613. doi: 10.1161/01.ATV.0000254679.42583.88
29. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, Ahn HJ, Ait-Mohamed O, Ait-Si-Ali S, Akematsu T, Akira S, Al-Younes HM, Al-Zeer MA, Albert ML, Albin RL, Alegre-Abarrategui J, Aleo MF, Alirezaei M, Almasan A, Almonte-Becerril M, Amano A, Amaravadi R, Amarnath S, Amer AO, Andrieu-Abadie N, Anantharam V, Ann DK, Anoopkumar-Dukie S, Aoki H, Apostolova N, Arancia G, Aris JP, Asanuma K, Asare NY, Ashida H, Askanas V, Askew DS, Auberger P, Baba M, Backues SK, Baehrecke EH, Bahr BA, Bai XY, Bailly Y, Baiocchi R, Baldini G, Balduini W, Ballabio A, Bamber BA, Bampton ET, Banhegyi G, Bartholomew CR, Bassham DC, Bast RC, Jr., Batoko H, Bay BH, Beau I, Bechet DM, Begley TJ, Behl C, Behrends C, Bekri S, Bellaire B, Bendall LJ, Benetti L, Berliocchi L, Bernardi H, Bernassola F, Besteiro S, Bhatia-Kissova I, Bi X, Biard-Piechaczyk M, Blum JS, Boise LH, Bonaldo P, Boone DL, Bornhauser BC, Bortoluci KR, Bossis I, Bost F, Bourquin JP, Boya P, Boyer-Guittaut M, Bozhkov PV, Brady NR, Brancolini C, Brech A, Brenman JE, Brennand A, Bresnick EH, Brest P, Bridges D, Bristol ML, Brookes PS, Brown EJ, Brumell JH, Brunetti-Pierri N, Brunk UT, Bulman DE, Bultman SJ, Bultynck G, Burbulla LF, Bursch W, Butchar JP, Buzgariu W, Bydlowski SP, Cadwell K, Cahova M, Cai D, Cai J, Cai Q, Calabretta B, Calvo-Garrido J, Camougrand N, Campanella M, Campos-Salinas J, Candi E, Cao L, Caplan AB, Carding SR, Cardoso SM, Carew JS, Carlin CR, Carmignac V, Carneiro LA, Carra S, Caruso RA, Casari G, Casas C, Castino R, Cebollero E, Cecconi F, Celli J, Chaachouay H, Chae HJ, Chai CY, Chan DC, Chan EY, Chang RC, Che CM, Chen CC, Chen GC, Chen GQ, Chen M, Chen Q, Chen SS, Chen W, Chen X, Chen X, Chen X, Chen YG, Chen Y, Chen Y, Chen YJ, Chen Z, Cheng A, Cheng CH, Cheng Y, Cheong H, Cheong JH, Cherry S, Chess-Williams R, Cheung ZH, Chevet E, Chiang HL, Chiarelli R, Chiba T, Chin LS, Chiou SH, Chisari FV, Cho CH, Cho DH, Choi AM, Choi D, Choi KS, Choi ME, Chouaib S, Choubey D, Choubey V, Chu CT, Chuang TH, Chueh SH, Chun T, Chwae YJ, Chye ML, Ciarcia R, Ciriolo MR, Clague MJ, Clark RS, Clarke PG, Clarke R, Codogno P, Coller HA, Colombo MI, Comincini S, Condello M, Condorelli F, Cookson MR, Coombs GH, Coppens I, Corbalan R, Cossart P, Costelli P, Costes S, Coto-Montes A, Couve E, Coxon FP, Cregg JM, Crespo JL, Cronje MJ, Cuervo AM, Cullen JJ, Czaja MJ, D'Amelio M, Darfeuille-Michaud A, Davids LM, Davies FE, De FM, de Groot JF, de Haan CA, De ML, De MA, De T, V, Debnath J, Degterev A, Dehay B, Delbridge LM, Demarchi F, Deng YZ, Dengjel J, Dent P, Denton D, Deretic V, Desai SD, Devenish RJ, Di GM, Di PG, Di PC, Diaz-Araya G, Diaz-Laviada I, Diaz-Meco MT, Diaz-Nido J, Dikic I, Dinesh-Kumar SP, Ding WX, Distelhorst CW, Diwan A, Djavaheri-Mergny M, Dokudovskaya S, Dong Z, Dorsey FC et al. (2012) Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 8:445-544. doi: 10.4161/auto.19496
30. Larigauderie G, Furman C, Jaye M, Lasselin C, Copin C, Fruchart JC, Castro G, Rouis M (2004) Adipophilin enhances lipid accumulation and prevents lipid efflux from THP-1 macrophages: potential role in atherogenesis. Arterioscler Thromb Vasc Biol 24:504-510. doi: 10.1161/01.ATV.0000115638.27381. 97 (Pubitemid 38326145)
31. Lavigne MC, Grimsby JL, Eppihimer MJ (2012) Antirestenotic mechanisms of everolimus on human coronary artery smooth muscle cells: inhibition of human coronary artery smooth muscle cell proliferation, but not migration. J Cardiovasc Pharmacol 59:165-174. doi: 10.1097/FJC.0b013e31823a39c7
32. Law BY, Wang M, Ma DL, Al-Mousa F, Michelangeli F, Cheng SH, Ng MH, To KF, Mok AY, Ko RY, Lam SK, Chen F, Che CM, Chiu P, Ko BC (2010) Alisol B, a novel inhibitor of the sarcoplasmic/endoplasmic reticulum Ca(2+) ATPase pump, induces autophagy, endoplasmic reticulum stress, and apoptosis. Mol Cancer Ther 9:718-730. doi: 10.1158/1535-7163.MCT-09-0700
33. Levine B, Yuan J (2005) Autophagy in cell death: an innocent convict? J Clin Invest 115:2679-2688. doi: 10.1172/JCI26390 (Pubitemid 41434392)
34. Liao A, Hu R, Zhao Q, Li J, Li Y, Yao K, Zhang R, Wang H, Yang W, Liu Z (2012) Autophagy induced by FTY720 promotes apoptosis in U266 cells. Eur J Pharm Sci 45:600-605. doi: 10.1016/j.ejps.2011.12.014
35. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J, Tabas I (2012) Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab 15:545-553. doi: 10.1016/j.cmet.2012.01.022
36. Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ (1999) Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res 41:473-479 (Pubitemid 29087344)
37. Ma KL, Ruan XZ, Powis SH, Moorhead JF, Varghese Z (2007) Anti-atherosclerotic effects of sirolimus on human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 292:H2721-H2728. doi: 10.1152/ajpheart.01174. 2006 (Pubitemid 47084520)
38. Ma KL, Varghese Z, Ku Y, Powis SH, Chen Y, Moorhead JF, Ruan XZ (2010) Sirolimus inhibits endogenous cholesterol synthesis induced by inflammatory stress in human vascular smooth muscle cells. Am J Physiol Heart Circ Physiol 298:H1646-H1651. doi: 10.1152/ajpheart.00492.2009
39. Martin KA, Rzucidlo EM, Merenick BL, Fingar DC, Brown DJ, Wagner RJ, Powell RJ (2004) The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation. Am J Physiol Cell Physiol 286:C507-C517. doi: 10.1152/ajpcell.00201.2003
40. Martinet W, Agostinis P, Vanhoecke B, Dewaele M, De Meyer GRY (2009) Autophagy in disease: a double-edged sword with therapeutic potential. Clin Sci (Lond) 116:697-712. doi: 10.1042/CS20080508
41. Martinet W, De Meyer GR (2008) Autophagy in atherosclerosis. Curr Atheroscler Rep 10:216-223
42. Martinet W, De Meyer GRY (2009) Autophagy in atherosclerosis: a cell survival and death phenomenon with therapeutic potential. Circ Res 104:304-317. doi: 10.1161/CIRCRESAHA.108.188318
43. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM (2006) Detection of autophagy in tissue by standard immunohistochemistry: possibilities and limitations. Autophagy 2:55-57
44. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM (2006) In situ detection of starvation-induced autophagy. J Histochem Cytochem 54:85-96. doi: 10.1369/jhc.5A6743.2005 (Pubitemid 43049418)
45. Martinet W, De Meyer I, Cools N, Timmerman V, Bult H, Bosmans J, De Meyer GRY (2010) Cell death-mediated cleavage of the attraction signal p43 in human atherosclerosis: implications for plaque destabilization. Arterioscler Thromb Vasc Biol 30:1415-1422. doi: 10.1161/ATVBAHA.110.206029
46. Martinet W, De BM, Schrijvers DM, De Meyer GR, Herman AG, Kockx MM (2004) 7-ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 24:2296-2301. doi: 10.1161/01.ATV.0000146266.65820.a1 (Pubitemid 39658032)
47. Martinet W, Knaapen MW, De Meyer GRY, Herman AG, Kockx MM (2002) Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation 106:927-932. doi: 10.1161/01.CIR.0000026393.47805.21 (Pubitemid 34925325)
48. Martinet W, Schrijvers DM, De Meyer GRY (2012) Molecular and cellular mechanisms of macrophage survival in atherosclerosis. Basic Res Cardiol 107:297. doi: 10.1007/s00395-012-0297-x
49. Martinet W, Verheye S, De Meyer GRY (2007) Everolimus-induced mTOR inhibition selectively depletes macrophages in atherosclerotic plaques by autophagy. Autophagy 3:241-244 (Pubitemid 46752686)
50. Martinet W, Verheye S, De Meyer GRY (2007) Selective depletion of macrophages in atherosclerotic plaques via macrophage-specific initiation of cell death. Trends Cardiovasc Med 17:69-75. doi: 10.1016/j.tcm.2006.12.004 (Pubitemid 46205331)
51. Martinet W, Verheye S, De Meyer I, Timmermans JP, Schrijvers DM, Van Brussel I, Bult H, De Meyer GRY (2012) Everolimus triggers cytokine release by macrophages: rationale for stents eluting everolimus and a glucocorticoid. Arterioscler Thromb Vasc Biol 32:1228-1235. doi: 10.1161/ATVBAHA.112.245381
52. Mathis AS, Jin S, Friedman GS, Peng F, Carl SM, Knipp GT (2007) The pharmacodynamic effects of sirolimus and sirolimus-calcineurin inhibitor combinations on macrophage scavenger and nuclear hormone receptors. J Pharm Sci 96:209-222. doi: 10.1002/jps.20751 (Pubitemid 46087351)
53. Matsuzawa T, Kim BH, Shenoy AR, Kamitani S, Miyake M, Macmicking JD (2012) IFN-gamma elicits macrophage autophagy via the p38 MAPK signaling pathway. J Immunol 189:813-818. doi: 10.4049/jimmunol.1102041
54. Mizushima N, Komatsu M (2011) Autophagy: renovation of cells and tissues. Cell 147:728-741. doi: 10.1016/j.cell.2011.10.026
55. Mizushima N, Levine B, Cuervo AM, Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451:1069-1075. doi: 10.1038/nature06639 (Pubitemid 351317450)
56. Mueller MA, Beutner F, Teupser D, Ceglarek U, Thiery J (2008) Prevention of atherosclerosis by the mTOR inhibitor everolimus in LDLR-/- mice despite severe hypercholesterolemia. Atherosclerosis 198:39-48. doi: 10.1016/j.atherosclerosis.2007.09.019 (Pubitemid 351406366)
57. Muller C, Salvayre R, Negre-Salvayre A, Vindis C (2011) HDLs inhibit endoplasmic reticulum stress and autophagic response induced by oxidized LDLs. Cell Death Differ 18:817-828. doi: 10.1038/cdd.2010.149
58. Onuma Y, Serruys PW, Perkins LE, Okamura T, Gonzalo N, Garcia-Garcia HM, Regar E, Kamberi M, Powers JC, Rapoza R, van BH, van der Giessen W, Virmani R (2010) Intracoronary optical coherence tomography and histology at 1 month and 2, 3, and 4 years after implantation of everolimus-eluting bioresorbable vascular scaffolds in a porcine coronary artery model: an attempt to decipher the human optical coherence tomography images in the ABSORB trial. Circulation 122:2288-2300. doi: 10.1161/CIRCULATIONAHA.109.921528
59. Ouimet M, Franklin V, Mak E, Liao X, Tabas I, Marcel YL (2011) Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab 13:655-667. doi: 10.1016/j.cmet.2011.03.023
60. Petrovski G, Ayna G, Majai G, Hodrea J, Benko S, Madi A, Fesus L (2011) Phagocytosis of cells dying through autophagy induces inflammasome activation and IL-1beta release in human macrophages. Autophagy 7:321-330. doi: 10.4161/auto.7.3.14583
61. Petrovski G, Zahuczky G, Majai G, Fesus L (2007) Phagocytosis of cells dying through autophagy evokes a pro-inflammatory response in macrophages. Autophagy 3:509-511 (Pubitemid 47293742)
62. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting JP, Virgin HW, Kastan MB, Semenkovich CF (2012) Autophagy links inflammasomes to atherosclerotic progression. Cell Metab 15:534-544. doi: 10.1016/j.cmet.2012.02. 011
63. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein. J Biol Chem 282:5641-5652. doi: 10.1074/jbc.M609532200 (Pubitemid 47093730)
64. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC (2005) Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170:1101-1111. doi: 10.1083/jcb.200504035 (Pubitemid 41362642)
65. Sarkar S, Perlstein EO, Imarisio S, Pineau S, Cordenier A, Maglathlin RL, Webster JA, Lewis TA, O'Kane CJ, Schreiber SL, Rubinsztein DC (2007) Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat Chem Biol 3:331-338. doi: 10.1038/nchembio883 (Pubitemid 46789270)
66. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC (2009) Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine- expanded huntingtin and related proteinopathies. Cell Death Differ 16:46-56. doi: 10.1038/cdd.2008.110
67. Scaffidi P, Misteli T, Bianchi ME (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418:191-195. doi: 10.1038/nature00858 (Pubitemid 34773774)
68. Schrijvers DM, De Meyer GRY, Kockx MM, Herman AG, Martinet W (2005) Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol 25:1256-1261. doi: 10.1161/01.ATV.0000166517. 18801.a7 (Pubitemid 40776618)
69. Schrijvers DM, De Meyer GRY, Martinet W (2011) Autophagy in atherosclerosis: a potential drug target for plaque stabilization. Arterioscler Thromb Vasc Biol 31:2787-2791. doi: 10.1161/ATVBAHA.111.224899
70. Serruys PW, Ormiston JA, Onuma Y, Regar E, Gonzalo N, Garcia-Garcia HM, Nieman K, Bruining N, Dorange C, Miquel-Hebert K, Veldhof S, Webster M, Thuesen L, Dudek D (2009) A bioabsorbable everolimus-eluting coronary stent system (ABSORB): 2-year outcomes and results from multiple imaging methods. Lancet 373:897-910. doi: 10.1016/S0140-6736(09)60325-1
71. Shalak V, Guigou L, Kaminska M, Wautier MP, Wautier JL, Mirande M (2007) Characterization of p43(ARF), a derivative of the p43 component of multiaminoacyl-tRNA synthetase complex released during apoptosis. J Biol Chem 282:10935-10943. doi: 10.1074/jbc.M611737200 (Pubitemid 47100748)
72. Shen S, Kepp O, Kroemer G (2012) The end of autophagic cell death? Autophagy 8:1-3. doi: 10.4161/auto.8.1.16618
73. Shi CS, Kehrl JH (2008) MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages. J Biol Chem 283:33175-33182. doi: 10.1074/jbc. M804478200
74. Sridhar S, Botbol Y, Macian F, Cuervo AM (2012) Autophagy and disease: always two sides to a problem. J Pathol 226:255-273. doi: 10.1002/path.3025
75. Verheye S, Martinet W, Kockx MM, Knaapen MW, Salu K, Timmermans JP, Ellis JT, Kilpatrick DL, De Meyer GRY (2007) Selective clearance of macrophages in atherosclerotic plaques by autophagy. J Am Coll Cardiol 49:706-715. doi: 10.1016/j.jacc.2006.09.047 (Pubitemid 46205042)
76. Vingtdeux V, Giliberto L, Zhao H, Chandakkar P, Wu Q, Simon JE, Janle EM, Lobo J, Ferruzzi MG, Davies P, Marambaud P (2010) AMP-activated protein kinase signaling activation by resveratrol modulates amyloid-beta peptide metabolism. J Biol Chem 285:9100-9113. doi: 10.1074/jbc.M109.060061
77. Wang SH, Shih YL, Ko WC, Wei YH, Shih CM (2008) Cadmium-induced autophagy and apoptosis are mediated by a calcium signaling pathway. Cell Mol Life Sci 65:3640-3652. doi: 10.1007/s00018-008-8383-9
78. Wang X, Proud CG (2011) mTORC1 signaling: what we still don't know. J Mol Cell Biol 3:206-220. doi: 10.1093/jmcb/mjq038
79. Yang H, Wang H, Czura CJ, Tracey KJ (2005) The cytokine activity of HMGB1. J Leukoc Biol 78:1-8. doi: 10.1189/jlb.1104648 (Pubitemid 40979937)
80. Yang Z, Klionsky DJ (2010) Eaten alive: a history of macroautophagy. Nat Cell Biol 12:814-822. doi: 10.1038/ncb0910-814
81. Yorimitsu T, Nair U, Yang Z, Klionsky DJ (2006) Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281:30299-30304. doi: 10.1074/jbc.M607007200 (Pubitemid 44537037)
82. Zhang N, Qi Y, Wadham C, Wang L, Warren A, Di W, Xia P (2010) FTY720 induces necrotic cell death and autophagy in ovarian cancer cells: a protective role of autophagy. Autophagy 6:1157-1167. doi: 10.4161/auto.6.8.13614
83. Zhang YL, Cao YJ, Zhang X, Liu HH, Tong T, Xiao GD, Yang YP, Liu CF (2010) The autophagy-lysosome pathway: a novel mechanism involved in the processing of oxidized LDL in human vascular endothelial cells. Biochem Biophys Res Commun 394:377-382. doi: 10.1016/j.bbrc.2010.03.026