The ubiquitin proteasome system and myocardial ischemia

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 304, Issue 3, 2013, Pages

  Calise, Justine ^a,b   Powell, Saul R ^a  

^a FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b Long Island University Post Campus ^*  (United States)

Author keywords

Ischemic preconditioning; Myocardial ischemia; Ubiquitin; Ubiquitin proteasome system

Indexed keywords

BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; BORTEZOMIB; CARFILZOMIB; CYCLIC AMP DEPENDENT PROTEIN KINASE; DEUBIQUITINASE; LACTACYSTIN BETA LACTONE; PEPTIDES AND PROTEINS; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN; UNCLASSIFIED DRUG;

AUTOPHAGY; BRAIN ISCHEMIA; HEART MUSCLE ISCHEMIA; HUMAN; ISCHEMIC PRECONDITIONING; MEDICAL LITERATURE; MULTIPLE MYELOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; UBIQUITINATION;

ANIMALS; AUTOPHAGY; HEART; HUMANS; ISCHEMIC PRECONDITIONING; MYOCARDIAL ISCHEMIA; MYOCARDIUM; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

EID: 84873319952     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00604.2012     Document Type: Review

References (176)

1. Arastu-Kapur S, Anderl JL, Kraus M, Parlati F, Shenk KD, Lee SJ, Muchamuel T, Bennett MK, Driessen C, Ball AJ, Kirk CJ. Nonproteasomal targets of the proteasome inhibitors bortezomib and carfilzomib: a link to clinical adverse events. Clin Cancer Res 17: 2734-2743, 2011.
2. Asai A, Tanahashi N, Qiu JH, Saito N, Chi S, Kawahara N, Tanaka K, Kirino T. Selective proteasomal dysfunction in the hippocampal CA1 region after transient forebrain ischemia. J Cereb Blood Flow Metab 22: 705-710, 2002.
3. 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 46: 452-462, 2009.
4. Baines CP. How and when do myocytes die during ischemia and reperfusion: the late phase. J Cardiovasc Pharmacol Ther 16: 239-243, 2011.
5. Baines CP, Song CX, Zheng YT, Wang GW, Zhang J, Wang OL, Guo Y, Bolli R, Cardwell EM, Ping P. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 92: 873-880, 2003.
6. Basler M, Dajee M, Moll C, Groettrup M, Kirk CJ. Prevention of experimental colitis by a selective inhibitor of the immunoproteasome. J Immunol 185: 634-641, 2010.
7. Berti R, Williams AJ, Velarde LC, Moffett JR, Elliott PJ, Adams J, Yao C, Dave JR, Tortella FC. Effect of the proteasome inhibitor MLN519 on the expression of inflammatory molecules following middle cerebral artery occlusion and reperfusion in the rat. Neurotox Res 5: 505-514, 2003.
8. Blickwedehl J, Agarwal M, Seong C, Pandita RK, Melendy T, Sung P, Pandita TK, Bangia N. Role for proteasome activator PA200 and postglutamyl proteasome activity in genomic stability. Proc Natl Acad Sci USA 105: 16165-16170, 2008.
9. Bolli R. Preconditioning: a paradigm shift in the biology of myocardial ischemia. Am J Physiol Heart Circ Physiol 292: H19-H27, 2007.
10. 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 378: 177-184, 2004.
11. 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 276: 30057-30063, 2001.
12. Burrows JF, Johnston JA. Regulation of cellular responses by deubiquitinating enzymes: an update. Front Biosci 17: 1184-1200, 2012.
13. Cai Z, Semenza GL. PTEN activity is modulated during ischemia and reperfusion: involvement in the induction and decay of preconditioning. Circ Res 97: 1351-1359, 2005.
14. Cai ZP, Shen Z, Van Kaer L, Becker LC. Ischemic preconditioning-induced cardioprotection is lost in mice with immunoproteasome subunit low molecular mass polypeptide-2 deficiency. FASEB J 22: 4248-4257, 2008.
15. Campbell B, Adams J, Shin YK, Lefer AM. Cardioprotective effects of a novel proteasome inhibitor following ischemia and reperfusion in the isolated perfused rat heart. J Mol Cell Cardiol 31: 467-476, 1999.
16. Canton M, Neverova I, Menabo R, Van Eyk J, Di Lisa F. Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. Am J Physiol Heart Circ Physiol 286: H870-H877, 2004.
17. Carrier L, Schlossarek S, Willis MS, Eschenhagen T. The ubiquitin-proteasome system and nonsense-mediated mRNA decay in hypertrophic cardiomyopathy. Cardiovasc Res 85: 330-338, 2010.
18. Castano JG, Mahillo E, Arizti P, Arribas J. Phosphorylation of C8 and C9 subunits of the multicatalytic proteinase by casein kinase II and identification of the C8 phosphorylation sites by direct mutagenesis. Biochemistry 35: 3782-3789, 1996.
19. Castro A, Bernis C, Vigneron S, Labbe JC, Lorca T. The anaphase-promoting complex: a key factor in the regulation of cell cycle. Oncogene 24: 314-325, 2005.
20. Churchill EN, Ferreira JC, Brum PC, Szweda LI, Mochly-Rosen D. Ischaemic preconditioning improves proteasomal activity and increases the degradation of deltaPKC during reperfusion. Cardiovasc Res 85: 385-394, 2010.
21. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 6: 79-87, 2005.
22. Ciechanover A, Orian A, Schwartz AL. Ubiquitin-mediated proteolysis: biological regulation via destruction. Bioessays 22: 442-451, 2000.
23. Cilenti L, Balakrishnan MP, Wang XL, Ambivero C, Sterlicchi M, del MF, Ma XL, Zervos AS. Regulation of Abro1/KIAA0157 during myocardial infarction and cell death reveals a novel cardioprotective mechanism for Lys63-specific deubiquitination. J Mol Cell Cardiol 50: 652-661, 2011.
24. Davies KJ, Delsignore ME. Protein damage and degradation by oxygen radicals. III. Modification of secondary and tertiary structure. J Biol Chem 262: 9908-9913, 1987.
25. Davies KJ, Lin SW, Pacifici RE. Protein damage and degradation by oxygen radicals. IV. Degradation of denatured protein. J Biol Chem 262: 9914-9920, 1987.
26. DeMartino GN. Purification of PA700, the 19S regulatory complex of the 26S proteasome. Methods Enzymol 398: 295-306, 2005.
27. Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434, 2009.
28. Ding WX, Yin XM. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4: 141-150, 2008.
29. 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 106: 1829-1838, 2010.
30. Divald A, Powell SR. Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radic Biol Med 40: 156-164, 2006.
31. Drews O, Tsukamoto O, Liem D, Streicher J, Wang Y, Ping P. Differential regulation of proteasome function in isoproterenol-induced cardiac hypertrophy. Circ Res 107: 1094-1101, 2010.
32. Drews O, Wildgruber R, Zong C, Sukop U, Nissum M, Weber G, Gomes AV, Ping P. Mammalian proteasome subpopulations with distinct molecular compositions and proteolytic activities. Mol Cell Proteomics 6: 2021-2031, 2007.
33. Drews O, Zong C, Ping P. Exploring proteasome complexes by proteomic approaches. Proteomics 7: 1047-1058, 2007.
34. Ebstein F, Kloetzel PM, Kruger E, Seifert U. Emerging roles of immunoproteasomes beyond MHC class I antigen processing. Cell Mol Life Sci 69: 2543-2558, 2012.
35. Elliott PJ, Zollner TM, Boehncke WH. Proteasome inhibition: a new anti-inflammatory strategy. J Mol Med 81: 235-245, 2003.
36. Enrico O, Gabriele B, Nadia C, Sara G, Daniele V, Giulia C, Antonio S, Mario P. Unexpected cardiotoxicity in haematological bortezomib treated patients. Br J Haematol 138: 396-397, 2007.
37. Farout L, Mary J, Vinh J, Szweda LI, Friguet B. Inactivation of the proteasome by 4-hydroxy-2-nonenal is site specific and dependant on 20S proteasome subtypes. Arch Biochem Biophys 453: 135-142, 2006.
38. Gaczynska M, Rock KL, Goldberg AL. Role of proteasomes in antigen presentation. Enzyme Protein 47: 354-369, 1993.
39. Gaczynska M, Rock KL, Spies T, Goldberg AL. Peptidase activities of proteasomes are differentially regulated by the major histocompatibility complex-encoded genes for LMP2 and LMP7. Proc Natl Acad Sci USA 91: 9213-9217, 1994.
40. Ge P, Luo Y, Liu CL, Hu B. Protein aggregation and proteasome dysfunction after brain ischemia. Stroke 38: 3230-3236, 2007.
41. Geng Q, Romero J, Saini V, Baker TA, Picken MM, Gamelli RL, Majetschak M. A subset of 26S proteasomes is activated at critically low ATP concentrations and contributes to myocardial injury during cold ischemia. Biochem Biophys Res Commun 390: 1136-1141, 2009.
42. Gillette TG, Kumar B, Thompson D, Slaughter CA, DeMartino GN. Differential roles of the COOH termini of AAA subunits of PA700 (19 S regulator) in asymmetric assembly and activation of the 26 S proteasome. J Biol Chem 283: 31813-31822, 2008.
43. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82: 373-428, 2002.
44. Gomes AV, Young GW, Wang Y, Zong C, Eghbali M, Drews O, Lu H, Stefani E, Ping P. Contrasting proteome biology and functional heterogeneity of the 20 S proteasome complexes in mammalian tissues. Mol Cell Proteomics 8: 302-315, 2009.
45. Gomes AV, Zong C, Edmondson RD, Berhane BT, Wang GW, Le S, Young G, Zhang J, Vondriska TM, Whitelegge JP, Jones RC, Joshua IG, Thyparambil S, Pantaleon D, Qiao J, Loo J, Ping P. The murine cardiac 26S proteasome: an organelle awaiting exploration. Ann NY Acad Sci 1047: 197-207, 2005.
46. Gomes AV, Zong C, Edmondson RD, Li X, Stefani E, Zhang J, Jones RC, Thyparambil S, Wang GW, Qiao X, Bardag-Gorce F, Ping P. Mapping the murine cardiac 26S proteasome complexes. Circ Res 99: 362-371, 2006.
47. Gong P, Canaan A, Wang B, Leventhal J, Snyder A, Nair V, Cohen CD, Kretzler M, D'Agati V, Weissman S, Ross MJ. The ubiquitin-like protein FAT10 mediates NF-kappaB activation. J Am Soc Nephrol 21: 316-326, 2010.
48. Gorbea C, Taillandier D, Rechsteiner M. Assembly of the regulatory complex of the 26S proteasome. Mol Biol Rep 26: 15-19, 1999.
49. Groettrup M, Pelzer C, Schmidtke G, Hofmann K. Activating the ubiquitin family: UBA6 challenges the field. Trends Biochem Sci 33: 230-237, 2008.
50. Groettrup M, Soza A, Eggers M, Kuehn L, Dick TP, Schild H, Rammensee HG, Koszinowski UH, Kloetzel PM. A role for the proteasome regulator PA28alpha in antigen presentation. Nature 381: 166-168, 1996.
51. Groll M, Huber R. Substrate access and processing by the 20S proteasome core particle. Int J Biochem Cell Biol 35: 606-616, 2003.
52. + channels and myocardial preconditioning. Circ Res 84: 973-979, 1999.
53. Gurusamy N, Goswami S, Malik G, Das DK. Oxidative injury induces selective rather than global inhibition of proteasomal activity. J Mol Cell Cardiol 44: 419-428, 2008.
54. Gustafsson AB, Gottlieb RA. Eat your heart out: role of autophagy in myocardial ischemia/reperfusion. Autophagy 4: 416-421, 2008.
55. Gustafsson AB, Gottlieb RA. Recycle or die: the role of autophagy in cardioprotection. J Mol Cell Cardiol 44: 654-661, 2008.
56. Gustafsson AB, Gottlieb RA. Autophagy in ischemic heart disease. Circ Res 104: 150-158, 2009.
57. Hacihanefioglu A, Tarkun P, Gonullu E. Acute severe cardiac failure in a myeloma patient due to proteasome inhibitor bortezomib. Int J Hematol 88: 219-222, 2008.
58. Hammond-Martel I, Yu H, Affar el B. Roles of ubiquitin signaling in transcription regulation. Cell Signal 24: 410-421, 2012.
59. Hariharan N, Zhai P, Sadoshima J. Oxidative stress stimulates autophagic flux during ischemia/reperfusion. Antioxid Redox Signal 14: 2179-2190, 2011.
60. Hasselgren PO, Fischer JE. Muscle cachexia: current concepts of intracellular mechanisms and molecular regulation. Ann Surg 233: 9-17, 2001.
61. Hayashi T, Takada K, Matsuda M. Post-transient ischemia increase in ubiquitin conjugates in the early reperfusion. Neuroreport 3: 519-520, 1992.
62. Herrmann J, Lerman LO, Lerman A. On to the road to degradation: atherosclerosis and the proteasome. Cardiovasc Res 85: 291-302, 2010.
63. Hershko A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr Opin Cell Biol 9: 788-799, 1997.
64. Hershko A, Ciechanover A, Rose IA. Resolution of the ATP-dependent proteolytic system from reticulocytes: a component that interacts with ATP. Proc Natl Acad Sci USA 76: 3107-3110, 1979.
65. Hochrainer K, Jackman K, Anrather J, Iadecola C. Reperfusion rather than ischemia drives the formation of ubiquitin aggregates after middle cerebral artery occlusion. Stroke 43: 2229-2235, 2012.
66. Horwitz AA, Navon A, Groll M, Smith DM, Reis C, Goldberg AL. ATP-induced structural transitions in PAN, the proteasome-regulatory ATPase complex in Archaea. J Biol Chem 282: 22921-22929, 2007.
67. Hu HY. Editorial: protein ubiquitination and deubiquitination. Curr Protein Pept Sci 13: 413, 2012.
68. Hua Z, Vierstra RD. The cullin-RING ubiquitin-protein ligases. Annu Rev Plant Biol 62: 299-334, 2011.
69. Huang H, Zhang X, Li S, Liu N, Lian W, McDowell E, Zhou P, Zhao C, Guo H, Zhang C, Yang C, Wen G, Dong X, Lu L, Ma N, Dong W, Dou QP, Wang X, Liu J. Physiological levels of ATP negatively regulate proteasome function. Cell Res 20: 1372-1385, 2010.
70. Huang S, Patterson E, Yu X, Garrett MW, De AI, Kem DC. Proteasome inhibition 1 h following ischemia protects GRK2 and prevents malignant ventricular tachyarrhythmias and SCD in a model of myocardial infarction. Am J Physiol Heart Circ Physiol 294: H1298-H1303, 2008.
71. Huber EM, Basler M, Schwab R, Heinemeyer W, Kirk CJ, Groettrup M, Groll M. Immuno- and constitutive proteasome crystal structures reveal differences in substrate and inhibitor specificity. Cell 148: 727-738, 2012.
72. Ichikawa HT, Conley T, Muchamuel T, Jiang J, Lee S, Owen T, Barnard J, Nevarez S, Goldman BI, Kirk CJ, Looney RJ, Anolik JH. Beneficial effect of novel proteasome inhibitors in murine lupus via dual inhibition of type I interferon and autoantibody-secreting cells. Arthritis Rheum 64: 493-503, 2012.
73. Inagaki K, Chen L, Ikeno F, Lee FH, Imahashi K, Bouley DM, Rezaee M, Yock PG, Murphy E, Mochly-Rosen D. Inhibition of delta-protein kinase C protects against reperfusion injury of the ischemic heart in vivo. Circulation 108: 2304-2307, 2003.
74. Ishii T, Sakurai T, Usami H, Uchida K. Oxidative modification of proteasome: identification of an oxidation-sensitive subunit in 26 s proteasome. Biochemistry 44: 13893-13901, 2005.
75. Jesenberger V, Jentsch S. Deadly encounter: ubiquitin meets apoptosis. Nat Rev Mol Cell Biol 3: 112-121, 2002.
76. Kamikubo T, Hayashi T. Changes in proteasome activity following transient ischemia. Neurochem Int 28: 209-212, 1996.
77. Kassiotis C, Ballal K, Wellnitz K, Vela D, Gong M, Salazar R, Frazier OH, Taegtmeyer H. Markers of autophagy are downregulated in failing human heart after mechanical unloading. Circulation 120: S191-S197, 2009.
78. Keller JN, Huang FF, Zhu H, Yu J, Ho YS, Kindy TS. Oxidative stress-associated impairment of proteasome activity during ischemia-reperfusion injury. J Cereb Blood Flow Metab 20: 1467-1473, 2000.
79. Khaliulin I, Schwalb H, Wang P, Houminer E, Grinberg L, Katzeff H, Borman JB, Powell SR. Preconditioning improves postischemic mitochondrial function and diminishes oxidation of mitochondrial proteins. Free Radic Biol Med 37: 1-9, 2004.
80. Kloetzel PM, Soza A, Stohwasser R. The role of the proteasome system and the proteasome activator PA28 complex in the cellular immune response. Biol Chem 380: 293-297, 1999.
81. Komander D, Clague MJ, Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10: 550-563, 2009.
82. Korge P, Honda HM, Weiss JN. Protection of cardiac mitochondria by diazoxide and protein kinase C: implications for ischemic preconditioning. Proc Natl Acad Sci USA 99: 3312-3317, 2002.
83. Krappmann D, Scheidereit C. A pervasive role of ubiquitin conjugation in activation and termination of IkappaB kinase pathways. EMBO Rep 6: 321-326, 2005.
84. Kruger E, Kloetzel PM. Immunoproteasomes at the interface of innate and adaptive immune responses: two faces of one enzyme. Curr Opin Immunol 24: 77-83, 2012.
85. 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 121: 3689-3700, 2011.
86. Li J, Powell SR, Wang X. Enhancement of proteasome function by PA28alpha; overexpression protects against oxidative stress. FASEB J 25: 883-893, 2011.
87. Lin KI, Baraban JM, Ratan RR. Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ 5: 577-583, 1998.
88. Liu C, Chen S, Kamme F, Hu BR. Ischemic preconditioning prevents protein aggregation after transient cerebral ischemia. Neuroscience 134: 69-80, 2005.
89. 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 7: 2073-2089, 2008.
90. Lu L, Wang H. Transient focal cerebral ischemia upregulates immuno-proteasomal subunits. Cell Mol Neurobiol 32: 965-970, 2012.
91. Matsui Y, Kyoi S, Takagi H, Hsu CP, Hariharan N, Ago T, Vatner SF, Sadoshima J. Molecular mechanisms and physiological significance of autophagy during myocardial ischemia and reperfusion. Autophagy 4: 409-415, 2008.
92. McCullock S, Kinard T, McCullough L, Formosa T. blm3-1 is an allele of UBP3, a ubiquitin protease that appears to act during transcription of damaged DNA. J Mol Biol 363: 660-672, 2006.
93. Meiners S, Heyken D, Weller A, Ludwig A, Stangl K, Kloetzel PM, Kruger E. Inhibition of proteasome activity induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J Biol Chem 278: 21517-21525, 2003.
94. Meiners S, Ludwig A, Lorenz M, Dreger H, Baumann G, Stangl V, Stangl K. Nontoxic proteasome inhibition activates a protective antioxidant defense response in endothelial cells. Free Radic Biol Med 40: 2232-2241, 2006.
95. Meiners S, Ludwig A, Stangl V, Stangl K. Proteasome inhibitors: poisons and remedies. Med Res Rev 28: 309-327, 2008.
96. Meller R, Cameron JA, Torrey DJ, Clayton CE, Ordonez AN, Henshall DC, Minami M, Schindler CK, Saugstad JA, Simon RP. Rapid degradation of Bim by the ubiquitin-proteasome pathway mediates short-term ischemic tolerance in cultured neurons. J Biol Chem 281: 7429-7436, 2006.
97. Moss NC, Tang RH, Willis M, Stansfield WE, Baldwin AS, Selzman CH. Inhibitory kappa B kinase-beta is a target for specific nuclear factor kappa B-mediated delayed cardioprotection. J Thorac Cardiovasc Surg 136: 1274-1279, 2008.
98. Muchamuel T, Basler M, Aujay MA, Suzuki E, Kalim KW, Lauer C, Sylvain C, Ring ER, Shields J, Jiang J, Shwonek P, Parlati F, Demo SD, Bennett MK, Kirk CJ, Groettrup M. A selective inhibitor of the immunoproteasome subunit LMP7 blocks cytokine production and attenuates progression of experimental arthritis. Nat Med 15: 781-787, 2009.
99. Murata S, Kawahara H, Tohma S, Yamamoto K, Kasahara M, Nabeshima Y, Tanaka K, Chiba T. Growth retardation in mice lacking the proteasome activator PA28gamma. J Biol Chem 274: 38211-38215, 1999.
100. Neefjes J, Jongsma ML, Paul P, Bakke O. Towards a systems understanding of MHC class I and MHC class II antigen presentation. Nat Rev Immunol 11: 823-836, 2011.
101. Orlowski M, Wilk S. Catalytic activities of the 20 S proteasome, a multicatalytic proteinase complex. Arch Biochem Biophys 383: 1-16, 2000.
102. Park Y, Kanekal S, Kehrer JP. Oxidative changes in hypoxic rat heart tissue. Am J Physiol Heart Circ Physiol 260: H1395-H1405, 1991.
103. Pickering AM, Davies KJ. Differential roles of proteasome and immunoproteasome regulators Pa28alphabeta, Pa28gamma and Pa200 in the degradation of oxidized proteins. Arch Biochem Biophys 523: 181-190, 2012.
104. Pickering AM, Koop AL, Teoh CY, Ermak G, Grune T, Davies KJ. The immunoproteasome, the 20S proteasome and the PA28alphabeta proteasome regulator are oxidative-stress-adaptive proteolytic complexes. Biochem J 432: 585-594, 2010.
105. Portbury AL, Ronnebaum SM, Zungu M, Patterson C, Willis MS. Back to your heart: ubiquitin proteasome system-regulated signal transduction. J Mol Cell Cardiol 52: 526-537, 2012.
106. Powell SR. The cardiac 26S proteasome: regulating the regulator. Circ Res 99: 342-345, 2006.
107. Powell SR. Proteasome inhibitors in myocardial ischemia, some concerns. Ann Thorac Surg 85: 1503-1504, 2008.
108. Powell SR, Davies KJA, Divald A. Optimal determination of heart tissue 26S Proteasome activity requires maximal stimulating concentrations of ATP. J Mol Cell Cardiol 42: 265-269, 2007.
109. Powell SR, Divald A. The ubiquitin-proteasome system in myocardial ischaemia and preconditioning. Cardiovasc Res 85: 303-311, 2010.
110. Powell SR, Gurzenda EM, Wahezi SE. Actin is oxidized during myocardial ischemia. Free Radic Biol Med 30: 1171-1176, 2001.
111. Powell SR, Hall D. Use of salicylate as a probe for·OH formation in isolated ischemic rat hearts. Free Radic Biol Med 9: 133-141, 1990.
112. Powell SR, Samuel SM, Wang P, Divald A, Thirunavukkarasu M, Koneru S, Wang X, Maulik N. Upregulation of myocardial 11S-activated proteasome in experimental hyperglycemia. J Mol Cell Cardiol 44: 618-621, 2008.
113. Powell SR, Wang P, Katzeff HL, Shringarpure R, Teoh C, Khaliulin I, Das DK, Schwalb H. Oxidized and ubiquitinated proteins may predict recovery of postischemic cardiac function. Essential role of the proteasome. Antioxid Redox Signal 7: 538-535, 2005.
114. Pradillo JM, Romera C, Hurtado O, Cardenas A, Moro MA, Leza JC, Davalos A, Castillo J, Lorenzo P, Lizasoain I. TNFR1 upregulation mediates tolerance after brain ischemic preconditioning. J Cereb Blood Flow Metab 25: 193-203, 2005.
115. 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 21: 997-1004, 2010.
116. Price SR. Increased transcription of ubiquitin-proteasome system components: molecular responses associated with muscle atrophy. Int J Biochem Cell Biol 35: 617-628, 2003.
117. Przyklenk K, Dong Y, Undyala VV, Whittaker P. Autophagy as a therapeutic target for ischaemia /reperfusion injury? Concepts, controversies, and challenges. Cardiovasc Res 94: 197-205, 2012.
118. 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 7: 432-433, 2011.
119. Pye J, Ardeshirpour F, McCain A, Bellinger DA, Merricks E, Adams J, Elliott PJ, Pien C, Fischer TH, Baldwin AS Jr, Nichols TC. Proteasome inhibition ablates activation of NF-kB in myocardial reperfusion and reduces reperfusion injury. Am J Physiol Heart Circ Physiol 284: H919-H926, 2003.
120. Rabl J, Smith DM, Yu Y, Chang SC, Goldberg AL, Cheng Y. Mechanism of gate opening in the 20S proteasome by the proteasomal ATPases. Mol Cell 30: 360-368, 2008.
121. 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 335: 637-642, 1998.
122. Reinheckel T, Ullrich O, Sitte N, Grune T. Differential impairment of 20S and 26S proteasome activities in human hematopoietic K562 cells during oxidative stress. Arch Biochem Biophys 377: 65-68, 2000.
123. Rock KL, York IA, Saric T, Goldberg AL. Protein degradation and the generation of MHC class I-presented peptides. Adv Immunol 80: 1-70, 2002.
124. Rodriguez JE, Schisler JC, Patterson C, Willis MS. Seek and destroy: the ubiquitin-proteasome system in cardiac disease. Curr Hypertens Rep 11: 396-405, 2009.
125. Rotin D, Kumar S. Physiological functions of the HECT family of ubiquitin ligases. Nat Rev Mol Cell Biol 10: 398-409, 2009.
126. Sala-Mercado JA, Wider J, Undyala VV, Jahania S, Yoo W, Mentzer RM Jr, Gottlieb RA, Przyklenk K. Profound cardioprotection with chloramphenicol succinate in the swine model of myocardial ischemia-reperfusion injury. Circulation 122: S179-S184, 2010.
127. Sarikas A, Hartmann T, Pan ZQ. The cullin protein family. Genome Biol 12: 220, 2011.
128. Satoh K, Sasajima H, Nyoumura KI, Yokosawa H, Sawada H. Assembly of the 26S proteasome is regulated by phosphorylation of the p45/Rpt6 ATPase subunit. Biochemistry 40: 314-319, 2001.
129. Schulman BA. Twists and turns in ubiquitin-like protein conjugation cascades. Protein Sci 20: 1941-1954, 2011.
130. Schulman BA, Harper JW. Ubiquitin-like protein activation by E1 enzymes: the apex for downstream signalling pathways. Nat Rev Mol Cell Biol 10: 319-331, 2009.
131. 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 303: H9-H18, 2012.
132. Seifert U, Bialy LP, Ebstein F, Bech-Otschir D, Voigt A, Schröter F, Prozorovski T, Lange N, Steffen J, Rieger M, Kuckelkorn U, Aktas O, Kloetzel PM, Krüger E. Immunoproteasomes preserve protein homeostasis upon interferon-induced oxidative stress. Cell 142: 613-624, 2010.
133. Song X, von Kampen J, Slaughter CA, DeMartino GN. Relative functions of the alpha and beta subunits of the proteasome activator, PA28. J Biol Chem 272: 27994-28000, 1997.
134. Stadtmueller BM, Hill CP. Proteasome activators. Mol Cell 41: 8-19, 2011.
135. Stangl K, Gunther C, Frank T, Lorenz M, Meiners S, Ropke T, Stelter L, Moobed M, Baumann G, Kloetzel PM, Stangl V. Inhibition of the ubiquitin-proteasome pathway induces differential heat-shock protein response in cardiomyocytes and renders early cardiac protection. Biochem Biophys Res Commun 291: 542-549, 2002.
136. Stanley WC. Myocardial energy metabolism during ischemia and the mechanisms of metabolic therapies. J Cardiovasc Pharmacol Ther 9, Suppl 1: S31-S45, 2004.
137. Stohwasser R, Salzmann U, Giesebrecht J, Kloetzel PM, Holzhutter HG. Kinetic evidences for facilitation of peptide channelling by the proteasome activator PA28. Eur J Biochem 267: 6221-6230, 2000.
138. Su H, Wang X. The ubiquitin-proteasome system in cardiac proteinopathy: a quality control perspective. Cardiovasc Res 85: 253-262, 2010.
139. 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 21: 224-228, 2011.
140. Sucharov CC. Beta-adrenergic pathways in human heart failure. Expert Rev Cardiovasc Ther 5: 119-124, 2007.
141. 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 107: 642-649, 2010.
142. Takagi H, Matsui Y, Sadoshima J. The role of autophagy in mediating cell survival and death during ischemia and reperfusion in the heart. Antioxid Redox Signal 9: 1373-1381, 2007.
143. Takamatsu H, Yamashita T, Kotani T, Sawazaki A, Okumura H, Nakao S. Ischemic heart disease associated with bortezomib treatment combined with dexamethasone in a patient with multiple myeloma. Int J Hematol 91: 903-906, 2010.
144. Taylor RG, Tassy C, Briand M, Robert N, Briand Y, Ouali A. Proteolytic activity of proteasome on myofibrillar structures. Mol Biol Rep 21: 71-73, 1995.
145. Tian Z, Zheng H, Li J, Li YF, Su H, Wang X. Genetically induced moderate inhibition of the proteasome in cardiomyocytes exacerbates myocardial ischemia-teperfusion injury in mice. Circ Res 111: 532-542, 2012.
146. Tisdale MJ. Pathogenesis of cancer cachexia. J Support Oncol 1: 159-168, 2003.
147. Um JW, Im E, Park J, Oh Y, Min B, Lee HJ, Yoon JB, Chung KC. ASK1 negatively regulates the 26 S proteasome. J Biol Chem 285: 36434-36446, 2010.
148. Ustrell V, Hoffman L, Pratt G, Rechsteiner M. PA200, a nuclear proteasome activator involved in DNA repair. EMBO J 21: 3516-3525, 2002.
149. van Wijk SJ, Timmers HT. The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J 24: 981-993, 2010.
150. Versari D, Herrmann J, Gossl M, Mannheim D, Sattler K, Meyer FB, Lerman LO, Lerman A. Dysregulation of the ubiquitin-proteasome system in human carotid atherosclerosis. Arterioscler Thromb Vasc Biol 26: 2132-2139, 2006.
151. Visekruna A, Joeris T, Seidel D, Kroesen A, Loddenkemper C, Zeitz M, Kaufmann SH, Schmidt-Ullrich R, Steinhoff U. Proteasome-mediated degradation of IkappaBalpha and processing of p105 in Crohn disease and ulcerative colitis. J Clin Invest 116: 3195-3203, 2006.
152. Voortman J, Giaccone G. Severe reversible cardiac failure after bortezomib treatment combined with chemotherapy in a non-small cell lung cancer patient: a case report. BMC Cancer 6: 129, 2006.
153. Vucic D, Dixit VM, Wertz IE. Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death. Nat Rev Mol Cell Biol 12: 439-452, 2011.
154. Wang D, Zong C, Koag MC, Wang Y, Drews O, Fang C, Scruggs SB, Ping P. Proteome dynamics and proteome function of cardiac 19S proteasomes. Mol Cell Proteomics 10: M110, 2011.
155. Wang X, Li J, Zheng H, Su H, Powell SR. Proteasome functional insufficiency in cardiac pathogenesis. Am J Physiol Heart Circ Physiol 301: H2207-H2219, 2011.
156. Wang X, Robbins J. Heart failure and protein quality control. Circ Res 99: 1315-1328, 2006.
157. Wenzel DM, Stoll KE, Klevit RE. E2s: structurally economical and functionally replete. Biochem J 433: 31-42, 2011.
158. Whitby FG, Masters EI, Kramer L, Knowlton JR, Yao Y, Wang CC, Hill CP. Structural basis for the activation of 20S proteasomes by 11S regulators. Nature 408: 115-120, 2000.
159. Williams AJ, Berti R, Dave JR, Elliot PJ, Adams J, Tortella FC. Delayed treatment of ischemia/reperfusion brain injury: extended therapeutic window with the proteosome inhibitor MLN519. Stroke 35: 1186-1191, 2004.
160. Williams AJ, Hale SL, Moffett JR, Dave JR, Elliott PJ, Adams J, Tortella FC. Delayed treatment with MLN519 reduces infarction and associated neurologic deficit caused by focal ischemic brain injury in rats via antiinflammatory mechanisms involving nuclear factor-kappaB activation, gliosis, and leukocyte infiltration. J Cereb Blood Flow Metab 23: 75-87, 2003.
161. Williams AJ, Myers TM, Cohn SI, Sharrow KM, Lu XC, Tortella FC. Recovery from ischemic brain injury in the rat following a 10 h delayed injection with MLN519. Pharmacol Biochem Behav 81: 182-189, 2005.
162. Willis MS, Schisler JC, Portbury AL, Patterson C. Build it up-tear it down: protein quality control in the cardiac sarcomere. Cardiovasc Res 81: 439-448, 2009.
163. 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 106: 463-478, 2010.
164. Yan L, Sadoshima J, Vatner DE, Vatner SF. Autophagy in ischemic preconditioning and hibernating myocardium. Autophagy 5: 709-712, 2009.
165. Young GW, Wang Y, Ping P. Understanding proteasome assembly and regulation: importance to cardiovascular medicine. Trends Cardiovasc Med 18: 93-98, 2008.
166. Young LH, Li J, Baron SJ, Russell RR. AMP-activated protein kinase: a key stress signaling pathway in the heart. Trends Cardiovasc Med 15: 110-118, 2005.
167. Yu X, Huang S, Patterson E, Garrett MW, Kaufman KM, Metcalf JP, Zhu M, Dunn ST, Kem DC. Proteasome degradation of GRK2 during ischemia and ventricular tachyarrhythmias in a canine model of myocardial infarction. Am J Physiol Heart Circ Physiol 289: H1960-H1967, 2005.
168. 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 282: 22460-22471, 2007.
169. Zhang Z, Krutchinsky A, Endicott S, Realini C, Rechsteiner M, Standing KG. Proteasome activator 11S REG or PA28: recombinant REG alpha/REG beta hetero-oligomers are heptamers. Biochemistry 38: 5651-5658, 1999.
170. Zheng Q, Su H, Ranek MJ, Wang X. Autophagy and p62 in cardiac proteinopathy. Circ Res 109: 296-308, 2011.
171. Zheng Q, Su H, Tian Z, Wang X. Proteasome malfunction activates macroautophagy in the heart. Am J Cardiovasc Dis 1: 214-226, 2011.
172. Zheng Q, Wang X. Autophagy and the ubiquitin-proteasome system in cardiac dysfunction. Panminerva Med 52: 9-25, 2010.
173. Zhou HJ, Aujay MA, Bennett MK, Dajee M, Demo SD, Fang Y, Ho MN, Jiang J, Kirk CJ, Laidig GJ, Lewis ER, Lu Y, Muchamuel T, Parlati F, Ring E, Shenk KD, Shields J, Shwonek PJ, Stanton T, Sun CM, Sylvain C, Woo TM, Yang J. Design and synthesis of an orally bioavailable and selective peptide epoxyketone proteasome inhibitor (PR-047). J Med Chem 52: 3028-3038, 2009.
174. Zimmerman ES, Schulman BA, Zheng N. Structural assembly of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 20: 714-721, 2010.
175. 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 99: 372-380, 2006.
176. Zong C, Young GW, Wang Y, Lu H, Deng N, Drews O, Ping P. Two-dimensional electrophoresis-based characterization of post-translational modifications of mammalian 20S proteasome complexes. Proteomics 8: 5025-5037, 2008.