Transcription factors mediate condensin recruitment and global chromosomal organization in fission yeast

It is becoming clear that structural-maintenance-of-chromosomes (SMC) complexes such as condensin and cohesin are involved in three-dimensional genome organization, yet their exact roles in functional organization remain unclear. We used chromatin interaction analysis by paired-end tag sequencing (ChIA-PET) to comprehensively identify genome-wide associations mediated by condensin and cohesin in fission yeast. We found that although cohesin and condensin often bind to the same loci, they direct different association networks and generate small and larger chromatin domains, respectively. Cohesin mediates associations between loci positioned within 100 kb of each other; condensin can drive longer-range associations. Moreover, condensin, but not cohesin, connects cell cycle–regulated genes bound by mitotic transcription factors. This study describes the different functions of condensin and cohesin in genome organization and how specific transcription factors function in condensin loading, cell cycle–dependent genome organization and mitotic chromosome organization to support faithful chromosome segregation.

[1]  K. Shirahige,et al.  Condensin targets and reduces unwound DNA structures associated with transcription in mitotic chromosome condensation , 2015, Nature Communications.

[2]  J. Sedat,et al.  Spatial partitioning of the regulatory landscape of the X-inactivation centre , 2012, Nature.

[3]  Sigal Shachar,et al.  3D Chromosome Regulatory Landscape of Human Pluripotent Cells. , 2016, Cell stem cell.

[4]  Michael P. Snyder,et al.  Mango: a bias-correcting ChIA-PET analysis pipeline , 2015, Bioinform..

[5]  K. Gould,et al.  Ace2p contributes to fission yeast septin ring assembly by regulating mid2+ expression , 2005, Journal of Cell Science.

[6]  Neva C. Durand,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2014, Cell.

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

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

[9]  M. Yanagida,et al.  RNA pol II transcript abundance controls condensin accumulation at mitotically up-regulated and heat-shock-inducible genes in fission yeast , 2015, Genes to cells : devoted to molecular & cellular mechanisms.

[10]  O. Iwasaki,et al.  New vectors for epitope tagging and gene disruption in Schizosaccharomyces pombe. , 2013, BioTechniques.

[11]  Laura E. DeMare,et al.  The genomic landscape of cohesin-associated chromatin interactions , 2013, Genome research.

[12]  E. Nimmo,et al.  Mutations derepressing silent centromeric domains in fission yeast disrupt chromosome segregation. , 1995, Genes & development.

[13]  David A. Orlando,et al.  Supplemental Information Multiple Structural Maintenance of Chromosome Complexes at Transcriptional Regulatory Elements , 2013 .

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

[15]  W. Sung,et al.  ChIA-PET tool for comprehensive chromatin interaction analysis with paired-end tag sequencing , 2010, Genome Biology.

[16]  M. Yanagida,et al.  Condensin Architecture and Interaction with DNA Regulatory Non-SMC Subunits Bind to the Head of SMC Heterodimer , 2002, Current Biology.

[17]  Jesse R. Dixon,et al.  Topological Domains in Mammalian Genomes Identified by Analysis of Chromatin Interactions , 2012, Nature.

[18]  M. Yanagida,et al.  A cell cycle-regulated GATA factor promotes centromeric localization of CENP-A in fission yeast. , 2003, Molecular cell.

[19]  Jill M Dowen,et al.  Control of Cell Identity Genes Occurs in Insulated Neighborhoods in Mammalian Chromosomes , 2014, Cell.

[20]  Hideki Tanizawa,et al.  Centromeric motion facilitates the mobility of interphase genomic regions in fission yeast , 2013, Journal of Cell Science.

[21]  Marc W. Schmid,et al.  Hi-C analysis in Arabidopsis identifies the KNOT, a structure with similarities to the flamenco locus of Drosophila. , 2014, Molecular cell.

[22]  Yanli Wang,et al.  Topologically associating domains are stable units of replication-timing regulation , 2014, Nature.

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

[24]  B. Jones,et al.  Global identification of yeast chromosome interactions using Genome conformation capture. , 2009, Fungal genetics and biology : FG & B.

[25]  Yoshinori Watanabe,et al.  Condensin association with histone H2A shapes mitotic chromosomes , 2011, Nature.

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

[27]  L. Mirny,et al.  High-Resolution Mapping of the Spatial Organization of a Bacterial Chromosome , 2013, Science.

[28]  K. Zhao,et al.  Characterization of genome-wide enhancer-promoter interactions reveals co-expression of interacting genes and modes of higher order chromatin organization , 2012, Cell Research.

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

[30]  H. Erickson,et al.  Bimodal activation of SMC ATPase by intra‐ and inter‐molecular interactions , 2001, The EMBO journal.

[31]  Job Dekker,et al.  Cohesin-dependent globules and heterochromatin shape 3D genome architecture in S. pombe , 2014, Nature.

[32]  T. Misteli Beyond the Sequence: Cellular Organization of Genome Function , 2011 .

[33]  K. L. Gould,et al.  Ace2p controls the expression of genes required for cell separation in Schizosaccharomyces pombe. , 2005, Molecular biology of the cell.

[34]  J. Dekker,et al.  Condensin-Driven Remodeling of X-Chromosome Topology during Dosage Compensation , 2015, Nature.

[35]  Zhaohui S. Qin,et al.  Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. , 2012, Molecular cell.

[36]  Eric S. Lander,et al.  A 3D Map of the Human Genome at Kilobase Resolution Reveals Principles of Chromatin Looping , 2015, Cell.

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

[38]  E. Skordalakes,et al.  Interaction between TBP and Condensin Drives the Organization and Faithful Segregation of Mitotic Chromosomes. , 2015, Molecular cell.

[39]  M. Yanagida,et al.  Dissection of the essential steps for condensin accumulation at kinetochores and rDNAs during fission yeast mitosis , 2008, The Journal of cell biology.

[40]  G. Schroth,et al.  Cohesin-mediated interactions organize chromosomal domain architecture , 2013, The EMBO journal.

[41]  P. Philippsen,et al.  Heterologous modules for efficient and versatile PCR‐based gene targeting in Schizosaccharomyces pombe , 1998, Yeast.

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

[43]  Dariusz M Plewczynski,et al.  CTCF-Mediated Human 3D Genome Architecture Reveals Chromatin Topology for Transcription , 2015, Cell.

[44]  Jesse R. Dixon,et al.  Cohesin and CTCF differentially affect chromatin architecture and gene expression in human cells , 2013, Proceedings of the National Academy of Sciences.

[45]  Michael Q. Zhang,et al.  Genome-wide map of regulatory interactions in the human genome , 2014, Genome research.

[46]  A. Tanay,et al.  Three-Dimensional Folding and Functional Organization Principles of the Drosophila Genome , 2012, Cell.

[47]  William Stafford Noble,et al.  A Three-Dimensional Model of the Yeast Genome , 2010, Nature.

[48]  I. Amit,et al.  Comprehensive mapping of long range interactions reveals folding principles of the human genome , 2011 .

[49]  A. G. Chatterjee,et al.  Epigenetic regulation of condensin-mediated genome organization during the cell cycle and upon DNA damage through histone H3 lysine 56 acetylation. , 2012, Molecular cell.

[50]  P. Lio’,et al.  Periodic gene expression program of the fission yeast cell cycle , 2004, Nature Genetics.

[51]  N. Cozzarelli,et al.  13S Condensin Actively Reconfigures DNA by Introducing Global Positive Writhe Implications for Chromosome Condensation , 1999, Cell.

[52]  Chee Seng Chan,et al.  CTCF-Mediated Functional Chromatin Interactome in Pluripotent Cells , 2011, Nature Genetics.

[53]  Matteo Pellegrini,et al.  Genome-wide Hi-C analyses in wild-type and mutants reveal high-resolution chromatin interactions in Arabidopsis. , 2014, Molecular cell.

[54]  Zhaohui S. Qin,et al.  Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. , 2015, Molecular cell.

[55]  M. Yanagida,et al.  Fission yeast condensin complex: essential roles of non-SMC subunits for condensation and Cdc2 phosphorylation of Cut3/SMC4. , 1999, Genes & development.

[56]  Yijun Ruan,et al.  Chromatin Interaction Analysis Using Paired‐End Tag Sequencing , 2010, Current protocols in molecular biology.

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

[58]  Kohta Takahashi,et al.  Differential regulation of repeated histone genes during the fission yeast cell cycle , 2007, Nucleic acids research.

[59]  J. Keith Joung,et al.  Interactome Maps of Mouse Gene Regulatory Domains Reveal Basic Principles of Transcriptional Regulation , 2013, Cell.

[60]  F. Ishikawa,et al.  Tel1(ATM) and Rad3(ATR) phosphorylate the telomere protein Ccq1 to recruit telomerase and elongate telomeres in fission yeast. , 2012, Genes & development.

[61]  Raymond K. Auerbach,et al.  Extensive Promoter-Centered Chromatin Interactions Provide a Topological Basis for Transcription Regulation , 2012, Cell.

[62]  Zhaohui S. Qin,et al.  Insulator function and topological domain border strength scale with architectural protein occupancy , 2014, Genome Biology.

[63]  K. Nasmyth,et al.  Characterization of fission yeast cohesin: essential anaphase proteolysis of Rad21 phosphorylated in the S phase. , 2000, Genes & development.

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

[65]  Hideki Tanizawa,et al.  Mapping of long-range associations throughout the fission yeast genome reveals global genome organization linked to transcriptional regulation , 2010, Nucleic acids research.

[66]  G. Felsenfeld,et al.  Specific Sites in the C Terminus of CTCF Interact with the SA2 Subunit of the Cohesin Complex and Are Required for Cohesin-Dependent Insulation Activity , 2011, Molecular and Cellular Biology.