Global analysis of SUMO chain function reveals multiple roles in chromatin regulation

Multiple large-scale analyses in yeast implicate SUMO chain function in the maintenance of higher-order chromatin structure and transcriptional repression of environmental stress response genes.

[1]  A. Santiago,et al.  Identification of two independent SUMO-interacting motifs in Daxx: Evolutionary conservation from Drosophila to humans and their biochemical functions , 2009, Cell cycle.

[2]  Gary D. Bader,et al.  DRYGIN: a database of quantitative genetic interaction networks in yeast , 2009, Nucleic Acids Res..

[3]  J. Delrow,et al.  Degringolade, a SUMO‐targeted ubiquitin ligase, inhibits Hairy/Groucho‐mediated repression , 2011, The EMBO journal.

[4]  Grant W. Brown,et al.  Dissecting DNA damage response pathways by analyzing protein localization and abundance changes during DNA replication stress , 2012, Nature Cell Biology.

[5]  W. Neupert,et al.  Mitochondria‐targeted green fluorescent proteins: convenient tools for the study of organelle biogenesis in Saccharomyces cerevisiae , 2000, Yeast.

[6]  I. Hickson,et al.  Processing of homologous recombination repair intermediates by the Sgs1-Top3-Rmi1 and Mus81-Mms4 complexes , 2011, Cell cycle.

[7]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[8]  D. Pattabiraman,et al.  A functional SUMO-interacting motif in the transactivation domain of c-Myb regulates its myeloid transforming ability , 2011, Oncogene.

[9]  L. Beatty,et al.  The CTCF Insulator Protein Is Posttranslationally Modified by SUMO , 2008, Molecular and Cellular Biology.

[10]  Patrick G. A. Pedrioli,et al.  An improved SUMmOn‐based methodology for the identification of ubiquitin and ubiquitin‐like protein conjugation sites identifies novel ubiquitin‐like protein chain linkages , 2010, Proteomics.

[11]  M. J. Mazur,et al.  Global SUMO Proteome Responses Guide Gene Regulation, mRNA Biogenesis, and Plant Stress Responses , 2012, Front. Plant Sci..

[12]  S. Gygi,et al.  Role for perinuclear chromosome tethering in maintenance of genome stability , 2008, Nature.

[13]  Ming-Ming Zhou,et al.  PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. , 2007, Molecular cell.

[14]  Franco J. Vizeacoumar,et al.  Integrating high-throughput genetic interaction mapping and high-content screening to explore yeast spindle morphogenesis , 2010, The Journal of cell biology.

[15]  R. Dammann,et al.  Transcription in the yeast rRNA gene locus: distribution of the active gene copies and chromatin structure of their flanking regulatory sequences , 1995, Molecular and cellular biology.

[16]  I. Matic,et al.  Purification and identification of endogenous polySUMO conjugates , 2011, EMBO reports.

[17]  A. Emili,et al.  Perinuclear cohibin complexes maintain replicative life span via roles at distinct silent chromatin domains. , 2011, Developmental cell.

[18]  Stefan Hohmann,et al.  Control of high osmolarity signalling in the yeast Saccharomyces cerevisiae , 2009, FEBS letters.

[19]  Taras Makhnevych,et al.  The role of karyopherins in the regulated sumoylation of septins , 2007, The Journal of cell biology.

[20]  M. Gebbia,et al.  Genomic approaches for determining nucleosome occupancy in yeast. , 2012, Methods in molecular biology.

[21]  John A Tainer,et al.  A SIM-ultaneous role for SUMO and ubiquitin. , 2008, Trends in biochemical sciences.

[22]  M. Foiani,et al.  Template Switching: From Replication Fork Repair to Genome Rearrangements , 2007, Cell.

[23]  D. J. Clarke,et al.  In vivo analysis of chromosome condensation in Saccharomyces cerevisiae. , 2006, Molecular biology of the cell.

[24]  Huilin Zhou,et al.  Global Analyses of Sumoylated Proteins in Saccharomyces cerevisiae , 2004, Journal of Biological Chemistry.

[25]  I. Hickson,et al.  DNA helicases required for homologous recombination and repair of damaged replication forks. , 2006, Annual review of genetics.

[26]  R. D. Gietz,et al.  Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. , 2002, Methods in enzymology.

[27]  D. Botstein,et al.  Genomic expression programs in the response of yeast cells to environmental changes. , 2000, Molecular biology of the cell.

[28]  R. Hay,et al.  SUMO: a history of modification. , 2005, Molecular cell.

[29]  T. Hunter,et al.  Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. , 2007, Nature Reviews Molecular Cell Biology.

[30]  M. Lei,et al.  Arsenic degrades PML or PML–RARα through a SUMO-triggered RNF4/ubiquitin-mediated pathway , 2008, Nature Cell Biology.

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

[32]  T. Itoh,et al.  Identification of cis-acting sites for condensin loading onto budding yeast chromosomes. , 2008, Genes & development.

[33]  J. Manley,et al.  SUMO functions in constitutive transcription and during activation of inducible genes in yeast. , 2010, Genes & development.

[34]  Joseph A. Loo,et al.  Genetic and Proteomic Evidence for Roles of Drosophila SUMO in Cell Cycle Control, Ras Signaling, and Early Pattern Formation , 2009, PloS one.

[35]  F. Johnson,et al.  Sumoylation and the Structural Maintenance of Chromosomes (Smc) 5/6 Complex Slow Senescence through Recombination Intermediate Resolution* , 2010, The Journal of Biological Chemistry.

[36]  T. Eydmann,et al.  SMC5 and SMC6 genes are required for the segregation of repetitive chromosome regions , 2005, Nature Cell Biology.

[37]  J. Reyes,et al.  SUMO association with repressor complexes, emerging routes for transcriptional control. , 2009, Biochimica et biophysica acta.

[38]  Bruce Futcher,et al.  Role of a ubiquitin-conjugating enzyme in degradation of S- and M-phase cyclins , 1995, Nature.

[39]  A. Strunnikov,et al.  Cooperation of Sumoylated Chromosomal Proteins in rDNA Maintenance , 2008, PLoS genetics.

[40]  M. Hochstrasser,et al.  A new protease required for cell-cycle progression in yeast , 1999, Nature.

[41]  John A Tainer,et al.  SUMO‐targeted ubiquitin ligases in genome stability , 2007, The EMBO journal.

[42]  M. Lopes,et al.  Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. , 2005, Genes & development.

[43]  M. Tatham,et al.  RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation , 2008, Nature Cell Biology.

[44]  Takashi Horiuchi,et al.  The cis element and factors required for condensin recruitment to chromosomes. , 2009, Molecular cell.

[45]  D. Sterner,et al.  Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. , 2006, Genes & development.

[46]  Erica S. Johnson,et al.  Protein modification by SUMO. , 2004, Annual review of biochemistry.

[47]  G. Gill,et al.  Something about SUMO inhibits transcription. , 2005, Current opinion in genetics & development.

[48]  A. Toh-E,et al.  Smt3, a SUMO-1 homolog, is conjugated to Cdc3, a component of septin rings at the mother-bud neck in budding yeast. , 1999, Biochemical and biophysical research communications.

[49]  T. Stevens,et al.  Voa1p functions in V-ATPase assembly in the yeast endoplasmic reticulum. , 2008, Molecular Biology of the Cell.

[50]  V. Guacci,et al.  Chromosome condensation and sister chromatid pairing in budding yeast , 1994, The Journal of cell biology.

[51]  A. Lehmann,et al.  Gaps and forks in DNA replication: Rediscovering old models. , 2006, DNA repair.

[52]  Kam-Leung Siu,et al.  Loss of Yeast Peroxiredoxin Tsa1p Induces Genome Instability through Activation of the DNA Damage Checkpoint and Elevation of dNTP Levels , 2009, PLoS genetics.

[53]  J. Yates,et al.  Dual Recruitment of Cdc48 (p97)-Ufd1-Npl4 Ubiquitin-selective Segregase by Small Ubiquitin-like Modifier Protein (SUMO) and Ubiquitin in SUMO-targeted Ubiquitin Ligase-mediated Genome Stability Functions* , 2012, The Journal of Biological Chemistry.

[54]  Steven P. Gygi,et al.  A Proteomic Strategy for Gaining Insights into Protein Sumoylation in Yeast*S , 2005, Molecular & Cellular Proteomics.

[55]  Divya Subramonian,et al.  SUMOylation in Control of Accurate Chromosome Segregation during Mitosis , 2012, Current protein & peptide science.

[56]  F. Young.  Biochemistry , 1955, The Indian Medical Gazette.

[57]  Z. Wang,et al.  Genetic Analysis Connects SLX5 and SLX8 to the SUMO Pathway in Saccharomyces cerevisiae , 2006, Genetics.

[58]  O. J. Semmes,et al.  The Sumo-targeted ubiquitin ligase RNF4 regulates the localization and function of the HTLV-1 oncoprotein Tax. , 2012, Blood.

[59]  A. Sapetschnig,et al.  SUMO‐modified Sp3 represses transcription by provoking local heterochromatic gene silencing , 2008, EMBO reports.

[60]  Jeffrey G. Linger,et al.  The Yeast Histone Chaperone Chromatin Assembly Factor 1 Protects Against Double-Strand DNA-Damaging Agents , 2005, Genetics.

[61]  E. Delorme.  Transformation of Saccharomyces cerevisiae by electroporation , 1989, Applied and environmental microbiology.

[62]  J. Bachant,et al.  The SUMO Isopeptidase Ulp2p Is Required to Prevent Recombination-Induced Chromosome Segregation Lethality following DNA Replication Stress , 2011, PLoS genetics.

[63]  Tharan Srikumar,et al.  Global map of SUMO function revealed by protein-protein interaction and genetic networks. , 2009, Molecular cell.

[64]  Gary D Bader,et al.  The Genetic Landscape of a Cell , 2010, Science.

[65]  R. Wright.  Transmission electron microscopy of yeast , 2000, Microscopy research and technique.

[66]  M. Malumbres,et al.  A SUMOylation Motif in Aurora-A: Implications for Spindle Dynamics and Oncogenesis , 2011, Front. Oncol..

[67]  A. Murray,et al.  Genes involved in sister chromatid separation and segregation in the budding yeast Saccharomyces cerevisiae. , 2001, Genetics.

[68]  Matthias Mann,et al.  Phosphorylation of SUMO-1 occurs in vivo and is conserved through evolution. , 2008, Journal of proteome research.

[69]  K. Ohta,et al.  Ubc9- and Mms21-Mediated Sumoylation Counteracts Recombinogenic Events at Damaged Replication Forks , 2006, Cell.

[70]  V. G. Panse,et al.  Unconventional tethering of Ulp1 to the transport channel of the nuclear pore complex by karyopherins , 2003, Nature Cell Biology.

[71]  I. Hickson,et al.  Yeast as a model system to study RecQ helicase function. , 2010, DNA repair.

[72]  C. Grant,et al.  The thioredoxin system protects ribosomes against stress-induced aggregation. , 2005, Molecular biology of the cell.

[73]  V. Bohr,et al.  Roles of Werner syndrome protein in protection of genome integrity. , 2010, DNA repair.

[74]  Gary D Bader,et al.  Quantitative analysis of fitness and genetic interactions in yeast on a genome scale , 2010, Nature Methods.

[75]  G. Giaever,et al.  Yeast Barcoders: a chemogenomic application of a universal donor-strain collection carrying bar-code identifiers , 2008, Nature Methods.

[76]  A. Sharrocks,et al.  SUMO promotes HDAC-mediated transcriptional repression. , 2004, Molecular cell.

[77]  Jack A. M. Leunissen,et al.  Turning CFCs into salt. , 1996, Nucleic Acids Res..

[78]  D. Tempé,et al.  SUMO under stress. , 2008, Biochemical Society transactions.

[79]  M. Nakao,et al.  Involvement of SUMO Modification in MBD1- and MCAF1-mediated Heterochromatin Formation* , 2006, Journal of Biological Chemistry.

[80]  M. Hochstrasser,et al.  Ulp2 and the DNA damage response: Desumoylation enables safe passage through mitosis , 2008, Cell cycle.

[81]  D. Koshland,et al.  Evidence that the MIF2 gene of Saccharomyces cerevisiae encodes a centromere protein with homology to the mammalian centromere protein CENP-C. , 1995, Molecular biology of the cell.

[82]  L. Zon,et al.  SUMO-1 modification represses Sp3 transcriptional activation and modulates its subnuclear localization. , 2002, Molecular cell.

[83]  Charles Boone,et al.  16 High-Throughput Strain Construction and Systematic Synthetic Lethal Screening in Saccharomycescerevisiae , 2007 .

[84]  L. Steinmetz,et al.  Antisense artifacts in transcriptome microarray experiments are resolved by actinomycin D , 2007, Nucleic acids research.

[85]  E. O’Shea,et al.  Global analysis of protein localization in budding yeast , 2003, Nature.

[86]  M. Avantaggiati,et al.  An acetylation switch regulates SUMO-dependent protein interaction networks. , 2012, Molecular cell.

[87]  S. Lovett,et al.  DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. , 2006, Molecular cell.

[88]  C. Slaughter,et al.  Identification of a Multifunctional Binding Site on Ubc9p Required for Smt3p Conjugation* , 2002, The Journal of Biological Chemistry.

[89]  Erica S. Johnson,et al.  Deficient SUMO attachment to Flp recombinase leads to homologous recombination-dependent hyperamplification of the yeast 2 microm circle plasmid. , 2009, Molecular biology of the cell.

[90]  M. Hochstrasser,et al.  Modification of proteins by ubiquitin and ubiquitin-like proteins. , 2006, Annual review of cell and developmental biology.

[91]  P. Georgiev,et al.  SUMO conjugation is required for the assembly of Drosophila Su(Hw) and Mod(mdg4) into insulator bodies that facilitate insulator complex formation , 2012, Journal of Cell Science.

[92]  Mike Tyers,et al.  Systematic Identification of Pathways That Couple Cell Growth and Division in Yeast , 2002, Science.

[93]  M. Boutros,et al.  Identification of SUMO-dependent chromatin-associated transcriptional repression components by a genome-wide RNAi screen. , 2008, Molecular cell.

[94]  S. Gasser,et al.  The PIAS homologue Siz2 regulates perinuclear telomere position and telomerase activity in budding yeast , 2011, Nature Cell Biology.

[95]  Erica S. Johnson,et al.  Topoisomerase I-Dependent Viability Loss in Saccharomyces cerevisiae Mutants Defective in Both SUMO Conjugation and DNA Repair , 2007, Genetics.

[96]  Erica S. Johnson,et al.  The SUMO Isopeptidase Ulp2 Prevents Accumulation of SUMO Chains in Yeast* , 2003, Journal of Biological Chemistry.

[97]  M. Hochstrasser.  All in the Ubiquitin Family , 2000, Science.

[98]  Z. Wang,et al.  Quality Control of a Transcriptional Regulator by SUMO-Targeted Degradation , 2009, Molecular and Cellular Biology.

[99]  J. Stark,et al.  Role of SUMO:SIM-mediated protein–protein interaction in non-homologous end joining , 2010, Oncogene.

[100]  B. Oh,et al.  DeSUMOylating isopeptidase: a second class of SUMO protease , 2012, EMBO reports.

[101]  Xiaolan Zhao,et al.  Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. , 2012, Molecular cell.

[102]  Ji Luo,et al.  A SUMOylation-Dependent Transcriptional Subprogram Is Required for Myc-Driven Tumorigenesis , 2012, Science.

[103]  R. Eisenman,et al.  Histone sumoylation is associated with transcriptional repression , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[104]  Yan Xuan,et al.  Direct binding of CoREST1 to SUMO-2/3 contributes to gene-specific repression by the LSD1/CoREST1/HDAC complex. , 2009, Molecular cell.

[105]  John R Yates,et al.  Global Analysis of Protein Sumoylation in Saccharomyces cerevisiae* , 2004, Journal of Biological Chemistry.

[106]  D. Schwartz,et al.  The Ulp2 SUMO Protease Is Required for Cell Division following Termination of the DNA Damage Checkpoint , 2007, Molecular and Cellular Biology.

[107]  R. Tavares,et al.  SUMO, a heavyweight player in plant abiotic stress responses , 2012, Cellular and Molecular Life Sciences.

[108]  S. Philipsen,et al.  Epigenetic Silencing of Spermatocyte-Specific and Neuronal Genes by SUMO Modification of the Transcription Factor Sp3 , 2010, PLoS genetics.

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

[110]  H. Klein.  A SUMOry of DNA Replication: Synthesis, Damage, and Repair , 2006, Cell.

[111]  Ronald W. Davis,et al.  High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing , 2007, Proceedings of the National Academy of Sciences.

[112]  J. Sogo,et al.  Two different chromatin structures coexist in ribosomal RNA genes throughout the cell cycle , 1989, Cell.

[113]  G. Coupland,et al.  Proteome-wide screens for small ubiquitin-like modifier (SUMO) substrates identify Arabidopsis proteins implicated in diverse biological processes , 2010, Proceedings of the National Academy of Sciences.

[114]  R. Heller,et al.  Replication fork reactivation downstream of a blocked nascent leading strand , 2006, Nature.