Role of Deubiquitinating Enzymes in DNA Repair

ABSTRACT Both proteolytic and nonproteolytic functions of ubiquitination are essential regulatory mechanisms for promoting DNA repair and the DNA damage response in mammalian cells. Deubiquitinating enzymes (DUBs) have emerged as key players in the maintenance of genome stability. In this minireview, we discuss the recent findings on human DUBs that participate in genome maintenance, with a focus on the role of DUBs in the modulation of DNA repair and DNA damage signaling.

[1]  V. Smits,et al.  Dub3 controls DNA damage signalling by direct deubiquitination of H2AX , 2017, Molecular oncology.

[2]  Edward S. Miller,et al.  USP7 is essential for maintaining Rad18 stability and DNA damage tolerance , 2016, Oncogene.

[3]  J. Huibregtse,et al.  Ubiquitin‐Activated Interaction Traps (UBAITs) identify E3 ligase binding partners , 2015, EMBO reports.

[4]  Chunaram Choudhary,et al.  Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage , 2015, Nature.

[5]  S. Jackson,et al.  USP4 Auto-Deubiquitylation Promotes Homologous Recombination , 2015, Molecular cell.

[6]  L. Symington,et al.  Mre11-Sae2 and RPA Collaborate to Prevent Palindromic Gene Amplification. , 2015, Molecular cell.

[7]  J. Masson,et al.  The RNF138 E3 ligase displaces Ku to promote DNA end resection and regulate DNA repair pathway choice , 2015, Nature Cell Biology.

[8]  W. Gu,et al.  USP11 Is a Negative Regulator to γH2AX Ubiquitylation by RNF8/RNF168* , 2015, The Journal of Biological Chemistry.

[9]  X. Xia,et al.  Evolution of the highly networked deubiquitinating enzymes USP4, USP15, and USP11 , 2015, BMC Evolutionary Biology.

[10]  W. Guo,et al.  The Deubiquitylating Enzyme USP4 Cooperates with CtIP in DNA Double-Strand Break End Resection. , 2015, Cell reports.

[11]  Matylda Sczaniecka-Clift,et al.  Systematic E2 screening reveals a UBE2D–RNF138–CtIP axis promoting DNA repair , 2015, Nature Cell Biology.

[12]  N. Mailand,et al.  SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair , 2015, Nature Communications.

[13]  H. van Attikum,et al.  The de-ubiquitylating enzymes USP26 and USP37 regulate homologous recombination by counteracting RAP80 , 2015, Nucleic acids research.

[14]  N. Mosammaparast,et al.  Noncanonical regulation of alkylation damage resistance by the OTUD4 deubiquitinase , 2015, The EMBO journal.

[15]  Peter Bouwman,et al.  REV7 counteracts DNA double-strand break resection and affects PARP inhibition , 2015, Nature.

[16]  J. Olsen,et al.  Ubiquitin-specific Protease 11 (USP11) Deubiquitinates Hybrid Small Ubiquitin-like Modifier (SUMO)-Ubiquitin Chains to Counteract RING Finger Protein 4 (RNF4)* , 2015, The Journal of Biological Chemistry.

[17]  Jürgen Cox,et al.  Proteomics reveals dynamic assembly of repair complexes during bypass of DNA cross-links , 2015, Science.

[18]  J. Lukas,et al.  Ectopic expression of RNF168 and 53BP1 increases mutagenic but not physiological non-homologous end joining , 2015, Nucleic acids research.

[19]  G. Wani,et al.  USP7 deubiquitinase promotes ubiquitin-dependent DNA damage signaling by stabilizing RNF168* , 2015, Cell cycle.

[20]  P. Jallepalli,et al.  ATR-mediated phosphorylation of FANCI regulates dormant origin firing in response to replication stress. , 2015, Molecular cell.

[21]  Anindya Dutta,et al.  MCM8-9 complex promotes resection of double-strand break ends by MRE11-RAD50-NBS1 complex , 2015, Nature Communications.

[22]  D. Durocher,et al.  MAD2L2 controls DNA repair at telomeres and DNA breaks by inhibiting 5′ end-resection , 2015, Nature.

[23]  D. Stuart,et al.  The Human Otubain2-Ubiquitin Structure Provides Insights into the Cleavage Specificity of Poly-Ubiquitin-Linkages , 2015, PloS one.

[24]  R. Aebersold,et al.  RNF168 promotes noncanonical K27 ubiquitination to signal DNA damage. , 2015, Cell reports.

[25]  T. Harris,et al.  The deubiquitinating enzyme USP24 is a regulator of the UV damage response. , 2015, Cell reports.

[26]  C. Vogel,et al.  K63 polyubiquitination is a new modulator of the oxidative stress response , 2014, Nature Structural &Molecular Biology.

[27]  Anindya Dutta,et al.  MCM 8-9 complex promotes resection of double-strand break ends by MRE 11-RAD 50-NBS 1 complex , 2015 .

[28]  David J. Chen,et al.  PTIP associates with Artemis to dictate DNA repair pathway choice , 2014, Genes & development.

[29]  Jiri Bartek,et al.  TRIP12 and UBR5 Suppress Spreading of Chromatin Ubiquitylation at Damaged Chromosomes , 2014, Cell.

[30]  J. Parsons,et al.  Regulation of base excision repair proteins by ubiquitylation. , 2014, Experimental cell research.

[31]  Amit Kumar Srivastava,et al.  USP7 modulates UV-induced PCNA monoubiquitination by regulating DNA polymerase eta stability , 2014, Oncogene.

[32]  Shin-Ai Lee,et al.  Stabilization and targeting of INO80 to replication forks by BAP1 during normal DNA synthesis , 2014, Nature Communications.

[33]  M. Steinlage,et al.  Polo-like kinase 3 regulates CtIP during DNA double-strand break repair in G1 , 2014, The Journal of cell biology.

[34]  M. Serresi,et al.  Tight regulation of ubiquitin-mediated DNA damage response by USP3 preserves the functional integrity of hematopoietic stem cells , 2014, The Journal of experimental medicine.

[35]  J. Gagné,et al.  Germline mutations in BAP1 impair its function in DNA double-strand break repair. , 2014, Cancer research.

[36]  J. Qian,et al.  Ubiquitin-specific Protease 7 Regulates Nucleotide Excision Repair through Deubiquitinating XPC Protein and Preventing XPC Protein from Undergoing Ultraviolet Light-induced and VCP/p97 Protein-regulated Proteolysis* , 2014, The Journal of Biological Chemistry.

[37]  S. Jackson,et al.  Systematic characterization of deubiquitylating enzymes for roles in maintaining genome integrity , 2014, Nature Cell Biology.

[38]  J. Yeo,et al.  CtIP mediates replication fork recovery in a FANCD2-regulated manner. , 2014, Human molecular genetics.

[39]  Hailong Wang,et al.  Catalytic and noncatalytic roles of the CtIP endonuclease in double-strand break end resection. , 2014, Molecular cell.

[40]  T. Ludwig,et al.  CtIP-mediated resection is essential for viability and can operate independently of BRCA1 , 2014, The Journal of experimental medicine.

[41]  O. Murina,et al.  FANCD2 and CtIP cooperate to repair DNA interstrand crosslinks. , 2014, Cell reports.

[42]  H. Kurumizaka,et al.  FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. , 2014, Cell reports.

[43]  K. J. Patel,et al.  Mouse SLX4 Is a Tumor Suppressor that Stimulates the Activity of the Nuclease XPF-ERCC1 in DNA Crosslink Repair , 2014, Molecular cell.

[44]  P. Knipscheer,et al.  XPF-ERCC1 acts in Unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. , 2014, Molecular cell.

[45]  M. Rapé,et al.  Enhanced Protein Degradation by Branched Ubiquitin Chains , 2014, Cell.

[46]  Anton Simeonov,et al.  A selective USP1-UAF1 inhibitor links deubiquitination to DNA damage responses. , 2014, Nature chemical biology.

[47]  D. Komander,et al.  The JAMM in the proteasome , 2014, Nature Structural &Molecular Biology.

[48]  Eric C Greene,et al.  RPA Antagonizes Microhomology-Mediated Repair of DNA Double-Strand Breaks , 2014, Nature Structural &Molecular Biology.

[49]  Andreas Martin,et al.  Structure of the Rpn11–Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation , 2014, Nature Structural &Molecular Biology.

[50]  Ilya J. Finkelstein,et al.  Nucleosome Acidic Patch Promotes RNF168- and RING1B/BMI1-Dependent H2AX and H2A Ubiquitination and DNA Damage Signaling , 2014, PLoS genetics.

[51]  H. Ogiwara,et al.  Fine-tuning of DNA damage-dependent ubiquitination by OTUB2 supports the DNA repair pathway choice. , 2014, Molecular cell.

[52]  Michal Zimmermann,et al.  53BP1: pro choice in DNA repair. , 2014, Trends in cell biology.

[53]  S. Nakajima,et al.  Ubiquitin-Specific Protease 5 Is Required for the Efficient Repair of DNA Double-Strand Breaks , 2014, PloS one.

[54]  G. Wani,et al.  USP3 counteracts RNF168 via deubiquitinating H2A and γH2AX at lysine 13 and 15 , 2014, Cell cycle.

[55]  M. Steinlage,et al.  Polo like kinase 3 regulates CtIP during DNA double strand break repair in G 1 , 2014 .

[56]  Helen Yu,et al.  Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair , 2013, Proceedings of the National Academy of Sciences.

[57]  R. Greenberg,et al.  A BRISC-SHMT complex deubiquitinates IFNAR1 and regulates interferon responses. , 2013, Cell reports.

[58]  K. Helin,et al.  Transcriptional regulation by Polycomb group proteins , 2013, Nature Structural &Molecular Biology.

[59]  A. Emili,et al.  Ubp2 Regulates Rsp5 Ubiquitination Activity In Vivo and In Vitro , 2013, PloS one.

[60]  A. Shibata,et al.  Co-operation of BRCA1 and POH1 relieves the barriers posed by 53BP1 and RAP80 to resection , 2013, Nucleic acids research.

[61]  A. D’Andrea,et al.  Inactivation of Uaf1 Causes Defective Homologous Recombination and Early Embryonic Lethality in Mice , 2013, Molecular and Cellular Biology.

[62]  C. Wolberger,et al.  E2 ubiquitin conjugating enzymes regulate the deubiquitinating activity of OTUB1 , 2013, Nature Structural &Molecular Biology.

[63]  W. O,et al.  The ubiquitin specific protease USP34 promotes ubiquitin signaling at DNA double-strand breaks , 2013, Nucleic acids research.

[64]  P. R. Elliott,et al.  OTU Deubiquitinases Reveal Mechanisms of Linkage Specificity and Enable Ubiquitin Chain Restriction Analysis , 2013, Cell.

[65]  K. Baek,et al.  Deubiquitinating enzymes as therapeutic targets in cancer. , 2013, Current pharmaceutical design.

[66]  A. D’Andrea,et al.  FANCD2 activates transcription of TAp63 and suppresses tumorigenesis. , 2013, Molecular cell.

[67]  Anindya Dutta,et al.  Deubiquitination of Tip60 by USP7 Determines the Activity of the p53-Dependent Apoptotic Pathway , 2013, Molecular and Cellular Biology.

[68]  W. Vermeulen,et al.  UVSSA and USP7, a new couple in transcription-coupled DNA repair , 2013, Chromosoma.

[69]  D. Durocher,et al.  53BP1 is a reader of the DNA damage-induced H2A Lys15 ubiquitin mark , 2013, Nature.

[70]  Sebastian A. Wagner,et al.  RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response , 2013, The Journal of cell biology.

[71]  B. Gerrits,et al.  Prolyl isomerase PIN1 regulates DNA double-strand break repair by counteracting DNA end resection. , 2013, Molecular cell.

[72]  Maya Raghunandan,et al.  FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery , 2013, Nucleic acids research.

[73]  M. Saijo.  The role of Cockayne syndrome group A (CSA) protein in transcription-coupled nucleotide excision repair , 2013, Mechanisms of Ageing and Development.

[74]  G. Dianov,et al.  Co-ordination of base excision repair and genome stability. , 2013, DNA repair.

[75]  David E. Williams,et al.  HDAC turnover, CtIP acetylation and dysregulated DNA damage signaling in colon cancer cells treated with sulforaphane and related dietary isothiocyanates , 2013, Epigenetics.

[76]  N. Mailand,et al.  The Deubiquitylating Enzyme USP44 Counteracts the DNA Double-strand Break Response Mediated by the RNF8 and RNF168 Ubiquitin Ligases* , 2013, Journal of Biological Chemistry.

[77]  Lin Feng,et al.  RIF1 Counteracts BRCA1-mediated End Resection during DNA Repair* , 2013, The Journal of Biological Chemistry.

[78]  Adam P. Rosebrock,et al.  A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. , 2013, Molecular cell.

[79]  Facundo D. Batista,et al.  RIF1 Is Essential for 53BP1-Dependent Nonhomologous End Joining and Suppression of DNA Double-Strand Break Resection , 2013, Molecular cell.

[80]  Y. Ye,et al.  Reversible inactivation of deubiquitinases by reactive oxygen species in vitro and in cells , 2013, Nature Communications.

[81]  David Komander,et al.  Regulation of A20 and other OTU deubiquitinases by reversible oxidation , 2013, Nature Communications.

[82]  P. Fei,et al.  Recruitment of DNA polymerase eta by FANCD2 in the early response to DNA damage , 2013, Cell cycle.

[83]  J. Olsen,et al.  RNF4 is required for DNA double-strand break repair in vivo , 2012, Cell Death and Differentiation.

[84]  B. Chait,et al.  Activation of DSB processing requires phosphorylation of CtIP by ATR. , 2013, Molecular cell.

[85]  Michel C. Nussenzweig,et al.  Rif1 Prevents Resection of DNA Breaks and Promotes Immunoglobulin Class Switching , 2013, Science.

[86]  S. B. Buonomo,et al.  53BP1 Regulates DSB Repair Using Rif1 to Control 5′ End Resection , 2013, Science.

[87]  J. Diedrich,et al.  A two-step mechanism for TRF2-mediated chromosome end protection , 2013, Nature.

[88]  G. Dianov,et al.  USP7S-dependent inactivation of Mule regulates DNA damage signalling and repair , 2012, Nucleic acids research.

[89]  Michael S. Y. Huen,et al.  The ubiquitin specific protease USP 34 promotes ubiquitin signaling at DNA double-strand breaks , 2013 .

[90]  J. Huibregtse,et al.  The Rsp 5 ubiquitin ligase is coupled to and antagonized by the Ubp 2 deubiquitinating enzyme , 2013 .

[91]  S. Gasser,et al.  Distinct roles for SWR 1 and INO 80 chromatin remodeling complexes at chromosomal double-strand breaks , 2013 .

[92]  A. Varshavsky,et al.  The auto-generated fragment of the Usp1 deubiquitylase is a physiological substrate of the N-end rule pathway. , 2012, Molecular cell.

[93]  Tony T. Huang.  Deubiquitinases as a signaling target of oxidative stress , 2012, Cell reports.

[94]  Christopher E. Berndsen,et al.  RNF4-Dependent Hybrid SUMO-Ubiquitin Chains Are Signals for RAP80 and Thereby Mediate the Recruitment of BRCA1 to Sites of DNA Damage , 2012, Science Signaling.

[95]  Ying Zhang,et al.  USP44 regulates centrosome positioning to prevent aneuploidy and suppress tumorigenesis. , 2012, The Journal of clinical investigation.

[96]  Ling Zhang,et al.  The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability , 2012, Cell cycle.

[97]  David Klenerman,et al.  Ubiquitin chain conformation regulates recognition and activity of interacting proteins , 2012, Nature.

[98]  F. Festy,et al.  The proteasomal de‐ubiquitinating enzyme POH1 promotes the double‐strand DNA break response , 2012, The EMBO journal.

[99]  Wim Vermeulen,et al.  RNF168 Ubiquitinates K13-15 on H2A/H2AX to Drive DNA Damage Signaling , 2012, Cell.

[100]  S. Boulton,et al.  Playing the end game: DNA double-strand break repair pathway choice. , 2012, Molecular cell.

[101]  Cheryl H Arrowsmith,et al.  Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. , 2012, Molecular cell.

[102]  Liewei Wang,et al.  Sumoylation of MDC1 is important for proper DNA damage response , 2012, The EMBO journal.

[103]  E. Domany,et al.  RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. , 2012, Molecular cell.

[104]  M. Rapé,et al.  The Ubiquitin Code , 2012, Annual review of biochemistry.

[105]  S. Jackson,et al.  RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. , 2012, Genes & development.

[106]  R. Hay,et al.  SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. , 2012, Genes & development.

[107]  A. Yasui,et al.  Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair , 2012, Nature Genetics.

[108]  Jeroen A. A. Demmers,et al.  UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair , 2012, Nature Genetics.

[109]  A. Utani,et al.  Mutations in UVSSA cause UV-sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair , 2012, Nature Genetics.

[110]  Junjie Chen,et al.  RAP80 Protein Is Important for Genomic Stability and Is Required for Stabilizing BRCA1-A Complex at DNA Damage Sites in Vivo* , 2012, The Journal of Biological Chemistry.

[111]  Frédérick A. Mallette,et al.  RNF8‐ and RNF168‐dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites , 2012, The EMBO journal.

[112]  G. Dianov,et al.  ATM-Dependent Downregulation of USP7/HAUSP by PPM1G Activates p53 Response to DNA Damage , 2012, Molecular cell.

[113]  Roger Woodgate,et al.  Y-family DNA polymerases and their role in tolerance of cellular DNA damage , 2012, Nature Reviews Molecular Cell Biology.

[114]  Tony T. Huang,et al.  Dysregulation of DNA polymerase κ recruitment to replication forks results in genomic instability , 2012, The EMBO journal.

[115]  D. Durocher,et al.  OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. , 2012, Molecular cell.

[116]  Liewei Wang,et al.  Sumoylation of MDC 1 is important for proper DNA damage response , 2012 .

[117]  D. Cleveland,et al.  The deubiquitinase USP44 is a tumor suppressor that protects against chromosome missegregation. , 2012, The Journal of clinical investigation.

[118]  T. Sixma,et al.  The differential modulation of USP activity by internal regulatory domains, interactors and eight ubiquitin chain types. , 2011, Chemistry & biology.

[119]  Z. Herceg,et al.  Mammalian Ino80 Mediates Double-Strand Break Repair through Its Role in DNA End Strand Resection , 2011, Molecular and Cellular Biology.

[120]  V. Dixit,et al.  USP1 Deubiquitinates ID Proteins to Preserve a Mesenchymal Stem Cell Program in Osteosarcoma , 2011, Cell.

[121]  A. D’Andrea,et al.  Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. , 2011, Genes & development.

[122]  Alexander A. Ishchenko,et al.  The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol η in response to oxidative DNA damage in human cells. , 2011, Molecular cell.

[123]  J. V. van Deursen,et al.  Overexpression of Ubiquitin Specific Protease 44 (USP44) Induces Chromosomal Instability and Is Frequently Observed in Human T-Cell Leukemia , 2011, PloS one.

[124]  L. Poole,et al.  Overview of peroxiredoxins in oxidant defense and redox regulation. , 2011, Current protocols in toxicology.

[125]  M. Pagano,et al.  APC/CCdh1-dependent proteolysis of USP1 regulates the response to UV-mediated DNA damage , 2011, The Journal of cell biology.

[126]  G. Peng,et al.  Monoubiquitination of H2AX Protein Regulates DNA Damage Response Signaling , 2011, The Journal of Biological Chemistry.

[127]  F. Colland,et al.  Ubiquitin-specific proteases as cancer drug targets. , 2011, Future oncology.

[128]  M. Nussenzweig,et al.  Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. , 2011, Molecular cell.

[129]  B. Nicholson,et al.  The Multifaceted Roles of USP7: New Therapeutic Opportunities , 2011, Cell Biochemistry and Biophysics.

[130]  B. Sobhian,et al.  RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. , 2011, Genes & development.

[131]  Shridar Ganesan,et al.  BMI1 Is Recruited to DNA Breaks and Contributes to DNA Damage-Induced H2A Ubiquitination and Repair , 2011, Molecular and Cellular Biology.

[132]  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.

[133]  R. Greenberg,et al.  The BRCA1-RAP80 Complex Regulates DNA Repair Mechanism Utilization by Restricting End Resection* , 2011, The Journal of Biological Chemistry.

[134]  Xin Hu,et al.  NBA1/MERIT40 and BRE Interaction Is Required for the Integrity of Two Distinct Deubiquitinating Enzyme BRCC36-containing Complexes* , 2011, The Journal of Biological Chemistry.

[135]  S. Elledge,et al.  The DNA damage response: making it safe to play with knives. , 2010, Molecular cell.

[136]  M. Hendzel,et al.  BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair , 2010, The Journal of cell biology.

[137]  S. Jackson,et al.  Human SIRT6 Promotes DNA End Resection Through CtIP Deacetylation , 2010, Science.

[138]  A. Gingras,et al.  Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1 , 2010, Nature.

[139]  A. D’Andrea,et al.  Expanded roles of the Fanconi anemia pathway in preserving genomic stability. , 2010, Genes & development.

[140]  Junya Chen,et al.  FAN1 Acts with FANCI-FANCD2 to Promote DNA Interstrand Cross-Link Repair , 2010, Science.

[141]  R. Greenberg,et al.  Differential Regulation of JAMM Domain Deubiquitinating Enzyme Activity within the RAP80 Complex* , 2010, The Journal of Biological Chemistry.

[142]  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.

[143]  J Wade Harper,et al.  A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. , 2010, Molecular cell.

[144]  M. Hengartner,et al.  Deficiency of FANCD2-Associated Nuclease KIAA1018/FAN1 Sensitizes Cells to Interstrand Crosslinking Agents , 2010, Cell.

[145]  Kay Hofmann,et al.  Identification of KIAA1018/FAN1, a DNA Repair Nuclease Recruited to DNA Damage by Monoubiquitinated FANCD2 , 2010, Cell.

[146]  S. Elledge,et al.  The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. , 2010, Genes & development.

[147]  R. Greenberg,et al.  ATM-Dependent Chromatin Changes Silence Transcription In cis to DNA Double-Strand Breaks , 2010, Cell.

[148]  M. Wilm,et al.  Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB , 2010, Nature.

[149]  Jeremy M. Stark,et al.  53BP1 Inhibits Homologous Recombination in Brca1-Deficient Cells by Blocking Resection of DNA Breaks , 2010, Cell.

[150]  E. Jensen,et al.  The 19S proteasomal lid subunit POH1 enhances the transcriptional activation by Mitf in osteoclasts , 2010, Journal of cellular biochemistry.

[151]  M. O’Connor,et al.  Sensitivity to Poly(ADP-ribose) Polymerase (PARP) Inhibition Identifies Ubiquitin-specific Peptidase 11 (USP11) as a Regulator of DNA Double-strand Break Repair* , 2010, The Journal of Biological Chemistry.

[152]  S. Gygi,et al.  WDR20 Regulates Activity of the USP12·UAF1 Deubiquitinating Enzyme Complex* , 2010, The Journal of Biological Chemistry.

[153]  A. D’Andrea,et al.  Human ELG1 Regulates the Level of Ubiquitinated Proliferating Cell Nuclear Antigen (PCNA) through Its Interactions with PCNA and USP1* , 2010, The Journal of Biological Chemistry.

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

[155]  David Komander,et al.  Mechanism, specificity and structure of the deubiquitinases. , 2010, Sub-cellular biochemistry.

[156]  M. Hendzel,et al.  BMI 1-mediated histone ubiquitylation promotes DNA double-strand break repair , 2010 .

[157]  G. Dianov,et al.  Ubiquitin ligase ARF‐BP1/Mule modulates base excision repair , 2009, The EMBO journal.

[158]  Eleni P. Mimitou,et al.  DNA end resection: many nucleases make light work. , 2009, DNA repair.

[159]  C. Deng,et al.  A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. , 2009, Molecular cell.

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

[161]  Fan Zhang,et al.  PALB2 Functionally Connects the Breast Cancer Susceptibility Proteins BRCA1 and BRCA2 , 2009, Molecular Cancer Research.

[162]  Junjie Chen,et al.  PALB2 is an integral component of the BRCA complex required for homologous recombination repair , 2009, Proceedings of the National Academy of Sciences.

[163]  D. Durocher,et al.  Regulatory ubiquitylation in response to DNA double-strand breaks. , 2009, DNA repair.

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

[165]  R. Greenberg,et al.  MERIT40 controls BRCA1-Rap80 complex integrity and recruitment to DNA double-strand breaks. , 2009, Genes & development.

[166]  Kay Hofmann,et al.  NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control. , 2009, Genes & development.

[167]  R. Greenberg,et al.  The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks , 2009, Proceedings of the National Academy of Sciences.

[168]  Steven P. Gygi,et al.  UAF1 Is a Subunit of Multiple Deubiquitinating Enzyme Complexes* , 2009, Journal of Biological Chemistry.

[169]  Min Huang,et al.  Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. , 2009, Developmental cell.

[170]  Edward S. Miller,et al.  The RIDDLE Syndrome Protein Mediates a Ubiquitin-Dependent Signaling Cascade at Sites of DNA Damage , 2009, Cell.

[171]  J. Ellenberg,et al.  RNF168 Binds and Amplifies Ubiquitin Conjugates on Damaged Chromosomes to Allow Accumulation of Repair Proteins , 2009, Cell.

[172]  R. Greenberg,et al.  MERIT40 controls BRCA1-Rap80 complex integrity and recruitment to DNA double-strand breaks. , 2009, Genes & development.

[173]  P. Hanawalt,et al.  Transcription-coupled DNA repair: two decades of progress and surprises , 2008, Nature Reviews Molecular Cell Biology.

[174]  Paul Modrich,et al.  Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair , 2008, Proceedings of the National Academy of Sciences.

[175]  Eleni P. Mimitou,et al.  Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing , 2008, Nature.

[176]  S. Jackson,et al.  CDK targets Sae2 to control DNA-end resection and homologous recombination , 2008, Nature.

[177]  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.

[178]  Sang Eun Lee,et al.  Sgs1 Helicase and Two Nucleases Dna2 and Exo1 Resect DNA Double-Strand Break Ends , 2008, Cell.

[179]  Erwin G. Van Meir,et al.  BRCA1-associated protein-1 is a tumor suppressor that requires deubiquitinating activity and nuclear localization. , 2008, Cancer research.

[180]  Robert E. Johnson,et al.  Regulation of polymerase exchange between Polη and Polδ by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme , 2008, Proceedings of the National Academy of Sciences.

[181]  G. Dianov,et al.  CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. , 2008, Molecular cell.

[182]  D. Barford,et al.  Methods for preparing crystals of reversibly oxidized proteins: crystallization of protein tyrosine phosphatase 1B as an example. , 2008, Methods in molecular biology.

[183]  Samuel H. Wilson,et al.  XRCC1 and DNA polymerase β in cellular protection against cytotoxic DNA single-strand breaks , 2008, Cell Research.

[184]  L. Mullenders,et al.  Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects , 2008, Cell Research.

[185]  S. Elledge,et al.  Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage , 2007, Proceedings of the National Academy of Sciences.

[186]  Steven P Gygi,et al.  A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. , 2007, Molecular cell.

[187]  J. Sale,et al.  Deubiquitination of FANCD2 Is Required for DNA Crosslink Repair , 2007, Molecular cell.

[188]  Laurence Pelletier,et al.  Orchestration of the DNA-Damage Response by the RNF8 Ubiquitin Ligase , 2007, Science.

[189]  R. Ghirlando,et al.  Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. , 2007, Molecular cell.

[190]  Michael B. Yaffe,et al.  RNF8 Transduces the DNA-Damage Signal via Histone Ubiquitylation and Checkpoint Protein Assembly , 2007, Cell.

[191]  Jiri Bartek,et al.  RNF8 Ubiquitylates Histones at DNA Double-Strand Breaks and Promotes Assembly of Repair Proteins , 2007, Cell.

[192]  Jiri Bartek,et al.  Human CtIP promotes DNA end resection , 2007, Nature.

[193]  Pier Paolo Di Fiore,et al.  Human USP3 Is a Chromatin Modifier Required for S Phase Progression and Genome Stability , 2007, Current Biology.

[194]  Shunichi Takeda,et al.  Ctp1/CtIP and the MRN complex collaborate in the initial steps of homologous recombination. , 2007, Molecular cell.

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

[196]  S. Gasser,et al.  Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double‐strand breaks , 2007, The EMBO journal.

[197]  Junjie Chen,et al.  CCDC98 is a BRCA1-BRCT domain–binding protein involved in the DNA damage response , 2007, Nature Structural &Molecular Biology.

[198]  Xiaochun Yu,et al.  CCDC98 targets BRCA1 to DNA damage sites , 2007, Nature Structural &Molecular Biology.

[199]  F. Xia,et al.  The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. , 2007, Cancer research.

[200]  E. Spiteri,et al.  FANCI is a second monoubiquitinated member of the Fanconi anemia pathway , 2007, Nature Structural &Molecular Biology.

[201]  Aedín C Culhane,et al.  RAP80 Targets BRCA1 to Specific Ubiquitin Structures at DNA Damage Sites , 2007, Science.

[202]  Junjie Chen,et al.  Ubiquitin-Binding Protein RAP80 Mediates BRCA1-Dependent DNA Damage Response , 2007, Science.

[203]  Steven P Gygi,et al.  Abraxas and RAP80 Form a BRCA1 Protein Complex Required for the DNA Damage Response , 2007, Science.

[204]  G. Dianov,et al.  Overexpression of DNA polymerase beta results in an increased rate of frameshift mutations during base excision repair. , 2007, Mutagenesis.

[205]  S. Elledge,et al.  Identification of the FANCI Protein, a Monoubiquitinated FANCD2 Paralog Required for DNA Repair , 2007, Cell.

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

[207]  G. Dianov,et al.  Co-ordination of DNA single strand break repair. , 2007, DNA repair.

[208]  P. Bates,et al.  Repair of alkylated DNA: recent advances. , 2007, DNA repair.

[209]  Xin Wang,et al.  A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. , 2007, Molecular cell.

[210]  R. Ghirlando,et al.  Supplemental Data Sae 2 Is an Endonuclease that Processes Hairpin DNA Cooperatively with the Mre 11 / Rad 50 / Xrs 2 Complex , 2007 .

[211]  Yeast Rad 55 and Rad 57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad 51 recombinase , 2007 .

[212]  J. Huibregtse,et al.  The Deubiquitinating Enzyme Ubp2 Modulates Rsp5-dependent Lys63-linked Polyubiquitin Conjugates in Saccharomyces cerevisiae*> , 2006, Journal of Biological Chemistry.

[213]  N. Tonks,et al.  Protein tyrosine phosphatases: from genes, to function, to disease , 2006, Nature Reviews Molecular Cell Biology.

[214]  Junjie Chen,et al.  BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. , 2006, Genes & development.

[215]  A. Harel-Bellan,et al.  CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. , 2006, Genes & development.

[216]  A. D’Andrea,et al.  Regulation of DNA repair by ubiquitylation , 2006, Nature Reviews Molecular Cell Biology.

[217]  A. G. Murachelli,et al.  Crystal Structure of the Ubiquitin Binding Domains of Rabex-5 Reveals Two Modes of Interaction with Ubiquitin , 2006, Cell.

[218]  Xiaodong Cheng,et al.  The Ubiquitin Binding Domain ZnF UBP Recognizes the C-Terminal Diglycine Motif of Unanchored Ubiquitin , 2006, Cell.

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

[220]  René Bernards,et al.  A Genomic and Functional Inventory of Deubiquitinating Enzymes , 2005, Cell.

[221]  Xiaofeng Jiang,et al.  A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[222]  J. Huibregtse,et al.  The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme , 2005, The EMBO journal.

[223]  N. Tonks.  Redox Redux: Revisiting PTPs and the Control of Cell Signaling , 2005, Cell.

[224]  Keiji Tanaka,et al.  UV-Induced Ubiquitylation of XPC Protein Mediated by UV-DDB-Ubiquitin Ligase Complex , 2005, Cell.

[225]  F. Liu,et al.  Inactivation of CtIP Leads to Early Embryonic Lethality Mediated by G1 Restraint and to Tumorigenesis by Haploid Insufficiency , 2005, Molecular and Cellular Biology.

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

[227]  J. den Hertog,et al.  Redox regulation of protein-tyrosine phosphatases. , 2005, Archives of biochemistry and biophysics.

[228]  G. Cagney,et al.  Proteasome involvement in the repair of DNA double-strand breaks. , 2004, Molecular cell.

[229]  N. Krogan,et al.  INO80 and γ-H2AX Interaction Links ATP-Dependent Chromatin Remodeling to DNA Damage Repair , 2004, Cell.

[230]  Barbara Hohn,et al.  Recruitment of the INO80 Complex by H2A Phosphorylation Links ATP-Dependent Chromatin Remodeling with DNA Double-Strand Break Repair , 2004, Cell.

[231]  Tom J. Petty,et al.  Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks , 2004, Nature.

[232]  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.

[233]  N. Larebeke,et al.  Endogenous DNA damage in humans: a review of quantitative data , 2004 .

[234]  N. Van Larebeke,et al.  Endogenous DNA damage in humans: a review of quantitative data. , 2004, Mutagenesis.

[235]  Nevan J Krogan,et al.  INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. , 2004, Cell.

[236]  Ali Shilatifard,et al.  Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. , 2003, Genes & development.

[237]  R. Shiekhattar,et al.  Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. , 2003, Molecular cell.

[238]  Samuel H. Wilson,et al.  Base excision repair deficiency caused by polymerase beta haploinsufficiency: accelerated DNA damage and increased mutational response to carcinogens. , 2003, Cancer research.

[239]  Stephen J. Elledge,et al.  Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes , 2003, Science.

[240]  Stephen J. Elledge,et al.  MDC1 is a mediator of the mammalian DNA damage checkpoint , 2003, Nature.

[241]  T. Yao,et al.  A cryptic protease couples deubiquitination and degradation by the proteasome , 2002, Nature.

[242]  L. Aravind,et al.  Role of Rpn11 Metalloprotease in Deubiquitination and Degradation by the 26S Proteasome , 2002, Science.

[243]  S. Ganesan,et al.  Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. , 2001, Molecular cell.

[244]  V. Yamazaki,et al.  A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage , 2000, Current Biology.

[245]  G. Sutherland,et al.  Characterization and Chromosomal Localization of USP3, a Novel Human Ubiquitin-specific Protease* , 1999, The Journal of Biological Chemistry.

[246]  Y. Canitrot,et al.  Overexpression of DNA polymerase β: a genomic instability enhancer process , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[247]  Samuel H. Wilson,et al.  Cells deficient in DNA polymerase beta are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. , 1999, Cancer research.

[248]  C. Pickart,et al.  Noncanonical MMS2-Encoded Ubiquitin-Conjugating Enzyme Functions in Assembly of Novel Polyubiquitin Chains for DNA Repair , 1999, Cell.

[249]  Y. Canitrot,et al.  Overexpression of DNA polymerase beta: a genomic instability enhancer process. , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[250]  J. Haber,et al.  Saccharomyces Ku70, Mre11/Rad50, and RPA Proteins Regulate Adaptation to G2/M Arrest after DNA Damage , 1998, Cell.

[251]  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.

[252]  A. Amerik,et al.  In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome , 1997, The EMBO journal.

[253]  P. Sung.  Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. , 1997, Genes & development.

[254]  S. Kowalczykowski,et al.  A Single-stranded DNA-binding Protein Is Needed for Efficient Presynaptic Complex Formation by the Saccharomyces cerevisiae Rad51 Protein* , 1997, The Journal of Biological Chemistry.

[255]  G. Lucchini,et al.  The 70 kDa subunit of replication protein A is required for the G1/S and intra-S DNA damage checkpoints in budding yeast. , 1996, Nucleic acids research.

[256]  Sebastian A. Wagner,et al.  RNF 111 / Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response , 2022 .