Biochemistry (Moscow)

, Volume 83, Issue 6, pp 690–700 | Cite as

Mobility of Nuclear Components and Genome Functioning

  • E. A. ArifulinEmail author
  • Y. R. Musinova
  • Y. S. Vassetzky
  • E. V. Sheval


Cell nucleus is characterized by strong compartmentalization of structural components in its three-dimensional space. Certain genomic functions are accompanied by changes in the localization of chromatin loci and nuclear bodies. Here we review recent data on the mobility of nuclear components and the role of this mobility in genome functioning.


nucleus genome chromatin nuclear bodies mobility 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Benabdallah, N. S., and Bickmore, W. A. (2015) Regulatory domains and their mechanisms, Cold Spring Harb. Symp. Quant. Biol., 80, 45–51.PubMedCrossRefGoogle Scholar
  2. 2.
    Erokhin, M., Vassetzky, Y., Georgiev, P., and Chetverina, D. (2015) Eukaryotic enhancers: common features, regula-tion, and participation in diseases, Cell. Mol. Life Sci., 72, 2361–2375.PubMedCrossRefGoogle Scholar
  3. 3.
    Dion, V., and Gasser, S. M. (2013) Chromatin movement in the maintenance of genome stability, Cell, 152, 1355–1364.PubMedCrossRefGoogle Scholar
  4. 4.
    Dekker, J., and Misteli, T. (2015) Long-range chromatin interactions, Cold Spring Harb. Perspect. Biol., 7, a019356.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Shachar, S., and Misteli, T. (2017) Causes and conse-quences of nuclear gene positioning, J. Cell. Sci., 130, 1501–1508.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Kuznetsova, M. A., and Sheval, E. V. (2016) Chromatin fibers: from classical descriptions to modern interpretation, Cell. Biol. Int., 40, 1140–1151.PubMedCrossRefGoogle Scholar
  7. 7.
    Finch, J. T., and Klug, A. (1976) Solenoidal model for superstructure in chromatin, Proc. Natl. Acad. Sci. USA, 73, 1897–1901.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Woodcock, C. L., Frado, L. L., and Rattner, J. B. (1984) The higher-order structure of chromatin: evidence for a helical ribbon arrangement, J. Cell Biol., 99, 42–52.PubMedCrossRefGoogle Scholar
  9. 9.
    Grigoryev, S. A., Arya, G., Correll, S., Woodcock, C. L., and Schlick, T. (2009) Evidence for heteromorphic chro-matin fibers from analysis of nucleosome interactions, Proc. Natl. Acad. Sci. USA, 106, 13317–13322.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    McDowall, A. W., Smith, J. M., and Dubochet, J. (1986) Cryo-electron microscopy of vitrified chromosomes in situ, EMBO J., 5, 1395–1402.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Eltsov, M., Maclellan, K. M., Maeshima, K., Frangakis, A. S., and Dubochet, J. (2008) Analysis of cryo-electron microscopy images does not support the existence of 30-nm chromatin fibers in mitotic chromosomes in situ, Proc. Natl. Acad. Sci. USA, 105, 19732–19737.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Gan, L., Ladinsky, M. S., and Jensen, G. J. (2013) Chromatin in a marine picoeukaryote is a disordered assemblage of nucleosomes, Chromosoma, 122, 377–386.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Mahamid, J., Pfeffer, S., Schaffer, M., Villa, E., Danev, R., Cuellar, L. K., Forster, F., Hyman, A. A., Plitzko, J. M., and Baumeister, W. (2016) Visualizing the molecular soci-ology at the HeLa cell nuclear periphery, Science, 351, 969–972.PubMedCrossRefGoogle Scholar
  14. 14.
    Razin, S. V., and Gavrilov, A. A. (2014) Chromatin without the 30-nm fiber: constrained disorder instead of hierarchi-cal folding, Epigenetics, 9, 653–657.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Maeshima, K., Hihara, S., and Eltsov, M. (2010) Chromatin structure: does the 30-nm fibre exist in vivo? Curr. Opin. Cell Biol., 22, 291–297.PubMedCrossRefGoogle Scholar
  16. 16.
    Hihara, S., Pack, C.-G., Kaizu, K., Tani, T., Hanafusa, T., Nozaki, T., Takemoto, S., Yoshimi, T., Yokota, H., Imamoto, N., Sako, Y., Kinjo, M., Takahashi, K., Nagai, T., and Maeshima, K. (2012) Local nucleosome dynamics facilitate chromatin accessibility in living mammalian cells, Cell Rep., 2, 1645–1656.PubMedCrossRefGoogle Scholar
  17. 17.
    Nozaki, T., Kaizu, K., Pack, C.-G., Tamura, S., Tani, T., Hihara, S., Nagai, T., Takahashi, K., and Maeshima, K. (2013) Flexible and dynamic nucleosome fiber in living mammalian cells, Nucleus, 4, 349–356.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Nozaki, T., Imai, R., Tanbo, M., Nagashima, R., Tamura, S., Tani, T., Joti, Y., Tomita, M., Hibino, K., Kanemaki, M. T., Wendt, K. S., Okada, Y., Nagai, T., and Maeshima, K. (2017) Dynamic organization of chromatin domains revealed by super-resolution live-cell imaging, Mol. Cell, 67, 282–293.PubMedCrossRefGoogle Scholar
  19. 19.
    Branco, M. R., and Pombo, A. (2006) Intermingling of chromosome territories in interphase suggests role in translocations and transcription-dependent associations, PLoS Biol., 4, e138.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Boettiger, A. N., Bintu, B., Moffitt, J. R., Wang, S., Beliveau, B. J., Fudenberg, G., Imakaev, M., Mirny, L. A., Wu, C.-T., and Zhuang, X. (2016) Super-resolution imag-ing reveals distinct chromatin folding for different epige-netic states, Nature, 529, 418–422.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Liang, Z., Zickler, D., Prentiss, M., Chang, F. S., Witz, G., Maeshima, K., and Kleckner, N. (2015) Chromosomes progress to metaphase in multiple discrete steps via global compaction/expansion cycles, Cell, 161, 1124–1137.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Nagasaka, K., Hossain, M. J., Roberti, M. J., Ellenberg, J., and Hirota, T. (2016) Sister chromatid resolution is an intrinsic part of chromosome organization in prophase, Nat. Cell Biol., 18, 692–699.PubMedCrossRefGoogle Scholar
  23. 23.
    Robinett, C. C., Straight, A., Li, G., Willhelm, C., Sudlow, G., Murray, A., and Belmont, A. S. (1996) In vivo localiza-tion of DNA sequences and visualization of large-scale chromatin organization using lac operator/repressor recog-nition, J. Cell Biol., 135, 1685–1700.PubMedCrossRefGoogle Scholar
  24. 24.
    Chen, B., Gilbert, L. A., Cimini, B. A., Schnitzbauer, J., Zhang, W., Li, G.-W., Park, J., Blackburn, E. H., Weissman, J. S., Qi, L. S., and Huang, B. (2013) Dynamic imaging of genomic loci in living human cells by an opti-mized CRISPR/Cas system, Cell, 155, 1479–1491.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Ma, H., Naseri, A., Reyes-Gutierrez, P., Wolfe, S. A., Zhang, S., and Pederson, T. (2015) Multicolor CRISPR labeling of chromosomal loci in human cells, Proc. Natl. Acad. Sci. USA, 112, 3002–3007.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Ma, H., Tu, L.-C., Naseri, A., Huisman, M., Zhang, S., Grunwald, D., and Pederson, T. (2016) Multiplexed label-ing of genomic loci with dCas9 and engineered sgRNAs using CRISPRainbow, Nat. Biotechnol., 34, 528–530.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Dreissig, S., Schiml, S., Schindele, P., Weiss, O., Rutten, T., Schubert, V., Gladilin, E., Mette, M. F., Puchta, H., and Houben, A. (2017) Live-cell CRISPR imaging in plants reveals dynamic telomere movements, Plant J., 91, 565–573.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Germier, T., Kocanova, S., Walther, N., Bancaud, A., Shaban, H. A., Sellou, H., Politi, A. Z., Ellenberg, J., Gallardo, F., and Bystricky, K. (2017) Real-time imaging of a single gene reveals transcription-initiated local confine-ment, Biophys. J., 113, 1383–1394.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Lanctot, C., Cheutin, T., Cremer, M., Cavalli, G., and Cremer, T. (2007) Dynamic genome architecture in the nuclear space: regulation of gene expression in three dimensions, Nat. Rev. Genet., 8, 104–115.PubMedCrossRefGoogle Scholar
  31. 31.
    Marshall, W. F., Straight, A., Marko, J. F., Swedlow, J., Dernburg, A., Belmont, A., Murray, A. W., Agard, D. A., and Sedat, J. W. (1997) Interphase chromosomes undergo constrained diffusional motion in living cells, Curr. Biol., 7, 930–939.PubMedCrossRefGoogle Scholar
  32. 32.
    Mine-Hattab, J., and Rothstein, R. (2013) DNA in motion during double-strand break repair, Trends Cell Biol., 23, 529–536.PubMedCrossRefGoogle Scholar
  33. 33.
    Bystricky, K., Van Attikum, H., Montiel, M.-D., Dion, V., Gehlen, L., and Gasser, S. M. (2009) Regulation of nuclear positioning and dynamics of the silent mating type loci by the yeast Ku70/Ku80 complex, Mol. Cell. Biol., 29, 835–848.PubMedCrossRefGoogle Scholar
  34. 34.
    Hajjoul, H., Mathon, J., Ranchon, H., Goiffon, I., Mozziconacci, J., Albert, B., Carrivain, P., Victor, J.-M., Gadal, O., Bystricky, K., and Bancaud, A. (2013) High-throughput chromatin motion tracking in living yeast reveals the flexibility of the fiber throughout the genome, Genome Res., 23, 1829–1838.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Tamm, M. V., Nazarov, L. I., Gavrilov, A. A., and Chertovich, A. V. (2015) Anomalous diffusion in fractal globules, Phys. Rev. Lett., 114, 178102.PubMedCrossRefGoogle Scholar
  36. 36.
    Ma, H., Tu, L.-C., Naseri, A., Chung, Y.-C., Grunwald, D., Zhang, S., and Pederson, T. (2017) CRISPR-based DNA imaging in living cells reveals cell cycle-dependent chromosome dynamics, bioRxiv, 195966.Google Scholar
  37. 37.
    Pliss, A., Malyavantham, K., Bhattacharya, S., Zeitz, M., and Berezney, R. (2009) Chromatin dynamics is correlated with replication timing, Chromosoma, 118, 459–470.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Krawczyk, P. M., Borovski, T., Stap, J., Cijsouw, T., ten Cate, R., Medema, J. P., Kanaar, R., Franken, N. A. P., and Aten, J. A. (2012) Chromatin mobility is increased at sites of DNA double-strand breaks, J. Cell. Sci., 125, 2127–2133.PubMedCrossRefGoogle Scholar
  39. 39.
    Neumann, F. R., Dion, V., Gehlen, L. R., Tsai-Pflugfelder, M., Schmid, R., Taddei, A., and Gasser, S. M. (2012) Targeted INO80 enhances subnuclear chromatin move-ment and ectopic homologous recombination, Genes Dev., 26, 369–383.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Ochiai, H., Sugawara, T., and Yamamoto, T. (2015) Simultaneous live imaging of the transcription and nuclear position of specific genes, Nucleic Acids Res., 43, e127.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Sorokin, D. V., Peterlik, I., Tektonidis, M., Rohr, K., and Matula, P. (2018) Non-rigid contour-based registration of cell nuclei in 2D live cell microscopy images using a dynamic elasticity model, IEEE Trans. Med. Imaging, 37, 173–184.PubMedCrossRefGoogle Scholar
  42. 42.
    Zidovska, A., Weitz, D. A., and Mitchison, T. J. (2013) Micron-scale coherence in interphase chromatin dynam-ics, Proc. Natl. Acad. Sci. USA, 110, 15555–15560.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Jaunin, F., Visser, A. E., Cmarko, D., Aten, J. A., and Fakan, S. (2000) Fine structural in situ analysis of nascent DNA movement following DNA replication, Exp. Cell Res., 260, 313–323.PubMedCrossRefGoogle Scholar
  44. 44.
    Jaunin, F., and Fakan, S. (2002) DNA replication and nuclear architecture, J. Cell. Biochem., 85, 1–9.PubMedCrossRefGoogle Scholar
  45. 45.
    Arifulin, E. A. (2015) Ultrastructural organization of repli-cating chromatin in prematurely condensed chromosomes, Biopolym. Cell, 31, 249–254.CrossRefGoogle Scholar
  46. 46.
    Leonhardt, H., Rahn, H. P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D., and Cardoso, M. C. (2000) Dynamics of DNA replication factories in living cells, J. Cell. Biol., 149, 271–280.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Pliss, A., Malyavantham, K. S., Bhattacharya, S., and Berezney, R. (2013) Chromatin dynamics in living cells: identification of oscillatory motion, J. Cell. Physiol., 228, 609–616.PubMedCrossRefGoogle Scholar
  48. 48.
    Chagin, V. O., Casas-Delucchi, C. S., Reinhart, M., Schermelleh, L., Markaki, Y., Maiser, A., Bolius, J. J., Bensimon, A., Fillies, M., Domaing, P., Rozanov, Y. M., Leonhardt, H., and Cardoso, M. C. (2016) 4D visualiza-tion of replication foci in mammalian cells corresponding to individual replicons, Nat. Commun., 7, 11231.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Nakamura, H., Morita, T., and Sato, C. (1986) Structural organizations of replicon domains during DNA synthetic phase in the mammalian nucleus, Exp. Cell Res., 165, 291–297.PubMedCrossRefGoogle Scholar
  50. 50.
    O’Keefe, R. T., Henderson, S. C., and Spector, D. L. (1992) Dynamic organization of DNA replication in mam-malian cell nuclei: spatially and temporally defined replica-tion of chromosome-specific alpha-satellite DNA sequences, J. Cell. Biol., 116, 1095–1110.PubMedCrossRefGoogle Scholar
  51. 51.
    Jackson, D. A., and Pombo, A. (1998) Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells, J. Cell. Biol., 140, 1285–1295.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Xiang, W., Julia Roberti, M., Heriche, J.-K., Huet, S., Alexander, S., and Ellenberg, J. (2017) Correlative live and super-resolution imaging reveals the dynamic structure of replication domains, bioRxiv, 189373.Google Scholar
  53. 53.
    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 recombi-nation machinery, Nat. Cell Biol., 14, 502–509.CrossRefGoogle Scholar
  54. 54.
    Mine-Hattab, J., and Rothstein, R. (2012) Increased chro-mosome mobility facilitates homology search during recombination, Nat. Cell Biol., 14, 510–517.PubMedCrossRefGoogle Scholar
  55. 55.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Seeber, A., and Gasser, S. M. (2017) Chromatin organiza-tion and dynamics in double-strand break repair, Curr. Opin. Genet. Dev., 43, 9–16.PubMedCrossRefGoogle Scholar
  57. 57.
    Nagai, S., Dubrana, K., Tsai-Pflugfelder, M., Davidson, M. B., Roberts, T. M., Brown, G. W., Varela, E., Hediger, F., Gasser, S. M., and Krogan, N. J. (2008) Functional tar-geting of DNA damage to a nuclear pore-associated SUMO-dependent ubiquitin ligase, Science, 322, 597–602.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Lisby, M., Mortensen, U. H., and Rothstein, R. (2003) Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre, Nat. Cell Biol., 5, 572–577.PubMedCrossRefGoogle Scholar
  59. 59.
    Dion, V., Kalck, V., Seeber, A., Schleker, T., and Gasser, S. M. (2013) Cohesin and the nucleolus constrain the mobili-ty of spontaneous repair foci, EMBO Rep., 14, 984–991.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Kruhlak, M. J., Celeste, A., Dellaire, G., Fernandez-Capetillo, O., Muller, W. G., McNally, J. G., Bazett-Jones, D. P., and Nussenzweig, A. (2006) Changes in chromatin structure and mobility in living cells at sites of DNA dou-ble-strand breaks, J. Cell. Biol., 172, 823–834.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Falk, M., Lukasova, E., Gabrielova, B., Ondrej, V., and Kozubek, S. (2007) Chromatin dynamics during DSB repair, Biochim. Biophys. Acta, 1773, 1534–1545.PubMedCrossRefGoogle Scholar
  62. 62.
    Soutoglou, E., Dorn, J. F., Sengupta, K., Jasin, M., Nussenzweig, A., Ried, T., Danuser, G., and Misteli, T. (2007) Positional stability of single double-strand breaks in mammalian cells, Nat. Cell. Biol., 9, 675–682.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Jakob, B., Splinter, J., Durante, M., and Taucher-Scholz, G. (2009) Live cell microscopy analysis of radiation-induced DNA double-strand break motion, Proc. Natl. Acad. Sci. USA, 106, 3172–3177.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    Liu, J., Vidi, P.-A., Lelievre, S. A., and Irudayaraj, J. M. K. (2015) Nanoscale histone localization in live cells reveals reduced chromatin mobility in response to DNA damage, J. Cell Sci., 128, 599–604.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Iarovaia, O. V., Rubtsov, M., Ioudinkova, E., Tsfasman, T., Razin, S. V., and Vassetzky, Y. S. (2014) Dynamics of dou-ble strand breaks and chromosomal translocations, Mol. Cancer, 13, 249.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Glukhov, S. I., Rubtsov, M. A., Alexeyevsky, D. A., Alexeevski, A. V., Razin, S. V., and Iarovaia, O. V. (2013) The broken MLL gene is frequently located outside the inherent chromosome territory in human lymphoid cells treated with DNA topoisomerase II poison etoposide, PLoS One, 8, e75871.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Chiolo, I., Minoda, A., Colmenares, S. U., Polyzos, A., Costes, S. V., and Karpen, G. H. (2011) Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair, Cell, 144, 732–744.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Ryu, T., Spatola, B., Delabaere, L., Bowlin, K., Hopp, H., Kunitake, R., Karpen, G. H., and Chiolo, I. (2015) Heterochromatic breaks move to the nuclear periphery to continue recombinational repair, Nat. Cell Biol., 17, 1401–1411.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Roukos, V., Voss, T. C., Schmidt, C. K., Lee, S., Wangsa, D., and Misteli, T. (2013) Spatial dynamics of chromosome translocations in living cells, Science, 341, 660–664.PubMedCrossRefGoogle Scholar
  70. 70.
    Nikiforova, M. N., Stringer, J. R., Blough, R., Medvedovic, M., Fagin, J. A., and Nikiforov, Y. E. (2000) Proximity of chromosomal loci that participate in radia-tion-induced rearrangements in human cells, Science, 290, 138–141.PubMedCrossRefGoogle Scholar
  71. 71.
    Roix, J. J., McQueen, P. G., Munson, P. J., Parada, L. A., and Misteli, T. (2003) Spatial proximity of translocation-prone gene loci in human lymphomas, Nat. Genet., 34, 287–291.PubMedCrossRefGoogle Scholar
  72. 72.
    Parada, L. A., McQueen, P. G., and Misteli, T. (2004) Tissue-specific spatial organization of genomes, Genome Biol., 5, R44.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Germini, D., Tsfasman, T., Klibi, M., El-Amine, R., Pichugin, A., Iarovaia, O. V., Bilhou-Nabera, C., Subra, F., Bou Saada, Y., Sukhanova, A., Boutboul, D., Raphael, M., Wiels, J., Razin, S. V., Bury-Mone, S., Oksenhendler, E., Lipinski, M., and Vassetzky, Y. S. (2017) HIV Tat induces a prolonged MYC relocalization next to IGH in circulating B-cells, Leukemia, 31, 2515–2522.PubMedCrossRefGoogle Scholar
  74. 74.
    Pombo, A., and Dillon, N. (2015) Three-dimensional genome architecture: players and mechanisms, Nat. Rev. Mol. Cell Biol., 16, 245–257.PubMedCrossRefGoogle Scholar
  75. 75.
    Dekker, J., Marti-Renom, M. A., and Mirny, L. A. (2013) Exploring the three-dimensional organization of genomes: interpreting chromatin interaction data, Nat. Rev. Genet., 14, 390–403.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Bickmore, W. A., and Van Steensel, B. (2013) Genome architecture: domain organization of interphase chromo-somes, Cell, 152, 1270–1284.PubMedCrossRefGoogle Scholar
  77. 77.
    Cremer, T., and Cremer, C. (2001) Chromosome territo-ries, nuclear architecture and gene regulation in mam-malian cells, Nat. Rev. Genet., 2, 292–301.PubMedCrossRefGoogle Scholar
  78. 78.
    Boyle, S., Gilchrist, S., Bridger, J. M., Mahy, N. L., Ellis, J. A., and Bickmore, W. A. (2001) The spatial organization of human chromosomes within the nuclei of normal and emerin-mutant cells, Hum. Mol. Genet., 10, 211–219.PubMedCrossRefGoogle Scholar
  79. 79.
    Croft, J. A., Bridger, J. M., Boyle, S., Perry, P., Teague, P., and Bickmore, W. A. (1999) Differences in the localization and morphology of chromosomes in the human nucleus, J. Cell. Biol., 145, 1119–1131.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Mehta, I. S., Kulashreshtha, M., Chakraborty, S., Kolthur-Seetharam, U., and Rao, B. J. (2013) Chromosome territo-ries reposition during DNA damage-repair response, Genome Biol., 14, R135.Google Scholar
  81. 81.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    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.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Bridger, J. M., Boyle, S., Kill, I. R., and Bickmore, W. A. (2000) Re-modelling of nuclear architecture in quiescent and senescent human fibroblasts, Curr. Biol., 10, 149–152.PubMedCrossRefGoogle Scholar
  84. 84.
    Essers, J., Van Cappellen, W. A., Theil, A. F., Van Drunen, E., Jaspers, N. G. J., Hoeijmakers, J. H. J., Wyman, C., Vermeulen, W., and Kanaar, R. (2004) Dynamics of relative chromosome position during the cell cycle, Mol. Biol. Cell, 16, 769–775.PubMedCrossRefGoogle Scholar
  85. 85.
    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 main-tained during subsequent interphase stages, J. Cell Biol., 160, 685–697.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Thomson, I., Gilchrist, S., Bickmore, W. A., and Chubb, J. R. (2004) The radial positioning of chromatin is not inher-ited through mitosis but is established de novo in early G1, Curr. Biol., 14, 166–172.PubMedCrossRefGoogle Scholar
  87. 87.
    Zhang, Q., Kota, K. P., Alam, S. G., Nickerson, J. A., Dickinson, R. B., and Lele, T. P. (2016) Coordinated dynamics of RNA splicing speckles in the nucleus, J. Cell. Physiol., 231, 1269–1275.PubMedCrossRefGoogle Scholar
  88. 88.
    Arifulin, E. A., Sorokin, D. V., Musinova, Y. R., Zhironkina, O. A., Golyshev, S. A., Abramchuk, S. S., Vassetzky, Y. S., and Sheval, E. V. (2017) Heterochromatin restricts the mobility of nuclear bodies, Chromosoma, (in press).Google Scholar
  89. 89.
    Dundr, M., Ospina, J. K., Sung, M.-H., John, S., Upender, M., Ried, T., Hager, G. L., and Matera, A. G. (2007) Actin-dependent intranuclear repositioning of an active gene locus in vivo, J. Cell. Biol., 179, 1095–1103.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Chang, L., Godinez, W. J., Kim, I.-H., Tektonidis, M., De Lanerolle, P., Eils, R., Rohr, K., and Knipe, D. M. (2011) Herpesviral replication compartments move and coalesce at nuclear speckles to enhance export of viral late mRNA, Proc. Natl. Acad. Sci. USA, 108, 136–144.CrossRefGoogle Scholar
  91. 91.
    Khanna, N., Hu, Y., and Belmont, A. S. (2014) HSP70 transgene directed motion to nuclear speckles facilitates heat shock activation, Curr. Biol., 24, 1138–1144.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Ondrej, V., Kozubek, S., Lukasova, E., Falk, M., Matula, P., Matula, P., and Kozubek, M. (2006) Directional motion of foreign plasmid DNA to nuclear HP1 foci, Chromosome Res., 14, 505–514.PubMedCrossRefGoogle Scholar
  93. 93.
    Arbona, J.-M., Herbert, S., Fabre, E., and Zimmer, C. (2017) Inferring the physical properties of yeast chromatin through Bayesian analysis of whole nucleus simulations, Genome Biol., 18, 81.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Matheson, T. D., and Kaufman, P. D. (2016) Grabbing the genome by the NADs, Chromosoma, 125, 361–371.PubMedCrossRefGoogle Scholar
  95. 95.
    Gonzalez-Sandoval, A., and Gasser, S. M. (2016) On TADs and LADs: spatial control over gene expression, Trends Genet., 32, 485–495.PubMedCrossRefGoogle Scholar
  96. 96.
    Yanez-Cuna, J. O., and Van Steensel, B. (2017) Genome–nuclear lamina interactions: from cell popula-tions to single cells, Curr. Opin. Genet. Dev., 43, 67–72.PubMedCrossRefGoogle Scholar
  97. 97.
    Van Steensel, B., and Belmont, A. S. (2017) Lamina-asso-ciated domains: links with chromosome architecture, hete-rochromatin, and gene repression, Cell, 169, 780–791.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Padeken, J., and Heun, P. (2014) Nucleolus and nuclear periphery: velcro for heterochromatin, Curr. Opin. Cell Biol., 28, 54–60.PubMedCrossRefGoogle Scholar
  99. 99.
    Kind, J., Pagie, L., Ortabozkoyun, H., Boyle, S., De Vries, S. S., Janssen, H., Amendola, M., Nolen, L. D., Bickmore, W. A., and Van Steensel, B. (2013) Single-cell dynamics of genome–nuclear lamina interactions, Cell, 153, 178–192.PubMedCrossRefGoogle Scholar
  100. 100.
    van Koningsbruggen, S., Gierlinski, M., Schofield, P., Martin, D., Barton, G. J., Ariyurek, Y., Den Dunnen, J. T., and Lamond, A. I. (2010) High-resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli, Mol. Biol. Cell, 21, 3735–3748.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Ogushi, S., Yamagata, K., Obuse, C., Furuta, K., Wakayama, T., Matzuk, M. M., and Saitou, M. (2017) Reconstitution of the oocyte nucleolus in mice through a single nucleolar protein, NPM2, J. Cell Sci., 130, 2416–2429.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Solovei, I., Kreysing, M., Lanctot, C., Kosem, S., Peichl, L., Cremer, T., Guck, J., and Joffe, B. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution, Cell, 137, 356–368.PubMedCrossRefGoogle Scholar
  103. 103.
    Eberhart, A., Feodorova, Y., Song, C., Wanner, G., Kiseleva, E., Furukawa, T., Kimura, H., Schotta, G., Leonhardt, H., Joffe, B., and Solovei, I. (2013) Epigenetics of eu-and heterochromatin in inverted and conventional nuclei from mouse retina, Chromosome Res., 21, 535–554.PubMedCrossRefGoogle Scholar
  104. 104.
    Thanisch, K., Song, C., Engelkamp, D., Koch, J., Wang, A., Hallberg, E., Foisner, R., Leonhardt, H., Stewart, C. L., Joffe, B., and Solovei, I. (2017) Nuclear envelope localization of LEMD2 is developmentally dynamic and lamin A/C dependent yet insufficient for heterochromatin tethering, Differentiation, 94, 58–70.PubMedCrossRefGoogle Scholar
  105. 105.
    Musinova, Y. R., Lisitsyna, O. M., Sorokin, D. V., Arifulin, E. A., Smirnova, T. A., Zinovkin, R. A., Potashnikova, D. M., Vassetzky, Y. S., and Sheval, E. V. (2016) RNA-dependent disassembly of nuclear bodies, J. Cell Sci., 129, 4509–4520.PubMedCrossRefGoogle Scholar
  106. 106.
    Cremer, T., Kreth, G., Koester, H., Fink, R. H., Heintzmann, R., Cremer, M., Solovei, I., Zink, D., and Cremer, C. (2000) Chromosome territories, interchro-matin domain compartment, and nuclear matrix: an inte-grated view of the functional nuclear architecture, Crit. Rev. Eukaryot. Gene Expr., 10, 179–212.PubMedCrossRefGoogle Scholar
  107. 107.
    Albiez, H., Cremer, M., Tiberi, C., Vecchio, L., Schermelleh, L., Dittrich, S., Kupper, K., Joffe, B., Thormeyer, T., Von Hase, J., Yang, S., Rohr, K., Leonhardt, H., Solovei, I., Cremer, C., Fakan, S., and Cremer, T. (2006) Chromatin domains and the interchro-matin compartment form structurally defined and func-tionally interacting nuclear networks, Chromosome Res., 14, 707–733.PubMedCrossRefGoogle Scholar
  108. 108.
    Rouquette, J., Genoud, C., Vazquez-Nin, G. H., Kraus, B., Cremer, T., and Fakan, S. (2009) Revealing the high-resolution three-dimensional network of chromatin and interchromatin space: a novel electron-microscopic approach to reconstructing nuclear architecture, Chromosome Res., 17, 801–810.PubMedCrossRefGoogle Scholar
  109. 109.
    Arai, R., Sugawara, T., Sato, Y., Minakuchi, Y., Toyoda, A., Nabeshima, K., Kimura, H., and Kimura, A. (2017) Reduction in chromosome mobility accompanies nuclear organization during early embryogenesis in Caenorhabditis elegans, Sci. Rep., 7, 3631.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Vinogradov, A. E. (2005) Genome size and chromatin condensation in vertebrates, Chromosoma, 113, 362–369.PubMedCrossRefGoogle Scholar
  111. 111.
    Sparvoli, E., Gay, H., and Kaufmann, B. P. (1965) Number and pattern of association of chromonemata in the chro-mosomes of Tradescantia, Chromosoma, 16, 415–435.PubMedCrossRefGoogle Scholar
  112. 112.
    Hao, S., Jiao, M., Zhao, J., Xing, M., and Huang, B. (1994) Reorganization and condensation of chromatin in mitotic prophase nuclei of Allium cepa, Chromosoma, 103, 432–440.PubMedCrossRefGoogle Scholar
  113. 113.
    Kuznetsova, M. A., Chaban, I. A., and Sheval, E. V. (2017) Visualization of chromosome condensation in plants with large chromosomes, BMC Plant Biol., 17, 153.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 114.
    Macadangdang, B. R., Oberai, A., Spektor, T., Campos, O. A., Sheng, F., Carey, M. F., Vogelauer, M., and Kurdistani, S. K. (2014) Evolution of histone 2A for chro-matin compaction in eukaryotes, eLife, 3, e02792.PubMedCentralCrossRefGoogle Scholar
  115. 115.
    Bronshtein, I., Kepten, E., Kanter, I., Berezin, S., Lindner, M., Redwood, A. B., Mai, S., Gonzalo, S., Foisner, R., Shav-Tal, Y., and Garini, Y. (2015) Loss of lamin A function increases chromatin dynamics in the nuclear interior, Nat. Commun., 6, 8044.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Bronshtein, I., Kanter, I., Kepten, E., Lindner, M., Berezin, S., Shav-Tal, Y., and Garini, Y. (2016) Exploring chromatin organization mechanisms through its dynamic properties, Nucleus, 7, 27–33.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Stixova, L., Matula, P., Kozubek, S., Gombitova, A., Cmarko, D., Raska, I., and Bartova, E. (2012) Trajectories and nuclear arrangement of PML bodies are influenced by A-type lamin deficiency, Biol. Cell., 104, 418–432.PubMedCrossRefGoogle Scholar
  118. 118.
    Orlova, D. Y., Stixova, L., Kozubek, S., Gierman, H. J., Sustackova, G., Chernyshev, A. V., Medvedev, R. N., Legartova, S., Versteeg, R., Matula, P., Stoklasa, R., and Bartova, E. (2012) Arrangement of nuclear structures is not transmitted through mitosis but is identical in sister cells, J. Cell. Biochem., 113, 3313–3329.PubMedCrossRefGoogle Scholar
  119. 119.
    Strickfaden, H., Zunhammer, A., van Koningsbruggen, S., Kohler, D., and Cremer, T. (2010) 4D chromatin dynam-ics in cycling cells: Theodor Boveri’s hypotheses revisited, Nucleus, 1, 284–297.PubMedPubMedCentralGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • E. A. Arifulin
    • 1
    Email author
  • Y. R. Musinova
    • 1
    • 2
    • 3
  • Y. S. Vassetzky
    • 1
    • 2
    • 3
    • 4
  • E. V. Sheval
    • 1
    • 2
  1. 1.Belozersky Institute of Physico-Chemical BiologyLomonosov Moscow State UniversityMoscowRussia
  2. 2.LIA 1066 LFR2O French-Russian Joint Cancer Research LaboratoryVillejuifFrance
  3. 3.Koltzov Institute of Developmental BiologyRussian Academy of SciencesMoscowRussia
  4. 4.UMR8126, CNRS, Université Paris-SudInstitut de Cancérologie Gustave RoussyVillejuifFrance

Personalised recommendations