Deubiquitinases in cancer: new functions and therapeutic options

Deubiquitinases (DUBs) have fundamental roles in the ubiquitin system through their ability to specifically deconjugate ubiquitin from targeted proteins. The human genome encodes at least 98 DUBs, which can be grouped into 6 families, reflecting the need for specificity in their function. The activity of these enzymes affects the turnover rate, activation, recycling and localization of multiple proteins, which in turn is essential for cell homeostasis, protein stability and a wide range of signaling pathways. Consistent with this, altered DUB function has been related to several diseases, including cancer. Thus, multiple DUBs have been classified as oncogenes or tumor suppressors because of their regulatory functions on the activity of other proteins involved in tumor development. Therefore, recent studies have focused on pharmacological intervention on DUB activity as a rationale to search for novel anticancer drugs. This strategy may benefit from our current knowledge of the physiological regulatory mechanisms of these enzymes and the fact that growth of several tumors depends on the normal activity of certain DUBs. Further understanding of these processes may provide answers to multiple remaining questions on DUB functions and lead to the development of DUB-targeting strategies to expand the repertoire of molecular therapies against cancer.

[1]  C. López-Otín,et al.  The regulatory crosstalk between kinases and proteases in cancer , 2010, Nature Reviews Cancer.

[2]  Han Liu,et al.  Regulation of ErbB2 Receptor Status by the Proteasomal DUB POH1 , 2009, PloS one.

[3]  John Rush,et al.  Polyubiquitin Linkage Profiles in Three Models of Proteolytic Stress Suggest the Etiology of Alzheimer Disease* , 2011, The Journal of Biological Chemistry.

[4]  Ryan D. Morin,et al.  Mutational evolution in a lobular breast tumour profiled at single nucleotide resolution , 2009, Nature.

[5]  Ramin Massoumi,et al.  Cyld Inhibits Tumor Cell Proliferation by Blocking Bcl-3-Dependent NF-κB Signaling , 2006, Cell.

[6]  K. Lindsten,et al.  The ubiquitin specific protease 4 (USP4) is a new player in the Wnt signalling pathway , 2009 .

[7]  Gonzalo R. Ordóñez,et al.  The Degradome database: mammalian proteases and diseases of proteolysis , 2008, Nucleic Acids Res..

[8]  S. Elledge,et al.  Non-Oncogene Addiction and the Stress Phenotype of Cancer Cells , 2007, Cell.

[9]  L. Crawford,et al.  Proteasome inhibitors in cancer therapy , 2011, Journal of Cell Communication and Signaling.

[10]  A. Sorkin,et al.  RNA interference screen identifies Usp18 as a regulator of epidermal growth factor receptor synthesis. , 2009, Molecular biology of the cell.

[11]  I. Wertz,et al.  A20: from ubiquitin editing to tumour suppression , 2010, Nature Reviews Cancer.

[12]  A. Bosserhoff,et al.  Reduced expression of CYLD in human colon and hepatocellular carcinomas. , 2007, Carcinogenesis.

[13]  K. Baek,et al.  Lys-63-specific Deubiquitination of SDS3 by USP17 Regulates HDAC Activity* , 2011, The Journal of Biological Chemistry.

[14]  S. Gygi,et al.  Regulation of monoubiquitinated PCNA by DUB autocleavage , 2006, Nature Cell Biology.

[15]  K. Kinzler,et al.  Cancer genes and the pathways they control , 2004, Nature Medicine.

[16]  J. Derry,et al.  Impaired regulation of NF-kappaB and increased susceptibility to colitis-associated tumorigenesis in CYLD-deficient mice. , 2006, The Journal of clinical investigation.

[17]  L. Hartwell,et al.  Integrating genetic approaches into the discovery of anticancer drugs. , 1997, Science.

[18]  T. Ludwig,et al.  Inactivation of HAUSP in vivo modulates p53 function , 2010, Oncogene.

[19]  René Bernards,et al.  Loss of the cylindromatosis tumour suppressor inhibits apoptosis by activating NF-κB , 2003, Nature.

[20]  Jing Wang,et al.  MCP-induced protein 1 deubiquitinates TRAF proteins and negatively regulates JNK and NF-κB signaling , 2010, The Journal of experimental medicine.

[21]  P. Febbo,et al.  The isopeptidase USP2a protects human prostate cancer from apoptosis. , 2006, Cancer research.

[22]  Keith D Wilkinson,et al.  Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. , 2009, Annual review of biochemistry.

[23]  Yi Zhang Transcriptional regulation by histone ubiquitination and deubiquitination. , 2003, Genes & development.

[24]  W. Schwenk,et al.  The COP9 signalosome mediates beta-catenin degradation by deneddylation and blocks adenomatous polyposis coli destruction via USP15. , 2009, Journal of molecular biology.

[25]  K. Wilkinson Regulation of ubiquitin‐dependent processes by deubiquitinating enzymes , 1997, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[26]  A. Ashworth,et al.  Dysregulated TRK Signalling is a Therapeutic Target in CYLD Defective Tumours , 2011, Oncogene.

[27]  Howard Y. Chang,et al.  CSN5 isopeptidase activity links COP9 signalosome activation to breast cancer progression. , 2008, Cancer research.

[28]  V. Dixit,et al.  Deubiquitinases in the regulation of NF-κB signaling , 2011, Cell Research.

[29]  S. Perkins,et al.  The de-ubiquitinase UCH-L1 is an oncogene that drives the development of lymphoma in vivo by deregulating PHLPP1 and Akt signaling , 2010, Leukemia.

[30]  I. A. Rose,et al.  Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. , 1985, The Journal of biological chemistry.

[31]  Min Jae Lee,et al.  Enhancement of Proteasome Activity by a Small-Molecule Inhibitor of Usp14 , 2010, Nature.

[32]  James Lowe,et al.  Ubiquitin-like protein conjugation and the ubiquitin–proteasome system as drug targets , 2010, Nature Reviews Drug Discovery.

[33]  Jun Qin,et al.  Ubiquitin-specific Peptidase 21 Inhibits Tumor Necrosis Factor α-induced Nuclear Factor κB Activation via Binding to and Deubiquitinating Receptor-interacting Protein 1* , 2009, The Journal of Biological Chemistry.

[34]  K. Knobeloch,et al.  Essential Role of Ubiquitin-Specific Protease 8 for Receptor Tyrosine Kinase Stability and Endocytic Trafficking In Vivo , 2007, Molecular and Cellular Biology.

[35]  C. López-Otín,et al.  Proteases: Multifunctional Enzymes in Life and Disease* , 2008, Journal of Biological Chemistry.

[36]  S. Elledge,et al.  The ubiquitin-specific protease USP28 is required for MYC stability , 2007, Nature Cell Biology.

[37]  M. Naumann,et al.  CSN controls NF‐κB by deubiquitinylation of IκBα , 2007 .

[38]  F. Colland The therapeutic potential of deubiquitinating enzyme inhibitors. , 2010, Biochemical Society transactions.

[39]  G. Peters,et al.  Ubiquitin-specific proteases 7 and 11 modulate Polycomb regulation of the INK4a tumour suppressor , 2010, The EMBO journal.

[40]  J. Joyce,et al.  Proteolytic networks in cancer. , 2011, Trends in cell biology.

[41]  M. Balakirev,et al.  Otubains: a new family of cysteine proteases in the ubiquitin pathway , 2003, EMBO reports.

[42]  K. Baek,et al.  Deubiquitinating enzyme USP36 contains the PEST motif and is polyubiquitinated. , 2005, Biochemical and biophysical research communications.

[43]  G. Morgan,et al.  Gene mapping and expression analysis of 16q loss of heterozygosity identifies WWOX and CYLD as being important in determining clinical outcome in multiple myeloma. , 2007, Blood.

[44]  René Bernards,et al.  The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. , 2005, Molecular cell.

[45]  G. Salvesen,et al.  Emerging principles in protease-based drug discovery , 2010, Nature Reviews Drug Discovery.

[46]  P. Galle,et al.  Down-regulation of CYLD as a trigger for NF-κB activation and a mechanism of apoptotic resistance in hepatocellular carcinoma cells. , 2010, International journal of oncology.

[47]  J. Cheville,et al.  USP10 Regulates p53 Localization and Stability by Deubiquitinating p53 , 2010, Cell.

[48]  D. Alessi,et al.  Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. , 2008, The Biochemical journal.

[49]  T. Milman,et al.  Frequent Mutation of BAP1 in Metastasizing Uveal Melanomas , 2011 .

[50]  Pier Paolo Pandolfi,et al.  The deubiquitinylation and localization of PTEN are regulated by a HAUSP–PML network , 2008, Nature.

[51]  R. Ueda,et al.  Elevated expression of Unph, a proto-oncogene at 3p21.3, in human lung tumors. , 1995, Oncogene.

[52]  Gordon B. Mills,et al.  Derailed endocytosis: an emerging feature of cancer , 2008, Nature Reviews Cancer.

[53]  G. Glinsky Death-From-Cancer Signatures and Stem Cell Contribution to Metastatic Cancer , 2005, Cell cycle.

[54]  M. J. Clague,et al.  Endocytosis: the DUB version. , 2006, Trends in cell biology.

[55]  K. Wilkinson,et al.  Protein partners of deubiquitinating enzymes. , 2008, The Biochemical journal.

[56]  M. Reboud-Ravaux Proteasome inhibitors. , 2002, Progress in molecular and subcellular biology.

[57]  Troels Z. Kristiansen,et al.  K 63-specific deubiquitination by two JAMM / MPN þ complexes : BRISC-associated Brcc 36 and proteasomal Poh 1 , 2009 .

[58]  Qiuyan Wang,et al.  The zinc finger protein A20 targets TRAF2 to the lysosomes for degradation. , 2009, Biochimica et biophysica acta.

[59]  H. Ichijo,et al.  Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. , 2009, Molecular cell.

[60]  K. Baek,et al.  The role of deubiquitinating enzymes in apoptosis , 2010, Cellular and Molecular Life Sciences.

[61]  K. Baek,et al.  DUB-1A, a Novel Deubiquitinating Enzyme Subfamily Member, Is Polyubiquitinated and Cytokine-inducible in B-lymphocytes* , 2004, Journal of Biological Chemistry.

[62]  E. Koonin,et al.  A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. , 2000, Trends in biochemical sciences.

[63]  Takashi Matsumoto,et al.  Identification of novel chemical inhibitors for ubiquitin C-terminal hydrolase-L3 by virtual screening. , 2007, Bioorganic & medicinal chemistry.

[64]  H. Tagawa,et al.  TNFAIP3/A20 functions as a novel tumor suppressor gene in several subtypes of non-Hodgkin lymphomas. , 2009, Blood.

[65]  C. Sander,et al.  The nuclear deubiquitinase BAP1 is commonly inactivated by somatic mutations and 3p21.1 losses in malignant pleural mesothelioma , 2011, Nature Genetics.

[66]  Jian-Dong Li,et al.  The Tumor Suppressor Cylindromatosis (CYLD) Acts as a Negative Regulator for Toll-like Receptor 2 Signaling via Negative Cross-talk with TRAF6 and TRAF7* , 2005, Journal of Biological Chemistry.

[67]  K. Baek Cytokine-regulated protein degradation by the ubiquitination system. , 2006, Current protein & peptide science.

[68]  Xinna Zhang,et al.  USP 4 Inhibits p 53 through Deubiquitinating and Stabilizing ARF-BP 1 , 2011 .

[69]  Xinna Zhang,et al.  USP4 inhibits p53 through deubiquitinating and stabilizing ARF‐BP1 , 2011, The EMBO journal.

[70]  M. Kudo,et al.  USP15 plays an essential role for caspase-3 activation during Paclitaxel-induced apoptosis. , 2009, Biochemical and biophysical research communications.

[71]  A. Ciechanover,et al.  Components of ubiquitin-protein ligase system. Resolution, affinity purification, and role in protein breakdown. , 1983, The Journal of biological chemistry.

[72]  B. Aggarwal,et al.  NF-κB and cancer: how intimate is this relationship , 2010, Molecular and Cellular Biochemistry.

[73]  M. Rolfe,et al.  The human UNP locus at 3p21.31 encodes two tissue-selective, cytoplasmic isoforms with deubiquitinating activity that have reduced expression in small cell lung carcinoma cell lines , 1998, Oncogene.

[74]  K. Connelly,et al.  Histone deacetylase inhibition attenuates diabetes-associated kidney growth: potential role for epigenetic modification of the epidermal growth factor receptor. , 2011, Kidney international.

[75]  P. C. Janiesch,et al.  The Machado-Joseph disease deubiquitylase ATX-3 couples longevity and proteostasis , 2011, Nature Cell Biology.

[76]  Jun Yu,et al.  Epigenetic identification of ubiquitin carboxyl‐terminal hydrolase L1 as a functional tumor suppressor and biomarker for hepatocellular carcinoma and other digestive tumors , 2008, Hepatology.

[77]  F. Fitzpatrick,et al.  Pharmacophore model for novel inhibitors of ubiquitin isopeptidases that induce p53-independent cell death. , 2002, Molecular pharmacology.

[78]  N. Donato,et al.  Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. , 2010, Cancer research.

[79]  R. Pardi,et al.  CSN5/Jab1 controls multiple events in the mammalian cell cycle , 2010, FEBS letters.

[80]  L. Pasqualucci,et al.  The NF-{kappa}B negative regulator TNFAIP3 (A20) is inactivated by somatic mutations and genomic deletions in marginal zone lymphomas. , 2008, Blood.

[81]  A. Ciechanover,et al.  Components of Ubiquitin-Protein Ligase System , 1983 .

[82]  M. Bienz,et al.  Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains. , 2008, Genes & development.

[83]  Giuseppe Nicastro,et al.  The solution structure of the Josephin domain of ataxin-3: structural determinants for molecular recognition. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[84]  A. Levine,et al.  The p53 pathway: positive and negative feedback loops , 2005, Oncogene.

[85]  D. Durocher,et al.  The ubiquitous role of ubiquitin in the DNA damage response , 2010, DNA Repair.

[86]  P. Dijke,et al.  The deubiquitinating enzyme UCH37 interacts with Smads and regulates TGF-β signalling , 2005, Oncogene.

[87]  Akhilesh Pandey,et al.  Cloning of a novel signaling molecule, AMSH-2, that potentiates transforming growth factor β signaling , 2004, BMC Cell Biology.

[88]  J. Chin,et al.  Engineered diubiquitin synthesis reveals Lys29-isopeptide specificity of an OTU deubiquitinase. , 2010, Nature chemical biology.

[89]  K. Baek,et al.  HAUSP, a deubiquitinating enzyme for p53, is polyubiquitinated, polyneddylated, and dimerized , 2005, FEBS letters.

[90]  Ying Zhang,et al.  DUBs and cancer: The role of deubiquitinating enzymes as oncogenes, non-oncogenes and tumor suppressors , 2009, Cell cycle.

[91]  S. Aaronson,et al.  BRCA2 Is Ubiquitinated In Vivo and Interacts with USP11, a Deubiquitinating Enzyme That Exhibits Prosurvival Function in the Cellular Response to DNA Damage , 2004, Molecular and Cellular Biology.

[92]  S. Gygi,et al.  Defining the Human Deubiquitinating Enzyme Interaction Landscape , 2009, Cell.

[93]  J. Rain,et al.  Synthesis and Biological Evaluation of 9‐Oxo‐9H‐indeno[1,2‐b]pyrazine‐2,3‐dicarbonitrile Analogues as Potential Inhibitors of Deubiquitinating Enzymes , 2010, ChemMedChem.

[94]  S. H. Baek,et al.  UCH-L1 promotes cancer metastasis in prostate cancer cells through EMT induction. , 2011, Cancer letters.

[95]  M. Boutros,et al.  An RNAi screen identifies USP2 as a factor required for TNF‐α‐induced NF‐κB signaling , 2011, International journal of cancer.

[96]  N. Nakamura,et al.  Regulation of mitochondrial morphology by USP30, a deubiquitinating enzyme present in the mitochondrial outer membrane. , 2008, Molecular biology of the cell.

[97]  O. Nureki,et al.  Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains , 2008, Nature.

[98]  Erik Meulmeester,et al.  Mechanism and consequences for paralog-specific sumoylation of ubiquitin-specific protease 25. , 2008, Molecular cell.

[99]  M. Valtorta,et al.  Ataxin‐3 is subject to autolytic cleavage , 2006, The FEBS journal.

[100]  J. Fletcher,et al.  USP6 (Tre2) Fusion Oncogenes in Aneurysmal Bone Cyst , 2004, Cancer Research.

[101]  B. Kessler,et al.  PTMs in Conversation: Activity and Function of Deubiquitinating Enzymes Regulated via Post-Translational Modifications , 2011, Cell Biochemistry and Biophysics.

[102]  C. Lacroix,et al.  The Ubiquitin-Specific Protease USP34 Regulates Axin Stability and Wnt/β-Catenin Signaling , 2011, Molecular and Cellular Biology.

[103]  Mingming Jia,et al.  COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer , 2010, Nucleic Acids Res..

[104]  W. Gu,et al.  The p53–Mdm2–HAUSP complex is involved in p53 stabilization by HAUSP , 2007, Oncogene.

[105]  K. Nakayama,et al.  USP19 Deubiquitinating Enzyme Supports Cell Proliferation by Stabilizing KPC1, a Ubiquitin Ligase for p27Kip1 , 2008, Molecular and Cellular Biology.

[106]  Barrington G. Burnett,et al.  The polyglutamine neurodegenerative protein ataxin-3 binds polyubiquitylated proteins and has ubiquitin protease activity. , 2003, Human molecular genetics.

[107]  I. Adcock,et al.  Hydrogen Peroxide Prolongs Nuclear Localization of NF-κB in Activated Cells by Suppressing Negative Regulatory Mechanisms* , 2008, Journal of Biological Chemistry.

[108]  K. Gevaert,et al.  T‐cell receptor‐induced JNK activation requires proteolytic inactivation of CYLD by MALT1 , 2011, The EMBO journal.

[109]  S. Wing,et al.  Identification of Distinctive Patterns of USP19-Mediated Growth Regulation in Normal and Malignant Cells , 2011, PloS one.

[110]  P. Nuciforo,et al.  An Atlas of Altered Expression of Deubiquitinating Enzymes in Human Cancer , 2011, PloS one.

[111]  G. Hart,et al.  The Ubiquitin Carboxyl Hydrolase BAP1 Forms a Ternary Complex with YY1 and HCF-1 and Is a Critical Regulator of Gene Expression , 2010, Molecular and Cellular Biology.

[112]  Traian Sulea,et al.  High incidence of ubiquitin‐like domains in human ubiquitin‐specific proteases , 2007, Proteins.

[113]  F. Bazan,et al.  Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival , 2010, Nature.

[114]  A. Amerik,et al.  Mechanism and function of deubiquitinating enzymes. , 2004, Biochimica et biophysica acta.

[115]  Junjie Chen,et al.  The Lys63-specific Deubiquitinating Enzyme BRCC36 Is Regulated by Two Scaffold Proteins Localizing in Different Subcellular Compartments* , 2010, The Journal of Biological Chemistry.

[116]  M. Mattern,et al.  Characterization of selective ubiquitin and ubiquitin-like protease inhibitors using a fluorescence-based multiplex assay format. , 2011, Assay and drug development technologies.

[117]  Viji M. Draviam,et al.  Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities , 2007, Nature.

[118]  J. Rain,et al.  Small-molecule inhibitor of USP 7 / HAUSP ubiquitin protease stabilizes and activates p 53 in cells , 2009 .

[119]  T. Mak,et al.  DJ-1 Enhances Cell Survival through the Binding of Cezanne, a Negative Regulator of NF-κB* , 2010, The Journal of Biological Chemistry.

[120]  Z. Ronai,et al.  Ubiquitin-recognition protein Ufd1 couples the endoplasmic reticulum (ER) stress response to cell cycle control , 2011, Proceedings of the National Academy of Sciences.

[121]  Shao-Cong Sun,et al.  Negative Regulation of JNK Signaling by the Tumor Suppressor CYLD* , 2004, Journal of Biological Chemistry.

[122]  D. Malide,et al.  JTV1 co‐activates FBP to induce USP29 transcription and stabilize p53 in response to oxidative stress , 2011, The EMBO journal.

[123]  Alan Ashworth,et al.  Synthetic lethal approaches to breast cancer therapy , 2010, Nature Reviews Clinical Oncology.

[124]  Xiaohua Li,et al.  Relative structural and functional roles of multiple deubiquitylating proteins associated with mammalian 26S proteasome. , 2007, Molecular biology of the cell.

[125]  Songbin Fu,et al.  USP4 targets TAK1 to downregulate TNFα-induced NF-κB activation , 2011, Cell Death and Differentiation.

[126]  Dengwen Li,et al.  CYLD regulates angiogenesis by mediating vascular endothelial cell migration. , 2010, Blood.

[127]  Ziad M. Eletr,et al.  An Emerging Model for BAP1’s Role in Regulating Cell Cycle Progression , 2011, Cell Biochemistry and Biophysics.

[128]  A. Oberst,et al.  Proteasome inhibitors in cancer therapy: death by indigestion , 2005, Cell Death and Differentiation.

[129]  C. Glass,et al.  A histone H2A deubiquitinase complex coordinating histone acetylation and H1 dissociation in transcriptional regulation. , 2007, Molecular cell.

[130]  H. Paulson,et al.  Ubiquitination directly enhances activity of the deubiquitinating enzyme ataxin‐3 , 2009, The EMBO journal.

[131]  Keith D Wilkinson,et al.  BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression , 1998, Oncogene.

[132]  Yigong Shi,et al.  Structure and mechanisms of the proteasome‐associated deubiquitinating enzyme USP14 , 2005, The EMBO journal.

[133]  M. Naumann,et al.  CSN controls NF-kappaB by deubiquitinylation of IkappaBalpha. , 2007, The EMBO journal.

[134]  R. Beyaert,et al.  ABINs: A20 binding inhibitors of NF-kappa B and apoptosis signaling. , 2009, Biochemical pharmacology.

[135]  C. López-Otín,et al.  Protease degradomics: A new challenge for proteomics , 2002, Nature Reviews Molecular Cell Biology.

[136]  J. F. Burrows,et al.  The deubiquitinating enzyme USP17 is essential for GTPase subcellular localization and cell motility , 2011, Nature communications.

[137]  H. Clevers,et al.  Loss of the tumor suppressor CYLD enhances Wnt/beta-catenin signaling through K63-linked ubiquitination of Dvl. , 2010, Molecular cell.

[138]  J. E. V. van Leeuwen,et al.  UBPY-mediated Epidermal Growth Factor Receptor (EGFR) De-ubiquitination Promotes EGFR Degradation* , 2007, Journal of Biological Chemistry.

[139]  H. Stein,et al.  Differential expression and function of A20 and TRAF1 in Hodgkin lymphoma and anaplastic large cell lymphoma and their induction by CD30 stimulation , 2003, The Journal of pathology.

[140]  P. Evans,et al.  NF-kappaB suppression by the deubiquitinating enzyme Cezanne: a novel negative feedback loop in pro-inflammatory signaling. , 2008, The Journal of biological chemistry.

[141]  A. Ashworth,et al.  The structure of the CYLD USP domain explains its specificity for Lys63-linked polyubiquitin and reveals a B box module. , 2008, Molecular cell.

[142]  J. Coulson,et al.  Deciphering histone 2A deubiquitination , 2008, Genome Biology.

[143]  P. Lansbury,et al.  Reversible Monoubiquitination Regulates the Parkinson Disease-associated Ubiquitin Hydrolase UCH-L1*♦ , 2007, Journal of Biological Chemistry.

[144]  W. Birchmeier,et al.  Wnt signalling and its impact on development and cancer , 2008, Nature Reviews Cancer.

[145]  F. Giancotti,et al.  Faculty Opinions recommendation of Cyld inhibits tumor cell proliferation by blocking Bcl-3-dependent NF-kappaB signaling. , 2006 .

[146]  M. Cazales,et al.  A screen for deubiquitinating enzymes involved in the G2/M checkpoint identifies USP50 as a regulator of HSP90-dependent Wee1 stability , 2010, Cell cycle.

[147]  B. Turk Targeting proteases: successes, failures and future prospects , 2006, Nature Reviews Drug Discovery.

[148]  David Komander,et al.  Lys11-linked ubiquitin chains adopt compact conformations and are preferentially hydrolyzed by the deubiquitinase Cezanne , 2010, Nature Structural &Molecular Biology.

[149]  E. Messing,et al.  Identification of a deubiquitinating enzyme subfamily as substrates of the von Hippel-Lindau tumor suppressor. , 2002, Biochemical and biophysical research communications.

[150]  Kermit L. Carraway,et al.  Neuregulin-Induced ErbB3 Downregulation Is Mediated by a Protein Stability Cascade Involving the E3 Ubiquitin Ligase Nrdp1 , 2007, Molecular and Cellular Biology.

[151]  H. Paulson,et al.  The Deubiquitinating Enzyme Ataxin-3, a Polyglutamine Disease Protein, Edits Lys63 Linkages in Mixed Linkage Ubiquitin Chains* , 2008, Journal of Biological Chemistry.

[152]  Pier Paolo Di Fiore,et al.  Deubiquitinating function of ataxin-3: insights from the solution structure of the Josephin domain. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[153]  W. Gu,et al.  Suppression of cancer cell growth by promoting cyclin D1 degradation. , 2009, Molecular cell.

[154]  A. Bosserhoff,et al.  GLI1-dependent transcriptional repression of CYLD in basal cell carcinoma , 2011, Oncogene.

[155]  M. Glickman,et al.  Deubiquitinating enzymes are IN/(trinsic to proteasome function). , 2004, Current protein & peptide science.

[156]  Carlos López-Otín,et al.  Protease Addiction and Synthetic Lethality in Cancer , 2011, Front. Oncol..

[157]  F. Colland,et al.  Patented small molecule inhibitors in the ubiquitin proteasome system , 2007, BMC Biochemistry.

[158]  L. Komuves,et al.  Ubiquitin hydrolase Dub3 promotes oncogenic transformation by stabilizing Cdc25A , 2010, Nature Cell Biology.

[159]  Víctor Quesada,et al.  Cloning and enzymatic analysis of 22 novel human ubiquitin-specific proteases. , 2004, Biochemical and biophysical research communications.

[160]  H. Ploegh,et al.  Mechanisms, biology and inhibitors of deubiquitinating enzymes. , 2007, Nature chemical biology.

[161]  M. Saville,et al.  The deubiquitinating enzyme USP2a regulates the p53 pathway by targeting Mdm2 , 2007, The EMBO journal.

[162]  X. Puente,et al.  Human and mouse proteases: a comparative genomic approach , 2003, Nature Reviews Genetics.

[163]  A. Moustakas,et al.  Actions of TGF-beta as tumor suppressor and pro-metastatic factor in human cancer. , 2007, Biochimica et biophysica acta.

[164]  T. Sixma,et al.  Ubiquitin-specific protease 4 is inhibited by its ubiquitin-like domain , 2011, EMBO reports.

[165]  Yvonne A. Evrard,et al.  Gcn5 and SAGA regulate shelterin protein turnover and telomere maintenance. , 2009, Molecular cell.

[166]  Muyang Li,et al.  Crystal Structure of a UBP-Family Deubiquitinating Enzyme in Isolation and in Complex with Ubiquitin Aldehyde , 2002, Cell.

[167]  M. Chevrette,et al.  The Unp proto-oncogene encodes a nuclear protein. , 1994, Oncogene.

[168]  L. Fitzpatrick,et al.  Deubiquitinating enzyme CYLD negatively regulates the ubiquitin-dependent kinase Tak1 and prevents abnormal T cell responses , 2007, The Journal of experimental medicine.

[169]  A. D’Andrea,et al.  Analysis of cis-acting sequences and trans-acting factors regulating the interleukin-3 response element of the DUB-1 gene. , 1999, Biochimica et biophysica acta.

[170]  Troels Z. Kristiansen,et al.  K63‐specific deubiquitination by two JAMM/MPN+ complexes: BRISC‐associated Brcc36 and proteasomal Poh1 , 2009, The EMBO journal.

[171]  A. Ciechanover,et al.  The 26 S Proteasome: From Basic Mechanisms to Drug Targeting* , 2009, The Journal of Biological Chemistry.

[172]  David Komander,et al.  Molecular discrimination of structurally equivalent Lys 63‐linked and linear polyubiquitin chains , 2009, EMBO reports.

[173]  Peter T Lansbury,et al.  Discovery of inhibitors that elucidate the role of UCH-L1 activity in the H1299 lung cancer cell line. , 2003, Chemistry & biology.

[174]  F. Rosselli,et al.  USP1 deubiquitinase maintains phosphorylated CHK1 by limiting its DDB1-dependent degradation , 2011, Human molecular genetics.

[175]  Leonardo Morsut,et al.  FAM/USP9x, a Deubiquitinating Enzyme Essential for TGFβ Signaling, Controls Smad4 Monoubiquitination , 2009, Cell.

[176]  J. Rain,et al.  Small-molecule inhibitor of USP7/HAUSP ubiquitin protease stabilizes and activates p53 in cells , 2009, Molecular Cancer Therapeutics.

[177]  D. Lane,et al.  The deubiquitinating enzyme USP 2 a regulates the p 53 pathway by targeting Mdm 2 , 2013 .

[178]  S. Dent,et al.  The role of deubiquitinating enzymes in chromatin regulation , 2011, FEBS letters.

[179]  T. Sixma,et al.  Usp39 is essential for mitotic spindle checkpoint integrity and controls mRNA-levels of Aurora B , 2008, Cell cycle.

[180]  S. Elledge,et al.  The tumor suppressor CYLD regulates entry into mitosis , 2007, Proceedings of the National Academy of Sciences.

[181]  F. Colland,et al.  Targeting ubiquitin specific proteases for drug discovery. , 2008, Biochimie.

[182]  K. Lindsten,et al.  The ubiquitin specific protease 4 (USP4) is a new player in the Wnt signalling pathway , 2009, Journal of cellular and molecular medicine.

[183]  M. Washburn,et al.  Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. , 2008, Molecular cell.

[184]  Claude C. Warzecha,et al.  The putative cancer stem cell marker USP22 is a subunit of the human SAGA complex required for activated transcription and cell-cycle progression. , 2008, Molecular cell.

[185]  J. F. Burrows,et al.  DUB-3, a Cytokine-inducible Deubiquitinating Enzyme That Blocks Proliferation* , 2004, Journal of Biological Chemistry.

[186]  M. Komada,et al.  Nucleolar structure and function are regulated by the deubiquitylating enzyme USP36 , 2009, Journal of Cell Science.

[187]  T. Mak,et al.  A Role for the Deubiquitinating Enzyme USP28 in Control of the DNA-Damage Response , 2006, Cell.

[188]  A. Sorkin,et al.  Usp18 Regulates Epidermal Growth Factor (EGF) Receptor Expression and Cancer Cell Survival via MicroRNA-7* , 2011, The Journal of Biological Chemistry.

[189]  V. Dixit,et al.  Deubiquitinase USP37 is activated by CDK2 to antagonize APC(CDH1) and promote S phase entry. , 2011, Molecular cell.

[190]  P. Marynen,et al.  T cell antigen receptor stimulation induces MALT1 paracaspase–mediated cleavage of the NF-κB inhibitor A20 , 2008, Nature Immunology.

[191]  W. Kaelin The Concept of Synthetic Lethality in the Context of Anticancer Therapy , 2005, Nature Reviews Cancer.

[192]  E. Messing,et al.  Ubiquitination of a Novel Deubiquitinating Enzyme Requires Direct Binding to von Hippel-Lindau Tumor Suppressor Protein* , 2002, The Journal of Biological Chemistry.

[193]  David Komander,et al.  Breaking the chains: structure and function of the deubiquitinases , 2009, Nature Reviews Molecular Cell Biology.

[194]  F. Colland,et al.  FOXO4 transcriptional activity is regulated by monoubiquitination and USP7/HAUSP , 2006, Nature Cell Biology.

[195]  Vishva M. Dixit,et al.  Ubiquitylation in apoptosis: a post-translational modification at the edge of life and death , 2011, Nature Reviews Molecular Cell Biology.

[196]  L. Horev,et al.  CYLD mutations in familial skin appendage tumours , 2008, Journal of Medical Genetics.

[197]  Carlos López-Otín,et al.  A genomic analysis of rat proteases and protease inhibitors. , 2004, Genome research.

[198]  N. Donato,et al.  Bcr-Abl ubiquitination and Usp9x inhibition block kinase signaling and promote CML cell apoptosis. , 2011, Blood.

[199]  Qiaojun He,et al.  Preclinical Development Synergistic Antitumor Activity of Gemcitabine and ABT-737 In Vitro and In Vivo through Disrupting the Interaction of USP 9 X and Mcl-1 , 2011 .

[200]  Hengbin Wang,et al.  Regulation of cell cycle progression and gene expression by H2A deubiquitination , 2007, Nature.

[201]  A. Giaccia,et al.  Harnessing synthetic lethal interactions in anticancer drug discovery , 2011, Nature Reviews Drug Discovery.

[202]  Somasekar Seshagiri,et al.  De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-κB signalling , 2004, Nature.

[203]  L. Eckmann,et al.  Interleukin 1 receptor signaling regulates DUBA expression and facilitates Toll-like receptor 9–driven antiinflammatory cytokine production , 2010, The Journal of experimental medicine.

[204]  M. Loda,et al.  The isopeptidase USP2a regulates the stability of fatty acid synthase in prostate cancer. , 2004, Cancer cell.

[205]  J. F. Burrows,et al.  The deubiquitinating enzyme USP17 is highly expressed in tumor biopsies, is cell cycle regulated, and is required for G1-S progression. , 2010, Cancer research.

[206]  M. Glickman,et al.  Complementary Roles for Rpn11 and Ubp6 in Deubiquitination and Proteolysis by the Proteasome* , 2004, Journal of Biological Chemistry.

[207]  J. McCullough,et al.  AMSH is an endosome-associated ubiquitin isopeptidase , 2004, The Journal of cell biology.

[208]  Y. Miki,et al.  The Deubiquitinating Enzyme USP11 Controls an IκB Kinase α (IKKα)-p53 Signaling Pathway in Response to Tumor Necrosis Factor α (TNFα)* , 2007, Journal of Biological Chemistry.

[209]  G. Dianov,et al.  USP47 is a deubiquitylating enzyme that regulates base excision repair by controlling steady-state levels of DNA polymerase β. , 2011, Molecular cell.

[210]  D. Lane,et al.  Suppression of the Deubiquitinating Enzyme USP5 Causes the Accumulation of Unanchored Polyubiquitin and the Activation of p53* , 2009, Journal of Biological Chemistry.

[211]  C. Dumontet,et al.  A20/TNFAIP3, a new estrogen-regulated gene that confers tamoxifen resistance in breast cancer cells , 2007, Oncogene.

[212]  E. Messing,et al.  VHL protein‐interacting deubiquitinating enzyme 2 deubiquitinates and stabilizes HIF‐1α , 2005, EMBO reports.

[213]  Ivan Dikic,et al.  Atypical ubiquitin chains: new molecular signals , 2008, EMBO reports.

[214]  A. D’Andrea,et al.  The USP1/UAF1 Complex Promotes Double-Strand Break Repair through Homologous Recombination , 2011, Molecular and Cellular Biology.