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Review

Putative Role of SUMOylation in Controlling the Activity of Deubiquitinating Enzymes in Cancer

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Pages 565-574 | Received 08 Sep 2015, Accepted 06 Nov 2015, Published online: 18 Jan 2016

References

  • Ikeda F , DikicI. Atypical ubiquitin chains: new molecular signals. ‘Protein Modifications: Beyond the Usual Suspects’ review series. EMBO Rep.9(6), 536–542 (2008).
  • Li W , YeY. Polyubiquitin chains: functions, structures, and mechanisms. Cell. Mol. Life Sci.65(15), 2397–2406 (2008).
  • Kulathu Y , KomanderD. Atypical ubiquitylation – the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat. Rev. Mol. Cell Biol.13(8), 508–523 (2012).
  • Reyes-Turcu FE , VentiiKH, WilkinsonKD. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem.78, 363–397 (2009).
  • Amerik AY , HochstrasserM. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta1695(1–3), 189–207 (2004).
  • Ventii KH , WilkinsonKD. Protein partners of deubiquitinating enzymes. Biochem. J.414, 161–175 (2008).
  • Bhattacharya S , GhoshMK. Cell death and deubiquitinases: perspectives in cancer. Biomed Res. Int.2014, 435197 (2014).
  • Hussain S , ZhangY, GalardyPJ. DUBs and cancer: the role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors. Cell Cycle8(11), 1688–1697 (2009).
  • Massoumi R . CYLD: a deubiquitination enzyme with multiple roles in cancer. Future Oncol.7(2), 285–297 (2011).
  • Pal A , YoungMA, DonatoNJ. Emerging potential of therapeutic targeting of ubiquitin-specific proteases in the treatment of cancer. Cancer Res.74(18), 4955–4966 (2014).
  • Nijman SM , Luna-VargasMP, VeldsAet al. A genomic and functional inventory of deubiquitinating enzymes. Cell123(5), 773–786 (2005).
  • Evers MM , ToonenLJ, Van Roon-MomWM. Ataxin-3 protein and RNA toxicity in spinocerebellar ataxia type 3: current insights and emerging therapeutic strategies. Mol. Neurobiol.49(3), 1513–1531 (2014).
  • Ward JM , La SpadaAR. Ataxin-3, DNA damage repair, and SCA3 cerebellar degeneration: on the path to parsimony?PLoS Genet.11(1), e1004937 (2015).
  • Winborn BJ , TravisSM, TodiSVet al. The deubiquitinating enzyme ataxin-3, a polyglutamine disease protein, edits Lys63 linkages in mixed linkage ubiquitin chains. J. Biol. Chem.283(39), 26436–26443 (2008).
  • Faesen AC , Luna-VargasMP, SixmaTK. The role of UBL domains in ubiquitin-specific proteases. Biochem. Soc. Trans.40(3), 539–545 (2012).
  • Geiss-Friedlander R , MelchiorF. Concepts in sumoylation: a decade on. Nat. Rev. Mol. Cell Biol.8(12), 947–956 (2007).
  • Wilkinson KA , HenleyJM. Mechanisms, regulation and consequences of protein SUMOylation. Biochem. J.428(2), 133–145 (2010).
  • Kim JH , BaekSH. Emerging roles of desumoylating enzymes. Biochim. Biophys. Acta1792(3), 155–162 (2009).
  • Flotho A , MelchiorF. Sumoylation: a regulatory protein modification in health and disease. Annu. Rev. Biochem.82, 357–385 (2013).
  • Gareau JR , LimaCD. The SUMO pathway: emerging mechanisms that shape specificity, conjugation and recognition. Nat. Rev. Mol. Cell Biol.11(12), 861–871 (2010).
  • Desterro JM , RodriguezMS, HayRT. SUMO-1 modification of IkappaBalpha inhibits NF-kappaB activation. Mol. Cell2(2), 233–239 (1998).
  • Carter S , BischofO, DejeanA, VousdenKH. C-terminal modifications regulate MDM2 dissociation and nuclear export of p53. Nat. Cell Biol.9(4), 428–435 (2007).
  • Santiago A , LiD, ZhaoLY, GodseyA, LiaoD. p53 SUMOylation promotes its nuclear export by facilitating its release from the nuclear export receptor CRM1. Mol. Biol. Cell24(17), 2739–2752 (2013).
  • Huang TT , Wuerzberger-DavisSM, WuZH, MiyamotoS. Sequential modification of NEMO/IKKgamma by SUMO-1 and ubiquitin mediates NF-kappaB activation by genotoxic stress. Cell115(5), 565–576 (2003).
  • Burnett B , LiF, PittmanRN. The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. Hum. Mol. Genet.12(23), 3195–3205 (2003).
  • Guzzo CM , MatunisMJ. Expanding SUMO and ubiquitin-mediated signaling through hybrid SUMO-ubiquitin chains and their receptors. Cell Cycle12(7), 1015–1017 (2013).
  • Gusella JF , MacdonaldME. Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat. Rev. Neurosci.1(2), 109–115 (2000).
  • Tang B , LiuC, ShenLet al. Frequency of SCA1, SCA2, SCA3/MJD, SCA6, SCA7, and DRPLA CAG trinucleotide repeat expansion in patients with hereditary spinocerebellar ataxia from Chinese kindreds. Arch. Neurol.57(4), 540–544 (2000).
  • Riley BE , ZoghbiHY, OrrHT. SUMOylation of the polyglutamine repeat protein, ataxin-1, is dependent on a functional nuclear localization signal. J. Biol. Chem.280(23), 21942–21948 (2005).
  • Janer A , WernerA, Takahashi-FujigasakiJet al. SUMOylation attenuates the aggregation propensity and cellular toxicity of the polyglutamine expanded ataxin-7. Hum. Mol. Genet.19(1), 181–195 (2010).
  • Shen L , TangJG, TangBSet al. Research on screening and identification of proteins interacting with ataxin-3. Zhonghua Yi Xue Yi Chuan Xue Za Zhi22(3), 242–247 (2005).
  • Zhou YF , LiaoSS, LuoYYet al. SUMO-1 modification on K166 of polyQ-expanded ataxin-3 strengthens its stability and increases its cytotoxicity. PLoS ONE8(1), e54214 (2013).
  • Almeida B , AbreuIA, MatosCAet al. SUMOylation of the brain-predominant Ataxin-3 isoform modulates its interaction with p97. Biochim. Biophys. Acta1852(9), 1950–1959 (2015).
  • Ye Y , MeyerHH, RapoportTA. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol.162(1), 71–84 (2003).
  • Dantuma NP , HoppeT. Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin. Trends Cell Biol.22(9), 483–491 (2012).
  • Fessart D , MarzaE, TaoujiS, DelomF, ChevetE. P97/CDC-48: proteostasis control in tumor cell biology. Cancer Lett.337(1), 26–34 (2013).
  • Faggiano S , MenonRP, KellyGPet al. Allosteric regulation of deubiquitylase activity through ubiquitination. Front. Mol. Biosci.2, 2 (2015).
  • Sacco JJ , YauTY, DarlingSet al. The deubiquitylase ataxin-3 restricts PTEN transcription in lung cancer cells. Oncogene33(33), 4265–4272 (2014).
  • Bignell GR , WarrenW, SealSet al. Identification of the familial cylindromatosis tumour-suppressor gene. Nat. Genet.25(2), 160–165 (2000).
  • Saito K , KigawaT, KoshibaSet al. The CAP-Gly domain with the proline-rich of CYLD associates sequence in NEMO/IKK gamma. Structure12(9), 1719–1728 (2004).
  • Gao J , HuoL, SunXet al. The tumor suppressor CYLD regulates microtubule dynamics and plays a role in cell migration. J. Biol. Chem.283(14), 8802–8809 (2008).
  • Sun L , GaoJ, HuoLet al. Tumour suppressor CYLD is a negative regulator of the mitotic kinase Aurora-B. J. Pathol.221(4), 425–432 (2010).
  • Wickstrom SA , MasoumiKC, KhochbinS, FasslerR, MassoumiR. CYLD negatively regulates cell-cycle progression by inactivating HDAC6 and increasing the levels of acetylated tubulin. EMBO J.29(1), 131–144 (2010).
  • Komander D , LordCJ, ScheelHet al. The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B box module. Mol. Cell29(4), 451–464 (2008).
  • Masoumi KC , Shaw-HallgrenG, MassoumiR. Tumor suppressor function of CYLD in nonmelanoma skin cancer. J. Skin Cancer2011, 614097 (2011).
  • Massoumi R . Ubiquitin chain cleavage: CYLD at work. Trends Biochem. Sci.35(7), 392–399 (2010).
  • Trompouki E , HatzivassiliouE, TsichritzisT, FarmerH, AshworthA, MosialosG. CYLD is a deubiquitinating enzyme that negatively regulates NF-kappa B activation by TNFR family members. Nature424(6950), 793–796 (2003).
  • Kovalenko A , Chable-BessiaC, CantarellaG, IsraelA, WallachD, CourtoisG. The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature424(6950), 801–805 (2003).
  • Brummelkamp TR , NijmanSMB, DiracAMG, BernardsR. Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-kappa B. Nature424(6950), 797–801 (2003).
  • Kobayashi T , MasoumiKC, MassoumiR. Deubiquitinating activity of CYLD is impaired by SUMOylation in neuroblastoma cells. Oncogene34(17), 2251–2260 (2015).
  • Valero R , MarfanyG, Gonzalez-AnguloO, Gonzalez-GonzalezG, PuellesL, Gonzalez-DuarteR. USP25, a novel gene encoding a deubiquitinating enzyme, is located in the gene-poor region 21q11.2. Genomics62(3), 395–405 (1999).
  • Zhong B , LiuX, WangXet al. Negative regulation of IL-17-mediated signaling and inflammation by the ubiquitin-specific protease USP25. Nat. Immunol.13(11), 1110–1117 (2012).
  • Ma AI . The ubiquitous nature of IL-17. Nat. Immunol.13(11), 1034–1035 (2012).
  • Li J , TanQ, YanMet al. miRNA-200c inhibits invasion and metastasis of human non-small cell lung cancer by directly targeting ubiquitin specific peptidase 25. Mol. Cancer13, 166 (2014).
  • Blount JR , BurrAA, DenucA, MarfanyG, TodiSV. Ubiquitin-specific protease 25 functions in endoplasmic reticulum-associated degradation. PLoS ONE7(5), e36542 (2012).
  • Jung ES , HongH, KimC, Mook-JungI. Acute ER stress regulates amyloid precursor protein processing through ubiquitin-dependent degradation. Sci. Rep.5, 8805 (2015).
  • Kim S , LeeD, LeeJ, SongH, KimHJ, KimKT. Vaccinia-related kinase 2 controls the stability of the eukaryotic chaperonin TRiC/CCT by inhibiting the deubiquitinating enzyme USP25. Mol. Cell. Biol.35(10), 1754–1762 (2015).
  • Meulmeester E , KunzeM, HsiaoHH, UrlaubH, MelchiorF. Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. Mol. Cell30(5), 610–619 (2008).
  • Denuc A , Bosch-ComasA, Gonzalez-DuarteR, MarfanyG. The UBA-UIM domains of the USP25 regulate the enzyme ubiquitination state and modulate substrate recognition. PLoS ONE4(5), e5571 (2009).
  • Cholay M , ReverdyC, BenarousR, CollandF, DavietL. Functional interaction between the ubiquitin-specific protease 25 and the SYK tyrosine kinase. Exp. Cell Res.316(4), 667–675 (2010).
  • Deng S , ZhouH, XiongRet al. Over-expression of genes and proteins of ubiquitin specific peptidases (USPs) and proteasome subunits (PSs) in breast cancer tissue observed by the methods of RFDD-PCR and proteomics. Breast Cancer Res. Treat.104(1), 21–30 (2007).
  • Valero R , BayesM, Francisca Sanchez-FontM, Gonzalez-AnguloO, Gonzalez-DuarteR, MarfanyG. Characterization of alternatively spliced products and tissue-specific isoforms of USP28 and USP25. Genome Biol.2(10), RESEARCH0043 (2001).
  • Zhang D , ZauggK, MakTW, ElledgeSJ. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell126(3), 529–542 (2006).
  • Jacq X , KempM, MartinNM, JacksonSP. Deubiquitylating enzymes and DNA damage response pathways. Cell Biochem. Biophys.67(1), 25–43 (2013).
  • Knobel PA , BelotserkovskayaR, GalantyY, SchmidtCK, JacksonSP, StrackerTH. USP28 is recruited to sites of DNA damage by the tandem BRCT domains of 53BP1 but plays a minor role in double-strand break metabolism. Mol. Cell. Biol.34(11), 2062–2074 (2014).
  • Bassermann F , FrescasD, GuardavaccaroD, BusinoL, PeschiaroliA, PaganoM. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell134(2), 256–267 (2008).
  • Zhen Y , KnobelPA, StrackerTH, ReverterD. Regulation of USP28 deubiquitinating activity by SUMO conjugation. J. Biol. Chem.289(50), 34838–34850 (2014).
  • Popov N , WanzelM, MadiredjoMet al. The ubiquitin-specific protease USP28 is required for MYC stability. Nat. Cell Biol.9(7), 765–774 (2007).
  • Diefenbacher ME , PopovN, BlakeSMet al. The deubiquitinase USP28 controls intestinal homeostasis and promotes colorectal cancer. J. Clin. Invest.124(8), 3407–3418 (2014).
  • Popov N , HeroldS, LlamazaresM, SchuleinC, EilersM. Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell Cycle6(19), 2327–2331 (2007).
  • Zhang L , XuB, QiangYet al. Overexpression of deubiquitinating enzyme USP28 promoted non-small cell lung cancer growth. J. Cell. Mol. Med.19(4), 799–805 (2015).
  • Lygerou Z , ChristophidesG, SeraphinB. A novel genetic screen for snRNP assembly factors in yeast identifies a conserved protein, Sad1p, also required for pre-mRNA splicing. Mol. Cell. Biol.19(3), 2008–2020 (1999).
  • Makarova OV , MakarovEM, LuhrmannR. The 65 and 110 kDa SR-related proteins of the U4/U6.U5 tri-snRNP are essential for the assembly of mature spliceosomes. EMBO J.20(10), 2553–2563 (2001).
  • Hadjivassiliou H , RosenbergOS, GuthrieC. The crystal structure of S. cerevisiae Sad1, a catalytically inactive deubiquitinase that is broadly required for pre-mRNA splicing. RNA20(5), 656–669 (2014).
  • Van Leuken RJ , Luna-VargasMP, SixmaTK, WolthuisRM, MedemaRH. Usp39 is essential for mitotic spindle checkpoint integrity and controls mRNA-levels of aurora B. Cell Cycle7(17), 2710–2719 (2008).
  • Rios Y , MelmedS, LinS, LiuNA. Zebrafish usp39 mutation leads to rb1 mRNA splicing defect and pituitary lineage expansion. PLoS Genet.7(1), e1001271 (2011).
  • Liu S , LiuX, WangHet al. Lentiviral vector-mediated doxycycline-inducible USP39 shRNA or cDNA expression in triple-negative breast cancer cells. Oncol. Rep.33(5), 2477–2483 (2015).
  • Pan Z , PanH, ZhangJet al. Lentivirus mediated silencing of ubiquitin specific peptidase 39 inhibits cell proliferation of human hepatocellular carcinoma cells in vitro. Biol. Res.48(1), 18 (2015).
  • Wang H , JiX, LiuXet al. Lentivirus-mediated inhibition of USP39 suppresses the growth of breast cancer cells in vitro. Oncol. Rep.30(6), 2871–2877 (2013).
  • Wen D , XuZ, XiaLet al. Important role of SUMOylation of Spliceosome factors in prostate cancer cells. J. Proteome Res.13(8), 3571–3582 (2014).
  • Denuc A , MarfanyG. SUMO and ubiquitin paths converge. Biochem. Soc. Trans.38(Pt 1), 34–39 (2010).
  • Kessler BM , EdelmannMJ. PTMs in conversation: activity and function of deubiquitinating enzymes regulated via post-translational modifications. Cell Biochem. Biophys.60(1–2), 21–38 (2011).
  • Rodriguez JA . Interplay between nuclear transport and ubiquitin/SUMO modifications in the regulation of cancer-related proteins. Semin. Cancer Biol.27, 11–19 (2014).

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