Posttranslational modification and quality control

Circulation Research

Volumn 112, Issue 2, 2013, Pages 367-381

  Wang, Xuejun ^a   Pattison, J Scott ^a   Su, Huabo ^a  

^a UNIVERSITY OF SOUTH DAKOTA   (United States)

Author keywords

autophagy; chaperone mediated autophagy; chaperones; deubiquitination; neddylation; phosphorylation; ubiquitin proteasome system

Indexed keywords

ADENOSINE TRIPHOSPHATE; ATAXIN 3; BECLIN 1; CASEIN KINASE II; CHAPERONE; CHECKPOINT KINASE 1; COP9 SIGNALOSOME; CULLIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DESMIN; GAMMA INTERFERON; HEAT SHOCK PROTEIN 22; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HYDROLASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIGASE; MITOGEN ACTIVATED PROTEIN KINASE; NEDD8 PROTEIN; PARKIN; PROTEASOME; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN P27; SIRTUIN 1; THREONINE; UBIQUITIN; UNINDEXED DRUG;

AUTOPHAGOSOME; AUTOPHAGY; CARDIOMYOPATHY; CELL ORGANELLE; CYTOPLASM; CYTOSOL; CYTOTOXICITY; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME BINDING; GENE MUTATION; HEART DISEASE; HEART INFARCTION; HEART MUSCLE CELL; HUMAN; HYDROPHOBICITY; ISCHEMIA; ISCHEMIC PRECONDITIONING; LYSOSOME; MACROAUTOPHAGY; MICROTUBULE; MITOCHONDRION; MOLECULAR INTERACTION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN QUALITY; PROTEIN STABILITY; PROTEIN STRUCTURE; QUALITY CONTROL; REGULATORY MECHANISM; REVIEW; UBIQUITINATION;

ANIMALS; CARDIOVASCULAR DISEASES; HUMANS; MOLECULAR CHAPERONES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; QUALITY CONTROL; UBIQUITIN;

EID: 84872865382     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.268706     Document Type: Review

References (145)

1. Wang X, Li J, Zheng H, Su H, Powell SR. Proteasome functional insufficiency in cardiac pathogenesis. Am J Physiol Heart Circ Physiol. 2011;301:H2207-H2219.
2. Li J, Horak KM, Su H, Sanbe A, Robbins J, Wang X. Enhancement of proteasomal function protects against cardiac proteinopathy and ischemia/reperfusion injury in mice. J Clin Invest. 2011;121:3689-3700.
3. Scruggs SB, Zong NC, Wang D, Stefani E, Ping P. Post-translational modification of cardiac proteasomes: functional delineation enabled by proteomics. Am J Physiol Heart Circ Physiol. 2012;303:H9-18.
4. Pattison JS, Sanbe A, Maloyan A, Osinska H, Klevitsky R, Robbins J. Cardiomyocyte expression of a polyglutamine preamyloid oligomer causes heart failure. Circulation. 2008;117:2743-2751.
5. Kopito RR. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 2000;10:524-530.
6. Willis MS, Townley-Tilson WH, Kang EY, Homeister JW, Patterson C. Sent to destroy: the ubiquitin proteasome system regulates cell signaling and protein quality control in cardiovascular development and disease. Circ Res. 2010;106:463-478.
7. Kaushik S, Cuervo AM. Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol. 2012;22:407-417.
8. Kiffin R, Christian C, Knecht E, Cuervo AM. Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell. 2004;15:4829-4840.
9. Zhang C, Cuervo AM. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med. 2008;14:959-965.
10. Massey AC, Kaushik S, Sovak G, Kiffin R, Cuervo AM. Consequences of the selective blockage of chaperone-mediated autophagy. Proc Natl Acad Sci USA. 2006;103:5805-5810.
11. Kaushik S, Massey AC, Mizushima N, Cuervo AM. Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol Biol Cell. 2008;19:2179-2192.
12. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science. 2004;305:1292-1295.
13. Martinez-Vicente M, Talloczy Z, Kaushik S, et al. Dopamine-modified alpha-synuclein blocks chaperone-mediated autophagy. J Clin Invest. 2008;118:777-788.
14. Rodriguez-Navarro JA, Kaushik S, Koga H, Dall'Armi C, Shui G, Wenk MR, Di Paolo G, Cuervo AM. Inhibitory effect of dietary lipids on chaperone-mediated autophagy. Proc Natl Acad Sci USA. 2012;109:E705-E714.
15. Baker BM, Haynes CM. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci. 2011;36:254-261.
16. Lau E, Wang D, Zhang J, Yu H, Lam MP, Liang X, Zong N, Kim TY, Ping P. Substrate-and isoform-specific proteome stability in normal and stressed cardiac mitochondria. Circ Res. 2012;110:1174-1178.
17. McLendon PM, Robbins J. Desmin-related cardiomyopathy: an unfolding story. Am J Physiol Heart Circ Physiol. 2011;301:H1220-H1228.
18. Tian Z, Zheng H, Li J, Li Y, Su H, Wang X. Genetically induced moderate inhibition of the proteasome in cardiomyocytes exacerbates myocardial ischemia-reperfusion injury in mice. Circ Res. 2012;111: 532-542.
19. Kumarapeli AR, Wang X. Genetic modification of the heart: chaperones and the cytoskeleton. J Mol Cell Cardiol. 2004;37:1097-1109.
20. Kumarapeli AR, Su H, Huang W, Tang M, Zheng H, Horak KM, Li M, Wang X. Alpha B-crystallin suppresses pressure overload cardiac hypertrophy. Circ Res. 2008;103:1473-1482.
21. Qian J, Vafiadaki E, Florea SM, et al. Small heat shock protein 20 interacts with protein phosphatase-1 and enhances sarcoplasmic reticulum calcium cycling. Circ Res. 2011;108:1429-1438.
22. Ma X, Liu H, Foyil SR, Godar RJ, Weinheimer CJ, Hill JA, Diwan A. Impaired autophagosome clearance contributes to cardiomyocyte death in ischemia/reperfusion injury. Circulation. 2012;125:3170-3181.
23. Przyklenk K, Undyala VV, Wider J, Sala-Mercado JA, Gottlieb RA, Mentzer RM Jr. Acute induction of autophagy as a novel strategy for cardioprotection: getting to the heart of the matter. Autophagy. 2011;7:432-433.
24. Willis MS, Patterson C. Hold me tight: Role of the heat shock protein family of chaperones in cardiac disease. Circulation. 2010;122:1740-1751.
25. Taipale M, Jarosz DF, Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol. 2010;11:515-528.
26. Kovacs JJ, Murphy PJ, Gaillard S, Zhao X, Wu JT, Nicchitta CV, Yoshida M, Toft DO, Pratt WB, Yao TP. HDAC6 regulates Hsp90 acetylation and chaperone-dependent activation of glucocorticoid receptor. Mol Cell. 2005;18:601-607.
27. Scroggins BT, Robzyk K, Wang D, Marcu MG, Tsutsumi S, Beebe K, Cotter RJ, Felts S, Toft D, Karnitz L, Rosen N, Neckers L. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell. 2007;25:151-159.
28. Retzlaff M, Stahl M, Eberl HC, Lagleder S, Beck J, Kessler H, Buchner J. Hsp90 is regulated by a switch point in the C-terminal domain. EMBO Rep. 2009;10:1147-1153.
29. Martínez-Ruiz A, Villanueva L, González de Orduña C, López-Ferrer D, Higueras MA, Tarín C, Rodríguez-Crespo I, Vázquez J, Lamas S. S-nitrosylation of Hsp90 promotes the inhibition of its ATPase and endothelial nitric oxide synthase regulatory activities. Proc Natl Acad Sci USA. 2005;102:8525-8530.
30. Duval M, Le Boeuf F, Huot J, Gratton JP. Src-mediated phosphorylation of Hsp90 in response to vascular endothelial growth factor (VEGF) is required for VEGF receptor-2 signaling to endothelial NO synthase. Mol Biol Cell. 2007;18:4659-4668.
31. Ogiso H, Kagi N, Matsumoto E, Nishimoto M, Arai R, Shirouzu M, Mimura J, Fujii-Kuriyama Y, Yokoyama S. Phosphorylation analysis of 90 kDa heat shock protein within the cytosolic arylhydrocarbon receptor complex. Biochemistry. 2004;43:15510-15519.
32. Barral JM, Hutagalung AH, Brinker A, Hartl FU, Epstein HF. Role of the myosin assembly protein UNC-45 as a molecular chaperone for myosin. Science. 2002;295:669-671.
33. Kee HJ, Eom GH, Joung H, Shin S, Kim JR, Cho YK, Choe N, Sim BW, Jo D, Jeong MH, Kim KK, Seo JS, Kook H. Activation of histone deacetylase 2 by inducible heat shock protein 70 in cardiac hypertrophy. Circ Res. 2008;103:1259-1269.
34. Morrison LE, Hoover HE, Thuerauf DJ, Glembotski CC. Mimicking phosphorylation of alphaB-crystallin on serine-59 is necessary and sufficient to provide maximal protection of cardiac myocytes from apoptosis. Circ Res. 2003;92:203-211.
35. Jin JK, Whittaker R, Glassy MS, Barlow SB, Gottlieb RA, Glembotski CC. Localization of phosphorylated alphaB-crystallin to heart mitochondria during ischemia-reperfusion. Am J Physiol Heart Circ Physiol. 2008;294:H337-H344.
36. You W, Min X, Zhang X, Qian B, Pang S, Ding Z, Li C, Gao X, Di R, Cheng Y, Liu L. Cardiac-specific expression of heat shock protein 27 attenuated endotoxin-induced cardiac dysfunction and mortality in mice through a PI3K/Akt-dependent mechanism. Shock. 2009;32:108-117.
37. Liu L, Zhang X, Qian B, Min X, Gao X, Li C, Cheng Y, Huang J. Overexpression of heat shock protein 27 attenuates doxorubicin-induced cardiac dysfunction in mice. Eur J Heart Fail. 2007;9:762-769.
38. Hollander JM, Martin JL, Belke DD, Scott BT, Swanson E, Krishnamoorthy V, Dillmann WH. Overexpression of wild-type heat shock protein 27 and a nonphosphorylatable heat shock protein 27 mutant protects against ischemia/reperfusion injury in a transgenic mouse model. Circulation. 2004;110:3544-3552.
39. Yang WL, Wang J, Chan CH, Lee SW, Campos AD, Lamothe B, Hur L, Grabiner BC, Lin X, Darnay BG, Lin HK. The E3 ligase TRAF6 regulates Akt ubiquitination and activation. Science. 2009;325:1134-1138.
40. Dupont S, Mamidi A, Cordenonsi M, et al. FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell. 2009;136:123-135.
41. Ravid T, Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol. 2008;9:679-690.
42. Fredrickson EK, Gardner RG. Selective destruction of abnormal proteins by ubiquitin-mediated protein quality control degradation. Semin Cell Dev Biol. 2012;23:530-537.
43. Sarikas A, Hartmann T, Pan ZQ. The cullin protein family. Genome Biol. 2011;12:220.
44. Watson IR, Irwin MS, Ohh M. NEDD8 pathways in cancer, Sine Quibus Non. Cancer Cell. 2011;19:168-176.
45. Kato JY, Yoneda-Kato N. Mammalian COP9 signalosome. Genes Cells. 2009;14:1209-1225.
46. Su H, Li J, Menon S, Liu J, Kumarapeli AR, Wei N, Wang X. Perturbation of cullin deneddylation via conditional Csn8 ablation impairs the ubiquitin-proteasome system and causes cardiomyocyte necrosis and dilated cardiomyopathy in mice. Circ Res. 2011;108:40-50.
47. Qian SB, McDonough H, Boellmann F, Cyr DM, Patterson C. CHIPmediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature. 2006;440:551-555.
48. Naito AT, Okada S, Minamino T, Iwanaga K, Liu ML, Sumida T, Nomura S, Sahara N, Mizoroki T, Takashima A, Akazawa H, Nagai T, Shiojima I, Komuro I. Promotion of CHIP-mediated p53 degradation protects the heart from ischemic injury. Circ Res. 2010;106:1692-1702.
49. Yang K, Zhang TP, Tian C, Jia LX, Du J, Li HH. Carboxyl terminus of heat shock protein 70-interacting protein inhibits angiotensin II-induced cardiac remodeling. Am J Hypertens. 2012;25:994-1001.
50. Zhang C, Xu Z, He XR, Michael LH, Patterson C. CHIP, a cochaperone/ubiquitin ligase that regulates protein quality control, is required for maximal cardioprotection after myocardial infarction in mice. Am J Physiol Heart Circ Physiol. 2005;288:H2836-H2842.
51. Scaglione KM, Zavodszky E, Todi SV, Patury S, Xu P, Rodríguez- Lebrón E, Fischer S, Konen J, Djarmati A, Peng J, Gestwicki JE, Paulson HL. Ube2w and ataxin-3 coordinately regulate the ubiquitin ligase CHIP. Mol Cell. 2011;43:599-612.
52. Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, Palmer LA, Rockenstein EM, Zhang Z, Masliah E, Uehara T, Lipton SA. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci USA. 2004;101:10810-10814.
53. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science. 2004;304:1328-1331.
54. Choo YS, Vogler G, Wang D, Kalvakuri S, Iliuk A, Tao WA, Bodmer R, Zhang Z. Regulation of parkin and PINK1 by neddylation. Hum Mol Genet. 2012;21:2514-2523.
55. Um JW, Han KA, Im E, Oh Y, Lee K, Chung KC. Neddylation positively regulates the ubiquitin E3 ligase activity of parkin. J Neurosci Res. 2012;90:1030-1042.
56. Exner N, Treske B, Paquet D, et al. Loss-of-function of human PINK1 results in mitochondrial pathology and can be rescued by parkin. J Neurosci. 2007;27:12413-12418.
57. Kitada T, Tong Y, Gautier CA, Shen J. Absence of nigral degeneration in aged parkin/DJ-1/PINK1 triple knockout mice. J Neurochem. 2009;111:696-702.
58. Huang C, Andres AM, Ratliff EP, Hernandez G, Lee P, Gottlieb RA. Preconditioning involves selective mitophagy mediated by Parkin and p62/SQSTM1. PLoS ONE. 2011;6:e20975.
59. Hunter T. The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell. 2007;28:730-738.
60. Zhang YW, Otterness DM, Chiang GG, Xie W, Liu YC, Mercurio F, Abraham RT. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol Cell. 2005;19:607-618.
61. Besson A, Gurian-West M, Chen X, Kelly-Spratt KS, Kemp CJ, Roberts JM. A pathway in quiescent cells that controls p27Kip1 stability, subcellular localization, and tumor suppression. Genes Dev. 2006;20:47-64.
62. Sowa ME, Bennett EJ, Gygi SP, Harper JW. Defining the human deubiquitinating enzyme interaction landscape. Cell. 2009;138:389-403.
63. Durcan TM, Kontogiannea M, Bedard N, Wing SS, Fon EA. Ataxin-3 deubiquitination is coupled to Parkin ubiquitination via E2 ubiquitinconjugating enzyme. J Biol Chem. 2012;287:531-541.
64. Durcan TM, Kontogiannea M, Thorarinsdottir T, Fallon L, Williams AJ, Djarmati A, Fantaneanu T, Paulson HL, Fon EA. The Machado-Joseph disease-associated mutant form of ataxin-3 regulates parkin ubiquitination and stability. Hum Mol Genet. 2011;20:141-154.
65. Lee BH, Lee MJ, Park S, Oh DC, Elsasser S, Chen PC, Gartner C, Dimova N, Hanna J, Gygi SP, Wilson SM, King RW, Finley D. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature. 2010;467:179-184.
66. Lu H, Zong C, Wang Y, Young GW, Deng N, Souda P, Li X, Whitelegge J, Drews O, Yang PY, Ping P. Revealing the dynamics of the 20 S proteasome phosphoproteome: a combined CID and electron transfer dissociation approach. Mol Cell Proteomics. 2008;7:2073-2089.
67. Zong C, Gomes AV, Drews O, Li X, Young GW, Berhane B, Qiao X, French SW, Bardag-Gorce F, Ping P. Regulation of murine cardiac 20S proteasomes: role of associating partners. Circ Res. 2006;99:372-380.
68. Zhang F, Hu Y, Huang P, Toleman CA, Paterson AJ, Kudlow JE. Proteasome function is regulated by cyclic AMP-dependent protein kinase through phosphorylation of Rpt6. J Biol Chem. 2007;282:22460-22471.
69. Asai M, Tsukamoto O, Minamino T, Asanuma H, Fujita M, Asano Y, Takahama H, Sasaki H, Higo S, Asakura M, Takashima S, Hori M, Kitakaze M. PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts. J Mol Cell Cardiol. 2009;46:452-462.
70. Drews O, Tsukamoto O, Liem D, Streicher J, Wang Y, Ping P. Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circ Res. 2010;107:1094-1101.
71. Djakovic SN, Schwarz LA, Barylko B, DeMartino GN, Patrick GN. Regulation of the proteasome by neuronal activity and calcium/calmodulin-dependent protein kinase II. J Biol Chem. 2009;284:26655-26665.
72. Bingol B, Wang CF, Arnott D, Cheng D, Peng J, Sheng M. Autophosphorylated CaMKIIalpha acts as a scaffold to recruit proteasomes to dendritic spines. Cell. 2010;140:567-578.
73. Swaminathan PD, Purohit A, Hund TJ, Anderson ME. Calmodulindependent protein kinase II: linking heart failure and arrhythmias. Circ Res. 2012;110:1661-1677.
74. Bose S, Stratford FL, Broadfoot KI, Mason GG, Rivett AJ. Phosphorylation of 20S proteasome alpha subunit C8 (alpha7) stabilizes the 26S proteasome and plays a role in the regulation of proteasome complexes by gamma-interferon. Biochem J. 2004;378:177-184.
75. Li J, Powell SR, Wang X. Enhancement of proteasome function by PA28α overexpression protects against oxidative stress. FASEB J. 2011;25:883-893.
76. Takagi H, Hsu CP, Kajimoto K, Shao D, Yang Y, Maejima Y, Zhai P, Yehia G, Yamada C, Zablocki D, Sadoshima J. Activation of PKN mediates survival of cardiac myocytes in the heart during ischemia/reperfusion. Circ Res. 2010;107:642-649.
77. Uchiki T, Kim HT, Zhai B, Gygi SP, Johnston JA, O'Bryan JP, Goldberg AL. The ubiquitin-interacting motif protein, S5a, is ubiquitinated by all types of ubiquitin ligases by a mechanism different from typical substrate recognition. J Biol Chem. 2009;284:12622-12632.
78. Isasa M, Katz EJ, Kim W, Yugo V, González S, Kirkpatrick DS, Thomson TM, Finley D, Gygi SP, Crosas B. Monoubiquitination of RPN10 regulates substrate recruitment to the proteasome. Mol Cell. 2010;38:733-745.
79. Bulteau AL, Lundberg KC, Humphries KM, Sadek HA, Szweda PA, Friguet B, Szweda LI. Oxidative modification and inactivation of the proteasome during coronary occlusion/reperfusion. J Biol Chem. 2001;276:30057-30063.
80. Divald A, Kivity S, Wang P, Hochhauser E, Roberts B, Teichberg S, Gomes AV, Powell SR. Myocardial ischemic preconditioning preserves postischemic function of the 26S proteasome through diminished oxidative damage to 19S regulatory particle subunits. Circ Res. 2010;106:1829-1838.
81. Predmore JM, Wang P, Davis F, Bartolone S, Westfall MV, Dyke DB, Pagani F, Powell SR, Day SM. Ubiquitin proteasome dysfunction in human hypertrophic and dilated cardiomyopathies. Circulation. 2010;121:997-1004.
82. Reinheckel T, Sitte N, Ullrich O, Kuckelkorn U, Davies KJ, Grune T. Comparative resistance of the 20S and 26S proteasome to oxidative stress. Biochem J. 1998;335(pt 3):637-642.
83. Amici M, Lupidi G, Angeletti M, Fioretti E, Eleuteri AM. Peroxynitriteinduced oxidation and its effects on isolated proteasomal systems. Free Radic Biol Med. 2003;34:987-996.
84. Osna NA, Haorah J, Krutik VM, Donohue TM Jr. Peroxynitrite alters the catalytic activity of rodent liver proteasome in vitro and in vivo. Hepatology. 2004;40:574-582.
85. Davies KJ. Degradation of oxidized proteins by the 20S proteasome. Biochimie. 2001;83:301-310.
86. Friguet B, Stadtman ER, Szweda LI. Modification of glucose-6-phosphate dehydrogenase by 4-hydroxy-2-nonenal. Formation of crosslinked protein that inhibits the multicatalytic protease. J Biol Chem. 1994;269:21639-21643.
87. Papa L, Gomes E, Rockwell P. Reactive oxygen species induced by proteasome inhibition in neuronal cells mediate mitochondrial dysfunction and a caspase-independent cell death. Apoptosis. 2007;12:1389-1405.
88. Yue Z, Jin S, Yang C, Levine AJ, Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA. 2003;100:15077-15082.
89. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T, Ohsumi Y, Tokuhisa T, Mizushima N. The role of autophagy during the early neonatal starvation period. Nature. 2004;432:1032-1036.
90. 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.
91. Pyo JO, Nah J, Jung YK. Molecules and their functions in autophagy. Exp Mol Med. 2012;44:73-80.
92. Zhu H, Tannous P, Johnstone JL, Kong Y, Shelton JM, Richardson JA, Le V, Levine B, Rothermel BA, Hill JA. Cardiac autophagy is a maladaptive response to hemodynamic stress. J Clin Invest. 2007;117:1782-1793.
93. Rothermel BA, Hill JA. Autophagy in load-induced heart disease. Circ Res. 2008;103:1363-1369.
94. Matsui Y, Takagi H, Qu X, Abdellatif M, Sakoda H, Asano T, Levine B, Sadoshima J. Distinct roles of autophagy in the heart during ischemia and reperfusion: roles of AMP-activated protein kinase and Beclin 1 in mediating autophagy. Circ Res. 2007;100:914-922.
95. Tannous P, Zhu H, Nemchenko A, Berry JM, Johnstone JL, Shelton JM, Miller FJ Jr, Rothermel BA, Hill JA. Intracellular protein aggregation is a proximal trigger of cardiomyocyte autophagy. Circulation. 2008;117:3070-3078.
96. Tannous P, Zhu H, Johnstone JL, Shelton JM, Rajasekaran NS, Benjamin IJ, Nguyen L, Gerard RD, Levine B, Rothermel BA, Hill JA. Autophagy is an adaptive response in desmin-related cardiomyopathy. Proc Natl Acad Sci USA. 2008;105:9745-9750.
97. Kang R, Zeh HJ, Lotze MT, Tang D. The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 2011;18:571-580.
98. Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R, Kimchi A. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep. 2009;10:285-292.
99. Shi CS, Kehrl JH. TRAF6 and A20 regulate lysine 63-linked ubiquitination of Beclin-1 to control TLR4-induced autophagy. Sci Signal. 2010;3:ra42.
100. 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.
101. Maiuri MC, Le Toumelin G, Criollo A, Rain JC, Gautier F, Juin P, Tasdemir E, Pierron G, Troulinaki K, Tavernarakis N, Hickman JA, Geneste O, Kroemer G. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 2007;26:2527-2539.
102. Wei Y, Pattingre S, Sinha S, Bassik M, Levine B. JNK1-mediated phosphorylation of Bcl-2 regulates starvation-induced autophagy. Mol Cell. 2008;30:678-688.
103. Tang D, Kang R, Livesey KM, Cheh CW, Farkas A, Loughran P, Hoppe G, Bianchi ME, Tracey KJ, Zeh HJ 3rd, Lotze MT. Endogenous HMGB1 regulates autophagy. J Cell Biol. 2010;190:881-892.
104. He C, Bassik MC, Moresi V, et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature. 2012;481:511-515.
105. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell. 2008;30:214-226.
106. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003;115:577-590.
107. Lee JW, Park S, Takahashi Y, Wang HG. The association of AMPK with ULK1 regulates autophagy. PLoS ONE. 2010;5:e15394.
108. Egan DF, Shackelford DB, Mihaylova MM, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science. 2011;331:456-461.
109. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132-141.
110. Chiacchiera F, Matrone A, Ferrari E, Ingravallo G, Lo Sasso G, Murzilli S, Petruzzelli M, Salvatore L, Moschetta A, Simone C. p38alpha blockade inhibits colorectal cancer growth in vivo by inducing a switch from HIF1alpha-to FoxO-dependent transcription. Cell Death Differ. 2009;16:1203-1214.
111. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007;6:458-471.
112. Takagi H, Matsui Y, Hirotani S, Sakoda H, Asano T, Sadoshima J. AMPK mediates autophagy during myocardial ischemia in vivo. Autophagy. 2007;3:405-407.
113. Nakai A, Yamaguchi O, Takeda T, Higuchi Y, Hikoso S, Taniike M, Omiya S, Mizote I, Matsumura Y, Asahi M, Nishida K, Hori M, Mizushima N, Otsu K. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007;13:619-624.
114. Sou YS, Tanida I, Komatsu M, Ueno T, Kominami E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. J Biol Chem. 2006;281:3017-3024.
115. Pattison JS, Osinska H, Robbins J. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res. 2011;109:151-160.
116. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J, Tabas I. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab. 2012;15:545-553.
117. Sciarretta S, Zhai P, Shao D, Maejima Y, Robbins J, Volpe M, Condorelli G, Sadoshima J. Rheb is a critical regulator of autophagy during myocardial ischemia: pathophysiological implications in obesity and metabolic syndrome. Circulation. 2012;125:1134-1146.
118. Lee IH, Finkel T. Regulation of autophagy by the p300 acetyltransferase. J Biol Chem. 2009;284:6322-6328.
119. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW, Finkel T. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA. 2008;105:3374-3379.
120. Guarente L, Picard F. Calorie restriction-the SIR2 connection. Cell. 2005;120:473-482.
121. Brunet A, Sweeney LB, Sturgill JF, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011-2015.
122. Hariharan N, Maejima Y, Nakae J, Paik J, Depinho RA, Sadoshima J. Deacetylation of FoxO by Sirt1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ Res. 2010;107:1470-1482.
123. Hsu CP, Zhai P, Yamamoto T, Maejima Y, Matsushima S, Hariharan N, Shao D, Takagi H, Oka S, Sadoshima J. Silent information regulator 1 protects the heart from ischemia/reperfusion. Circulation. 2010;122:2170-2182.
124. Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S, Wang D, Feng J, Yu L, Zhu WG. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol. 2010;12:665-675.
125. Schips TG, Wietelmann A, Höhn K, Schimanski S, Walther P, Braun T, Wirth T, Maier HJ. FoxO3 induces reversible cardiac atrophy and autophagy in a transgenic mouse model. Cardiovasc Res. 2011;91:587-597.
126. Su H, Li F, Ranek MJ, Wei N, Wang X. COP9 signalosome regulates autophagosome maturation. Circulation. 2011;124:2117-2128.
127. Soucy TA, Smith PG, Milhollen MA, et al. An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer. Nature. 2009;458:732-736.
128. Luo Z, Yu G, Lee HW, et al. The Nedd8-activating enzyme inhibitor MLN4924 induces autophagy and apoptosis to suppress liver cancer cell growth. Cancer Res. 2012;72:3360-3371.
129. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J, Rush J, Hochstrasser M, Finley D, Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell. 2009;137:133-145.
130. Tan JM, Wong ES, Kirkpatrick DS, Pletnikova O, Ko HS, Tay SP, Ho MW, Troncoso J, Gygi SP, Lee MK, Dawson VL, Dawson TM, Lim KL. Lysine 63-linked ubiquitination promotes the formation and autophagic clearance of protein inclusions associated with neurodegenerative diseases. Hum Mol Genet. 2008;17:431-439.
131. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011;7:279-296.
132. Matsumoto G, Wada K, Okuno M, Kurosawa M, Nukina N. Serine 403 phosphorylation of p62/SQSTM1 regulates selective autophagic clearance of ubiquitinated proteins. Mol Cell. 2011;44:279-289.
133. Zheng Q, Su H, Ranek MJ, Wang X. Autophagy and p62 in cardiac proteinopathy. Circ Res. 2011;109:296-308.
134. Komatsu M, Waguri S, Koike M, et al. Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell. 2007;131:1149-1163.
135. Su H, Wang X. p62 Stages an interplay between the ubiquitin-proteasome system and autophagy in the heart of defense against proteotoxic stress. Trends Cardiovasc Med. 2011;21:224-228.
136. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J, Cookson MR, Youle RJ. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol. 2010;8:e1000298.
137. Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death Differ. 2013;20:31-42.
138. Walden H, Martinez-Torres RJ. Regulation of Parkin E3 ubiquitin ligase activity. Cell Mol Life Sci. 2012;69:3053-3067.
139. Tanaka A, Cleland MM, Xu S, Narendra DP, Suen DF, Karbowski M, Youle RJ. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J Cell Biol. 2010;191:1367-1380.
140. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL, Hess S, Chan DC. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet. 2011;20:1726-1737.
141. Narendra D, Kane LA, Hauser DN, Fearnley IM, Youle RJ. p62/SQSTM1 is required for Parkin-induced mitochondrial clustering but not mitophagy; VDAC1 is dispensable for both. Autophagy. 2010;6:1090-1106.
142. Wang X, Robbins J. Heart failure and protein quality control. Circ Res. 2006;99:1315-1328.
143. Depre C, Wang Q, Yan L, Hedhli N, Peter P, Chen L, Hong C, Hittinger L, Ghaleh B, Sadoshima J, Vatner DE, Vatner SF, Madura K. Activation of the cardiac proteasome during pressure overload promotes ventricular hypertrophy. Circulation. 2006;114:1821-1828.
144. Tang M, Li J, Huang W, Su H, Liang Q, Tian Z, Horak KM, Molkentin JD, Wang X. Proteasome functional insufficiency activates the calcineurin-NFAT pathway in cardiomyocytes and promotes maladaptive remodelling of stressed mouse hearts. Cardiovasc Res. 2010;88: 424-433.
145. Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009;53:2231-2247.