Condensin and cohesin complexity: the expanding repertoire of functions

Condensin and cohesin complexes act in diverse nuclear processes in addition to their widely known roles in chromosome compaction and sister chromatid cohesion. Recent work has elucidated the contribution of condensin and cohesin to interphase genome organization, control of gene expression, metazoan development and meiosis. Despite these wide-ranging functions, several themes have come to light: both complexes establish higher-order chromosome structure by inhibiting or promoting interactions between distant genomic regions, both complexes influence the chromosomal association of other proteins, and both complexes achieve functional specialization by swapping homologous subunits. Emerging data are expanding the range of processes in which condensin and cohesin are known to participate and are enhancing our knowledge of how chromosome architecture is regulated to influence numerous cellular functions.

[1]  T. Orr-Weaver,et al.  Mutations in the Drosophila Condensin Subunit dCAP-G , 2004, Genetics.

[2]  J. Yates,et al.  Three Distinct Condensin Complexes Control C. elegans Chromosome Dynamics , 2009, Current Biology.

[3]  J. Lieb,et al.  The C. elegans Dosage Compensation Complex Propagates Dynamically and Independently of X Chromosome Sequence , 2009, Current Biology.

[4]  E. Revenkova,et al.  Shaping meiotic prophase chromosomes: cohesins and synaptonemal complex proteins , 2006, Chromosoma.

[5]  K. Nasmyth,et al.  Yeast cohesin complex requires a conserved protein, Eco1p(Ctf7), to establish cohesion between sister chromatids during DNA replication. , 1999, Genes & development.

[6]  Michael B. Eisen,et al.  Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome , 2008, Chromosoma.

[7]  K. Nasmyth,et al.  Human Scc4 Is Required for Cohesin Binding to Chromatin, Sister-Chromatid Cohesion, and Mitotic Progression , 2006, Current Biology.

[8]  J. Kissil,et al.  Cohesins localize with CTCF at the KSHV latency control region and at cellular c‐myc and H19/Igf2 insulators , 2008, The EMBO journal.

[9]  J. Hurwitz,et al.  Cdc7-Drf1 kinase links chromosome cohesion to the initiation of DNA replication in Xenopus egg extracts. , 2008, Genes & development.

[10]  I. Krantz,et al.  Cornelia de Lange syndrome, cohesin, and beyond , 2009, Clinical genetics.

[11]  D. Dorsett,et al.  Functional links between Drosophila Nipped-B and cohesin in somatic and meiotic cells , 2008, Chromosoma.

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

[13]  Yoshinori Watanabe,et al.  Studies of meiosis disclose distinct roles of cohesion in the core centromere and pericentromeric regions , 2009, Chromosome Research.

[14]  A. F. Neuwald,et al.  Differential Contributions of Condensin I and Condensin II to Mitotic Chromosome Architecture in Vertebrate Cells , 2003, Cell.

[15]  A. Strunnikov,et al.  Transcriptional homogenization of rDNA repeats in the episome-based nucleolus induces genome-wide changes in the chromosomal distribution of condensin. , 2008, Plasmid.

[16]  Petra C. Schwalie,et al.  A CTCF-independent role for cohesin in tissue-specific transcription. , 2010, Genome research.

[17]  C. Lehner,et al.  Cell-Type-Specific TEV Protease Cleavage Reveals Cohesin Functions in Drosophila Neurons , 2008, Developmental cell.

[18]  Ryan Dale,et al.  Cell type specificity of chromatin organization mediated by CTCF and cohesin , 2010, Proceedings of the National Academy of Sciences.

[19]  B. Meyer,et al.  Condensin restructures chromosomes in preparation for meiotic divisions , 2004, The Journal of cell biology.

[20]  A. Efstratiadis,et al.  Parental imprinting of the mouse insulin-like growth factor II gene , 1991, Cell.

[21]  T. Hirano,et al.  Identification of Xenopus SMC protein complexes required for sister chromatid cohesion. , 1998, Genes & development.

[22]  K. P. Rabitsch,et al.  Functional Genomics Identifies Monopolin A Kinetochore Protein Required for Segregation of Homologs during Meiosis I , 2000, Cell.

[23]  S. Boulton,et al.  HTP-3 links DSB formation with homolog pairing and crossing over during C. elegans meiosis. , 2008, Developmental cell.

[24]  D. Koshland,et al.  Meiotic condensin is required for proper chromosome compaction, SC assembly, and resolution of recombination-dependent chromosome linkages , 2003, The Journal of cell biology.

[25]  J. Peters,et al.  How cohesin and CTCF cooperate in regulating gene expression , 2009, Chromosome Research.

[26]  T. Itoh,et al.  Cohesin relocation from sites of chromosomal loading to places of convergent transcription , 2004, Nature.

[27]  H. Aburatani,et al.  Cohesin mediates transcriptional insulation by CCCTC-binding factor , 2008, Nature.

[28]  T. Hirano,et al.  Reconstitution and subunit geometry of human condensin complexes , 2007, The EMBO journal.

[29]  A. Bateman,et al.  Metazoan Scc4 Homologs Link Sister Chromatid Cohesion to Cell and Axon Migration Guidance , 2006, PLoS biology.

[30]  W. Earnshaw,et al.  Condensin: Architect of mitotic chromosomes , 2009, Chromosome Research.

[31]  D. Dorsett,et al.  Nipped-B, a Drosophila homologue of chromosomal adherins, participates in activation by remote enhancers in the cut and Ultrabithorax genes. , 1999, Genetics.

[32]  K. Nairz,et al.  A Central Role for Cohesins in Sister Chromatid Cohesion, Formation of Axial Elements, and Recombination during Yeast Meiosis , 1999, Cell.

[33]  J. Gerton,et al.  Cohesinopathy mutations disrupt the subnuclear organization of chromatin , 2009, Journal of Cell Biology.

[34]  Wolf Reik,et al.  Interaction between differentially methylated regions partitions the imprinted genes Igf2 and H19 into parent-specific chromatin loops , 2004, Nature Genetics.

[35]  N. Kleckner,et al.  Meiotic chromosomes: integrating structure and function. , 1999, Annual review of genetics.

[36]  Xuewen Pan,et al.  Acetylation of Smc3 by Eco1 is required for S phase sister chromatid cohesion in both human and yeast. , 2008, Molecular cell.

[37]  David J. Reiss,et al.  CTCF physically links cohesin to chromatin , 2008, Proceedings of the National Academy of Sciences.

[38]  David G Mets,et al.  Condensins Regulate Meiotic DNA Break Distribution, thus Crossover Frequency, by Controlling Chromosome Structure , 2009, Cell.

[39]  A. Schleiffer,et al.  A Caenorhabditis elegans cohesion protein with functions in meiotic chromosome pairing and disjunction. , 2001, Genes & development.

[40]  V. Corces,et al.  CTCF: Master Weaver of the Genome , 2009, Cell.

[41]  P. Giresi,et al.  X chromosome repression by localization of the C. elegans dosage compensation machinery to sites of transcription initiation , 2007, Nature Genetics.

[42]  D. D'Amours,et al.  Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. , 2009, Molecular cell.

[43]  K Nasmyth,et al.  Cohesin's binding to chromosomes depends on a separate complex consisting of Scc2 and Scc4 proteins. , 2000, Molecular cell.

[44]  V. Guacci,et al.  The Scc2/Scc4 cohesin loader determines the distribution of cohesin on budding yeast chromosomes. , 2009, Genes & development.

[45]  A. Murray,et al.  Mutation of YCS4, a budding yeast condensin subunit, affects mitotic and nonmitotic chromosome behavior. , 2002, Molecular biology of the cell.

[46]  三代 剛.  Architectural roles of multiple chromatin insulators at the human apolipoprotein gene cluster , 2009 .

[47]  N. Proudfoot,et al.  Cohesin Complex Promotes Transcriptional Termination between Convergent Genes in S. pombe , 2008, Cell.

[48]  S. Grewal,et al.  Centromeric Localization of Dispersed Pol III Genes in Fission Yeast , 2010, Molecular biology of the cell.

[49]  C. K. Schmidt,et al.  Conserved features of cohesin binding along fission yeast chromosomes , 2009, Genome Biology.

[50]  E. Revenkova,et al.  Cohesin Smc1β determines meiotic chromatin axis loop organization , 2008, The Journal of cell biology.

[51]  E. Revenkova,et al.  Cohesin SMC1β protects telomeres in meiocytes , 2009, The Journal of cell biology.

[52]  Stephan Sauer,et al.  Cohesins Functionally Associate with CTCF on Mammalian Chromosome Arms , 2008, Cell.

[53]  S. Yokoyama,et al.  Negative regulation of condensin I by CK2‐mediated phosphorylation , 2006, The EMBO journal.

[54]  Jennifer A. Mitchell,et al.  Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells , 2010, Nature Genetics.

[55]  Takehiko Kobayashi.  Strategies to maintain the stability of the ribosomal RNA gene repeats--collaboration of recombination, cohesion, and condensation. , 2006, Genes & genetic systems.

[56]  Diana S Chu,et al.  A molecular link between gene-specific and chromosome-wide transcriptional repression. , 2002, Genes & development.

[57]  V. Guacci,et al.  A Direct Link between Sister Chromatid Cohesion and Chromosome Condensation Revealed through the Analysis of MCD1 in S. cerevisiae , 1997, Cell.

[58]  S. Yokoyama,et al.  Analysis of the role of Aurora B on the chromosomal targeting of condensin I , 2007, Nucleic acids research.

[59]  E. Liu,et al.  An Oestrogen Receptor α-bound Human Chromatin Interactome , 2009, Nature.

[60]  D. Engelke,et al.  Clustering of yeast tRNA genes is mediated by specific association of condensin with tRNA gene transcription complexes. , 2008, Genes & development.

[61]  N. Rhind,et al.  xo1-1 acts as an early switch in the C. elegans male/hermaphrodite decision , 1995, Cell.

[62]  B. Meyer,et al.  xol-1: A gene that controls the male modes of both sex determination and X chromosome dosage compensation in C. elegans , 1988, Cell.

[63]  V. Orlando,et al.  Drosophila chromosome condensation proteins Topoisomerase II and Barren colocalize with Polycomb and maintain Fab-7 PRE silencing. , 2001, Molecular cell.

[64]  O. Hamant,et al.  Alleles of afd1 dissect REC8 functions during meiotic prophase I , 2006, Journal of Cell Science.

[65]  Katsuhiko Shirahige,et al.  Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. , 2006, Molecular cell.

[66]  D. Dorsett.  Cohesin, gene expression and development: Lessons from Drosophila , 2009, Chromosome Research.

[67]  R. Dengler,et al.  Mutations in Arabidopsis condensin genes disrupt embryogenesis, meristem organization and segregation of homologous chromosomes during meiosis , 2003, Development.

[68]  Tobias Straub,et al.  Active promoters and insulators are marked by the centrosomal protein 190 , 2009, The EMBO journal.

[69]  A. Amon,et al.  The multiple roles of cohesin in meiotic chromosome morphogenesis and pairing. , 2008, Molecular biology of the cell.

[70]  K. Shearwin,et al.  Transcriptional interference--a crash course. , 2005, Trends in genetics : TIG.

[71]  K. Shirahige,et al.  Displacement and re-accumulation of centromeric cohesin during transient pre-anaphase centromere splitting , 2007, Chromosoma.

[72]  Karl Mechtler,et al.  Building sister chromatid cohesion: smc3 acetylation counteracts an antiestablishment activity. , 2009, Molecular cell.

[73]  B. Meyer.  X-Chromosome dosage compensation. , 2005, WormBook : the online review of C. elegans biology.

[74]  Zhe Zhang,et al.  Transcriptional Dysregulation in NIPBL and Cohesin Mutant Human Cells , 2009, PLoS biology.

[75]  Hui Ling Chen,et al.  CTCF Mediates Interchromosomal Colocalization Between Igf2/H19 and Wsb1/Nf1 , 2006, Science.

[76]  P. Nurse,et al.  Cohesin Rec8 is required for reductional chromosome segregation at meiosis , 1999, Nature.

[77]  E. Revenkova,et al.  Cohesin SMC1β is required for meiotic chromosome dynamics, sister chromatid cohesion and DNA recombination , 2004, Nature Cell Biology.

[78]  D. Koshland,et al.  Chromosome Morphogenesis: Condensin-Dependent Cohesin Removal during Meiosis , 2005, Cell.

[79]  B. Meyer,et al.  The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation. , 2009, Genes & development.

[80]  L. Reinholdt,et al.  Positional cloning and characterization of mouse mei8, a disrupted allele of the meiotic cohesin Rec8 , 2004, Genesis.

[81]  N. Cobbe,et al.  Diverse Mitotic and Interphase Functions of Condensins in Drosophila , 2006, Genetics.

[82]  L. Makaroff,et al.  A mutation in a chromosome condensin II subunit, kleisin β, specifically disrupts T cell development , 2007, Proceedings of the National Academy of Sciences.

[83]  C. Goodnow,et al.  Defective T‐cell function leading to reduced antibody production in a kleisin‐β mutant mouse , 2008, Immunology.

[84]  Philip East,et al.  Eco1-Dependent Cohesin Acetylation During Establishment of Sister Chromatid Cohesion , 2008, Science.

[85]  B. Meyer.  Targeting X chromosomes for repression. , 2010, Current opinion in genetics & development.

[86]  L. Luo,et al.  piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. , 2008, Developmental cell.

[87]  M. McKay,et al.  Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. , 2005, Developmental cell.

[88]  M. Jantsch,et al.  The Caenorhabditis elegans SCC-3 homologue is required for meiotic synapsis and for proper chromosome disjunction in mitosis and meiosis. , 2003, Experimental cell research.

[89]  J. Peters,et al.  Cohesin Cleavage by Separase Required for Anaphase and Cytokinesis in Human Cells , 2001, Science.

[90]  Kim Nasmyth,et al.  Cohesin: its roles and mechanisms. , 2009, Annual review of genetics.

[91]  M. Eisen,et al.  A condensin-like dosage compensation complex acts at a distance to control expression throughout the genome. , 2009, Genes & development.

[92]  G. Bosco,et al.  Condensin II Resolves Chromosomal Associations to Enable Anaphase I Segregation in Drosophila Male Meiosis , 2008, PLoS genetics.

[93]  J. Peters,et al.  Aurora B controls the association of condensin I but not condensin II with mitotic chromosomes , 2007, Journal of Cell Science.

[94]  P. Fraser,et al.  Cohesins form chromosomal cis-interactions at the developmentally regulated IFNG locus , 2009, Nature.

[95]  D. Engelke,et al.  Nucleolar Clustering of Dispersed tRNA Genes , 2003, Science.

[96]  S. Dheur,et al.  A Screen for Cohesion Mutants Uncovers Ssl3, the Fission Yeast Counterpart of the Cohesin Loading Factor Scc4 , 2006, Current Biology.

[97]  A. Villeneuve,et al.  Synaptonemal complex assembly in C. elegans is dispensable for loading strand-exchange proteins but critical for proper completion of recombination. , 2003, Developmental cell.

[98]  G. Felsenfeld,et al.  Insulators: exploiting transcriptional and epigenetic mechanisms , 2006, Nature Reviews Genetics.

[99]  K. Nasmyth,et al.  Cohesins: Chromosomal Proteins that Prevent Premature Separation of Sister Chromatids , 1997, Cell.

[100]  N. Kleckner.  Chiasma formation: chromatin/axis interplay and the role(s) of the synaptonemal complex , 2006, Chromosoma.

[101]  D. Albertson,et al.  DPY-27: A chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome , 1994, Cell.

[102]  C. Nusbaum,et al.  Dosage compensation proteins targeted to X chromosomes by a determinant of hermaphrodite fate. , 1999, Science.

[103]  Christel Krueger,et al.  Cohesin Is Required for Higher-Order Chromatin Conformation at the Imprinted IGF2-H19 Locus , 2009, PLoS genetics.

[104]  V. Guacci,et al.  The kleisin subunit of cohesin dictates damage-induced cohesion. , 2008, Molecular cell.

[105]  Barbara J Meyer,et al.  C. elegans condensin promotes mitotic chromosome architecture, centromere organization, and sister chromatid segregation during mitosis and meiosis. , 2002, Genes & development.

[106]  Steven P. Gygi,et al.  A Molecular Determinant for the Establishment of Sister Chromatid Cohesion , 2008, Science.

[107]  J. Rine,et al.  The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. , 1999, Genes & development.

[108]  K. Shirahige,et al.  Postreplicative Formation of Cohesion Is Required for Repair and Induced by a Single DNA Break , 2007, Science.

[109]  Karl Mechtler,et al.  Phosphorylation of the Cohesin Subunit Scc1 by Polo/Cdc5 Kinase Regulates Sister Chromatid Separation in Yeast , 2001, Cell.

[110]  Earl F. Glynn,et al.  Genome-Wide Mapping of the Cohesin Complex in the Yeast Saccharomyces cerevisiae , 2004, PLoS biology.

[111]  D. Glover,et al.  Drosophila Aurora B Kinase Is Required for Histone H3 Phosphorylation and Condensin Recruitment during Chromosome Condensation and to Organize the Central Spindle during Cytokinesis , 2001, The Journal of cell biology.

[112]  A. Amon,et al.  The FK506 Binding Protein Fpr3 Counteracts Protein Phosphatase 1 to Maintain Meiotic Recombination Checkpoint Activity , 2005, Cell.

[113]  D. Koshland,et al.  DNA Double-Strand Breaks Trigger Genome-Wide Sister-Chromatid Cohesion Through Eco1 (Ctf7) , 2007, Science.

[114]  Kim Nasmyth,et al.  Cleavage of Cohesin by the CD Clan Protease Separin Triggers Anaphase in Yeast , 2000, Cell.

[115]  C. Lister,et al.  The DIF1 gene of Arabidopsis is required for meiotic chromosome segregation and belongs to the REC8/RAD21 cohesin gene family. , 1999, The Plant journal : for cell and molecular biology.

[116]  L. Aragón,et al.  The unnamed complex: what do we know about Smc5-Smc6? , 2009, Chromosome Research.

[117]  B. Meyer,et al.  Clustered DNA motifs mark X chromosomes for repression by a dosage compensation complex , 2006, Nature.

[118]  N. Dhillon,et al.  Long-Range Communication between the Silencers of HMR , 2008, Molecular and Cellular Biology.

[119]  Austen R. D. Ganley,et al.  Recombination Regulation by Transcription-Induced Cohesin Dissociation in rDNA Repeats , 2005, Science.

[120]  T. Hirano.  At the heart of the chromosome: SMC proteins in action , 2006, Nature Reviews Molecular Cell Biology.

[121]  A. Villeneuve,et al.  Crossovers trigger a remodeling of meiotic chromosome axis composition that is linked to two-step loss of sister chromatid cohesion. , 2008, Genes & development.

[122]  David G Mets,et al.  Meiotic crossover number and distribution are regulated by a dosage compensation protein that resembles a condensin subunit. , 2008, Genes & development.

[123]  C. Tsang,et al.  Compacting DNA During the Interphase: Condensin Maintains rDNA Integrity , 2007, Cell cycle.

[124]  G. Bosco,et al.  Chromosome Alignment and Transvection Are Antagonized by Condensin II , 2008, Science.

[125]  N. Proudfoot,et al.  Transcriptional Termination Enhances Protein Expression in Human Cells , 2009, Molecular cell.

[126]  S. Grewal,et al.  A Role for TFIIIC Transcription Factor Complex in Genome Organization , 2006, Cell.

[127]  Lessons from drosophila: The LPS receptor , 2003 .