Physiological and pathological role of the ubiquitinproteasome system in the vascular smooth muscle cell

Cardiovascular Research

Volumn 95, Issue 2, 2012, Pages 183-193

  Demasi, Marilene ^a   Laurindo, Francisco R M ^b  

^a INSTITUTO BUTANTAN   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Endoplasmic reticulum stress; Proteolysis; Redox processes; Ubiquitinproteasome system; Vascular smooth muscle cells

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEASOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; UBIQUITIN; UBIQUITIN PROTEIN LIGASE;

APOPTOSIS; ATHEROSCLEROSIS; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SMOOTH MUSCLE FIBER; UBIQUITINATION; VASCULAR SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE CELL;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; HUMANS; MYOCYTES, SMOOTH MUSCLE; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84863655856     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvs128     Document Type: Review

References (105)

1. Majesky MW. Developmental basis of vascular smooth muscle diversity. Arterioscler Thromb Vasc Biol 2007;27:1248-1258. (Pubitemid 46809412)
2. Kültz D. Molecular and evolutionary basis of the cellular stress response. Annu Rev Physiol 2005;67:225-257. (Pubitemid 40404492)
3. Dahlmann B. Role of proteasomes in disease. BMC Biochem 2007;8(Suppl. 1):S3.
4. Kuhn JD, Orlowski ZR, Bjorklund CC. Second generation proteasome inhibitors: carfilzomib and immunoproteasome-specific inhibitors (IPSIs). Curr Cancer Drug Targets 2011;11:285-295.
5. Bedford L, Lowe J, Dick LR, Mayer RJ, Brownell JE. Ubiquitin-like protein conjugation and the ubiquitin-proteasome system as drug targets. Nat Rev Drug Disc 2011;10: 29-46.
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. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007;315:201-205. (Pubitemid 46166358)
8. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002;82:373-428. (Pubitemid 34654457)
9. Schwartz AL, Ciechanover A. Targeting proteins for destruction by the ubiquitin system: implications for human pathobiology. Annu Rev Pharmacol Toxicol 2009;49: 73-96.
10. Reyes-Turcu FE, Ventii KH, Wilkinson KD. Regulation and cellular roles of ubiquitinspecific deubiquitinating enzymes. Annu Rev Biochem 2009;78:363-397.
11. Varshavsky A. The N-end rule pathway and regulation by proteolysis. Protein Sci 2011;20:1298-1345.
12. Jung T, Catalgol B, Grune T. The proteasomal system. Mol Aspects Med 2009;30: 191-296.
13. Kriegenburg F, Poulsen EG, Koch A, Krüger E, Hartmann-Petersen R. Redox control of the ubiquitin-proteasome system: from molecular mechanisms to functional significance. Antioxid Redox Signal 2011;15:2265-2299.
14. Gomes AV, Zong C, Edmondson RD, Li X, Stefani E, Zhang J et al. Mapping the murine cardiac 26S proteasome complexes. Circ Res 2006;99:362-371. (Pubitemid 44253692)
15. Demasi M, Shringarpure R, Davies KJ. Glutathiolation of the proteasome is enhanced by proteolytic inhibitors. Arch Biochem Biophys 2001;389:254-263. (Pubitemid 32881951)
16. Carrard G, Dieu M, Raes M, Toussaint O, Friguet B. Impact of ageing on proteasome structure and function in human lymphocytes. Int J Biochem Cell Biol 2003;35: 728-739. (Pubitemid 36369520)
17. Asai M, Tsukamoto O, Minamino T, Asanuma H, Fujita M, Asano Y et al. PKA rapidly enhances proteasome assembly and activity in in vivo canine hearts. J Mol Cell Cardiol 2009;46:452-462.
18. Sixt SU, Dahlmann B. Extracellular, circulating proteasomes and ubiquitin-incidence and relevance. Biochim Biophys Acta 2008;1782:817-823.
19. Orlowski M, Wilk S. Ubiquitin-independent proteolytic functions of the proteasome. Arch Biochem Biophys 2003;415:1-5. (Pubitemid 36687910)
20. Baugh JM, Viktorova EG, Pilipenko EVJ. Proteasomes can degrade a significant proportion of cellular proteins independent of ubiquitylation. Mol Biol 2009;386: 814-827.
21. Davies KJ. Degradation of oxidized proteins by the 20S proteasome. Biochimie 2001; 83:301-310. (Pubitemid 32293650)
22. Shringapure R, Grune T, Mehlhase J, Davies KJ. Ubiquitin conjugation is not required for the degradation of oxidized proteins by proteasome. J Biol Chem 2003;278: 311-318. (Pubitemid 36043578)
23. Stadtman ER. Protein oxidation and aging. Free Radic Res 2006;40:1250-1258. (Pubitemid 44698274)
24. Adam PJ, Weissberg PL, Cary NR, Shanahan CM. Polyubiquitin is a new phenotypic marker of contractile vascular smooth muscle cells. Cardiovasc Res 1997;33: 416-421. (Pubitemid 27072647)
25. Thyberg J, Blomgren K. Effects of proteasome and calpain inhibitors on the structural reorganization and proliferation of vascular smooth muscle cells in primary culture. Lab Invest 1999;79:1077-1088. (Pubitemid 29444538)
26. Bond M, Wu YJ. Proliferation unleashed: the role of Skp2 in vascular smooth muscle cell proliferation. Front Biosci 2011;16:1517-1535.
27. Carrano AC, Eytan E, Hershko A, Pagano M. SKP2 is required for ubiquitinmediated degradation of the CDK inhibitor p27. Nat Cell Biol 1999;1:193-199. (Pubitemid 129500937)
28. Barringhaus KG, Matsumura ME. The proteasome inhibitor lactacystin attenuates growth and migration of vascular smooth muscle cells and limits the response to arterial injury. Exp Clin Cardiol 2007;12:119-24. (Pubitemid 47526936)
29. Wu YJ, Bond M, Sala-Newby GB, Newby AC. Altered S-phase kinase-associated protein-2 levels are a major mediator of cyclic nucleotide-induced inhibition of vascular smooth muscle cell proliferation. Circ Res 2006;98:1141-1150. (Pubitemid 43948100)
30. Wu YJ, Sala-Newby GB, Shu KT, Yeh HI, Nakayama KI, Nakayama K et al. S-phase kinase-associated protein-2 (Skp2) promotes vascular smooth muscle cell proliferation and neointima formation in vivo. J Vasc Surg 2009;50:1135-1142.
31. Kitagawa K, Kotake Y, Kitagawa M. Ubiquitin-mediated control of oncogene and tumor suppressor gene products. Cancer Sci 2009;100:1374-1381.
32. Bond M, Wu YJ, Sala-Newby GB, Newby AC. Rho GTPase, Rac1, regulates Skp2 levels, vascular smooth muscle cell proliferation, and intima formation in vitro and in vivo. Cardiovasc Res 2008;80:290-298.
33. Gizard F, Zhao Y, Findeisen HM, Qing H, Cohn D, Heywood EB et al. Transcriptional regulation of the S-Phase kinase-associated protein 2 by the NR4A orphan nuclear receptor NOR1 in vascular smooth muscle cells. J Biol Chem 2011;286: 35485-35493.
34. Song P, Wang S, He C, Wang S, Liang B, Viollet B et al. AMPKa2 deletion exacerbates neointima formation by upregulating Skp2 in vascular smooth muscle cells. Circ Res 2011;109:1230-1239.
35. Hernández-Negrete I, Sala-Newby GB, Perl A, Kunkel GR, Newby AC, Bond M. Adhesion-dependent Skp2 transcription requires selenocysteine tRNA gene transcription-activating factor (STAF). Biochem J 2011;436:133-143.
36. Xie P, Fan Y, Zhang H, Zhang Y, She M, Gu D et al. CHIP represses myocardin-induced smooth muscle cell differentiation via ubiquitin-mediated proteasomal degradation. Mol Cell Biol 2009;29:2398-2408.
37. Li F, Xie P, Fan Y, Zhang H, Zheng L, Gu D et al. C terminus of Hsc70-interacting protein promotes smooth muscle cell proliferation and survival through ubiquitinmediated degradation of FoxO1. J Biol Chem 2009;284:20090-20098.
38. Murata S, Chiba T, Tanaka K. CHIP: a quality-control E3-ligase collaborating with molecular chaperones. Intl J Biochem Cell Biol 2003;35:572-578. (Pubitemid 36369506)
39. Venugopal R, Jaiswal AK. Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 1998;17:3145-3156. (Pubitemid 29020810)
40. Fribley A, Zeng Q, Wang CY. Proteasome inhibitor PS-341 induces apoptosis through induction of endoplasmic reticulum stress-reactive oxygen species in head and neck squamous cell carcinoma cells. Mol Cell Biol 2004;24:9695-9704. (Pubitemid 39458799)
41. Sullivan PG, Dragicevic NB, Deng JH, Bai Y, Dimayuga E, Ding Q et al. Proteasome inhibition alters neural mitochondrial homeostasis and mitochondria turnover. J Biol Chem 2004;279:20699-20707. (Pubitemid 38656466)
42. Yamamoto N, Sawada H, Izumi Y, Kume T, Katsuki H, Shimohama S et al. Proteasome inhibition induces glutathione synthesis and protects cells from oxidative stress: relevance to Parkinson disease. J Biol Chem 2007;282:4364-4372. (Pubitemid 47101000)
43. Shang F, Taylor A. Oxidative stress and recovery from oxidative stress are associated with altered ubiquitin conjugating and proteolytic activities in bovine lens epithelial cells. Biochem J 1995;307:297-303.
44. Shang F, Gong X, Taylor A. Activity of ubiquitin-dependent pathway in response to oxidative stress. Ubiquitin-activating enzyme is transiently up-regulated. J Biol Chem 1997;272:23086-23093. (Pubitemid 27392436)
45. Jahngen-Hodge J, Obin MS, Gong X, Shang F, Nowell TR Jr, Gong J et al. Regulation of ubiquitinconjugating enzymes by glutathione following oxidative stress. J Biol Chem 1997;272:28218-28226. (Pubitemid 27517760)
46. Cunha FM, Demasi M, Kowaltowski AJ. Aging and calorie restriction modulate yeast redox state, oxidized protein removal, and the ubiquitin-proteasome system. Free Radic Biol Med 2011;51:664-670.
47. Lassegue B, Griendling KK. NADPH oxidases: functions and pathologies in the vasculature. Arterioscler Thromb Vasc Biol 2010;30:653-661.
48. Janiszewski M, Lopes LR, Carmo AO, Pedro MA, Brandes RP, Santos CJ et al. Regulation of NAD(P)H oxidase by associated protein disulfide isomerase in vascular smooth muscle cells. J Biol Chem 2005;280:40813-40819. (Pubitemid 41780573)
49. Fernandes DC, Manoel AH, Wosniak J Jr, Laurindo FR. Protein disulfide isomerase overexpression in vascular smooth muscle cells induces spontaneous preemptive NADPH oxidase activation and Nox1 mRNA expression: effects of nitrosothiol exposure. Arch Biochem Biophys 2009;484:197-204.
50. Santos CX, Tanaka LY, Wosniak J, Laurindo FR. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 2009;11:2409-2427.
51. Block K, Gorin Y, Hoover P, Williams P, Chelmicki T, Clark RA et al. NAD(P)H oxidases regulate HIF-2alpha protein expression. J Biol Chem 2007;282:8019-8026. (Pubitemid 47093603)
52. Kovacic HN, Irani K, Goldschmidt-Clermont PJ. Redox regulation of human Rac1 stability by the proteasome in human aortic endothelial cells. J Biol Chem 2001; 276:45856-45861.
53. Musial A, Eissa NT. Inducible nitric-oxide synthase is regulated by the proteasome degradation pathway. J Biol Chem 2001;276:24268-24273.
54. Stangl V, Lorenz M, Meiners S, Ludwig A, Bartsch C, Moobed M et al. Long-term up-regulation of eNOS and improvement of endothelial function by inhibition of the ubiquitin-proteasome pathway. FASEB J 2004;18:272-279. (Pubitemid 38186246)
55. Cokic VP, Beleslin-Cokic BB, Noguchi CT, Schechter AN. Hydroxyurea increases eNOS protein levels through inhibition of proteasome activity. Nitric Oxide 2007; 16:371-378. (Pubitemid 46541670)
56. Kibbe MR, Li J, Nie S, Watkins SC, Lizonova A, Kovesdi I et al. Inducible nitric oxide synthase (iNOS) expression upregulates p21 and inhibits vascular smooth muscle cell proliferation through p42/44 mitogen-activated protein kinase activation and independent of p53 and cyclic guanosine monophosphate. J Vasc Surg 2000;31: 1214-1228. (Pubitemid 30418493)
57. Kapadia MR, Eng JW, Jiang Q, Stoyanovsky DA, Kibbe MR. Nitric oxide regulates the 26S proteasome in vascular smooth muscle cells. Nitric Oxide 2009;20:279-288.
58. Tsihlis ND, Oustwani CS, Vavra AK, Jiang Q, Keefer LK, Kibbe MR. Nitric oxide inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia by increasing the ubiquitination and degradation of UbcH10. Cell Biochem Biophys 2011;60: 89-97.
59. Oustwani CS, Tsihlis ND, Vavra AK, Jiang Q, Martinez J, Kibbe MR. Nitric oxide increases lysine 48-linked ubiquitination following arterial injury. J Surg Res 2011; 170:e169-e177.
60. Kaluz S, Kaluzova M, Stanbridge EJ. Does inhibition of degradation of hypoxia-inducible factor (HIF) always lead to activation of HIF? Lessons learnt from the effect of proteasomal inhibition on HIF activity. J Cell Biochem 2008;104: 536-544. (Pubitemid 351671642)
61. Brüne B, Zhou J. Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc Res 2007;75:275-282. (Pubitemid 46961919)
62. Bhat KP, Greer SF. Proteolytic and non-proteolytic roles of ubiquitin and the ubiquitin proteasome system in transcriptional regulation. Biochim Biophys Acta 2011;1809: 150-155.
63. Kodadek T. No Splicing, no dicing: non-proteolytic roles of the ubiquitinproteasome system in transcription. J Biol Chem 2010;285:2221-2226.
64. Yin H, Jiang Y, Li H, Li J, Gui Y, Zheng XL. Proteasomal degradation of myocardin is required for its transcriptional activity in vascular smooth muscle cells. J Cell Physiol 2011;226:1897-1906.
65. Karin M, Ben-Neriah Y. Phosphorylation meets ubiquitination: the control of NF-[kappa]B activity. Annu Rev Immunol 2000;18:621-663. (Pubitemid 30365393)
66. Souza HP, Souza LC, Anastacio VM, Pereira AC, Junqueira ML, Krieger JE et al. Vascular oxidant stress early after balloon injury: evidence for increased NAD(P)H oxidoreductase activity. Free Radic Biol Med 2000;28:1232-1242. (Pubitemid 30417466)
67. Oliver KM, Taylor CT, Cummins EP. Hypoxia. Regulation of NFkappaB signalling during inflammation: the role of hydroxylases. Arthritis Res Ther 2009;11:215-222.
68. Takami Y, Nakagami H, Morishita R, Katsuya T, Hayashi H, Mori M et al. Potential role of CYLD (cylindromatosis) as a deubiquitinating enzyme in vascular cells. Am J Pathol 2008;172:818-829. (Pubitemid 351354553)
69. Merk DR, Chin JT, Dake BA, Maegdefessel L, Miller MO, Kimura N et al. miR-29b Participates in early aneurysm development in Marfan syndrome. Circ Res 2012; 110:312-324.
70. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 2007;8:519-529. (Pubitemid 46985379)
71. Marciniak SJ, Ron D. Endoplasmic reticulum stress signaling in disease. Physiol Rev 2006;86:1133-1149. (Pubitemid 44521649)
72. Zhang K, Kaufman RJ. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008;454:455-462.
73. Tabas I, Ron D. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 2011;13:184-190.
74. Wu RF, Ma Z, Liu Z, Terada LS. Nox4-derived H2O2 mediates endoplasmic reticulum signaling through local Ras activation. Mol Cell Biol 2010;30:3553-3568.
75. Pedruzzi E, Guichard C, Ollivier V, Driss F, Fay M, Prunet C et al. NAD(P)H oxidase Nox-4 mediates 7-ketocholesterol-induced endoplasmic reticulum stress and apoptosis in human aortic smooth muscle cells. Mol Cell Biol 2004;24:10703-10717. (Pubitemid 39603128)
76. Bernasconi R, Molinari M. ERAD and ERAD tuning: disposal of cargo and of ERAD regulators from the mammalian ER. Curr Opin Cell Biol 2011;23:176-183.
77. Bagola K, Mehnert M, Jarosch E, Sommer T. Protein dislocation from the ER. Biochim Biophys Acta 2011;1808:925-936.
78. McConkey DJ, Zhu K. Mechanisms of proteasome inhibitor action and resistance in cancer. Drug Resist Updat 2008;11:164-179.
79. Meiners S, Laule M, Rother W, Guenther C, Prauka I, Muschick P et al. Ubiquitinproteasome pathway as a new target for the prevention of restenosis. Circulation 2002;105:483-489. (Pubitemid 34141706)
80. Van Herck JL, De Meyer GR, Martinet W, Bult H, Vrints CJ, Herman AG. Proteasome inhibitor bortezomib promotes a rupture-prone plaque phenotype in ApoEdeficient mice. Basic Res Cardiol 2010;105:39-50.
81. Amanso AM, Debbas V, Laurindo FR. Proteasome inhibition represses unfolded protein response and Nox4, sensitizing vascular cells to endoplasmic reticulum stress-induced death. PLoS One 2011;6:e14591.
82. Wang Q, Mora-Jensen H, Weniger MA, Perez-Galan P, Wolford C, Hai T et al. ERAD inhibitors integrate ER stress with an epigenetic mechanism to activate BH3-only protein NOXA in cancer cells. Proc Natl Acad Sci USA 2009;106: 2200-2205.
83. Bhat UG, Halasi M, Gartel AL. FoxM1 is a general target for proteasome inhibitors. PLoS One 2009;4:e6593.
84. Gray DC, Mahrus S,Wells JA. Activation of specific apoptotic caspases with an engineered small-molecule-activated protease. Cell 2010;142:637-646.
85. Egger L, Madden DT, Rheme C, Rao RV, Bredesen DE. Endoplasmic reticulum stress-induced cell death mediated by the proteasome. Cell Death Differ 2007;14: 1172-1180. (Pubitemid 46785108)
86. Lee AH, Iwakoshi NN, Anderson KC, Glimcher LH. Proteasome inhibitors disrupt the unfolded protein response in myeloma cells. Proc Natl Acad Sci USA 2003;100: 9946-9951. (Pubitemid 37087048)
87. Ding WX, Ni HM, GaoW, Yoshimori T, Stolz DB, Ron D et al. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007;171:513-524. (Pubitemid 47344684)
88. Dreger H, Westphal K, Wilck N, Baumann G, Stangl V, Stangl K et al. Protection of vascular cells from oxidative stress by proteasome inhibition depends on Nrf2. Cardiovasc Res 2010;85:395-403.
89. Lin PH, Chiang MT, Chau LY. Ubiquitin-proteasome system mediates heme oxygenase-1 degradation through endoplasmic reticulum-associated degradation pathway. Biochim Biophys Acta 2008;1783:1826-1834.
90. Myoishi M, Hao H, Minamino T, Watanabe K, Nishihira K, Hatakeyama K et al. Increased endoplasmic reticulum stress in atherosclerotic plaques associated with acute coronary syndrome. Circulation 2007;116:1226-1233. (Pubitemid 47517533)
91. Chade AR, Herrmann J, Zhu X, Krier JD, Lerman A, Lerman LO. Effects of proteasome inhibition on the kidney in experimental hypercholesterolemia. J Am Soc Nephrol 2005;16:1005-1012. (Pubitemid 41710311)
92. Feng B, Zhang Y, Mu J, Ye Z, Zeng W, Qi Wet al. Preventive effect of a proteasome inhibitor on the formation of accelerated atherosclerosis in rabbits with uremia. J Cardiovasc Pharmacol 2010;55:129-138.
93. Xu J,Wang S, Wu Y, Song P, Zou MH. Tyrosine nitration of PA700 activates the 26S proteasome to induce endothelial dysfunction in mice with angiotensin II-induced hypertension. Hypertension 2009;54:625-632.
94. Tanioka T, Tamura Y, Fukaya M, Shinozaki S, Mao J, Kim M et al. Inducible nitricoxide synthase and nitric oxide donor decrease insulin receptor substrate-2 protein expression by promoting proteasome-dependent degradation in pancreatic beta-cells: involvement of glycogen synthase kinase-3beta. J Biol Chem 2011;286: 29388-29396.
95. Ogura M, Ayaori M, Terao Y, Hisada T, Iizuka M, Takiguchi S et al. Proteasomal inhibition promotes ATP-binding cassette transporter A1 (ABCA1) and ABCG1 expression and cholesterol efflux from macrophages in vitro and in vivo. Arterioscler Thromb Vasc Biol 2011;31:1980-1987.
96. Yu H, Clarke MC, Figg N, Littlewood TD, Bennett MR. Smooth muscle cell apoptosis promotes vessel remodeling and repair via activation of cell migration, proliferation, and collagen synthesis. Arterioscler Thromb Vasc Biol 2011;31:2402-2409.
97. Herrmann J, Saguner AM, Versari D, Peterson TE, Chade A, Olson M et al. Chronic proteasome inhibition contributes to coronary atherosclerosis. Circ Res 2007;101: 865-874. (Pubitemid 350287173)
98. Ludwig A, Meiners S. Targeting of the proteasome worsens atherosclerosis? Circ Res 2008;102:e37. (Pubitemid 351271660)
99. Lee MJ, Pal K, Tasaki T, Roy S, Jiang Y, An JY et al. Synthetic heterovalent inhibitors targeting recognition E3 components of the N-end rule pathway. Proc Natl Acad Sci USA 2008;105:100-105.
100. Katsiki M, Chondrogianni N, Chinou I, Rivett AJ, Gonos ES. The olive constituent oleuropein exhibits proteasome stimulatory properties in vitro and confers life span extension of human embryonic fibroblasts. Rejuvenation Res 2007;10:157-172. (Pubitemid 46944984)
101. Chondrogianni N, Tzavelas C, Pemberton AJ, Nezis IP, Rivett AJ, Gonos ES. Overexpression of proteasome beta 5 subunit increases the amount of assembled proteasome and confers ameliorated response to oxidative stress and higher survival rates. J Biol Chem 2005;280:11840-11850. (Pubitemid 40418498)
102. Tan C, Li Y, Tan X, Pan H, Huang W. Inhibition of the ubiquitin-proteasome system: a new avenue for atherosclerosis. Clin Chem Lab Med 2006;44:1218-1225. (Pubitemid 44580804)
103. Chang TL. Inhibitory effect of flavonoids on 26S proteasome activity. J Agric Food Chem 2009;57:9706-9715.
104. Pashevin DA, Tumanovska LV, Dosenko VE, Nagibin VS, Gurianova VL, Moibenko AA. Antiatherogenic effect of quercetin is mediated by proteasome inhibition in the aorta and circulating leukocytes. Pharmacol Rep 2011;63:1009-1018.
105. Meister S, Frey B, Lang VR, Gaipl US, Schett G, Schlötzer-Schrehardt U et al. Calcium channel blocker verapamil enhances endoplasmic reticulum stress and cell death induced by proteasome inhibition in myeloma cells. Neoplasia 2010;12: 550-561.