Enhancement of 26S proteasome functionality connects oxidative stress and vascular endothelial inflammatory response in diabetes mellitus

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 9, 2012, Pages 2131-2140

  Liu, Hongtao ^a   Yu, Shujie ^a   Xu, Wenjia ^a,b   Xu, Jian ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b DUKE UNIVERSITY   (United States)

Author keywords

light chain enhancer of activated B cells; 26S proteasomes; diabetes mellitus; inflammatory response; nuclear factor; oxidative stress

Indexed keywords

26S PROTEASOME; 3 NITROTYROSINE; BENZYLOXYCARBONYLLEUCYLLEUCYLLEUCINAL; CHYMOTRYPSIN; GLUCOSE; GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MULTIPROTEIN COMPLEX; PEROXYNITRITE; PROTEASOME; PROTEASOME ACTIVATOR PROTEIN COMPLEX; SMALL INTERFERING RNA; SUPEROXIDE; TEMPOL; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; AUTOPHAGY; CELL NUCLEUS; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME ACTIVITY; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IN VIVO STUDY; KIDNEY PARENCHYMA; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REPORTER GENE; RETINA; UMBILICAL VEIN ENDOTHELIAL CELL; UNFOLDED PROTEIN RESPONSE; VASCULAR ENDOTHELIUM; VASCULITIS; WILD TYPE;

ANIMALS; BLOOD GLUCOSE; CELLS, CULTURED; CYSTEINE PROTEINASE INHIBITORS; DIABETES MELLITUS, EXPERIMENTAL; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; FREE RADICAL SCAVENGERS; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; OXIDATIVE STRESS; PEROXYNITROUS ACID; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA INTERFERENCE; TIME FACTORS; TYROSINE; UBIQUITINATION;

EID: 84865524171     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.253385     Document Type: Article

References (59)

1. King GL, Brownlee M. The cellular and molecular mechanisms of diabetic complications. Endocrinol Metab Clin North Am. 1996;25:255-270.
2. Giacco F, Brownlee M. Oxidative stress and diabetic complications. Circ Res. 2010;107:1058-1070.
3. Eizirik DL, Colli ML, Ortis F. The role of inflammation in insulitis and beta-cell loss in type 1 diabetes. Nat Rev Endocrinol. 2009;5:219-226.
4. Hotamisligil GS. Inflammation and endoplasmic reticulum stress in obesity and diabetes. Int J Obes (Lond). 2008;32 Suppl 7:S52-S54.
5. Wellen KE, Hotamisligil GS. Inflammation, stress, and diabetes. J Clin Invest. 2005;115:1111-1119.
6. Schwartz AL, Ciechanover A. The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu Rev Med. 1999;50:57-74.
7. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem. 1998;67:425-479.
8. Hershko A, Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992;61:761-807.
9. Castro A, Bernis C, Vigneron S, Labbé JC, Lorca T. The anaphase-promoting complex: a key factor in the regulation of cell cycle. Oncogene. 2005;24:314-325.
10. Hershko A. Roles of ubiquitin-mediated proteolysis in cell cycle control. Curr Opin Cell Biol. 1997;9:788-799.
11. Goldberg AL, Cascio P, Saric T, Rock KL. The importance of the proteasome and subsequent proteolytic steps in the generation of antigenic peptides. Mol Immunol. 2002;39:147-164.
12. 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. 1996;381:166-168.
13. Orlowski RZ. The role of the ubiquitin-proteasome pathway in apoptosis. Cell Death Differ. 1999;6:303-313.
14. Desterro JM, Rodriguez MS, Hay RT. Regulation of transcription factors by protein degradation. Cell Mol Life Sci. 2000;57:1207-1219.
15. Fuchs SY, Fried VA, Ronai Z. Stress-activated kinases regulate protein stability. Oncogene. 1998;17:1483-1490.
16. Edwards CM, Lwin ST, Fowler JA, Oyajobi BO, Zhuang J, Bates AL, Mundy GR. Myeloma cells exhibit an increase in proteasome activity and an enhanced response to proteasome inhibition in the bone marrow microenvironment in vivo. Am J Hematol. 2009;84:268-272.
17. Bence NF, Sampat RM, Kopito RR. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 2001;292:1552-1555.
18. Ciechanover A, Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron. 2003;40:427-446.
19. Cheroni C, Marino M, Tortarolo M, Veglianese P, De Biasi S, Fontana E, Zuccarello LV, Maynard CJ, Dantuma NP, Bendotti C. Functional alterations of the ubiquitin-proteasome system in motor neurons of a mouse model of familial amyotrophic lateral sclerosis. Hum Mol Genet. 2009;18:82-96.
20. Hershko A, Ciechanover A, Varshavsky A. Basic Medical Research Award. The ubiquitin system. Nat Med. 2000;6:1073-1081.
21. Herrmann J, Ciechanover A, Lerman LO, Lerman A. The ubiquitin-proteasome system in cardiovascular diseases-a hypothesis extended. Cardiovasc Res. 2004;61:11-21.
22. Yu X, Patterson E, Kem DC. Targeting proteasomes for cardioprotection. Curr Opin Pharmacol. 2009;9:167-172.
23. Divald A, Powell SR. Proteasome mediates removal of proteins oxidized during myocardial ischemia. Free Radic Biol Med. 2006;40:156-164.
24. Stansfield WE, Moss NC, Willis MS, Tang R, Selzman CH. Proteasome inhibition attenuates infarct size and preserves cardiac function in a murine model of myocardial ischemia-reperfusion injury. Ann Thorac Surg. 2007;84:120-125.
25. Gao Y, Lecker S, Post MJ, Hietaranta AJ, Li J, Volk R, Li M, Sato K, Saluja AK, Steer ML, Goldberg AL, Simons M. Inhibition of ubiquitin-proteasome pathway-mediated I kappa B alpha degradation by a naturally occurring antibacterial peptide. J Clin Invest. 2000;106:439-448.
26. Herrmann J, Soares SM, Lerman LO, Lerman A. Potential role of the ubiquitin-proteasome system in atherosclerosis: aspects of a protein quality disease. J Am Coll Cardiol. 2008;51:2003-2010.
27. Marfella R, D'Amico M, Esposito K, et al. The ubiquitin-proteasome system and inflammatory activity in diabetic atherosclerotic plaques: effects of rosiglitazone treatment. Diabetes. 2006;55:622-632.
28. Xu J, Wu Y, Song P, Zhang M, Wang S, Zou MH. Proteasome-dependent degradation of guanosine 5'-triphosphate cyclohydrolase I causes tetrahydrobiopterin deficiency in diabetes mellitus. Circulation. 2007;116:944-953.
29. 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.
30. Whitsett J, Picklo MJ Sr, Vasquez-Vivar J. 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation. Arterioscler Thromb Vasc Biol. 2007;27:2340-2347.
31. Queisser MA, Yao D, Geisler S, Hammes HP, Lochnit G, Schleicher ED, Brownlee M, Preissner KT. Hyperglycemia impairs proteasome function by methylglyoxal. Diabetes. 2010;59:670-678.
32. Dantuma NP, Lindsten K, Glas R, Jellne M, Masucci MG. Short-lived green fluorescent proteins for quantifying ubiquitin/proteasome-dependent proteolysis in living cells. Nat Biotechnol. 2000;18:538-543.
33. Lindsten K, Menéndez-Benito V, Masucci MG, Dantuma NP. A transgenic mouse model of the ubiquitin/proteasome system. Nat Biotechnol. 2003;21:897-902.
34. Luker GD, Pica CM, Song J, Luker KE, Piwnica-Worms D. Imaging 26S proteasome activity and inhibition in living mice. Nat Med. 2003;9:969-973.
35. Lindsten K, de Vrij FM, Verhoef LG, Fischer DF, van Leeuwen FW, Hol EM, Masucci MG, Dantuma NP. Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J Cell Biol. 2002;157:417-427.
36. Bowman AB, Yoo SY, Dantuma NP, Zoghbi HY. Neuronal dysfunction in a polyglutamine disease model occurs in the absence of ubiquitin-proteasome system impairment and inversely correlates with the degree of nuclear inclusion formation. Hum Mol Genet. 2005;14:679-691.
37. Xu J, Xie Z, Reece R, Pimental D, Zou MH. Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: role of NAD(P)H oxidase-derived superoxide and peroxynitrite. Arterioscler Thromb Vasc Biol. 2006;26:2688-2695.
38. Wang S, Xu J, Song P, Wu Y, Zhang J, Chul Choi H, Zou MH. Acute inhibition of guanosine triphosphate cyclohydrolase 1 uncouples endothelial nitric oxide synthase and elevates blood pressure. Hypertension. 2008;52:484-490.
39. Saccani S, Pantano S, Natoli G. Two waves of nuclear factor kappaB recruitment to target promoters. J Exp Med. 2001;193:1351-1359.
40. Geng H, Wittwer T, Dittrich-Breiholz O, Kracht M, Schmitz ML. Phosphorylation of NF-kappaB p65 at Ser468 controls its COMMD1-dependent ubiquitination and target gene-specific proteasomal elimination. EMBO Rep. 2009;10:381-386.
41. Szabó C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov. 2007;6:662-680.
42. Dikalova AE, Bikineyeva AT, Budzyn K, Nazarewicz RR, McCann L, Lewis W, Harrison DG, Dikalov SI. Therapeutic targeting of mitochondrial superoxide in hypertension. Circ Res. 2010;107:106-116.
43. Hsueh W, Abel ED, Breslow JL, Maeda N, Davis RC, Fisher EA, Dansky H, McClain DA, McIndoe R, Wassef MK, Rabadán-Diehl C, Goldberg IJ. Recipes for creating animal models of diabetic cardiovascular disease. Circ Res. 2007;100:1415-1427.
44. Xu J, Zou MH. Molecular insights and therapeutic targets for diabetic endothelial dysfunction. Circulation. 2009;120:1266-1286.
45. Stocker R, Keaney JF Jr. Role of oxidative modifications in atherosclerosis. Physiol Rev. 2004;84:1381-1478.
46. Traenckner EB, Wilk S, Baeuerle PA. A proteasome inhibitor prevents activation of NF-kappa B and stabilizes a newly phosphorylated form of I kappa B-alpha that is still bound to NF-kappa B. EMBO J. 1994;13:5433-5441.
47. Esteve-Rudd J, Campello L, Herrero MT, Cuenca N, Martín-Nieto J. Expression in the mammalian retina of parkin and UCH-L1, two components of the ubiquitin-proteasome system. Brain Res. 2010;1352:70-82.
48. Sun SC, Ganchi PA, Ballard DW, Greene WC. NF-kappa B controls expression of inhibitor I kappa B alpha: evidence for an inducible autoregulatory pathway. Science. 1993;259:1912-1915.
49. Ishida Y, Kimura A, Kuninaka Y, Inui M, Matsushima K, Mukaida N, Kondo T. Pivotal role of the CCL5/CCR5 interaction for recruitment of endothelial progenitor cells in mouse wound healing. J Clin Invest. 2012;122:711-721.
50. Longo CR, Arvelo MB, Patel VI, Daniel S, Mahiou J, Grey ST, Ferran C. A20 protects from CD40-CD40 ligand-mediated endothelial cell activation and apoptosis. Circulation. 2003;108:1113-1118.
51. Di Filippo C, Marfella R, D'Amico M. Possible dual role of ubiquitin-proteasome system in the atherosclerotic plaque progression. J Am Coll Cardiol. 2008;52:1350-1351; author reply 1351.
52. Jung T, Catalgol B, Grune T. The proteasomal system. Mol Aspects Med. 2009;30:191-296.
53. Sukhanov S, Semprun-Prieto L, Yoshida T, Michael Tabony A, Higashi Y, Galvez S, Delafontaine P. Angiotensin II, oxidative stress and skeletal muscle wasting. Am J Med Sci. 2011;342:143-147.
54. Fernandes R, Hosoya K, Pereira P. Reactive oxygen species downregulate glucose transport system in retinal endothelial cells. Am J Physiol, Cell Physiol. 2011;300:C927-C936.
55. Leng S, Zhang W, Zheng Y, Liberman Z, Rhodes CJ, Eldar-Finkelman H, Sun XJ. Glycogen synthase kinase 3 beta mediates high glucose-induced ubiquitination and proteasome degradation of insulin receptor substrate 1. J Endocrinol. 2010;206:171-181.
56. Sun X, Fratz S, Sharma S, et al. C-terminus of heat shock protein 70-interacting protein-dependent GTP cyclohydrolase I degradation in lambs with increased pulmonary blood flow. Am J Respir Cell Mol Biol. 2011;45:163-171.
57. Lefebvre B, Benomar Y, Guédin A, Langlois A, Hennuyer N, Dumont J, Bouchaert E, Dacquet C, Pénicaud L, Casteilla L, Pattou F, Ktorza A, Staels B, Lefebvre P. Proteasomal degradation of retinoid X receptor alpha reprograms transcriptional activity of PPARgamma in obese mice and humans. J Clin Invest. 2010;120:1454-1468.
58. Todd JA, Wicker LS. Genetic protection from the inflammatory disease type 1 diabetes in humans and animal models. Immunity. 2001;15:387-395.
59. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11:98-107.