Deubiquitinase USP9x confers radioresistance through stabilization of Mcl-1

Neoplasia (United States)

Volumn 14, Issue 10, 2012, Pages 893-904

  Trivigno, Donatella ^a   Essmann, Frank ^b   Huber, Stephan M ^a   Rudner, Justine ^a,c  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY HOSPITAL ESSEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; BIM PROTEIN; CASPASE; PROTEIN MCL 1; PROTEIN NOXA; PUMA PROTEIN; SMALL INTERFERING RNA; UBIQUITIN; UBIQUITIN SPECIFIC PROTEASE 9X; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER SURVIVAL; CELL DEATH; CELL PERMEABILIZATION; CLONOGENIC ASSAY; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FLOW CYTOMETRY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MYELOID LEUKEMIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STABILITY; RADIOSENSITIVITY; UBIQUITINATION; WESTERN BLOTTING;

EID: 84867806661     PISSN: 15228002     EISSN: 14765586     Source Type: Journal    
DOI: 10.1593/neo.12598     Document Type: Article

References (39)

1. Youle RJ and Strasser A (2008). The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 9, 47-59.
2. Adams JM and Cory S (2007). The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 26, 1324-1337.
3. Kelly PN and Strasser A (2011). The role of Bcl-2 and its pro-survival relatives in tumourigenesis and cancer therapy. Cell Death Differ 18, 1414-1424.
4. Chen L, Willis SN, Wei A, Smith BJ, Fletcher JI, Hinds MG, Colman PM, Day CL, Adams JM, and Huang DC (2005). Differential targeting of prosurvival Bcl-2 proteins by their BH3-only ligands allows complementary apoptotic function. Mol Cell 17, 393-403.
5. Rudner J, Elsaesser SJ, Jendrossek V, and Huber SM (2011). Anti-apoptotic Bcl-2 fails to form efficient complexes with pro-apoptotic Bak to protect from Celecoxib-induced apoptosis. Biochem Pharmacol 81, 32-42.
6. Rudner J, Elsaesser SJ, Muller AC, Belka C, and Jendrossek V (2010). Differential effects of anti-apoptotic Bcl-2 family members Mcl-1, Bcl-2, and Bcl-xL on celecoxib-induced apoptosis. Biochem Pharmacol 79, 10-20.
7. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, and Huang DC (2005). Proapoptotic Bak is sequestered by Mcl-1 and Bcl-xL, but not Bcl-2, until displaced by BH3-only proteins. Genes Dev 19, 1294-1305.
8. Allen JC, Talab F, Zuzel M, Lin K, and Slupsky JR (2011). c-Abl regulates Mcl-1 gene expression in chronic lymphocytic leukemia cells. Blood 117, 2414-2422.
9. Deng X, Gao F, Flagg T, and May WS Jr (2004). Mono- and multisite phosphorylation enhances Bcl2's antiapoptotic function and inhibition of cell cycle entry functions. Proc Natl Acad Sci USA 101, 153-158.
10. Huber S, Oelsner M, Decker T, zum Buschenfelde CM, Wagner M, Lutzny G, Kuhnt T, Schmidt B, Oostendorp RA, Peschel C, et al. (2011). Sorafenib induces cell death in chronic lymphocytic leukemia by translational downregulation of Mcl-1. Leukemia 25, 838-847.
11. Czabotar PE, Lee EF, van Delft MF, Day CL, Smith BJ, Huang DC, Fairlie WD, Hinds MG, and Colman PM (2007). Structural insights into the degradation of Mcl-1 induced by BH3 domains. Proc Natl Acad Sci USA 104, 6217-6222.
12. Domina AM, Vrana JA, Gregory MA, Hann SR, and Craig RW (2004). MCL1 is phosphorylated in the PEST region and stabilized upon ERK activation in viable cells, and at additional sites with cytotoxic okadaic acid or taxol. Oncogene 23, 5301-5315.
13. Gomez-Bougie P, Menoret E, Juin P, Dousset C, Pellat-Deceunynck C, and Amiot M (2011). Noxa controls Mule-dependent Mcl-1 ubiquitination through the regulation of the Mcl-1/USP9X interaction. Biochem Biophys Res Commun 413, 460-464.
14. Maurer U, Charvet C, Wagman AS, Dejardin E, and Green DR (2006). Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol Cell 21, 749-760.
15. Warr MR, Acoca S, Liu Z, Germain M, Watson M, Blanchette M, Wing SS, and Shore GC (2005). BH3-ligand regulates access of MCL-1 to its E3 ligase. FEBS Lett 579, 5603-5608.
16. Ding Q, He X, Hsu JM, Xia W, Chen CT, Li LY, Lee DF, Liu JC, Zhong Q, Wang X, et al. (2007). Degradation of Mcl-1 by β-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol Cell Biol 27, 4006-4017.
17. Inuzuka H, Shaik S, Onoyama I, Gao D, Tseng A, Maser RS, Zhai B, Wan L, Gutierrez A, Lau AW, et al. (2011). SCF(FBW7) regulates cellular apoptosis by targeting MCL1 for ubiquitylation and destruction. Nature 471, 104-109.
18. Wertz IE, Kusam S, Lam C, Okamoto T, Sandoval W, Anderson DJ, Helgason E, Ernst JA, Eby M, Liu J, et al. (2011). Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 471, 110-114.
19. Zhong Q, Gao W, Du F, and Wang X (2005). Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 121, 1085-1095.
20. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, et al. (2010). Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463, 103-107.
21. Rudner J, Belka C, Marini P, Wagner RJ, Faltin H, Lepple-Wienhues A, Bamberg M, and Budach W (2001). Radiation sensitivity and apoptosis in human lymphoma cells. Int J Radiat Biol 77, 1-11.
22. Murray RZ, Jolly LA, and Wood SA (2004). The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and β-catenin. Mol Biol Cell 15, 1591-1599.
23. An J, Chervin AS, Nie A, Ducoff HS, and Huang Z (2007). Overcoming the radioresistance of prostate cancer cells with a novel Bcl-2 inhibitor. Oncogene 26, 652-661.
24. Nix P, Cawkwell L, Patmore H, Greenman J, and Stafford N (2005). Bcl-2 expression predicts radiotherapy failure in laryngeal cancer. Br J Cancer 92, 2185-2189.
25. Skvara H, Thallinger C, Wacheck V, Monia BP, Pehamberger H, Jansen B, and Selzer E (2005). Mcl-1 blocks radiation-induced apoptosis and inhibits clonogenic cell death. Anticancer Res 25, 2697-2703.
26. Streffer JR, Rimner A, Rieger J, Naumann U, Rodemann HP, and Weller M (2002). BCL-2 family proteins modulate radiosensitivity in human malignant glioma cells. J Neurooncol 56, 43-49.
27. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN, and Sullenger BA (2010). Notch promotes radioresistance of glioma stem cells. Stem Cells 28, 17-28.
28. Kubota Y, Kinoshita K, Suetomi K, Fujimori A, and Takahashi S (2007). Mcl-1 depletion in apoptosis elicited by ionizing radiation in peritoneal resident macrophages of C3H mice. J Immunol 178, 2923-2931.
29. Lee EF, Czabotar PE, van Delft MF, Michalak EM, Boyle MJ, Willis SN, Puthalakath H, Bouillet P, Colman PM, Huang DC, et al. (2008). A novel BH3 ligand that selectively targets Mcl-1 reveals that apoptosis can proceed without Mcl-1 degradation. J Cell Biol 180, 341-355.
30. Sieghart W, Losert D, Strommer S, Cejka D, Schmid K, Rasoul-Rockenschaub S, Bodingbauer M, Crevenna R, Monia BP, Peck-Radosavljevic M, et al. (2006). Mcl-1 overexpression in hepatocellular carcinoma: a potential target for antisense therapy. J Hepatol 44, 151-157.
31. Wirth T, Kuhnel F, Fleischmann-Mundt B, Woller N, Djojosubroto M, Rudolph KL, Manns M, Zender L, and Kubicka S (2005). Telomerase-dependent virotherapy overcomes resistance of hepatocellular carcinomas against chemotherapy and tumor necrosis factor-related apoptosis-inducing ligand by elimination of Mcl-1. Cancer Res 65, 7393-7402.
32. Mei Y, Du W, Yang Y, and Wu M (2005). Puma*Mcl-1 interaction is not sufficient to prevent rapid degradation of Mcl-1. Oncogene 24, 7224-7237.
33. Erlacher M, Michalak EM, Kelly PN, Labi V, Niederegger H, Coultas L, Adams JM, Strasser A, and Villunger A (2005). BH3-only proteins Puma and Bim are rate-limiting for gamma-radiation- and glucocorticoid-induced apoptosis of lymphoid cells in vivo. Blood 106, 4131-4138.
34. Michalak EM, Villunger A, Adams JM, and Strasser A (2008). In several cell types tumour suppressor p53 induces apoptosis largely via Puma but Noxa can contribute. Cell Death Differ 15, 1019-1029.
35. Oda E, Ohki R, Murasawa H, Nemoto J, Shibue T, Yamashita T, Tokino T, Taniguchi T, and Tanaka N (2000). Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science 288, 1053-1058.
36. Garrison SP, Phillips DC, Jeffers JR, Chipuk JE, Parsons MJ, Rehg JE, Opferman JT, Green DR, and Zambetti GP (2012). Genetically defining the mechanism of Puma- and Bim-induced apoptosis. Cell Death Differ 19, 642-649.
37. Nakano K and Vousden KH (2001). PUMA, a novel proapoptotic gene, is induced by p53. Mol Cell 7, 683-694.
38. Yu J, Zhang L, Hwang PM, Kinzler KW, and Vogelstein B (2001). PUMA induces the rapid apoptosis of colorectal cancer cells. Mol Cell 7, 673-682.
39. Vigorito E, Plaza S, Mir L, Mongay L, Vinas O, Serra-Pages C, and Vives J (1999). Contributions of p53 and PMA to gamma-irradiation induced apoptosis in Jurkat cells. Hematol Cell Ther 41, 153-161.