Chromatin Dynamics upon DNA Damage

The dynamics organization of the nuclear genome is essential for many biological processes and is often altered in cells from diseased tissue. In the presence of double-strand break (DSBs) in S. cerevisiae and some mammalian cell lines, DNA mobility is dramatically altered. These changes in DNA mobility act as a double-edged sword since they promote homologous pairing in diploid yeast for example, but in some cases, they lead to potentially mutagenic DNA repair event and are the source of chromosomal translocations. In this chapter, we will present the state of the art in the field of chromosomes mobility in response to DNA damage. After introducing the importance of genome organization and dynamics, we will present in a clear and accessible manner several methods used in the literature to measure and quantify chromatin mobility inside living cells. We will then give an overview of the important findings in the field, both in yeast and in mammalian cells.

[1]  C. Damaren,et al.  Nuclear microtubule filaments mediate non-linear directional motion of chromatin and promote DNA repair , 2018, Nature Communications.

[2]  Emily Lin,et al.  Nuclear F-actin and myosins drive relocalization of heterochromatic breaks , 2018, Nature.

[3]  B. Chait,et al.  Nuclear Arp2/3 drives DNA break clustering for homology-directed repair , 2018, Nature.

[4]  Lili Tu,et al.  Evolutionary dynamics of 3D genome architecture following polyploidization in cotton , 2018, Nature Plants.

[5]  R. Tjian,et al.  Recent evidence that TADs and chromatin loops are dynamic structures , 2017, Nucleus.

[6]  X. Darzacq,et al.  Multi-scale tracking reveals scale-dependent chromatin dynamics after DNA damage , 2017, Molecular biology of the cell.

[7]  A. Thierry,et al.  Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle , 2017, The EMBO journal.

[8]  C. Zimmer,et al.  Chromatin stiffening underlies enhanced locus mobility after DNA damage in budding yeast , 2017, The EMBO journal.

[9]  K. Bloom,et al.  Microtubule dynamics drive enhanced chromatin motion and mobilize telomeres in response to DNA damage , 2017, Molecular biology of the cell.

[10]  William Stafford Noble,et al.  Form and function of topologically associating genomic domains in budding yeast , 2017, Proceedings of the National Academy of Sciences.

[11]  Marc A Marti-Renom,et al.  Defined chromosome structure in the genome-reduced bacterium Mycoplasma pneumoniae , 2017, Nature Communications.

[12]  M. Skrzypczak,et al.  Genome wide mapping of long range contacts unveils DNA Double Strand Breaks clustering at damaged active genes , 2017, Nature Structural &Molecular Biology.

[13]  S. Gasser,et al.  Visualization of Chromatin Decompaction and Break Site Extrusion as Predicted by Statistical Polymer Modeling of Single-Locus Trajectories. , 2017, Cell reports.

[14]  S. Gasser,et al.  Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates , 2017, Nature Structural &Molecular Biology.

[15]  K. Maeshima,et al.  Dynamic Nucleosome Movement Provides Structural Information of Topological Chromatin Domains in Living Human Cells , 2016, bioRxiv.

[16]  X. Darzacq,et al.  Chromatin mobility after DNA damage is modified to enhance long distance explorations and minimize local resampling , 2016, bioRxiv.

[17]  D. Durocher,et al.  DNA damage signalling targets the kinetochore to promote chromatin mobility , 2016, Nature Cell Biology.

[18]  S. Huet,et al.  Chromatin dynamics at DNA breaks: what, how and why? , 2015 .

[19]  J. Lukas,et al.  Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose) , 2015, Nature Communications.

[20]  L. Mirny,et al.  Formation of Chromosomal Domains in Interphase by Loop Extrusion , 2015, bioRxiv.

[21]  Nir Friedman,et al.  Mapping Nucleosome Resolution Chromosome Folding in Yeast by Micro-C , 2015, Cell.

[22]  W E Moerner,et al.  Chromosomal locus tracking with proper accounting of static and dynamic errors. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.

[23]  Peng Yin,et al.  Single-molecule super-resolution imaging of chromosomes and in situ haplotype visualization using Oligopaint FISH probes , 2015, Nature Communications.

[24]  M. Garcia-Parajo,et al.  Chromatin Fibers Are Formed by Heterogeneous Groups of Nucleosomes In Vivo , 2015, Cell.

[25]  R. Rothstein,et al.  Cell biology of mitotic recombination. , 2015, Cold Spring Harbor perspectives in biology.

[26]  G. Legube,et al.  DNA double strand break repair pathway choice: a chromatin based decision? , 2015, Nucleus.

[27]  Damian Roqueiro,et al.  Genome-wide analysis of local chromatin packing in Arabidopsis thaliana , 2015, Genome research.

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

[29]  T. Misteli,et al.  Activation of DNA damage response signaling by condensed chromatin. , 2014, Cell reports.

[30]  L. Symington,et al.  Mechanisms and Regulation of Mitotic Recombination in Saccharomyces cerevisiae , 2014, Genetics.

[31]  Andrey G. Cherstvy,et al.  Anomalous diffusion models and their properties: non-stationarity, non-ergodicity, and ageing at the centenary of single particle tracking. , 2014, Physical chemistry chemical physics : PCCP.

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

[33]  Moritz Herrmann,et al.  Comparative analysis of metazoan chromatin organization , 2014, Nature.

[34]  Yaojun Zhang,et al.  3D Trajectories Adopted by Coding and Regulatory DNA Elements: First-Passage Times for Genomic Interactions , 2014, Cell.

[35]  E. Gratton,et al.  Chromatin dynamics during DNA repair revealed by pair correlation analysis of molecular flow in the nucleus. , 2014, Biophysical journal.

[36]  S. Jackson,et al.  Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks , 2014, Nature Structural &Molecular Biology.

[37]  Nicolas Tanguy-le-Gac,et al.  DNA Dynamics during Early Double-Strand Break Processing Revealed by Non-Intrusive Imaging of Living Cells , 2014, PLoS genetics.

[38]  S. Gasser,et al.  Remodelers move chromatin in response to DNA damage , 2014, Cell cycle.

[39]  Ignacio Izeddin,et al.  Single cell correlation fractal dimension of chromatin , 2014, Nucleus.

[40]  R. Rothstein,et al.  DNA in motion during double-strand break repair. , 2013, Trends in cell biology.

[41]  Benjamin Albert,et al.  High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome , 2013, Genome research.

[42]  S. Gasser,et al.  Cohesin and the nucleolus constrain the mobility of spontaneous repair foci , 2013, EMBO reports.

[43]  K. Yoshikawa,et al.  Chromatin Compaction Protects Genomic DNA from Radiation Damage , 2013, PloS one.

[44]  S. Gasser,et al.  Checkpoint kinases and the INO80 nucleosome remodeling complex enhance global chromatin mobility in response to DNA damage , 2013, Genes & development.

[45]  T. Misteli,et al.  Spatial Dynamics of Chromosome Translocations in Living Cells , 2013, Science.

[46]  Krzysztof Burnecki,et al.  Universal algorithm for identification of fractional Brownian motion. A case of telomere subdiffusion. , 2012, Biophysical journal.

[47]  R. Metzler,et al.  Strange kinetics of single molecules in living cells , 2012 .

[48]  Yoshinori Nishino,et al.  Chromosomes without a 30-nm chromatin fiber , 2012, Nucleus.

[49]  B. Schuster-Böckler,et al.  Chromatin organization is a major influence on regional mutation rates in human cancer cells , 2012, Nature.

[50]  O Bénichou,et al.  Non-Markovian polymer reaction kinetics. , 2012, Nature chemistry.

[51]  J. Aten,et al.  Chromatin mobility is increased at sites of DNA double-strand breaks , 2012, Journal of Cell Science.

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

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

[54]  Rodney Rothstein,et al.  Increased chromosome mobility facilitates homology search during recombination , 2012, Nature Cell Biology.

[55]  Susan M. Gasser,et al.  Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery , 2012, Nature Cell Biology.

[56]  J. Elf,et al.  Single-molecule investigations of the stringent response machinery in living bacterial cells , 2011, Proceedings of the National Academy of Sciences.

[57]  Emmanuel Barillot,et al.  Live-Cell Chromosome Dynamics and Outcome of X Chromosome Pairing Events during ES Cell Differentiation , 2011, Cell.

[58]  Marco Durante,et al.  DNA double-strand breaks in heterochromatin elicit fast repair protein recruitment, histone H2AX phosphorylation and relocation to euchromatin , 2011, Nucleic acids research.

[59]  Aki Minoda,et al.  Double-Strand Breaks in Heterochromatin Move Outside of a Dynamic HP1a Domain to Complete Recombinational Repair , 2011, Cell.

[60]  X. Michalet.  Mean square displacement analysis of single-particle trajectories with localization error: Brownian motion in an isotropic medium. , 2010, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  T. Misteli.  Higher-order genome organization in human disease. , 2010, Cold Spring Harbor perspectives in biology.

[62]  Kazuhiro Maeshima,et al.  Chromatin structure: does the 30-nm fibre exist in vivo? , 2010, Current opinion in cell biology.

[63]  J. Theriot,et al.  Chromosomal Loci Move Subdiffusively through a Viscoelastic Cytoplasm , 2010 .

[64]  E. Soutoglou,et al.  DNA repair: easy to visualize, difficult to elucidate. , 2009, Trends in cell biology.

[65]  R. Rothstein,et al.  Choreography of recombination proteins during the DNA damage response. , 2009, DNA repair.

[66]  Y. Garini,et al.  Transient anomalous diffusion of telomeres in the nucleus of mammalian cells. , 2009, Physical review letters.

[67]  G. Taucher‐Scholz,et al.  Live cell microscopy analysis of radiation-induced DNA double-strand break motion , 2009, Proceedings of the National Academy of Sciences.

[68]  D. Spector,et al.  53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility , 2008, Nature.

[69]  Ilya J. Finkelstein,et al.  Single molecule studies of homologous recombination. , 2008, Molecular bioSystems.

[70]  M. Dutreix,et al.  Real-time measurements of the nucleation, growth and dissociation of single Rad51–DNA nucleoprotein filaments , 2007, Nucleic acids research.

[71]  J. Haber,et al.  Repair of DNA double strand breaks: in vivo biochemistry. , 2006, Methods in enzymology.

[72]  R. Kanaar,et al.  DNA double-strand break repair: all's well that ends well. , 2006, Annual review of genetics.

[73]  Y. Shiloh,et al.  Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM- and KAP-1 dependent pathway , 2006, Nature Cell Biology.

[74]  F. Hediger,et al.  Nuclear pore association confers optimal expression levels for an inducible yeast gene , 2006, Nature.

[75]  Jean-Christophe Olivo-Marin,et al.  SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope , 2006, Nature.

[76]  Louise Fairall,et al.  EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  James G. McNally,et al.  Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks , 2006, The Journal of cell biology.

[78]  Enrico Gratton,et al.  Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. , 2005, Biophysical journal.

[79]  T. Richmond,et al.  X-ray structure of a tetranucleosome and its implications for the chromatin fibre , 2005, Nature.

[80]  R. Rothstein,et al.  DNA Repair: Keeping It Together , 2004, Current Biology.

[81]  L. Symington,et al.  Recombination proteins in yeast. , 2004, Annual review of genetics.

[82]  R. Rothstein,et al.  Choreography of the DNA Damage Response Spatiotemporal Relationships among Checkpoint and Repair Proteins , 2004, Cell.

[83]  J. Aten,et al.  Dynamics of DNA Double-Strand Breaks Revealed by Clustering of Damaged Chromosome Domains , 2004, Science.

[84]  A. Knudson,et al.  Endogenous DNA double-strand breaks: Production, fidelity of repair, and induction of cancer , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[85]  J. Haber,et al.  In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. , 2003, Molecular cell.

[86]  Rodney Rothstein,et al.  Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre , 2003, Nature Cell Biology.

[87]  F. Rassool.  DNA double strand breaks (DSB) and non-homologous end joining (NHEJ) pathways in human leukemia. , 2003, Cancer letters.

[88]  W. Bickmore,et al.  Considering Nuclear Compartmentalization in the Light of Nuclear Dynamics , 2003, Cell.

[89]  S. Gasser,et al.  Chromosome Dynamics in the Yeast Interphase Nucleus , 2001, Science.

[90]  John W. Sedat,et al.  Multiple regimes of constrained chromosome motion are regulated in the interphase Drosophila nucleus , 2001, Current Biology.

[91]  F. Müller-Plathe,et al.  Chain stiffness intensifies the reptation characteristics of polymer dynamics in the melt. , 2000, Chemphyschem : a European journal of chemical physics and physical chemistry.

[92]  A. Murray,et al.  Interphase chromosomes undergo constrained diffusional motion in living cells , 1997, Current Biology.

[93]  A S Belmont,et al.  In vivo localization of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recognition , 1996, The Journal of cell biology.

[94]  M. Tomita,et al.  Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging , 2017 .

[95]  Susan M. Gasser,et al.  Visualizing yeast chromosomes and nuclear architecture. , 2010, Methods in enzymology.

[96]  M. Kupiec,et al.  Finding a match: how do homologous sequences get together for recombination? , 2008, Nature Reviews Genetics.

[97]  T. Misteli,et al.  Hyperdynamic plasticity of chromatin proteins in pluripotent embryonic stem cells. , 2006, Developmental cell.

[98]  W. Coffey,et al.  Diffusion and Reactions in Fractals and Disordered Systems , 2002 .

[99]  R. Rothstein,et al.  From the Cover: Rad52 forms DNA repair and recombination centers during S phase , 2001 .

[100]  H. Lodish,et al.  DNA Damage and Repair and Their Role in Carcinogenesis , 2000 .

[101]  K. Jacobson,et al.  Single-particle tracking: applications to membrane dynamics. , 1997, Annual review of biophysics and biomolecular structure.

[102]  I. Amit,et al.  Supporting Online Material Materials and Methods Som Text Comprehensive Mapping of Long-range Interactions Reveals Folding Principles of the Human Genome , 2022 .