The emerging role of the cytoskeleton in chromosome dynamics

Frontiers in Genetics

Volumn 8, Issue MAY, 2017, Pages

  Spichal, Maya ^a   Fabre, Emmanuelle ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITÉ PARIS DIDEROT   (France)

Author keywords

Chromosomes; Cytoskeleton; Dynamics; Nucleus; Yeast

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN; ADENOSINE TRIPHOSPHATASE; CRISPR ASSOCIATED PROTEIN; CYTOSKELETON PROTEIN; HISTONE; TRANSCRIPTION ACTIVATOR LIKE EFFECTOR;

ACTIN FILAMENT; CELL NUCLEUS MEMBRANE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CHROMOSOME STRUCTURE; CYTOSKELETON; DNA END JOINING REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DOWN REGULATION; ELECTRON MICROSCOPY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION REGULATION; HUMAN; INTERMEDIATE FILAMENT; KINETOCHORE; MICROTUBULE; MOLECULAR DYNAMICS; NONHUMAN; PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; TELOMERE;

EID: 85019936451     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2017.00060     Document Type: Review

References (103)

1. Ahmed, K., Dehghani, H., Rugg-Gunn, P., Fussner, E., Rossant, J., and Bazett-Jones, D. P. (2010). Global chromatin architecture reflects pluripotency and lineage commitment in the early mouse embryo. PLoS ONE 5:e10531. doi: 10.1371/journal.pone.0010531
2. Bronshtein, I., Kepten, E., Kanter, I., Berezin, S., Lindner, M., Redwood, A. B., et al. (2015). Loss of lamin A function increases chromatin dynamics in the nuclear interior. Nat. Commun. 6:8044. doi: 10.1038/ncomms9044
3. Bronstein, I., Israel, Y., Kepten, E., Mai, S., Shav-Tal, Y., Barkai, E., et al. (2009). Transient anomalous diffusion of telomeres in the nucleus of mammalian cells. Phys. Rev. Lett. 103:018102.
4. Burke, B., and Roux, K. J. (2009). Nuclei take a position: managing nuclear location. Dev. Cell 17, 587-597. doi: 10.1016/j.devcel.2009.10.018
5. Bystricky, K., Heun, P., Gehlen, L., Langowski, J., and Gasser, S. M. (2004). Long-range compaction and flexibility of interphase chromatin in budding yeast analyzed by high-resolution imaging techniques. Proc. Natl. Acad. Sci. U.S.A. 101, 16495-16500. doi: 10.1073/pnas.0402766101
6. Bystricky, K., Laroche, T., van Houwe, G., Blaszczyk, M., and Gasser, S. M. (2005). Chromosome looping in yeast: telomere pairing and coordinated movement reflect anchoring efficiency and territorial organization. J. Cell Biol. 168, 375-387. doi: 10.1083/jcb.200409091
7. Cabal, G. G., Genovesio, A., Rodriguez-Navarro, S., Zimmer, C., Gadal, O., Lesne, A., et al. (2006). SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441, 770-773. doi: 10.1038/nature04752
8. Cagliero, C., Grand, R. S., Jones, M. B., Jin, D. J., and O'Sullivan, J. M. (2013). Genome conformation capture reveals that the Escherichia coli chromosome is organized by replication and transcription. Nucleic Acids Res. 41, 6058-6071. doi: 10.1093/nar/gkt325
9. Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J., Zhang, W., Li, G.-W., et al. (2013). Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 155, 1479-1491. doi: 10.1016/j.cell.2013.12.001
10. Chuang, C.-H., Carpenter, A. E., Fuchsova, B., Johnson, T., de Lanerolle, P., and Belmont, A. S. (2006). Long-range directional movement of an interphase chromosome site. Curr. Biol. 16, 825-831. doi: 10.1016/j.cub.2006.03.059
11. Conrad, M. N., Lee, C. Y., Chao, G., Shinohara, M., Kosaka, H., Shinohara, A., et al. (2008). Rapid telomere movement in meiotic prophase is promoted by NDJ1, MPS3, and CSM4 and is modulated by recombination. Cell 133, 1175-1187. doi: 10.1016/j.cell.2008.04.047
12. Conrad, M. N., Lee, C.-Y., Wilkerson, J. L., and Dresser, M. E. (2007). MPS3 mediates meiotic bouquet formation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 104, 8863-8868. doi: 10.1073/pnas.0606165104
13. Dekker, J. (2008). Mapping in vivo chromatin interactions in yeast suggests an extended chromatin fiber with regional variation in compaction. J. Biol. Chem. 283, 34532-34540. doi: 10.1074/jbc.M806479200
14. Dekker, J., Rippe, K., Dekker, M., and Kleckner, N. (2002). Capturing chromosome conformation. Science 295, 1306-1311. doi: 10.1126/science.1067799
15. Dion, V., Kalck, V., Horigome, C., Towbin, B. D., and Gasser, S. M. (2012). Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat. Cell Biol. 14, 502-509. doi: 10.1038/ncb2465
16. Dion, V., Shimada, K., and Gasser, S. M. (2010). Actin-related proteins in the nucleus: life beyond chromatin remodelers. Curr. Opin. Cell Biol. 22, 383-391. doi: 10.1016/j.ceb.2010.02.006
17. Dixon, J. R., Selvaraj, S., Yue, F., Kim, A., Li, Y., Shen, Y., et al. (2012). Topological domains in mammalian genomes identified by analysis of chromatin interactions. Nature 485, 376-380. doi: 10.1038/nature11082
18. Dopie, J., Skarp, K.-P., Kaisa Rajakyla, E., Tanhuanpaa, K., and Vartiainen, M. K. (2012). Active maintenance of nuclear actin by importin 9 supports transcription. Proc. Natl. Acad. Sci. U.S.A. 109, E544-E552. doi: 10.1073/pnas.1118880109
19. Duan, Z., Andronescu, M., Schutz, K., McIlwain, S., Kim, Y. J., Lee, C., et al. (2010). A three-dimensional model of the yeast genome. Nature 465, 363-367. doi: 10.1038/nature08973
20. Dundr, M., Ospina, J. K., Sung, M.-H., John, S., Upender, M., Ried, T., et al. (2007). Actin-dependent intranuclear repositioning of an active gene locus in vivo. J. Cell Biol. 179, 1095-1103. doi: 10.1083/jcb.200710058
21. Espeli, O., Mercier, R., and Boccard, F. (2008). DNA dynamics vary according to macrodomain topography in the E. coli chromosome. Mol. Microbiol. 68, 1418-1427. doi: 10.1111/j.1365-2958.2008.06239.x
22. Fomproix, N., and Percipalle, P. (2004). An actin-myosin complex on actively transcribing genes. Exp. Cell Res. 294, 140-148. doi: 10.1016/j.yexcr.2003.10.028
23. Friederichs, J. M., Ghosh, S., Smoyer, C. J., McCroskey, S., Miller, B. D., Weaver, K. J., et al. (2011). The SUN protein Mps3 is required for spindle pole body insertion into the nuclear membrane and nuclear envelope homeostasis. PLoS Genet. 7:e1002365. doi: 10.1371/journal.pgen.1002365
24. Fussner, E., Ching, R. W., and Bazett-Jones, D. P. (2011). Living without 30nm chromatin fibers. Trends Biochem. Sci. 36, 1-6. doi: 10.1016/j.tibs.2010.09.002
25. Gartenberg, M. R., Neumann, F. R., Laroche, T., Blaszczyk, M., and Gasser, S. M. (2004). Sir-mediated repression can occur independently of chromosomal and subnuclear contexts. Cell 119, 955-967. doi: 10.1016/j.cell.2004.11.008
26. Gerlich, D., and Ellenberg, J. (2003). Dynamics of chromosome positioning during the cell cycle. Curr. Opin. Cell Biol. 15, 664-671.
27. Guérin, T., Bénichou, O., and Voituriez, R. (2012). Non-Markovian polymer reaction kinetics. Nat. Chem. 4, 568-573. doi: 10.1038/nchem.1378
28. Guidi, M., Ruault, M., Loïodice, M., Cournac, A., Billaudeau, C., Hocher, A., et al. (2015). Spatial reorganization of telomeres in long-lived quiescent cells. Genome Biol. 16, 206. doi: 10.1186/s13059-015-0766-2
29. Hajjoul, H., Mathon, J., Ranchon, H., Goiffon, I., Mozziconacci, J., Albert, B., et al. (2013). High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome. Genome Res. 23, 1829-1838. doi: 10.1101/gr.157008.113
30. Hasty, P., and Montagna, C. (2014). Chromosomal rearrangements in cancer: detection and potential causal mechanisms. Mol. Cell. Oncol. 1:e29904. doi: 10.4161/mco.29904
31. Hauer, M. H., Seeber, A., Singh, V., Thierry, R., Sack, R., Amitai, A., et al. (2017). Histone degradation in response to DNA damage enhances chromatin dynamics and recombination rates. Nat. Struct. Mol. Biol. 24, 99-107. doi: 10.1038/nsmb.3347
32. Hendzel, M. (2014). The F-act's of nuclear actin. Curr. Opin. Cell Biol. 28, 84-89. doi: 10.1016/j.ceb.2014.04.003
33. Heun, P., Laroche, T., Shimada, K., Furrer, P., and Gasser, S. M. (2001). Chromosome dynamics in the yeast interphase nucleus. Science 294, 2181-2186. doi: 10.1126/science.1065366
34. Hou, C., Li, L., Qin, Z. S., and Corces, V. G. (2012). Gene density, transcription, and insulators contribute to the partition of the Drosophila genome into physical domains. Mol. Cell 48, 471-484. doi: 10.1016/j.molcel.2012.08.031
35. Hsieh, T.-H. S., Weiner, A., Lajoie, B., Dekker, J., Friedman, N., and Rando, O. J. (2015). Mapping nucleosome resolution chromosome folding in yeast by micro-C. Cell 162, 108-119. doi: 10.1016/j.cell.2015.05.048
36. Jaiswal, D., Turniansky, R., and Green, E. M. (2016). Choose your own adventure: the role of histone modifications in yeast cell fate. J. Mol. Biol. doi: 10.1016/j.jmb.2016.10.018 [Epub ahead of print].
37. Jaspersen, S. L., Giddings, T. H., and Winey, M. (2002). Mps3p is a novel component of the yeast spindle pole body that interacts with the yeast centrin homologue Cdc31p. J. Cell Biol. 159, 945-956. doi: 10.1083/jcb.200208169
38. Jaspersen, S. L., Martin, A. E., Glazko, G., Giddings, T. H., Morgan, G., Mushegian, A., et al. (2006). The Sad1-UNC-84 homology domain in Mps3 interacts with Mps2 to connect the spindle pole body with the nuclear envelope. J. Cell Biol. 174, 665-675. doi: 10.1083/jcb.200601062
39. Javer, A., Long, Z., Nugent, E., Grisi, M., Siriwatwetchakul, K., Dorfman, K. D., et al. (2013). Short-time movement of E. coli chromosomal loci depends on coordinate and subcellular localization. Nat. Commun. 4:3003. doi: 10.1038/ncomms3003
40. Jenuwein, T., and Allis, C. D. (2001). Translating the histone code. Science 293, 1074-1080. doi: 10.1126/science.1063127
41. Kalhor, R., Tjong, H., Jayathilaka, N., Alber, F., and Chen, L. (2012). Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat. Biotechnol. 30, 90-98. doi: 10.1038/nbt.2057
42. Kapoor, P., Chen, M., Winkler, D. D., Luger, K., and Shen, X. (2013). Evidence for monomeric actin function in INO80 chromatin remodeling. Nat. Struct. Mol. Biol. 20, 426-432. doi: 10.1038/nsmb.2529
43. Kapoor, P., and Shen, X. (2014). Mechanisms of nuclear actin in chromatin-remodeling complexes. Trends Cell Biol. 24, 238-246. doi: 10.1016/j.tcb.2013.10.007
44. Kosaka, H., Shinohara, M., and Shinohara, A. (2008). Csm4-dependent telomere movement on nuclear envelope promotes meiotic recombination. PLoS Genet. 4:e1000196. doi: 10.1371/journal.pgen.1000196
45. Koszul, R., Kim, K. P., Prentiss, M., Kleckner, N., and Kameoka, S. (2008). Meiotic chromosomes move by linkage to dynamic actin cables with transduction of force through the nuclear envelope. Cell 133, 1188-1201. doi: 10.1016/j.cell.2008.04.050
46. Koszul, R., and Kleckner, N. (2009). Dynamic chromosome movements during meiosis: a way to eliminate unwanted connections? Trends Cell Biol. 19, 716-724. doi: 10.1016/j.tcb.2009.09.007
47. Kulashreshtha, M., Mehta, I. S., Kumar, P., and Rao, B. J. (2016). Chromosome territory relocation during DNA repair requires nuclear myosin 1 recruitment to chromatin mediated by γ-H2AX signaling. Nucleic Acids Res. 44, 8272-8291. doi: 10.1093/nar/gkw573
48. Laporte, D., Courtout, F., Salin, B., Ceschin, J., and Sagot, I. (2013). An array of nuclear microtubules reorganizes the budding yeast nucleus during quiescence. J. Cell Biol. 203, 585-594. doi: 10.1083/jcb.201306075
49. Laporte, D., Courtout, F., Tollis, S., and Sagot, I. (2016). Quiescent Saccharomyces cerevisiae forms telomere hyperclusters at the nuclear membrane vicinity through a multifaceted mechanism involving Esc1, the Sir complex, and chromatin condensation. Mol. Biol. Cell 27, 1875-1884. doi: 10.1091/mbc.E16-01-0069
50. Lassadi, I., and Bystricky, K. (2011). Tracking of single and multiple genomic loci in living yeast cells. Methods Mol. Biol. 745, 499-522. doi: 10.1007/978-1-61779-129-1_29
51. Lavelle, C., Victor, J.-M., and Zlatanova, J. (2010). Chromatin fiber dynamics under tension and torsion. Int. J. Mol. Sci. 11, 1557-1579. doi: 10.3390/ijms11041557
52. Levi, V., Ruan, Q., Plutz, M., Belmont, A. S., and Gratton, E. (2005). Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J. 89, 4275-4285. doi: 10.1529/biophysj.105.066670
53. Lieberman-Aiden, E., van Berkum, N. L., Williams, L., Imakaev, M., Ragoczy, T., Telling, A., et al. (2009). Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 326, 289-293. doi: 10.1126/science.1181369
54. Lottersberger, F., Karssemeijer, R. A., Dimitrova, N., and de Lange, T. (2015). 53BP1 and the LINC complex promote microtubule-dependent DSB mobility and DNA repair. Cell 163, 880-893. doi: 10.1016/j.cell.2015.09.057
55. Lui, D. Y., Cahoon, C. K., and Burgess, S. M. (2013). Multiple opposing constraints govern chromosome interactions during meiosis. PLoS Genet. 9:e1003197. doi: 10.1371/journal.pgen.1003197
56. Macvanin, M., and Adhya, S. (2012). Architectural organization in E. coli nucleoid. Biochim. Biophys. Acta 1819, 830-835. doi: 10.1016/j.bbagrm.2012.02.012
57. Maeshima, K., Hihara, S., and Takata, H. (2010). New insight into the mitotic chromosome structure: irregular folding of nucleosome fibers without 30-nm chromatin structure. Cold Spring Harb. Symp. Quant. Biol. 75, 439-444. doi: 10.1101/sqb.2010.75.034
58. Marshall, W. F., Straight, A., Marko, J. F., Swedlow, J., Dernburg, A., Belmont, A., et al. (1997). Interphase chromosomes undergo constrained diffusional motion in living cells. Curr. Biol. 7, 930-939.
59. Mehta, I. S., Amira, M., Harvey, A. J., and Bridger, J. M. (2010). Rapid chromosome territory relocation by nuclear motor activity in response to serum removal in primary human fibroblasts. Genome Biol. 11:R5. doi: 10.1186/gb-2010-11-1-r5
60. Mehta, I. S., Eskiw, C. H., Arican, H. D., Kill, I. R., and Bridger, J. M. (2011). Farnesyltransferase inhibitor treatment restores chromosome territory positions and active chromosome dynamics in Hutchinson-Gilford progeria syndrome cells. Genome Biol. 12:R74. doi: 10.1186/gb-2011-12-8-r74
61. Miné-hattab, J., and Rothstein, R. (2012). Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol. 14, 510-517. doi: 10.1038/ncb2472
62. Morton, W. M., Ayscough, K. R., and McLaughlin, P. J. (2000). Latrunculin alters the actin-monomer subunit interface to prevent polymerization. Nat. Cell Biol. 2, 376-378. doi: 10.1038/35014075
63. Nishino, Y., Eltsov, M., Joti, Y., Ito, K., Takata, H., Takahashi, Y., et al. (2012). Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fibres without a 30-nm chromatin structure. EMBO J. 31, 1644-1653. doi: 10.1038/emboj.2012.35
64. Nora, E. P., Lajoie, B. R., Schulz, E. G., Giorgetti, L., Okamoto, I., Servant, N., et al. (2012). Spatial partitioning of the regulatory landscape of the X-inactivation centre. Nature 485, 381-385. doi: 10.1038/nature11049
65. Obrdlik, A., Louvet, E., Kukalev, A., Naschekin, D., Kiseleva, E., Fahrenkrog, B., et al. (2010). Nuclear myosin 1 is in complex with mature rRNA transcripts and associates with the nuclear pore basket. FASEB J. 24, 146-157. doi: 10.1096/fj.09-135863
66. Padmakumar, V. C., Abraham, S., Braune, S., Noegel, A. A., Tunggal, B., Karakesisoglou, I., et al. (2004). Enaptin, a giant actin-binding protein, is an element of the nuclear membrane and the actin cytoskeleton. Exp. Cell Res. 295, 330-339. doi: 10.1016/j.yexcr.2004.01.014
67. Papamichos-Chronakis, M., and Peterson, C. L. (2008). The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat. Struct. Mol. Biol. 15, 338-345. doi: 10.1038/nsmb.1413
68. Philimonenko, V. V., Zhao, J., Iben, S., Dingová, H., Kyselá, K., Kahle, M., et al. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165-1172. doi: 10.1038/ncb1190
69. Poch, O., and Winsor, B. (1997). Who's who among the Saccharomyces cerevisiae actin-related proteins? A classification and nomenclature proposal for a large family. Yeast 13, 1053-1058.
70. Rajakylä, E. K., and Vartiainen, M. K. (2014). Rho, nuclear actin, and actin-binding proteins in the regulation of transcription and gene expression. Small GTPases. 5:e27539. doi: 10.4161/sgtp.27539
71. Razafsky, D., and Hodzic, D. (2009). Bringing KASH under the SUN: the many faces of nucleo-cytoskeletal connections. J. Cell Biol. 186, 461-472. doi: 10.1083/jcb.200906068
72. Rothballer, A., and Kutay, U. (2013). The diverse functional LINCs of the nuclear envelope to the cytoskeleton and chromatin. Chromosoma 122, 415-429. doi: 10.1007/s00412-013-0417-x
73. Rutledge, M. T., Russo, M., Belton, J.-M., Dekker, J., and Broach, J. R. (2015). The yeast genome undergoes significant topological reorganization in quiescence. Nucleic Acids Res. 43, 8299-8313. doi: 10.1093/nar/gkv723
74. Saad, H., Gallardo, F., Dalvai, M., Tanguy-le-Gac, N., Lane, D., and Bystricky, K. (2014). DNA dynamics during early double-strand break processing revealed by non-intrusive imaging of living cells. PLoS Genet. 10:e1004187. doi: 10.1371/journal.pgen.1004187
75. Scheffer, M. P., Eltsov, M., and Frangakis, A. S. (2011). Evidence for short-range helical order in the 30-nm chromatin fibers of erythrocyte nuclei. Proc. Natl. Acad. Sci. U.S.A. 108, 16992-16997. doi: 10.1073/pnas.1108268108
76. Schober, H., Ferreira, H., Kalck, V., Gehlen, L. R., and Gasser, S. M. (2009). Yeast telomerase and the SUN domain protein Mps3 anchor telomeres and repress subtelomeric recombination. Genes Dev. 23, 928-938. doi: 10.1101/gad.1787509
77. Schober, H., Kalck, V., Vega-Palas, M. A., Van Houwe, G., Sage, D., Unser, M., et al. (2008). Controlled exchange of chromosomal arms reveals principles driving telomere interactions in yeast. Genome Res. 18, 261-271. doi: 10.1101/gr.6687808
78. Schreiner, S. M., Koo, P. K., Zhao, Y., Mochrie, S. G. J., and King, M. C. (2015). The tethering of chromatin to the nuclear envelope supports nuclear mechanics. Nat. Commun. 6:7159. doi: 10.1038/ncomms8159
79. Seeber, A., Dion, V., and Gasser, S. M. (2013). Checkpoint kinases and the INO80 nucleosome remodeling complex enhance global chromatin mobility in response to DNA damage. Genes Dev. 27, 1999-2008. doi: 10.1101/gad.222992.113
80. Sellers, J. R. (2004). Fifty important papers in the history of muscle contraction and myosin motility. J. Muscle Res. Cell Motil. 25, 483-487.
81. Sexton, T., Yaffe, E., Kenigsberg, E., Bantignies, F., Leblanc, B., Hoichman, M., et al. (2012). Three-dimensional folding and functional organization principles of the Drosophila genome. Cell 148, 458-472. doi: 10.1016/j.cell.2012.01.010
82. Sharili, A. S., Kenny, F. N., Vartiainen, M. K., and Connelly, J. T. (2016). Nuclear actin modulates cell motility via transcriptional regulation of adhesive and cytoskeletal genes. Sci. Rep. 6:33893. doi: 10.1038/srep33893
83. Shimada, K., Oma, Y., Schleker, T., Kugou, K., Ohta, K., Harata, M., et al. (2008). Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr. Biol. 18, 566-575. doi: 10.1016/j.cub.2008.03.049
84. Spector, D. L. (2003). The dynamics of chromosome organization and gene regulation. Annu. Rev. Biochem. 72, 573-608. doi: 10.1146/annurev.biochem.72.121801.161724
85. Spichal, M., Brion, A., Herbert, S., Cournac, A., Marbouty, M., Zimmer, C., et al. (2016). Evidence for a dual role of actin in regulating chromosome organization and dynamics in yeast. J. Cell Sci. 129, 681-692. doi: 10.1242/jcs.175745
86. Starr, D. A., and Fridolfsson, H. N. (2010). Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 26, 421-444. doi: 10.1146/annurev-cellbio-100109-104037
87. Strecker, J., Gupta, G. D., Zhang, W., Bashkurov, M., Landry, M.-C., Pelletier, L., et al. (2016). DNA damage signalling targets the kinetochore to promote chromatin mobility. Nat. Cell Biol. 18, 281-290. doi: 10.1038/ncb3308
88. Swygert, S. G., and Peterson, C. L. (2014). Chromatin dynamics: interplay between remodeling enzymes and histone modifications. Biochim. Biophys. Acta 1839, 728-736. doi: 10.1016/j.bbagrm.2014.02.013
89. Thakar, R., and Csink, A. K. (2005). Changing chromatin dynamics and nuclear organization during differentiation in Drosophila larval tissue. J. Cell Sci. 118, 951-960. doi: 10.1242/jcs.01684
90. Therizols, P., Duong, T., Dujon, B., Zimmer, C., and Fabre, E. (2010). Chromosome arm length and nuclear constraints determine the dynamic relationship of yeast subtelomeres. Proc. Natl. Acad. Sci. U.S.A. 107, 2025-2030. doi: 10.1073/pnas.0914187107
91. Therizols, P., Illingworth, R. S., Courilleau, C., Boyle, S., Wood, A. J., and Bickmore, W. A. (2014). Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 346, 1238-1242. doi: 10.1126/science.1259587
92. Thoma, F., Koller, T., and Klug, A. (1979). Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol. 83, 403-427.
93. Tjong, H., Gong, K., Chen, L., and Alber, F. (2012). Physical tethering and volume exclusion determine higher-order genome organization in budding yeast. Genome Res. 22, 1295-1305. doi: 10.1101/gr.129437.111
94. Trelles-Sticken, E., Dresser, M. E., and Scherthan, H. (2000). Meiotic telomere protein Ndj1p is required for meiosis-specific telomere distribution, bouquet formation and efficient homologue pairing. J. Cell Biol. 151, 95-106. doi: 10.1083/jcb.151.1.95
95. Verdaasdonk, J. S., Vasquez, P. A., Barry, R. M., Barry, T., Goodwin, S., Forest, M. G., et al. (2013). Centromere tethering confines chromosome domains. Mol. Cell 52, 819-831. doi: 10.1016/j.molcel.2013.10.021
96. Vincent, J. A., Kwong, T. J., and Tsukiyama, T. (2008). ATP-dependent chromatin remodeling shapes the DNA replication landscape. Nat. Struct. Mol. Biol. 15, 477-484. doi: 10.1038/nsmb.1419
97. Walter, J., Schermelleh, L., Cremer, M., Tashiro, S., and Cremer, T. (2003). Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J. Cell Biol. 160, 685-697. doi: 10.1083/jcb.200211103
98. Wanat, J. J., Kim, K. P., Koszul, R., Zanders, S., Weiner, B., Kleckner, N., et al. (2008). Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet. 4:e1000188. doi: 10.1371/journal.pgen.1000188
99. Weber, C. M., and Henikoff, S. (2014). Histone variants: dynamic punctuation in transcription. Genes Dev. 28, 672-682. doi: 10.1101/gad.238873.114
100. Weber, S. C., Spakowitz, A. J., and Theriot, J. A. (2012). Nonthermal ATP-dependent fluctuations contribute to the in vivo motion of chromosomal loci. Proc. Natl. Acad. Sci. U.S.A. 109, 7338-7343. doi: 10.1073/pnas.1119505109
101. Wong, H., Marie-Nelly, H., Herbert, S., Carrivain, P., Blanc, H., Koszul, R., et al. (2012). A predictive computational model of the dynamic 3D interphase yeast nucleus. Curr. Biol. 22, 1881-1890. doi: 10.1016/j.cub.2012.07.069
102. Zhang, M., Wang, F., Li, S., Wang, Y., Bai, Y., and Xu, X. (2014). TALE: a tale of genome editing. Prog. Biophys. Mol. Biol. 114, 25-32. doi: 10.1016/j.pbiomolbio.2013.11.006
103. Zhang, Q., Ragnauth, C., Greener, M. J., Shanahan, C. M., and Roberts, R. G. (2002). The nesprins are giant actin-binding proteins, orthologous to Drosophila melanogaster muscle protein MSP-300. Genomics 80, 473-481. doi: 10.1016/S0888-7543(02)96859-X