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Deubiquitinating c-Myc: USP36 steps up in the nucleolus

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Pages 3786-3793 | Received 03 Sep 2015, Accepted 07 Sep 2015, Published online: 23 Dec 2015

References

  • Lin CY, Loven J, Rahl PB, Paranal RM, Burge CB, Bradner JE, Lee TI, Young RA. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012; 151:56-67; PMID:23021215; http://dx.doi.org/10.1016/j.cell.2012.08.026
  • Nie Z, Hu G, Wei G, Cui K, Yamane A, Resch W, Wang R, Green DR, Tessarollo L, Casellas R, et al. c-Myc is a universal amplifier of expressed genes in lymphocytes and embryonic stem cells. Cell 2012; 151:68-79; PMID:23021216; http://dx.doi.org/10.1016/j.cell.2012.08.033
  • Sabo A, Kress TR, Pelizzola M, de Pretis S, Gorski MM, Tesi A, Morelli MJ, Bora P, Doni M, Verrecchia A, et al. Selective transcriptional regulation by Myc in cellular growth control and lymphomagenesis. Nature 2014; 511: 488-92; PMID:25043028; http://dx.doi.org/10.1038/nature13537
  • Walz S, Lorenzin F, Morton J, Wiese KE, von Eyss B, Herold S, Rycak L, Dumay-Odelot H, Karim S, Bartkuhn M, et al. Activation and repression by oncogenic MYC shape tumour-specific gene expression profiles. Nature 2014; 511:483-7; PMID:25043018; http://dx.doi.org/10.1038/nature13473
  • Adhikary S, Eilers M. Transcriptional regulation and transformation by Myc proteins. Nat Rev Mol Cell Biol 2005; 6:635-45; PMID:16064138; http://dx.doi.org/doi:10.1038/nrm1703
  • Meyer N, Penn LZ. Reflecting on 25 years with MYC. Nat Rev Cancer 2008; 8:976-90; PMID:19029958; http://dx.doi.org/10.1038/nrc2231
  • van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 2010; 10: 301-9; PMID:19029958; http://dx.doi.org/10.1038/nrc2231
  • Nesbit CE, Tersak JM, aProchownik EV. MYC oncogenes and human neoplastic disease. Oncogene 1999; 18:3004-16; PMID:20332779; http://dx.doi.org/10.1038/nrc2819
  • Farrell AS, Sears RC. MYC degradation. Cold Spring Harb Perspect Med 2014; 4: pii: a014365; PMID:24591536; http://dx.doi.org/10.1101/cshperspect.a014365
  • Hann SR. Role of post-translational modifications in regulating c-Myc proteolysis, transcriptional activity and biological function. Semin Cancer Biol 2006; 16:288-302; PMID:16938463; http://dx.doi.org/10.1016/j.semcancer.2006.08.004; PMID:16938463
  • Sears R, Leone G, DeGregori J, Nevins JR. Ras enhances Myc protein stability. Mol Cell 1999; 3:169-79; PMID:10078200; http://dx.doi.org/10.1016/S1097-2765(00)80308-1
  • Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev 2000;14:2501-14; PMID:11018017; http://dx.doi.org/10.1101/gad.836800
  • Sears RC. The life cycle of C-myc: from synthesis to degradation. Cell cycle 2004; 3:1133-7; PMID:15467447; http://dx.doi.org/10.4161/cc.3.9.1145
  • Conacci-Sorrell M, McFerrin L, Eisenman, RN. An overview of MYC and its interactome. Cold Spring Harb Perspect Med 2014; 4, a014357; PMID:24384812; http://dx.doi.org/10.1101/cshperspect.a014357
  • Tu WB, Helander S, Pilstal R, Hickman KA, Lourenco C, Jurisica I, Raught B, Wallner B, Sunnerhagen M, Penn LZ. Myc and its interactors take shape. Biochim Biophys Acta 2015; 1849:469-83; PMID:24933113; http://dx.doi.org/10.1016/j.bbagrm.2014.06.002
  • Ciechanover A, DiGiuseppe JA, Bercovich B, Orian A, Richter JD, Schwartz AL, Brodeur GM. Degradation of nuclear oncoproteins by the ubiquitin system in vitro. Proc Natl Acad Sci U S A 1991; 88:139-43; PMID:1846034
  • Flinn EM, Busch CM, Wright AP. myc boxes, which are conserved in myc family proteins, are signals for protein degradation via the proteasome. Mol Cell Biol 1998; 18:5961-69; PMID:9742113
  • Lutterbach B, Hann SR. Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol Cell Biol 1994; 14:5510-22; PMID:8035827; http://dx.doi.org/10.1128/MCB.14.8.5510
  • Gregory MA, Qi Y, Hann SR. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J Biol Chem 2003; 278:51606-12; PMID:14563837; http://dx.doi.org/10.1074/jbc.M310722200
  • Chang DW, Claassen GF, Hann SR, Cole MD. The c-Myc transactivation domain is a direct modulator of apoptotic versus proliferative signals. Mol Cell Biol 2000; 20:4309-19; PMID:10825194; http://dx.doi.org/10.1128/MCB.20.12.4309-4319.2000
  • Lutterbach B, aHann SR. Hierarchical phosphorylation at N-terminal transformation-sensitive sites in c-Myc protein is regulated by mitogens and in mitosis. Mol Cell Biol 1994; 14:5510-22; PMID:8035827; http://dx.doi.org/10.1128/MCB.14.8.5510
  • Oster SK, Ho CS, Soucie EL, Penn LZ. The myc oncogene: MarvelouslY Complex. Adv Cancer Res 2002; 84:81-154; PMID:11885563; http://dx.doi.org/10.1016/S0065-230X(02)84004-0
  • Yeh E, Cunningham M, Arnold H, Chasse D, Monteith T, Ivaldi G, Hahn WC, Stukenberg PT, Shenolikar S, Uchida T, et al. A signalling pathway controlling c-Myc degradation that impacts oncogenic transformation of human cells. Nat Cell Biol 2004; 6:308-18; PMID:15048125; http://dx.doi.org/10.1038/ncb1110
  • Moberg KH, Mukherjee A, Veraksa A, Artavanis-Tsakonas S, Hariharan IK. The Drosophila F box protein archipelago regulates dMyc protein levels in vivo. Curr Biol 2004; 14:965-74; PMID:15182669; http://dx.doi.org/10.1016/j.cub.2004.04.040
  • Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, Nakayama KI. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J 2004; 23:2116-25; PMID:15103331; http://dx.doi.org/10.1038/sj.emboj.7600217
  • Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN, Clurman B E. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc Natl Acad Sci U S A 2004; 101:9085-90; PMID:15150404; http://dx.doi.org/10.1073/pnas.0402770101
  • Welcker M, Orian A, Grim JE, Eisenman RN, Clurman BE. A nucleolar isoform of the Fbw7 ubiquitin ligase regulates c-Myc and cell size. Curr Biol 2004; 14:965-74; PMID:15498494; http://dx.doi.org/10.1016/j.cub.2004.09.083
  • Bahram F, von der Lehr N, Cetinkaya C, Larsson LG. c-Myc hot spot mutations in lymphomas result in inefficient ubiquitination and decreased proteasome-mediated turnover. Blood 2000; 95:2104-10; PMID:10706881
  • Gregory MA, Hann SR. c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells. Mol Cell Biol. 2000; 20:2423-35; PMID:10713166; http://dx.doi.org/10.1128/MCB.20.7.2423-2435.2000
  • Salghetti SE, Kim SY, Tansey WP. Destruction of Myc by ubiquitin-mediated proteolysis: cancer-associated and transforming mutations stabilize Myc. EMBO J 1999; 18, 717-26; PMID:9927431
  • Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C, Cleveland JL, Tansey WP, Lowe SW. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 2005; 436:807-11; PMID:16094360; http://dx.doi.org/10.1038/nature03845
  • Wang X, Cunningham M, Zhang X, Tokarz S, Laraway B, Troxell M, Sears RC. Phosphorylation regulates c-Myc's oncogenic activity in the mammary gland. Cancer Res 2011; 71:925-36; PMID:21266350; http://dx.doi.org/10.1158/0008-5472.CAN-10-1032
  • Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 2008; 8:83-93; PMID:18094723; http://dx.doi.org/10.1038/nrc2290
  • von der Lehr N, Johansson S, Wu S, Bahram F, Castell A, Cetinkaya C, Hydbring P, Weidung I, Nakayama K, Nakayama KI, et al. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol Cell 2003; 11:1189-200; PMID:12769844; http://dx.doi.org/10.1016/S1097-2765(03)00193-X
  • von der Lehr N, Johansson S, Larsson LG. Implication of the ubiquitin/proteasome system in Myc-regulated transcription. Cell Cycle 2003; 2:403-7; PMID:12963825; http://dx.doi.org/10.4161/cc.2.5.484
  • Kim SY, Herbst A, Tworkowski KA, Salghetti SE, Tansey WP. Skp2 regulates Myc protein stability and activity. Mol Cell 2003; 11:1177-88; PMID:12769843; http://dx.doi.org/10.1016/S1097-2765(03)00173-4
  • Zhang Q, Spears E, Boone DN, Li Z, Gregory MA, Hann SR. Domain-specific c-Myc ubiquitylation controls c-Myc transcriptional and apoptotic activity. Proc Natl Acad Sci U S A 2013; 110:978-83; PMID:23277542; http://dx.doi.org/10.1073/pnas.1208334110
  • Farrell AS, Pelz C, Wang X, Daniel CJ, Wang Z, Su Y, Janghorban M, Zhang X, Morgan C, Impey S, et al. Pin1 regulates the dynamics of c-Myc DNA binding to facilitate target gene regulation and oncogenesis. Mol Cell Biol 2013; 33:2930-49; PMID:23716601; http://dx.doi.org/10.1128/MCB.01455-12
  • Chan CH, Lee SW, Li CF, Wang J, Yang WL, Wu CY, Wu J, Nakayama KI, Kang HY, Huang HY, et al. Deciphering the transcriptional complex critical for RhoA gene expression and cancer metastasis. Nat Cell Biol 2010;12:457-67; PMID:20383141; http://dx.doi.org/10.1038/ncb2047
  • Li X, Bian Y, Takizawa Y, Hashimoto T, Ikoma T, Tanaka J, Kitamura N, Inagaki Y, Komada M, Tanaka T. ERK-dependent downregulation of Skp2 reduces Myc activity with HGF, leading to inhibition of cell proliferation through a decrease in Id1 expression. Mol Cancer Res 2013; 11:1437-47; PMID:24177224; http://dx.doi.org/10.1158/1541-7786.MCR-12-0718
  • Adhikary S, Marinoni F, Hock A, Hulleman E, Popov N, Beier R, Bernard S, Quarto M, Capra M, Goettig S, et al. The ubiquitin ligase HectH9 regulates transcriptional activation by Myc and is essential for tumor cell proliferation. Cell 2005; 123:409-21; PMID:16269333; http://dx.doi.org/10.1016/j.cell.2005.08.016
  • Peter S, Bultinck J, Myant K, Jaenicke LA, Walz S, Muller J, Gmachl M, Treu M, Boehmelt G, Ade CP, et al. Tumor cell-specific inhibition of MYC function using small molecule inhibitors of the HUWE1 ubiquitin ligase. EMBO Mol Med 2014; 6:1525-41; PMID:25253726; http://dx.doi.org/10.15252/emmm.201403927
  • Cepeda D, Ng HF, Sharifi HR, Mahmoudi S, Cerrato VS, Fredlund E, Magnusson K, Nilsson H, Malyukova A, Rantala J, et al. CDK-mediated activation of the SCF(FBXO) (28) ubiquitin ligase promotes MYC-driven transcription and tumourigenesis and predicts poor survival in breast cancer. EMBO Mol Med 2013; 5:999-1018; PMID:23776131; http://dx.doi.org/10.1002/emmm.201202341
  • Popov N, Schulein C, Jaenicke LA, Eilers M. Ubiquitylation of the amino terminus of Myc by SCF(β-TrCP) antagonizes SCF(Fbw7)-mediated turnover. Nat Cell Biol 2010; 12:973-81; PMID:20852628; http://dx.doi.org/10.1038/ncb2104
  • Yi YW, Kang HJ, Bae EJ, Oh S, Seong YS, Bae I. β-TrCP1 degradation is a novel action mechanism of PI3K/mTOR inhibitors in triple-negative breast cancer cells. Exp Mol Med 2015; 47, e143; PMID:25721419; http://dx.doi.org/10.1038/emm.2014.127
  • Choi SH, Wright JB, Gerber SA, Cole MD. Myc protein is stabilized by suppression of a novel E3 ligase complex in cancer cells. Genes Dev 2010; 24:1236-41; PMID:20551172; http://dx.doi.org/10.1101/gad.1920310
  • Jamal A, Swarnalatha M, Sultana S, Joshi P, Panda SK, Kumar V. The G1 phase E3 ubiquitin ligase TRUSS that gets deregulated in human cancers is a novel substrate of the S-phase E3 ubiquitin ligase Skp2. Cell Cycle, 2015; 14:2688-700; PMID:26038816; http://dx.doi.org/10.1080/15384101.2015.1056946
  • Schwamborn JC, Berezikov E, Knoblich JA. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 2009; 136:913-25; PMID:19269368; http://dx.doi.org/10.1016/j.cell.2008.12.024
  • Hakem A, Bohgaki M, Lemmers B, Tai E, Salmena L, Matysiak-Zablocki E, Jung YS, Karaskova J, Kaustov L, Duan S, et al. Role of Pirh2 in mediating the regulation of p53 and c-Myc. PLoS genetics 2011; 7:e1002360; PMID:22125490; http://dx.doi.org/10.1371/journal.pgen.1002360
  • Ballinger CA, Connell P, Wu Y, Hu Z, Thompson LJ, Yin LY, Patterson C. Identification of CHIP, a novel tetratricopeptide repeat-containing protein that interacts with heat shock proteins and negatively regulates chaperone functions. Mol Cell Biol 1999; 19:4535-45; PMID:10330192
  • Paul I, Ahmed SF, Bhowmik A, Deb S, Ghosh MK. The ubiquitin ligase CHIP regulates c-Myc stability and transcriptional activity. Oncogene 2013; 32:1284-95; PMID:22543587; http://dx.doi.org/10.1038/onc.2012.144
  • Mei Z, Zhang D, Hu B, Wang J, Shen X, a Xiao W. FBXO32 Targets c-Myc for Proteasomal Degradation and Inhibits c-Myc Activity. J Biol Chem 2015; 290:16202-14; PMID:25944903; http://dx.doi.org/10.1074/jbc.M115.645978
  • Komander D, Clague MJ, Urbe S. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol 2009; 10:550-63; PMID:19626045; http://dx.doi.org/10.1038/nrm2731
  • Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R. A genomic and functional inventory of deubiquitinating enzymes. Cell 2005; 123:773-86; PMID:16325574; http://dx.doi.org/10.1016/j.cell.2005.11.007
  • Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R, Moll R, Elledge SJ, Eilers M. The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 2007; 9:765-74; PMID:17558397; http://dx.doi.org/10.1038/ncb1601
  • Popov N, Herold S, Llamazares M, Schulein C, Eilers M. Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell cycle 2007; 6:2327-31; PMID:17873522; http://dx.doi.org/10.1016/j.celrep.2014.09.057
  • Schulein-Volk C, Wolf E, Zhu J, Xu W, Taranets L, Hellmann A, Janicke LA, Diefenbacher ME, Behrens A, Eilers M, et al. Dual regulation of Fbw7 function and oncogenic transformation by Usp28. Cell Rep 2014; 9:1099-109; PMID:25437563; http://dx.doi.org/10.1016/j.celrep.2014.09.057
  • Diefenbacher ME, Chakraborty A, Blake SM, Mitter R, Popov N, Eilers M, Behrens A. Usp28 counteracts Fbw7 in intestinal homeostasis and cancer. Cancer Res 2015; 75:1181-6; PMID:25716680; http://dx.doi.org/10.1158/0008-5472.CAN-14-1726
  • Pan J, Deng Q, Jiang C, Wang X, Niu T, Li H, Chen T, Jin J, Pan W, Cai X, et al. USP37 directly deubiquitinates and stabilizes c-Myc in lung cancer. Oncogene 2015; 34:3957-67; PMID:25284584; http://dx.doi.org/10.1038/onc.2014.327
  • Arabi A, Wu S, Ridderstrale K, Bierhoff H, Shiue C, Fatyol K, Fahlen S, Hydbring P, Soderberg O, Grummt I, et al. c-Myc associates with ribosomal DNA and activates RNA polymerase I transcription. Nat Cell Biol 2005; 7:303-10; PMID:15723053; http://dx.doi.org/10.1038/ncb1225
  • Grandori C, Gomez-Roman N, Felton-Edkins ZA, Ngouenet C, Galloway DA, Eisenman RN, White RJ. c-Myc binds to human ribosomal DNA and stimulates transcription of rRNA genes by RNA polymerase I. Nat Cell Biol 2005; 7:311-8; PMID:15723054; http://dx.doi.org/10.1038/ncb1224
  • Dai MS, Lu H. Crosstalk between c-Myc and ribosome in ribosomal biogenesis and cancer. J Cell Biochem 2008; 105:670-7; PMID:18773413; http://dx.doi.org/10.1002/jcb.21895
  • van Riggelen J, Yetil A, Felsher DW. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat Rev Cancer 2010; 10:301-9; PMID:20332779; http://dx.doi.org/10.1038/nrc2819
  • Sun XX, He X, Yin L, Komada M, Sears RC, Dai MS. The nucleolar ubiquitin-specific protease USP36 deubiquitinates and stabilizes c-Myc. Proc Natl Acad Sci U S A 2015; 112:3734-9; PMID:25775507; http://dx.doi.org/10.1073/pnas.1411713112
  • Li J, Olson LM, Zhang Z, Li L, Bidder M, Nguyen L, Pfeifer J, Rader JS. Differential display identifies overexpression of the USP36 gene, encoding a deubiquitinating enzyme, in ovarian cancer. Int J Med Sci 2008; 5:133-42; PMID:18566677; http://dx.doi.org/10.7150/ijms.5.133
  • Endo A, Kitamura N, Komada M. Nucleophosmin/B23 regulates ubiquitin dynamics in nucleoli by recruiting deubiquitylating enzyme USP36. J Biol Chem 2009; 284:27918-23; PMID:19679658; http://dx.doi.org/10.1074/jbc.M109.037218
  • Endo A, Matsumoto M, Inada T, Yamamoto A, Nakayama KI, Kitamura N, Komada M. Nucleolar structure and function are regulated by the deubiquitylating enzyme USP36. J Cell Sci 2009; 122:678-86; PMID:19208757; http://dx.doi.org/10.1242/jcs.044461
  • Richardson LA, Reed BJ, Charette JM, Freed EF, Fredrickson EK, Locke MN, Baserga SJ, Gardner RG. A conserved deubiquitinating enzyme controls cell growth by regulating RNA polymerase I stability. Cell Rep 2012; 2:372-85; PMID:22902402; http://dx.doi.org/10.1016/j.celrep.2012.07.009
  • Taillebourg E, Gregoire I, Viargues P, Jacomin AC, Thevenon D, Faure M, Fauvarque MO. The deubiquitinating enzyme USP36 controls selective autophagy activation by ubiquitinated proteins. Autophagy 2012; 8:767-79; PMID:22622177; http://dx.doi.org/10.4161/auto.19381
  • Thevenon D, Engel E, Avet-Rochex A, Gottar M, Bergeret E, Tricoire H, Benaud C, Baudier J, Taillebourg E, Fauvarque MO. The Drosophila ubiquitin-specific protease dUSP36/Scny targets IMD to prevent constitutive immune signaling. Cell Host Microbe 2009; 6:309-20; PMID:19837371; http://dx.doi.org/10.1016/j.chom.2009.09.007
  • Amati B, Sanchez-Arevalo Lobo VJ. MYC degradation: deubiquitinating enzymes enter the dance. Nat Cell Biol 2007; 9:729-31; PMID:17603505; http://dx.doi.org/10.1038/ncb0707-729

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