The deubiquitinase Usp27x stabilizes the BH3-only protein Bim and enhances apoptosis

EMBO Reports

Volumn 17, Issue 5, 2016, Pages 724-738

  Weber, Arnim ^a   Heinlein, Melanie ^a   Dengjel, Jörn ^a,b   Alber, Claudia ^a   Singh, Prafull Kumar ^a,b   Häcker, Georg ^a,b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

apoptosis; Bcl 2; Bim; deubiquitinase; Usp27x

Indexed keywords

B RAF KINASE; BIM PROTEIN; DEUBIQUITINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN BCL X; PROTEIN BCL XL; PROTEIN MCL 1; RAF PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; USP27X DEUBIQUITINASE; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; BINDING SITE; CACO 2 CELL LINE; CANCER INHIBITION; CELL DIFFERENTIATION; CELL LABELING; CELL LEVEL; CELL STIMULATION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME BINDING; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXON; FIBROBLAST; GENE MUTATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG CANCER CELL LINE; MELANOMA CELL LINE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; TRANSIENT TRANSFECTION; UBIQUITINATION; UPREGULATION; ANIMAL; CHEMISTRY; GENE INACTIVATION; GENETICS; MELANOMA; METABOLISM; TUMOR CELL LINE;

ANIMALS; APOPTOSIS; BCL-2-LIKE PROTEIN 11; CELL LINE, TUMOR; DEUBIQUITINATING ENZYMES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GENE KNOCKOUT TECHNIQUES; HUMANS; MELANOMA; MICE; PROTEIN BINDING; PROTEIN STABILITY; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS B-RAF; SIGNAL TRANSDUCTION; UBIQUITINATION;

EID: 84961857208     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.15252/embr.201541392     Document Type: Article

References (53)

1. O'Reilly LA, Cullen L, Visvader J, Lindeman GJ, Print C, Bath ML, Huang DC, Strasser A, (2000) The proapoptotic BH3-only protein bim is expressed in hematopoietic, epithelial, neuronal, and germ cells. Am J Pathol 157: 449-461
2. Bouillet P, Metcalf D, Huang DC, Tarlinton DM, Kay TW, Kontgen F, Adams JM, Strasser A, (1999) Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 286: 1735-1738
3. Mestre-Escorihuela C, Rubio-Moscardo F, Richter JA, Siebert R, Climent J, Fresquet V, Beltran E, Agirre X, Marugan I, Marin M, et al, (2007) Homozygous deletions localize novel tumor suppressor genes in B-cell lymphomas. Blood 109: 271-280
4. Zantl N, Weirich G, Zall H, Seiffert BM, Fischer SF, Kirschnek S, Hartmann C, Fritsch RM, Gillissen B, Daniel PT, et al, (2007) Frequent loss of expression of the pro-apoptotic protein Bim in renal cell carcinoma: evidence for contribution to apoptosis resistance. Oncogene 26: 7038-7048
5. Sturm I, Stephan C, Gillissen B, Siebert R, Janz M, Radetzki S, Jung K, Loening S, Dorken B, Daniel PT, (2006) Loss of the tissue-specific proapoptotic BH3-only protein Nbk/Bik is a unifying feature of renal cell carcinoma. Cell Death Differ 13: 619-627
6. Tan TT, Degenhardt K, Nelson DA, Beaudoin B, Nieves-Neira W, Bouillet P, Villunger A, Adams JM, White E, (2005) Key roles of BIM-driven apoptosis in epithelial tumors and rational chemotherapy. Cancer Cell 7: 227-238
7. Costa DB, Halmos B, Kumar A, Schumer ST, Huberman MS, Boggon TJ, Tenen DG, Kobayashi S, (2007) BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Med 4: e315
8. Cragg MS, Kuroda J, Puthalakath H, Huang DC, Strasser A, (2007) Gefitinib-induced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS Med 4: e316
9. Gong Y, Somwar R, Politi K, Balak M, Chmielecki J, Jiang X, Pao W, (2007) Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Med 4: e294
10. Egle A, Harris AW, Bouillet P, Cory S, (2004) Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc Natl Acad Sci USA 101: 6164-6169
11. Czabotar PE, Westphal D, Dewson G, Ma S, Hockings C, Fairlie WD, Lee EF, Yao S, Robin AY, Smith BJ, et al, (2013) Bax crystal structures reveal how bh3 domains activate bax and nucleate its oligomerization to induce apoptosis. Cell 152: 519-531
12. Leshchiner ES, Braun CR, Bird GH, Walensky LD, (2013) Direct activation of full-length proapoptotic BAK. Proc Natl Acad Sci USA 110: E986-E995
13. Willis SN, Chen L, Dewson G, Wei A, Naik E, Fletcher JI, Adams JM, 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
14. Stahl M, Dijkers PF, Kops GJ, Lens SM, Coffer PJ, Burgering BM, Medema RH, (2002) The forkhead transcription factor FoxO regulates transcription of p27Kip1 and Bim in response to IL-2. J Immunol 168: 5024-5031
15. Gilley J, Coffer PJ, Ham J, (2003) FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 162: 613-622
16. Moustafa-Kamal M, Gamache I, Lu Y, Li S, Teodoro JG, (2013) BimEL is phosphorylated at mitosis by Aurora A and targeted for degradation by betaTrCP1. Cell Death Differ 20: 1393-1403
17. Wan L, Tan M, Yang J, Inuzuka H, Dai X, Wu T, Liu J, Shaik S, Chen G, Deng J, et al, (2014) APC(Cdc20) suppresses apoptosis through targeting Bim for ubiquitination and destruction. Dev Cell 29: 377-391
18. Yu H, (2007) Cdc20: a WD40 activator for a cell cycle degradation machine. Mol Cell 27: 3-16
19. Luciano F, Jacquel A, Colosetti P, Herrant M, Cagnol S, Pages G, Auberger P, (2003) Phosphorylation of Bim-EL by Erk1/2 on serine 69 promotes its degradation via the proteasome pathway and regulates its proapoptotic function. Oncogene 22: 6785-6793
20. Ley R, Balmanno K, Hadfield K, Weston C, Cook SJ, (2003) Activation of the ERK1/2 signaling pathway promotes phosphorylation and proteasome-dependent degradation of the BH3-only protein, Bim. J Biol Chem 278: 18811-18816
21. Hubner A, Barrett T, Flavell RA, Davis RJ, (2008) Multisite phosphorylation regulates Bim stability and apoptotic activity. Mol Cell 30: 415-425
22. Dehan E, Bassermann F, Guardavaccaro D, Vasiliver-Shamis G, Cohen M, Lowes KN, Dustin M, Huang DC, Taunton J, Pagano M, (2009) betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol Cell 33: 109-116
23. Komander D, Clague MJ, Urbe S, (2009) Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 10: 550-563
24. Grabbe C, Husnjak K, Dikic I, (2011) The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol 12: 295-307
25. Frank DO, Dengjel J, Wilfling F, Kozjak-Pavlovic V, Hacker G, Weber A, (2015) The pro-apoptotic BH3-only protein Bim interacts with components of the translocase of the outer mitochondrial membrane (TOM). PLoS One 10: e0123341
26. Kobayashi T, Iwamoto Y, Takashima K, Isomura A, Kosodo Y, Kawakami K, Nishioka T, Kaibuchi K, Kageyama R, (2015) Deubiquitinating enzymes regulate Hes1 stability and neuronal differentiation. FEBS J 282: 2475-2487
27. Wilfling F, Weber A, Potthoff S, Vogtle FN, Meisinger C, Paschen SA, Hacker G, (2012) BH3-only proteins are tail-anchored in the outer mitochondrial membrane and can initiate the activation of Bax. Cell Death Differ 19: 1328-1336
28. Quesada V, Diaz-Perales A, Gutierrez-Fernandez A, Garabaya C, Cal S, Lopez-Otin C, (2004) Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. Biochem Biophys Res Commun 314: 54-62
29. Soderberg O, Gullberg M, Jarvius M, Ridderstrale K, Leuchowius KJ, Jarvius J, Wester K, Hydbring P, Bahram F, Larsson LG, et al, (2006) Direct observation of individual endogenous protein complexes in situ by proximity ligation. Nat Methods 3: 995-1000
30. Bouillet P, Zhang LC, Huang DC, Webb GC, Bottema CD, Shore P, Eyre HJ, Sutherland GR, Adams JM, (2001) Gene structure alternative splicing, and chromosomal localization of pro-apoptotic Bcl-2 relative Bim. Mamm Genome 12: 163-168
31. Ritorto MS, Ewan R, Perez-Oliva AB, Knebel A, Buhrlage SJ, Wightman M, Kelly SM, Wood NT, Virdee S, Gray NS, et al, (2014) Screening of DUB activity and specificity by MALDI-TOF mass spectrometry. Nat Commun 5: 4763
32. Zhang XY, Varthi M, Sykes SM, Phillips C, Warzecha C, Zhu W, Wyce A, Thorne AW, Berger SL, McMahon SB, (2008) The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. Mol Cell 29: 102-111
33. Xiong J, Wang Y, Gong Z, Liu J, Li W, (2014) Identification of a functional nuclear localization signal within the human USP22 protein. Biochem Biophys Res Commun 449: 14-18
34. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, et al, (2002) Mutations of the BRAF gene in human cancer. Nature 417: 949-954
35. Dai DL, Wang Y, Liu M, Martinka M, Li G, (2008) Bim expression is reduced in human cutaneous melanomas. J Invest Dermatol 128: 403-407
36. Sheridan C, Brumatti G, Martin SJ, (2008) Oncogenic B-RafV600E inhibits apoptosis and promotes ERK-dependent inactivation of Bad and Bim. J Biol Chem 283: 22128-22135
37. Roring M, Herr R, Fiala GJ, Heilmann K, Braun S, Eisenhardt AE, Halbach S, Capper D, von Deimling A, Schamel WW, et al, (2012) Distinct requirement for an intact dimer interface in wild-type, V600E and kinase-dead B-Raf signalling. EMBO J 31: 2629-2647
38. Wagner SA, Beli P, Weinert BT, Nielsen ML, Cox J, Mann M, Choudhary C, (2011) A proteome-wide, quantitative survey of in vivo ubiquitylation sites reveals widespread regulatory roles. Mol Cell Proteomics 10: M111 013284
39. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E, Murray B, Latham V, Sullivan M, (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-D270
40. Happo L, Strasser A, Cory S, (2012) BH3-only proteins in apoptosis at a glance. J Cell Sci 125: 1081-1087
41. Mojsa B, Lassot I, Desagher S, (2014) Mcl-1 ubiquitination: unique regulation of an essential survival protein. Cells 3: 418-437
42. Brinkmann K, Zigrino P, Witt A, Schell M, Ackermann L, Broxtermann P, Schull S, Andree M, Coutelle O, Yazdanpanah B, et al, (2013) Ubiquitin C-terminal hydrolase-L1 potentiates cancer chemosensitivity by stabilizing NOXA. Cell Rep 3: 881-891
43. Ewings KE, Hadfield-Moorhouse K, Wiggins CM, Wickenden JA, Balmanno K, Gilley R, Degenhardt K, White E, Cook SJ, (2007) ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-xL. EMBO J 26: 2856-2867
44. Llambi F, Moldoveanu T, Tait SW, Bouchier-Hayes L, Temirov J, McCormick LL, Dillon CP, Green DR, (2011) A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol Cell 44: 517-531
45. Sowa ME, Bennett EJ, Gygi SP, Harper JW, (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138: 389-403
46. 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
47. Perez-Mancera PA, Rust AG, van der Weyden L, Kristiansen G, Li A, Sarver AL, Silverstein KA, Grutzmann R, Aust D, Rummele P, et al, (2012) The deubiquitinase USP9X suppresses pancreatic ductal adenocarcinoma. Nature 486: 266-270
48. Naik E, Webster JD, DeVoss J, Liu J, Suriben R, Dixit VM, (2014) Regulation of proximal T cell receptor signaling and tolerance induction by deubiquitinase Usp9X. J Exp Med 211: 1947-1955
49. Zhao Y, Majid MC, Soll JM, Brickner JR, Dango S, Mosammaparast N, (2015) Noncanonical regulation of alkylation damage resistance by the OTUD4 deubiquitinase. EMBO J 34: 1687-1703
50. Weber A, Paschen SA, Heger K, Wilfling F, Frankenberg T, Bauerschmitt H, Seiffert BM, Kirschnek S, Wagner H, Hacker G, (2007) BimS-induced apoptosis requires mitochondrial localization but not interaction with anti-apoptotic Bcl-2 proteins. J Cell Biol 177: 625-636
51. Vince JE, Wong WW, Khan N, Feltham R, Chau D, Ahmed AU, Benetatos CA, Chunduru SK, Condon SM, McKinlay M, et al, (2007) IAP antagonists target cIAP1 to induce TNFalpha-dependent apoptosis. Cell 131: 682-693
52. Sanjana NE, Shalem O, Zhang F, (2014) Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods 11: 783-784
53. Weber A, Kirejczyk Z, Besch R, Potthoff S, Leverkus M, Hacker G, (2010) Proapoptotic signalling through Toll-like receptor-3 involves TRIF-dependent activation of caspase-8 and is under the control of inhibitor of apoptosis proteins in melanoma cells. Cell Death Differ 17: 942-951