Autophagy in atherosclerosis: A cell survival and death phenomenon with therapeutic potential

Circulation Research

Volumn 104, Issue 3, 2009, Pages 304-317

  Martinet, Wim ^a   De Meyer, Guido R Y ^a  

^a UNIVERSITY OF ANTWERP   (Belgium)

Author keywords

Atherosclerosis; Autophagosome; Autophagy; Cell death; Lysosome

Indexed keywords

4 HYDROXYNONENAL; MALONALDEHYDE; MAMMALIAN TARGET OF RAPAMYCIN; REACTIVE OXYGEN METABOLITE; STEROL;

APOPTOSIS; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPHAGY; CELL DEATH; CELL HYPOXIA; CELL STRESS; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; HUMAN; INFLAMMATION; LIPID PEROXIDATION; MACROPHAGE; NONHUMAN; OXIDATIVE STRESS; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW; ANIMAL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; ATHEROSCLEROSIS; AUTOPHAGY; CELL DEATH; CELL SURVIVAL; HUMANS;

EID: 61949233502     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.108.188318     Document Type: Review

References (130)

1. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999; 340:115-126.
2. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
3. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
4. Linton MF, Fazio S. A practical approach to risk assessment to prevent coronary artery disease and its complications. Am J Cardiol. 2003;92: 19i-26i.
5. Kannel WB, D'Agostino RB, Sullivan L, Wilson PW. Concept and usefulness of cardiovascular risk profiles. Am Heart J. 2004;148:16-26.
6. Franklin BA, Kahn JK. Delayed progression or regression of coronary atherosclerosis with intensive risk factor modification. Effects of diet, drugs, and exercise. Sports Med. 1996;22:306-320.
7. Getz GS, Reardon CA. Diet and murine atherosclerosis. Arterioscler Thromb Vasc Biol. 2006;26:242-249.
8. Grines CL. The role of statins in reversing atherosclerosis: What the latest regression studies show. J Interv Cardiol. 2006;19:3-9.
9. Kockx MM, Herman AG. Apoptosis in atherosclerosis: Beneficial or detrimental? Cardiovasc Res. 2000;45:736-746.
10. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: The importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25: 2255-2264.
11. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12: 1075-1080.
12. Schrijvers DM, De Meyer GRY, Herman AG, Martinet W. Phagocytosis in atherosclerosis: Molecular mechanisms and implications for plaque progression and stability. Cardiovasc Res. 2007;73:470-480.
13. Clarke PG. Developmental cell death: Morphological diversity and multiple mechanisms. Anat Embryol (Berl). 1990;181:195-213.
14. Mallat Z, Tedgui A. Apoptosis in the vasculature: Mechanisms and functional importance. Br J Pharmacol. 2000;130:947-962.
15. Martinet W, Kockx MM. Apoptosis in atherosclerosis: Focus on oxidized lipids and inflammation. Curr Opin Lipidol. 2001;12:535-541.
16. Crisby M, Kallin B, Thyberg J, Zhivotovsky B, Orrenius S, Kostulas V, Nilsson J. Cell death in human atherosclerotic plaques involves both oncosis and apoptosis. Atherosclerosis. 1997;130:17-27.
17. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and selfkilling: Crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol. 2007;8:741-752.
18. Yoshimori T. Autophagy: A regulated bulk degradation process inside cells. Biochem Biophys Res Commun. 2004;313:453-458.
19. Levine B, Klionsky DJ. Development by self-digestion: Molecular mechanisms and biological functions of autophagy. Dev Cell. 2004;6: 463-477.
20. Yorimitsu T, Klionsky DJ. Autophagy: Molecular machinery for selfeating. Cell Death Differ. 2005;12:1542-1552.
21. Klionsky DJ. Autophagy: From phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007;8:931-937.
22. 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.
23. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441:880-884.
24. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki- Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature. 2006;441:885-889.
25. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15:1101-1111.
26. Azad MB, Chen Y, Henson ES, Cizeau J, Millan-Ward E, Israels SJ, Gibson SB. Hypoxia induces autophagic cell death in apoptosiscompetent cells through a mechanism involving BNIP3. Autophagy. 2008;4:195-204.
27. Kondomerkos DJ, Kalamidas SA, Kotoulas OB. An electron microscopic and biochemical study of the effects of glucagon on glycogen autophagy in the liver and heart of newborn rats. Microsc Res Tech. 2004;63:87-93.
28. Kanzawa T, Zhang L, Xiao L, Germano IM, Kondo Y, Kondo S. Arsenic trioxide induces autophagic cell death in malignant glioma cells by upregulation of mitochondrial cell death protein BNIP3. Oncogene. 2005;24:980-991.
29. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 2006;281:30299-30304.
30. Levine B, Yuan J. Autophagy in cell death: An innocent convict? J Clin Invest. 2005;115:2679-2688.
31. Debnath J, Baehrecke EH, Kroemer G. Does autophagy contribute to cell death? Autophagy. 2005;1:66-74.
32. Klionsky DJ. The molecular machinery of autophagy: Unanswered questions. J Cell Sci. 2005;118:7-18.
33. Abeliovich H. Regulation of autophagy by the target of rapamycin (Tor) proteins. In: Klionsky DJ, ed. Autophagy. Austin, Tex: Landes Bioscience; 2003:60-69.
34. Ichimura Y, Imamura Y, Emoto K, Umeda M, Noda T, Ohsumi Y. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. J Biol Chem. 2004;279:40584-40592.
35. Jager S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen EL. Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci. 2004;117:4837-4848.
36. Kimura S, Noda T, Yoshimori T. Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescenttagged LC3. Autophagy. 2007;3:452-460.
37. Klionsky DJ, Cuervo AM, Seglen PO. Methods for monitoring autophagy from yeast to human. Autophagy. 2007;3:181-206.
38. Klionsky DJ, Abeliovich H, Agostinis P, Agrawal DK, Aliev G, Askew DS, Baba M, Baehrecke EH, Bahr BA, Ballabio A, Bamber BA, Bassham DC, Bergamini E, Bi X, Biard-Piechaczyk M, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4:151-175.
39. Eskelinen EL. To be or not to be? Examples of incorrect identification of autophagic compartments in conventional transmission electron microscopy of mammalian cells. Autophagy. 2008;4:257-260.
40. Kockx MM, De Meyer GRY, Buyssens N, Knaapen MW, Bult H, Herman AG. Cell composition, replication, and apoptosis in atherosclerotic plaques after 6 months of cholesterol withdrawal. Circ Res. 1998;83:378-387.
41. Martinet W, De BM, Schrijvers DM, De Meyer GRY, Herman AG, Kockx MM. 7-ketocholesterol induces protein ubiquitination, myelin figure formation, and light chain 3 processing in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2004;24:2296-2301.
42. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM. In situ detection of starvation-induced autophagy. J Histochem Cytochem. 2006;54:85-96.
43. Martinet W, De Meyer GRY, Andries L, Herman AG, Kockx MM. Detection of autophagy in tissue by standard immunohistochemistry: Possibilities and limitations. Autophagy. 2006;2:55-57.
44. Laifer LI, O'Brien KM, Stetz ML, Gindi GR, Garrand TJ, Deckelbaum LI. Biochemical basis for the difference between normal and atherosclerotic arterial fluorescence. Circulation. 1989;80:1893-1901.
45. Knaapen MW, Davies MJ, De BM, Haven AJ, Martinet W, Kockx MM. Apoptotic versus autophagic cell death in heart failure. Cardiovasc Res. 2001;51:304-312.
46. Kostin S, Pool L, Elsasser A, Hein S, Drexler HC, Arnon E, Hayakawa Y, Zimmermann R, Bauer E, Klovekorn WP, Schaper J. Myocytes die by multiple mechanisms in failing human hearts. Circ Res. 2003;92: 715-724.
47. Hein S, Arnon E, Kostin S, Schonburg M, Elsasser A, Polyakova V, Bauer EP, Klovekorn WP, Schaper J. Progression from compensated hypertrophy to failure in the pressure-overloaded human heart: Structural deterioration and compensatory mechanisms. Circulation. 2003;107: 984-991.
48. Elsasser A, Vogt AM, Nef H, Kostin S, Mollmann H, Skwara W, Bode C, Hamm C, Schaper J. Human hibernating myocardium is jeopardized by apoptotic and autophagic cell death. J Am Coll Cardiol. 2004;43: 2191-2199.
49. Shimomura H, Terasaki F, Hayashi T, Kitaura Y, Isomura T, Suma H. Autophagic degeneration as a possible mechanism of myocardial cell death in dilated cardiomyopathy. Jpn Circ J. 2001;65:965-968.
50. Diskin T, Tal-Or P, Erlich S, Mizrachy L, Alexandrovich A, Shohami E, Pinkas-Kramarski R. Closed head injury induces upregulation of Beclin 1 at the cortical site of injury. J Neurotrauma. 2005;22:750-762.
51. Kihara A, Kabeya Y, Ohsumi Y, Yoshimori T. Beclinphosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep. 2001;2:330-335.
52. Kiffin R, Bandyopadhyay U, Cuervo AM. Oxidative stress and autophagy. Antioxid Redox Signal. 2006;8:152-162.
53. Martinet W, Schrijvers DM, Timmermans JP, Bult H. Interactions between cell death induced by statins and 7-ketocholesterol in rabbit aorta smooth muscle cells. Br J Pharmacol. 2008;154:1236-1246.
54. Gozuacik D, Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 2004;23:2891-2906.
55. Pan M, Maitin V, Parathath S, Andreo U, Lin SX, St GC, Yao Z, Maxfield FR, Williams KJ, Fisher EA. Presecretory oxidation, aggregation, and autophagic destruction of apoprotein-B: A pathway for late-stage quality control. Proc Natl Acad Sci U S A. 2008;105: 5862-5867.
56. Fisher EA, Pan M, Chen X, Wu X, Wang H, Jamil H, Sparks JD, Williams KJ. The triple threat to nascent apolipoprotein B. Evidence for multiple, distinct degradative pathways. J Biol Chem. 2001;276: 27855-27863.
57. Sparks JD, Phung TL, Bolognino M, Sparks CE. Insulin-mediated inhibition of apolipoprotein B secretion requires an intracellular trafficking event and phosphatidylinositol 3-kinase activation: Studies with brefeldin A and wortmannin in primary cultures of rat hepatocytes. Biochem J. 1996;313:567-574.
58. Pan M, Cederbaum AI, Zhang YL, Ginsberg HN, Williams KJ, Fisher EA. Lipid peroxidation and oxidant stress regulate hepatic apolipoprotein B degradation and VLDL production. J Clin Invest. 2004;113: 1277-1287.
59. von Schacky C. The role of omega-3 fatty acids in cardiovascular disease. Curr Atheroscler Rep. 2003;5:139-145.
60. Mitchinson MJ. Insoluble lipids in human atherosclerotic plaques. Atherosclerosis. 1982;45:11-15.
61. Kurz T, Terman A, Brunk UT. Autophagy, ageing and apoptosis: The role of oxidative stress and lysosomal iron. Arch Biochem Biophys. 2007;462:220-230.
62. Brunk UT, Jones CB, Sohal RS. A novel hypothesis of lipofuscinogenesis and cellular aging based on interactions between oxidative stress and autophagocytosis. Mutat Res. 1992;275:395-403.
63. Lee FY, Lee TS, Pan CC, Huang AL, Chau LY. Colocalization of iron and ceroid in human atherosclerotic lesions. Atherosclerosis. 1998;138: 281-288.
64. Yuan XM, Li W, Brunk UT, Dalen H, Chang YH, Sevanian A. Lysosomal destabilization during macrophage damage induced by cholesterol oxidation products. Free Radic Biol Med. 2000;28:208-218.
65. Persson HL, Kurz T, Eaton JW, Brunk UT. Radiation-induced cell death: Importance of lysosomal destabilization. Biochem J. 2005;389: 877-884.
66. Porter NA. Chemistry of lipid peroxidation. Methods Enzymol. 1984; 105:273-282.
67. Hill BG, Haberzettl P, Ahmed Y, Srivastava S, Bhatnagar A. Unsaturated lipid peroxidation-derived aldehydes activate autophagy in vascular smooth-muscle cells. Biochem J. 2008;410:525-534.
68. Bardag-Gorce F, Li J, French BA, French SW. The effect of ethanolinduced CYP2E1 on proteasome activity: The role of 4-hydroxynonenal. Exp Mol Pathol. 2005;78:109-115.
69. Nowicki M, Zabirnyk O, Duerrschmidt N, Borlak J, Spanel-Borowski K. No upregulation of lectin-like oxidized low-density lipoprotein receptor-1 in serum-deprived EA.hy926 endothelial cells under oxLDL exposure, but increase in autophagy. Eur J Cell Biol. 2007;86:605-616.
70. Martinet W, Schrijvers DM, De Meyer GRY, Thielemans J, Knaapen MW, Herman AG, Kockx MM. Gene expression profiling of apoptosis- related genes in human atherosclerosis: Upregulation of deathassociated protein kinase. Arterioscler Thromb Vasc Biol. 2002;22: 2023-2029.
71. Inbal B, Bialik S, Sabanay I, Shani G, Kimchi A. DAP kinase and DRP-1 mediate membrane blebbing and the formation of autophagic vesicles during programmed cell death. J Cell Biol. 2002;157:455-468.
72. Jin Y, Gallagher PJ. Antisense depletion of death-associated protein kinase promotes apoptosis. J Biol Chem. 2003;278:51587-51593.
73. Zhou J, Lhotak S, Hilditch BA, Austin RC. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation. 2005;111: 1814-1821.
74. Tabas I. Apoptosis and plaque destabilization in atherosclerosis: The role of macrophage apoptosis induced by cholesterol. Cell Death Differ. 2004;11:S12-S16.
75. Li J, Ni M, Lee B, Barron E, Hinton DR, Lee AS. The unfolded protein response regulator GRP78/BiP is required for endoplasmic reticulum integrity and stress-induced autophagy in mammalian cells. Cell Death Differ. 2008;15:1460-1471.
76. Frostegard J, Ulfgren AK, Nyberg P, Hedin U, Swedenborg J, Andersson U, Hansson GK. Cytokine expression in advanced human atherosclerotic plaques: Dominance of pro-inflammatory (Th1) and macrophage- stimulating cytokines. Atherosclerosis. 1999;145:33-43.
77. Deretic V. Autophagy as an immune defense mechanism. Curr Opin Immunol. 2006;18:375-382.
78. Heymann D. Autophagy: A protective mechanism in response to stress and inflammation. Curr Opin Investig Drugs. 2006;7:443-450.
79. Jia G, Cheng G, Gangahar DM, Agrawal DK. Insulin-like growth factor-1 and TNF-alpha regulate autophagy through c-jun N-terminal kinase and Akt pathways in human atherosclerotic vascular smooth cells. Immunol Cell Biol. 2006;84:448-454.
80. Gutierrez MG, Master SS, Singh SB, Taylor GA, Colombo MI, Deretic V. Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell. 2004;119: 753-766.
81. Cromheeke KM, Kockx MM, De Meyer GRY, Bosmans JM, Bult H, Beelaerts WJ, Vrints CJ, Herman AG. Inducible nitric oxide synthase colocalizes with signs of lipid oxidation/peroxidation in human atherosclerotic plaques. Cardiovasc Res. 1999;43:744-754.
82. Sluimer JC, Gasc JM, van Wanroij JL, Kisters N, Groeneweg M, Sollewijn G, Cleutjens JP, van den Akker LH, Corvol P, Wouters BG, Daemen MJ, Bijnens AP. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol. 2008;51:1258-1265.
83. Brunelle JK, Chandel NS. Oxygen deprivation induced cell death: An update. Apoptosis. 2002;7:475-482.
84. Jin S, White E. Role of autophagy in cancer: Management of metabolic stress. Autophagy. 2007;3:28-31. (Pubitemid 46100707)
85. Karantza-Wadsworth V, Patel S, Kravchuk O, Chen G, Mathew R, Jin S, White E. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev. 2007;21:1621-1635.
86. Kockx MM, De Meyer GRY, Muhring J, Jacob W, Bult H, Herman AG. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation. 1998;97:2307-2315.
87. Martinet W, Verheye S, De Meyer GRY. Selective depletion of macrophages in atherosclerotic plaques via macrophage-specific initiation of cell death. Trends Cardiovasc Med. 2007;17:69-75.
88. Yang YP, Liang ZQ, Gu ZL, Qin ZH. Molecular mechanism and regulation of autophagy. Acta Pharmacol Sin. 2005;26:1421-1434.
89. Easton JB, Houghton PJ. Therapeutic potential of target of rapamycin inhibitors. Expert Opin Ther Targets. 2004;8:551-564.
90. Easton JB, Houghton PJ. mTOR and cancer therapy. Oncogene. 2006; 25:6436-6446.
91. Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y. Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol. 2000;150:1507-1513.
92. 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)
93. 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.
94. Bjornheden T, Bondjers G. Oxygen consumption in aortic tissue from rabbits with diet-induced atherosclerosis. Arteriosclerosis. 1987;7: 238-247.
95. Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ. Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res. 1999;41:473-479.
96. Martinet W, Knaapen MW, De Meyer GRY, Herman AG, Kockx MM. Elevated levels of oxidative DNA damage and DNA repair enzymes in human atherosclerotic plaques. Circulation. 2002;106:927-932.
97. Martin KA, Rzucidlo EM, Merenick BL, Fingar DC, Brown DJ, Wagner RJ, Powell RJ. The mTOR/p70 S6K1 pathway regulates vascular smooth muscle cell differentiation. Am J Physiol Cell Physiol. 2004; 286:C507-C517.
98. Delgado MA, Elmaoued RA, Davis AS, Kyei G, Deretic V. Toll-like receptors control autophagy. EMBO J. 2008;27:1110-1121.
99. Heil F, hmad-Nejad P, Hemmi H, Hochrein H, Ampenberger F, Gellert T, Dietrich H, Lipford G, Takeda K, Akira S, Wagner H, Bauer S. The Toll-like receptor 7 (TLR7)-specific stimulus loxoribine uncovers a strong relationship within the TLR7, 8 and 9 subfamily. Eur J Immunol. 2003;33:2987-2997.
100. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sci U S A. 2004;101:5598-5603.
101. Koziczak-Holbro M, Joyce C, Gluck A, Kinzel B, Muller M, Tschopp C, Mathison JC, Davis CN, Gram H. IRAK-4 kinase activity is required for interleukin-1 (IL-1) receptor- and toll-like receptor 7-mediated signaling and gene expression. J Biol Chem. 2007;282:13552-13560.
102. Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927-939.
103. Corcelle E, Nebout M, Bekri S, Gauthier N, Hofman P, Poujeol P, Fenichel P, Mograbi B. Disruption of autophagy at the maturation step by the carcinogen lindane is associated with the sustained mitogen-activated protein kinase/extracellular signal-regulated kinase activity. Cancer Res. 2006;66:6861-6870.
104. Corcelle E, Djerbi N, Mari M, Nebout M, Fiorini C, Fenichel P, Hofman P, Poujeol P, Mograbi B. Control of the autophagy maturation step by the MAPK ERK and p38: Lessons from environmental carcinogens. Autophagy. 2007;3:57-59.
105. Djavaheri-Mergny M, Amelotti M, Mathieu J, Besancon F, Bauvy C, Souquere S, Pierron G, Codogno P. NF-kappaB activation represses tumor necrosis factor-alpha-induced autophagy. J Biol Chem. 2006;281: 30373-30382.
106. Criollo A, Maiuri MC, Tasdemir E, Vitale I, Fiebig AA, Andrews D, Molgo J, Diaz J, Lavandero S, Harper F, Pierron G, di SD, Rizzuto R, Szabadkai G, Kroemer G. Regulation of autophagy by the inositol trisphosphate receptor. Cell Death Differ. 2007;14:1029-1039. (Pubitemid 46629841)
107. Criollo A, Vicencio JM, Tasdemir E, Maiuri MC, Lavandero S, Kroemer G. The inositol trisphosphate receptor in the control of autophagy. Autophagy. 2007;3:350-353. (Pubitemid 46986340)
108. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, Rubinsztein DC. Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol. 2005;170:1101-1111.
109. Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, O'Kane CJ, Floto RA, Rubinsztein DC. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat Chem Biol. 2008;4:295-305.
110. Aikawa M, Rabkin E, Okada Y, Voglic SJ, Clinton SK, Brinckerhoff CE, Sukhova GK, Libby P. Lipid lowering by diet reduces matrix metalloproteinase activity and increases collagen content of rabbit atheroma: A potential mechanism of lesion stabilization. Circulation. 1998; 97:2433-2444.
111. Verhamme P, Quarck R, Hao H, Knaapen M, Dymarkowski S, Bernar H, Van CJ, Janssens S, Vermylen J, Gabbiani G, Kockx M, Holvoet P. Dietary cholesterol withdrawal reduces vascular inflammation and induces coronary plaque stabilization in miniature pigs. Cardiovasc Res. 2002;56:135-144.
112. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, Randolph GJ. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci U S A. 2004;101:11779-11784.
113. Cheng J, Ohsaki Y, Tauchi-Sato K, Fujita A, Fujimoto T. Cholesterol depletion induces autophagy. Biochem Biophys Res Commun. 2006;351: 246-252.
114. Elhyany S, ssa-Kunik E, Tsory S, Muller T, Fedida S, Segal S, Fishman D. The integrity of cholesterol-enriched microdomains is essential for the constitutive high activity of protein kinase B in tumour cells. Biochem Soc Trans. 2004;32:837-839.
115. Li YC, Park MJ, Ye SK, Kim CW, Kim YN. Elevated levels of cholesterol-rich lipid rafts in cancer cells are correlated with apoptosis sensitivity induced by cholesterol-depleting agents. Am J Pathol. 2006; 168:1107-1118.
116. Miettinen TA, Railo M, Lepantalo M, Gylling H. Plant sterols in serum and in atherosclerotic plaques of patients undergoing carotid endarterectomy. J Am Coll Cardiol. 2005;45:1794-1801.
117. Berge KE, Tian H, Graf GA, Yu L, Grishin NV, Schultz J, Kwiterovich P, Shan B, Barnes R, Hobbs HH. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science. 2000;290:1771-1775.
118. Katayama T, Satoh T, Yagi T, Hirose N, Kurita Y, Anzai T, Asakura Y, Yoshikawa T, Mitamura H, Ogawa S. A 19-year-old man with myocardial infarction and sitosterolemia. Intern Med. 2003;42:591-594.
119. Sudhop T, von BK. Sitosterolemia-a rare disease. Are elevated plant sterols an additional risk factor? Z Kardiol. 2004;93:921-928.
120. Tabas I, Feinmark SJ, Beatini N. The reactivity of desmosterol and other shellfish- and xanthomatosis-associated sterols in the macrophage sterol esterification reaction. J Clin Invest. 1989;84:1713-1721.
121. Liu J, Chang CC, Westover EJ, Covey DF, Chang TY. Investigating the allosterism of acyl-CoA:Cholesterol acyltransferase (ACAT) by using various sterols: In vitro and intact cell studies. Biochem J. 2005;391: 389-397.
122. Bao L, Li Y, Deng SX, Landry D, Tabas I. Sitosterol-containing lipoproteins trigger free sterol-induced caspase-independent death in ACAT-competent macrophages. J Biol Chem. 2006;281:33635-33649.
123. Martinet W, De Meyer GRY, Timmermans JP, Herman AG, Kockx MM. Macrophages but not smooth muscle cells undergo benzyloxycarbonyl-Val- Ala-DL-Asp(O-Methyl) -fluoromethylketone-induced nonapoptotic cell death depending on receptor-interacting protein 1 expression: Implications for the stabilization of macrophage-rich atherosclerotic plaques. J Pharmacol Exp Ther. 2006;317:1356-1364.
124. Wu YT, Tan HL, Huang Q, Kim YS, Pan N, Ong WY, Liu ZG, Ong CN, Shen HM. Autophagy plays a protective role during zVAD-induced necrotic cell death. Autophagy. 2008;4:457-466.
125. Kundu M, Thompson CB. Autophagy: Basic principles and relevance to disease. Annu Rev Pathol. 2008;3:427-455.
126. Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature. 2008;451:1069-1075.
127. Martinet W, Knaapen MW, Kockx MM, De Meyer GR. Autophagy in cardiovascular disease. Trends Mol Med. 2007;13:482-491.
128. Martinet W, Schrijvers DM, Herman AG, De Meyer GR. z-VAD-fmkinduced non-apoptotic cell death of macrophages: Possibilities and limitations for atherosclerotic plaque stabilization. Autophagy. 2006;2: 312-314.
129. Chau YP, Lin SY, Chen JH, Tai MH. Endostatin induces autophagic cell death in EAhy926 human endothelial cells. Histol Histopathol. 2003; 18:715-726.
130. Yamawaki H, Iwai N. Cytotoxicity of water-soluble fullerene in vascular endothelial cells. Am J Physiol Cell Physiol. 2006;290: C1495-C1502.