Regulation of the endothelial cell cycle by the ubiquitin-proteasome system

Cardiovascular Research

Volumn 85, Issue 2, 2010, Pages 272-280

  Fasanaro, Pasquale ^a   Capogrossi, Maurizio C ^a   Martelli, Fabio ^a  

^a LABORATORIO DI PATOLOGIA VASCOLARE   (Italy)

Author keywords

Cell cycle; Endothelium; Oxidative stress; Proteasome; Ubiquitin

Indexed keywords

ANAPHASE PROMOTING COMPLEX; PROTEIN P53; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR NRF2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3;

CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; DOWN REGULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME REGULATION; HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW;

ANIMALS; CARDIOVASCULAR DISEASES; CELL CYCLE; ENDOTHELIAL CELLS; HUMANS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTEASOME ENDOPEPTIDASE COMPLEX; SKP CULLIN F-BOX PROTEIN LIGASES; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN; UBIQUITIN-PROTEIN LIGASE COMPLEXES;

EID: 72949097617     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp244     Document Type: Review

References (119)

1. Besson A, Dowdy SF, Roberts JM. CDK inhibitors: cell cycle regulators and beyond. Dev Cell 2008;14:159-169.
2. Paul S. Dysfunction of the ubiquitin-proteasome system in multiple disease conditions: therapeutic approaches. Bioessays 2008;30:1172-1184.
3. Marques AJ, Palanimurugan R, Matias AC, Ramos PC, Dohmen RJ. Catalytic mechanism and assembly of the proteasome. Chem Rev 2009;109:1509-1536.
4. Hershko A. The ubiquitin system for protein degradation and some of its roles in the control of the cell division cycle. Cell Death Differ 2005;12:1191-1197. (Pubitemid 41195103)
5. Ciechanover A. Proteolysis: from the lysosome to ubiquitin and the proteasome. Nat Rev Mol Cell Biol 2005;6:79-87.
6. Mukhopadhyay D, Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007;315:201-205.
7. Huzil JT, Pannu R, Ptak C, Garen G, Ellison MJ. Direct catalysis of lysine 48-linked polyubiquitin chains by the ubiquitin-activating enzyme. J Biol Chem 2007;282: 37454-37460.
8. Verma R, Aravind L, Oania R, McDonald WH, Yates JR III, Koonin EV et al Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S pro-teasome. Science 2002;298:611-615.
9. Jin L, Williamson A, Banerjee S, Philipp I, Rape M. Mechanism of ubiquitin-chain formation by the human anaphase-promoting complex. Cell 2008;133:653-665.
10. Wang B, Elledge SJ. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci USA 2007;104:20759-20763.
11. Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A. Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 2006;21:737-748.
12. Xu P, Duong DM, Seyfried NT, Cheng D, Xie Y, Robert J et al Quantitative pro-teomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009;137:133-145.
13. Yeh ET. SUMOylation and De-SUMOylation: wrestling with life's processes. J Biol Chem 2009;284:8223-8227.
14. Gutierrez GJ, Ronai Z. Ubiquitin and SUMO systems in the regulation of mitotic checkpoints. Trends Biochem Sci 2006;31:324-332.
15. Wickliffe K, Williamson A, Jin L, Rape M. The multiple layers of ubiquitin-dependent cell cycle control. Chem Rev 2009;15:15.
16. Nakayama KI, Nakayama K. Ubiquitin ligases: cell-cycle control and cancer. Nat Rev Cancer 2006;6:369-381.
17. Thornton BR, Ng TM, Matyskiela ME, Carroll CW, Morgan DO, Toczyski DP. An architectural map of the anaphase-promoting complex. Genes Dev 2006;20: 449-460.
18. Nakayama KI, Nakayama K. Regulation of the cell cycle by SCF-type ubiquitin ligases. Semin Cell Dev Biol 2005;16:323-333.
19. Nakayama K, Nagahama H, Minamishima YA, Matsumoto M, Nakamichi I, Kitagawa K et al Targeted disruption of Skp2 results in accumulation of cyclin-E and p27(Kip1), polyploidy and centrosome overduplication. EMBO J 2000;19:2069-2081.
20. Egozi D, Shapira M, Paor G, Ben-Izhak O, Skorecki K, Hershko DD. Regulation of the cell cycle inhibitor p27 and its ubiquitin ligase Skp2 in differentiation of human embryonic stem cells. FASEB J 2007;21:2807-2817.
21. Lin HK, Wang G, Chen Z, Teruya-Feldstein J, Liu Y, Chan CH et al Phosphorylation-dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB. Nat Cell Biol 2009;11:420-432.
22. Gao D, Inuzuka H, Tseng A, Chin RY, Toker A, Wei W. Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction. Nat Cell Biol 2009;11:397-408.
23. Tsunematsu R, Nakayama K, Oike Y, Nishiyama M, Ishida N, Hatakeyama S et al Mouse Fbw7/Sel-10/Cdc4 is required for notch degradation during vascular development. J Biol Chem 2004;279:9417-9423.
24. Tetzlaff MT, Yu W, Li M, Zhang P, Finegold M, Mahon K et al Defective cardiovascular development and elevated cyclin-E and Notch proteins in mice lacking the Fbw7 F-box protein. Proc Natl Acad Sci USA 2004;101:3338-3345.
25. Watanabe N, Arai H, Nishihara Y, Taniguchi M, Hunter T, Osada H. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFbeta-TrCP. Proc Natl Acad Sci USA 2004;101:4419-4424.
26. Busino L, Donzelli M, Chiesa M, Guardavaccaro D, Ganoth D, Dorrello NV et al Degradation of Cdc25A by beta-TrCP during S phase and in response to DNA damage. Nature 2003;426:87-91.
27. Guardavaccaro D, Kudo Y, Boulaire J, Barchi M, Busino L, Donzelli M et al Control of meiotic and mitotic progression by the F box protein beta-Trcp1 in vivo. Dev Cell 2003;4:799-812.
28. Margottin-Goguet F, Hsu JY, Loktev A, Hsieh HM, Reimann JD, Jackson PK. Pro-phase destruction of Emi1 by the SCF(betaTrCP/Slimb) ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev Cell 2003;4:813-826.
29. Hart M, Concordet JP, Lassot I, Albert I, del los Santos R, Durand H et al The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr Biol 1999;9:207-210.
30. Peters JM. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 2006;7:644-656.
31. Kraft C, Herzog F, Gieffers C, Mechtler K, Hagting A, Pines J et al Mitotic regulation of the human anaphase-promoting complex by phosphorylation. EMBO J 2003;22:6598-6609.
32. Rape M, Kirschner MW. Autonomous regulation of the anaphase-promoting complex couples mitosis to S-phase entry. Nature 2004;432:588-595.
33. Tugendreich S, Tomkiel J, Earnshaw W, Hieter P. CDC27Hs colocalizes with CDC16Hs to the centrosome and mitotic spindle and is essential for the meta-phase to anaphase transition. Cell 1995;81:261-268.
34. Yanagida M. Cell cycle mechanisms of sister chromatid separation; roles of Cut1/ separin and Cut2/securin. Genes Cells 2000;5:1-8.
35. Hames RS, Wattam SL, Yamano H, Bacchieri R, Fry AM. APC/C-mediated destruction of the centrosomal kinase Nek2A occurs in early mitosis and depends upon a cyclin-A-type D-box. EMBO J 2001;20:7117-7127.
36. Sudakin V, Chan GK, Yen TJ. Checkpoint inhibition of the APC/C in HeLa cells is mediated by a complex of BUBR1, BUB3, CDC20, and MAD2. J Cell Biol 2001; 154:925-936.
37. Stegmeier F, Rape M, Draviam VM, Nalepa G, Sowa ME, Ang XL et al Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 2007;446:876-881.
38. Tang Z, Shu H, Oncel D, Chen S, Yu H. Phosphorylation of Cdc20 by Bub1 provides a catalytic mechanism for APC/C inhibition by the spindle checkpoint. Mol Cell 2004;16:387-397.
39. Jaspersen SL, Charles JF, Morgan DO. Inhibitory phosphorylation of the APC regulator Hct1 is controlled by the kinase Cdc28 and the phosphatase Cdc14. Curr Biol 1999;9:227-236.
40. Zachariae W, Schwab M, Nasmyth K, Seufert W. Control of cyclin ubiquitination by CDK-regulated binding of Hct1 to the anaphase promoting complex. Science 1998;282:1721-1724.
41. Bashir T, Dorrello NV, Amador V, Guardavaccaro D, Pagano M. Control of the SCF(Skp2-Cks1) ubiquitin ligase by the APC/C(Cdh1) ubiquitin ligase. Nature 2004;428:190-193.
42. Wei W, Ayad NG, Wan Y, Zhang GJ, Kirschner MW, Kaelin WG Jr. Degradation of the SCF component Skp2 in cell-cycle phase G1 by the anaphase-promoting complex. Nature 2004;428:194-198.
43. McGarry TJ, Kirschner MW. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998;93:1043-1053.
44. Taguchi S, Honda K, Sugiura K, Yamaguchi A, Furukawa K, Urano T. Degradation of human Aurora-A protein kinase is mediated by hCdh1. FEBS Lett 2002;519: 59-65.
45. Stewart S, Fang G. Destruction box-dependent degradation of aurora B is mediated by the anaphase-promoting complex/cyclosome and Cdh1. Cancer Res 2005;65:8730-8735.
46. Lindon C, Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J Cell Biol 2004;164:233-241.
47. Hayes MJ, Kimata Y, Wattam SL, Lindon C, Mao G, Yamano H et al Early mitotic degradation of Nek2A depends on Cdc20-independent interaction with the APC/C. Nat Cell Biol 2006;8:607-614.
48. Sorensen CS, Lukas C, Kramer ER, Peters JM, Bartek J, Lukas J. A conserved cyclin-binding domain determines functional interplay between anaphase-promoting complex-Cdh1 and cyclin-A-Cdk2 during cell cycle progression. Mol Cell Biol 2001;21:3692-3703.
49. Sutterluty H, Chatelain E, Marti A, Wirbelauer C, Senften M, Muller U et al p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat Cell Biol 1999;1:207-214.
50. Singh SK, Kagalwala MN, Parker-Thornburg J, Adams H, Majumder S. REST maintains self-renewal and pluripotency of embryonic stem cells. Nature 2008; 453:223-227.
51. Westbrook TF, Hu G, Ang XL, Mulligan P, Pavlova NN, Liang A et al SCFbeta-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature 2008;452:370-374.
52. Rape M, Reddy SK, Kirschner MW. The processivity of multiubiquitination by the APC determines the order of substrate degradation. Cell 2006;124:89-103.
53. Geley S, Kramer E, Gieffers C, Gannon J, Peters JM, Hunt T. Anaphase-promoting complex/cyclosome-dependent proteolysis of human cyclin-A starts at the beginning of mitosis and is not subject to the spindle assembly checkpoint. J Cell Biol 2001;153:137-148.
54. Amador V, Ge S, Santamaria PG, Guardavaccaro D, Pagano M. APC/C(Cdc20) controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol Cell 2007;27:462-473.
55. Bernassola F, Karin M, Ciechanover A, Melino G. The HECT family of E3 ubiqui-tin ligases: multiple players in cancer development. Cancer Cell 2008;14:10-21.
56. Yu J, Lan J, Zhu Y, Li X, Lai X, Xue Y et al The E3 ubiquitin ligase HECTD3 regulates ubiquitination and degradation of Tara. Biochem Biophys Res Commun 2008; 367:805-812.
57. Osmundson EC, Ray D, Moore FE, Gao Q, Thomsen GH, Kiyokawa H. The HECT E3 ligase Smurf2 is required for Mad2-dependent spindle assembly checkpoint. J Cell Biol 2008;183:267-277.
58. Joseph J, Liu ST, Jablonski SA, Yen TJ, Dasso M. The RanGAP1-RanBP2 complex is essential for microtubule-kinetochore interactions in vivo. Curr Biol 2004;14: 611-617.
59. Dawlaty MM, Malureanu L, Jeganathan KB, Kao E, Sustmann C, Tahk S et al Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoi-somerase IIalpha. Cell 2008;133:103-115.
60. Cummings CM, Bentley CA, Perdue SA, Baas PW, Singer JD. The Cul3/KLHDC5 E3 ligase regulates p60/katanin and is required for normal mitosis in mammalian cells. J Biol Chem 2009;284:11663-11675.
61. Maddika S, Chen J. Protein kinase DYRK2 is a scaffold that facilitates assembly of an E3 ligase. Nat Cell Biol 2009;11:409-419.
62. Grimmler M, Wang Y, Mund T, Cilensek Z, Keidel EM, Waddell MB et al Cdk-inhibitory activity and stability of p27Kip1 are directly regulated by onco-genic tyrosine kinases. Cell 2007;128:269-280.
63. Delston RB, Harbour JW. Rb at the interface between cell cycle and apoptotic decisions. Curr Mol Med 2006;6:713-718.
64. Hofmann F, Martelli F, Livingston DM, Wang Z. The retinoblastoma gene product protects E2F-1 from degradation by the ubiquitin-proteasome pathway. Genes Dev 1996;10:2949-2959.
65. Hateboer G, Kerkhoven RM, Shvarts A, Bernards R, Beijersbergen RL. Degradation of E2F by the ubiquitin-proteasome pathway: regulation by retinoblas-toma family proteins and adenovirus transforming proteins. Genes Dev 1996; 10:2960-2970.
66. Martelli F, Livingston DM. Regulation of endogenous E2F1 stability by the retino-blastoma family proteins. Proc Natl Acad Sci USA 1999;96:2858-2863.
67. Datta A, Nag A, Raychaudhuri P. Differential regulation of E2F1, DP1, and the E2F1/DP1 complex by ARF. Mol Cell Biol 2002;22:8398-8408.
68. Martelli F, Hamilton T, Silver DP, Sharpless NE, Bardeesy N, Rokas M et al p19ARF targets certain E2F species for degradation. Proc Natl Acad Sci USA 2001;98:4455-4460.
69. Rizos H, Scurr LL, Irvine M, Alling NJ, Kefford RF. p14ARF regulates E2F-1 ubi-quitination and degradation via a p53-dependent mechanism. Cell Cycle 2007;6: 1741-1747.
70. Marti A, Wirbelauer C, Scheffner M, Krek W. Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nat Cell Biol 1999;1:14-19.
71. Barre B, Perkins ND. A cell cycle regulatory network controlling NF-kappaB subunit activity and function. EMBO J 2007;26:4841-4855.
72. Wertz IE, O'Rourke KM, Zhou H, Eby M, Aravind L, Seshagiri S et al De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kappaB signalling. Nature 2004;430:694-699.
73. Takami Y, Nakagami H, Morishita R, Katsuya T, Cui TX, Ichikawa T et al Ubiqui-tin carboxyl-terminal hydrolase L1, a novel deubiquitinating enzyme in the vas-culature, attenuates NF-kappaB activation. Arterioscler Thromb Vasc Biol 2007;27: 2184-2190.
74. Enesa K, Zakkar M, Chaudhury H, Luong Le A, Rawlinson L, Mason JC et al NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in pro-inflammatory signaling. J Biol Chem 2008;283: 7036-7045.
75. 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.
76. Jono H, Lim JH, Chen LF, Xu H, Trompouki E, Pan ZK et al NF-kappaB is essential for induction of CYLD, the negative regulator of NF-kappaB: evidence for a novel inducible autoregulatory feedback pathway. J Biol Chem 2004;279: 36171-36174.
77. Pouyssegur J, Dayan F, Mazure NM. Hypoxia signalling in cancer and approaches to enforce tumour regression. Nature 2006;441:437-443.
78. Fong GH. Mechanisms of adaptive angiogenesis to tissue hypoxia. Angiogenesis 2008;11:121-140.
79. 2 sensing. Science 2001;292:464-468.
80. Ohh M, Park CW, Ivan M, Hoffman MA, Kim TY, Huang LE et al Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat Cell Biol 2000;2:423-427.
81. Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN et al The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci USA 2004;101: 9085-9090.
82. Finkel T. Oxidant signals and oxidative stress. Curr Opin Cell Biol 2003;15: 247-254.
83. Breusing N, Grune T. Regulation of proteasome-mediated protein degradation during oxidative stress and aging. Biol Chem 2008;389:203-209.
84. Sitte N, Huber M, Grune T, Ladhoff A, Doecke WD, Von Zglinicki T et al Pro-teasome inhibition by lipofuscin/ceroid during postmitotic aging of fibroblasts. FASEB J 2000;14:1490-1498.
85. Ishii T, Sakurai T, Usami H, Uchida K. Oxidative modification of proteasome: identification of an oxidation-sensitive subunit in 26 S proteasome. Biochemistry 2005;44:13893-13901.
86. Perez-Galan P, Roue G, Villamor N, Montserrat E, Campo E, Colomer D. The proteasome inhibitor bortezomib induces apoptosis in mantle-cell lymphoma through generation of ROS and Noxa activation independent of p53 status. Blood 2006;107:257-264.
87. Dasmahapatra G, Rahmani M, Dent P, Grant S. The tyrphostin adaphostin interacts synergistically with proteasome inhibitors to induce apoptosis in human leukemia cells through a reactive oxygen species (ROS)-dependent mechanism. Blood 2006;107:232-240.
88. Fernandes R, Ramalho J, Pereira P. Oxidative stress upregulates ubiquitin protea-some pathway in retinal endothelial cells. Mol Vis 2006;12:1526-1535.
89. Pickett CBPD, Nguyen T, Nioi P. The Nrf2-ARE signaling pathway and its activation by oxidative stress. J Biol Chem 2009;284:13291-13295.
90. Gao L, Mann GE. Vascular NAD(P)H oxidase activation in diabetes: a double-edged sword in redox signalling. Cardiovasc Res 2009;82:9-20.
91. Boon RA, Horrevoets AJ. Key transcriptional regulators of the vasoprotective effects of shear stress. Hamostaseologie 2009;29:39-40, 41-43.
92. Kobayashi A, Kang MI, Okawa H, Ohtsuji M, Zenke Y, Chiba T et al Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol Cell Biol 2004;24:7130-7139.
93. Reddy NM, Kleeberger SR, Bream JH, Fallon PG, Kensler TW, Yamamoto M et al Genetic disruption of the Nrf2 compromises cell-cycle progression by impairing GSH-induced redox signaling. Oncogene 2008;27:5821-5832.
94. Villacorta L, Zhang J, Garcia-Barrio MT, Chen XL, Freeman BA, Chen YE et al Nitro-linoleic acid inhibits vascular smooth muscle cell proliferation via the Keap1/Nrf2 signaling pathway. Am J Physiol Heart Circ Physiol 2007;293: H770-H776.
95. Murray-Zmijewski F, Slee EA, Lu X. A complex barcode underlies the heterogeneous response of p53 to stress. Nat Rev Mol Cell Biol 2008;9:702-712.
96. Vousden KH, Lane DP. p53 in health and disease. Nat Rev Mol Cell Biol 2007;8: 275-283.
97. Coutts AS, Adams CJ, La Thangue NB. p53 ubiquitination by Mdm2: A never ending tail? DNA Repair (Amst) 2009;8:483-490.
98. Wu X, Bayle JH, Olson D, Levine AJ. The p53-mdm-2 autoregulatory feedback loop. Genes Dev 1993;7:1126-1132.
99. Stommel JM, Wahl GM. Accelerated MDM2 auto-degradation induced by DNA-damage kinases is required for p53 activation. EMBO J 2004;23:1547-1556.
100. Lee JH, Jeong MW, Kim W, Choi YH, Kim KT. Cooperative roles of c-Abl and Cdk5 in regulation of p53 in response to oxidative stress. J Biol Chem 2008; 283:19826-19835.
101. Saito A, Hayashi T, Okuno S, Nishi T, Chan PH. Modulation of p53 degradation via MDM2-mediated ubiquitylation and the ubiquitin-proteasome system during reperfusion after stroke: role of oxidative stress. J Cereb Blood Flow Metab 2005; 25:267-280.
102. Wu C, Miloslavskaya I, Demontis S, Maestro R, Galaktionov K. Regulation of cellular response to oncogenic and oxidative stress by Seladin-1. Nature 2004;432: 640-645.
103. Maiese K, Chong ZZ, Shang YC, Hou J. FoxO proteins: cunning concepts and considerations for the cardiovascular system. Clin Sci (Lond) 2009;116:191-203.
104. van der Horst A, de Vries-Smits AM, Brenkman AB, van Triest MH, van den Broek N, Colland F et al FOXO4 transcriptional activity is regulated by mono-ubiquitination and USP7/HAUSP. Nat Cell Biol 2006;8:1064-1073.
105. Brenkman AB, de Keizer PL, van den Broek NJ, Jochemsen AG, Burgering BM. Mdm2 induces mono-ubiquitination of FOXO4. PLoS ONE 2008;3:e2819.
106. Cicchillitti L, Fasanaro P, Biglioli P, Capogrossi MC, Martelli F. Oxidative stress induces protein phosphatase 2A-dependent dephosphorylation of the pocket proteins pRb, p107, and p130. J Biol Chem 2003;278:19509-19517.
107. Magenta A, Fasanaro P, Romani S, Di Stefano V, Capogrossi MC, Martelli F. Protein phosphatase 2A subunit PR70 interacts with pRb and mediates its dephosphorylation. Mol Cell Biol 2008;28:873-882.
108. Fasanaro P, Magenta A, Zaccagnini G, Cicchillitti L, Fucile S, Eusebi F et al Cyclin-D1 degradation enhances endothelial cell survival upon oxidative stress. FASEB J 2006;20:1242-1244.
109. Diehl JA, Cheng M, Roussel MF, Sherr CJ. Glycogen synthase kinase-3beta regulates cyclin-D1 proteolysis and subcellular localization. Genes Dev 1998;12: 3499-3511.
110. Lim JH, Lee YM, Chun YS, Park JW. Reactive oxygen species-mediated cyclin-D1 degradation mediates tumor growth retardation in hypoxia, independently of p21cip1 and hypoxia-inducible factor. Cancer Sci 2008;99:1798-1805.
111. Casanovas O, Miro F, Estanyol JM, Itarte E, Agell N, Bachs O. Osmotic stress regulates the stability of cyclin-D1 in a p38SAPK2-dependent manner. J Biol Chem 2000;275:35091-35097.
112. Miyakawa Y, Matsushime H. Rapid downregulation of cyclin-D1 mRNA and protein levels by ultraviolet irradiation in murine macrophage cells. Biochem Biophys Res Commun 2001;284:71-76.
113. Chang TS, Jeong W, Lee DY, Cho CS, Rhee SG. The RING-H2-finger protein APC11 as a target of hydrogen peroxide. Free Radic Biol Med 2004;37:521-530.
114. Tadlock L, Yamagiwa Y, Hawker J, Marienfeld C, Patel T. Transforming growth factor-beta inhibition of proteasomal activity: a potential mechanism of growth arrest. Am J Physiol Cell Physiol 2003;285:C277-C285.
115. Kibbe M, Billiar T, Tzeng E. Inducible nitric oxide synthase and vascular injury. Cardiovasc Res 1999;43:650-657. (Pubitemid 29369263)
116. Kibbe MR, Nie S, Seol DW, Kovesdi I, Lizonova A, Makaroun M et al Nitric oxide prevents p21 degradation with the ubiquitin-proteasome pathway in vascular smooth muscle cells. J Vasc Surg 2000;31:364-374.
117. Kapadia MR, Eng JW, Jiang Q, Stoyanovsky DA, Kibbe MR. Nitric oxide regulates the 26S proteasome in vascular smooth muscle cells. Nitric Oxide 2009;31: 364-374.
118. Guedat P, Colland F. Patented small molecule inhibitors in the ubiquitin protea-some system. BMC Biochem 2007;8(Suppl. 1):S14.
119. Nalepa G, Rolfe M, Harper JW. Drug discovery in the ubiquitin-proteasome system. Nat Rev Drug Discov 2006;5:596-613.