Biochemistry (Moscow)

, Volume 83, Issue 4, pp 450–466 | Cite as

Who Needs This Junk, or Genomic Dark Matter

  • O. I. Podgornaya
  • D. I. Ostromyshenskii
  • N. I. Enukashvily


Centromeres (CEN), pericentromeric regions (periCEN), and subtelomeric regions (subTel) comprise the areas of constitutive heterochromatin (HChr). Tandem repeats (TRs or satellite DNA) are the main components of HChr forming no less than 10% of the mouse and human genome. HChr is assembled within distinct structures in the interphase nuclei of many species–chromocenters. In this review, the main classes of HChr repeat sequences are considered in the order of their number increase in the sequencing reads of the mouse chromocenters (ChrmC). TRs comprise ~70% of ChrmC occupying the first place. Non-LTR (-long terminal repeat) retroposons (mainly LINE, long interspersed nuclear element) are the next (~11%), and endogenous retroviruses (ERV; LTR-containing) are in the third position (~9%). HChr is not enriched with ERV in comparison with the whole genome, but there are differences in distribution of certain elements: while MaLR-like elements (ERV3) are dominant in the whole genome, intracisternal A-particles and corresponding LTR (ERV2) are prevalent in HChr. Most of LINE in ChrmC is represented by the 2-kb fragment at the end of the 2nd open reading frame and its flanking regions. Almost all tandem repeats classified as CEN or periCEN are contained in ChrmC. Our previous classification revealed 60 new mouse TR families with 29 of them being absent in ChrmC, which indicates their location on chromosome arms. TR transcription is necessary for maintenance of heterochromatic status of the HChr genome part. A burst of TR transcription is especially important in embryogenesis and other cases of radical changes in the cell program, including carcinogenesis. The recently discovered mechanism of epigenetic regulation with noncoding sequences transcripts, long noncoding RNA, and its role in embryogenesis and pluripotency maintenance is discussed.


heterochromatin sequencing tandem repeats dispersed repeats transposable elements retrotransposons long noncoding RNA in situ hybridization 




CENP-B box

CEN-binding site of CENP-B protein


dataset of sequence reads from mouse chromocenters


extracellular DNA


endogenous retrovirus


fluorescent in situ hybridization


golden path gap (unfilled gap in assembled genomes with size of 3 Mb reserved for CEN)


human artificial chromosome




high order repeat


heterochromatic protein 1


human satellites 1–3


heat shock factor-1 (transcription factor)


intracisternal A-particles


long interspersed nuclear element


long non-coding RNA


long terminal repeats in ERV


mouse major satellite (periCEN)


mouse minor satellite (CEN)


pericentromeric regions


satellite DNA


short interspersed nuclear element


subtelomeric region


transposable elements


tandem repeats


Whole Genome Shotgun (dataset of reads assembled to genome contigs).


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Koryakov, D. E., and Zhimulev, I. F. (2009) Chromosomes. Structure and Functions [in Russian], SO RAN Publishers, Novosibirsk.Google Scholar
  2. 2.
    Wijchers, P. J., Geeven, G., Eyres, M., Bergsma, A. J., Janssen, M., Verstegen, M., Zhu, Y., Schell, Y., Vermeulen, C., De Wit, E., and De Laat, W. (2015) Characterization and dynamics of pericentromere-associated domains in mice, Genome Res., 25, 958–969.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Guenatri, M., Bailly, D., Maison, C., and Almouzni, G. (2004) Mouse centric and pericentric satellite repeats form distinct functional heterochromatin, J. Cell Biol., 166, 493–505.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Snapp, R. R., Goveia, E., Peet, L., Bouffard, N. A., Badger, G. J., and Langevin, H. M. (2013) Spatial organization of fibroblast nuclear chromocenters: component tree analysis, J. Anat., 223, 255–261.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    De Koning, A. J., Gu, W., Castoe, T. A., Batzer, M. A., and Pollock, D. D. (2011) Repetitive elements may comprise over two-thirds of the human genome, PLoS Genet., 7, e1002384.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Probst, A. V., Okamoto, I., Casanova, M., Marjou, F., Le Baccon, P., and Almouzni, G. (2010) A strand-specific burst in transcription of pericentric satellites is required for chromocenter formation and early mouse development, Dev. Cell, 19, 625–638.PubMedCrossRefGoogle Scholar
  7. 7.
    Casanova, M., Pasternak, M., El Marjou, F., Le Baccon, P., Probst, A. V., and Almouzni, G. (2013) Heterochromatin reorganization during early mouse development requires a single-stranded noncoding transcript, Cell Rep., 4, 1156–1167.PubMedCrossRefGoogle Scholar
  8. 8.
    Zhu, Q., Pao, G. M., Huynh, A. M., Suh, H., Tonnu, N., Nederlof, P. M., and Verma, I. M. (2011) BRCA1 tumour suppression occurs via heterochromatin-mediated silencing, Nature, 477, 179–184.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Alexiadis, V., Ballestas, M. E., Sanchez, C., Winokur, S., Vedanarayanan, V., Warren, M., and Ehrlich, M. (2007) RNAPol-ChIP analysis of transcription from FSHD-linked tandem repeats and satellite DNA, Biochim. Biophys. Acta, 1769, 29–40.PubMedCrossRefGoogle Scholar
  10. 10.
    Elgin, S. C., and Reuter, G. (2013) Position-effect variegation, heterochromatin formation, and gene silencing in Drosophila, Cold Spring Harb. Perspect. Biol., 5, a01778.CrossRefGoogle Scholar
  11. 11.
    Shatskikh, A. S., and Gvozdev, V. A. (2013) Heterochromatin formation and transcription in relation to trans-inactivation of genes and their spatial organization in the nucleus, Biochemistry (Moscow), 78, 603–612.CrossRefGoogle Scholar
  12. 12.
    Mayer, R., Brero, A., Von Hase, J., Schroeder, T., Cremer, T., and Dietzel, S. (2005) Common themes and cell type specific variations of higher order chromatin arrangements in the mouse, BMC Cell. Biol., 6, 44.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Probst, A. V., and Almouzni, G. (2008) Pericentric heterochromatin: dynamic organization during early development in mammals, Differentiation, 76, 15–23.PubMedCrossRefGoogle Scholar
  14. 14.
    Prusov, A. N., and Zatsepina, O. V. (2002) Isolation of the chromocenter fraction from mouse liver nuclei, Biochemistry (Moscow), 67, 423–431.CrossRefGoogle Scholar
  15. 15.
    Zatsepina, O. V., Zharskaya, O. O., and Prusov, A. N. (2008) Isolation of the constitutive heterochromatin from mouse liver nuclei, in The Nucleus. Vol. 1: Nuclei and Subnuclear Components, Springer, pp. 169–180.CrossRefGoogle Scholar
  16. 16.
    Hutchins, A. P., and Pei, D. (2015) Transposable elements at the center of the crossroads between embryogenesis, embryonic stem cells, reprogramming, and long non-coding RNAs, Sci. Bull., 60, 1722–1733.Google Scholar
  17. 17.
    Ostromyshenskii, D. I., Chernyaeva, E. N., Kuznetsova, I. S., and Podgornaya, O. I. (2018) Mouse chromocenters DNA content: sequencing and in silico analysis, BMC Genomics, 19, 151.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Van der Kuyl, A. C. (2012) HIV infection and HERV expression: a review, Retrovirology, 9, 6.PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Wicker, T., Sabot, F., Hua-Van, A., Bennetzen, J. L., Capy, P., Chalhoub, B., and Paux, E. (2007) A unified classification system for eukaryotic transposable elements, Nat. Rev. Genet., 8, 973–982.PubMedCrossRefGoogle Scholar
  20. 20.
    Mouse Genome Sequencing Consortium; Waterston, R. H., Lindblad-Toh, K., Birney, E., Rogers, J., Abril, J. F., Agarwal, P., Agarwala, R., Ainscough, R., Alexandersson, M., An, P., Antonarakis, S. E., Attwood, J., Baertsch, R., Bailey, J., Barlow, K., Beck, S., Berry, E., Birren, B., Bloom, T., Bork, P., Botcherby, M., Bray, N., Brent, M. R., Brown, D. G., Brown, S. D., Bult, C., Burton, J., Butler, J., Campbell, R. D., Carninci, P., Cawley, S., Chiaromonte, F., Chinwalla, A. T., Church, D. M., Clamp, M., Clee, C., Collins, F. S., Cook, L. L., Copley, R. R., Coulson, A., Couronne, O., Cuff, J., Curwen, V., Cutts, T., Daly, M., David, R., Davies, J., Delehaunty, K. D., Deri, J., Dermitzakis, E. T., Dewey, C., Dickens, N. J., Diekhans, M., Dodge, S., Dubchak, I., Dunn, D. M., Eddy, S. R., Elnitski, L., Emes, R. D., Eswara, P., Eyras, E., Felsenfeld, A., Fewell, G. A., Flicek, P., Foley, K., Frankel, W. N., Fulton, L. A., Fulton, R. S., Furey, T. S., Gage, D., Gibbs, R. A., Glusman, G., Gnerre, S., Goldman, N., Goodstadt, L., Grafham, D., Graves, T. A., Green, E. D., Gregory, S., Guigo, R., Guyer, M., Hardison, R. C., Haussler, D., Hayashizaki, Y., Hillier, L. W., Hinrichs, A., Hlavina, W., Holzer, T., Hsu, F., Hua, A., Hubbard, T., Hunt, A., Jackson, I., Jaffe, D. B., Johnson, L. S., Jones, M., Jones, T. A., Joy, A., Kamal, M., Karlsson, E. K., Karolchik, D., Kasprzyk, A., Kawai, J., Keibler, E., Kells, C., Kent, W. J., Kirby, A., Kolbe, D. L., Korf, I., Kucherlapati, R. S., Kulbokas, E. J., Kulp, D., Landers, T., Leger, J. P., Leonard, S., Letunic, I., Levine, R., Li, J., Li, M., Lloyd, C., Lucas, S., Ma, B., Maglott, D. R., Mardis, E. R., Matthews, L., Mauceli, E., Mayer, J. H., McCarthy, M., McCombie, W. R., McLaren, S., McLay, K., McPherson, J. D., Meldrim, J., Meredith, B., Mesirov, J. P., Miller, W., Miner, T. L., Mongin, E., Montgomery, K. T., Morgan, M., Mott, R., Mullikin, J. C., Muzny, D. M., Nash, W. E., Nelson, J. O., Nhan, M. N., Nicol, R., Ning, Z., Nusbaum, C., O’Connor, M. J., Okazaki, Y., Oliver, K., Overton-Larty, E., Pachter, L., Parra, G., Pepin, K. H., Peterson, J., Pevzner, P., Plumb, R., Pohl, C. S., Poliakov, A., Ponce, T. C., Ponting, C. P., Potter, S., Quail, M., Reymond, A., Roe, B. A., Roskin, K. M., Rubin, E. M., Rust, A. G., Santos, R., Sapojnikov, V., Schultz, B., Schultz, J., Schwartz, M. S., Schwartz, S., Scott, C., Seaman, S., Searle, S., Sharpe, T., Sheridan, A., Shownkeen, R., Sims, S., Singer, J. B., Slater, G., Smit, A., Smith, D. R., Spencer, B., Stabenau, A., Stange-Thomann, N., Sugnet, C., Suyama, M., Tesler, G., Thompson, J., Torrents, D., Trevaskis, E., Tromp, J., Ucla, C., Ureta-Vidal, A., Vinson, J. P., Von Niederhausern, A. C., Wade, C. M., Wall, M., Weber, R. J., Weiss, R. B., Wendl, M. C., West, A. P., Wetterstrand, K., Wheeler, R., Whelan, S., Wierzbowski, J., Willey, D., Williams, S., Wilson, R. K., Winter, E., Worley, K. C., Wyman, D., Yang, S., Yang, S. P., Zdobnov, E. M., Zody, M. C., and Lander, E. S. (2002) Initial sequencing and comparative analysis of the mouse genome, Nature, 420, 520–562.CrossRefGoogle Scholar
  21. 21.
    Komissarov, A. S., Gavrilova, E. V., Demin, S. J., Ishov, A. M., and Podgornaya, O. I. (2011) Tandemly repeated DNA families in the mouse genome, BMC Genomics, 12, 531.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Dunn, C. A., Romanish, M. T., Gutierrez, L. E., Van de Lagemaat, L. N., and Mager, D. L. (2006) Transcription of two human genes from a bidirectional endogenous retrovirus promoter, Gene, 366, 335–342.PubMedCrossRefGoogle Scholar
  23. 23.
    Carone, D. M., Longo, M. S., Ferreri, G. C., Hall, L., Harris, M., Shook, N., and O’Neill, R. J. (2009) A new class of retroviral and satellite encoded small RNAs emanates from mammalian centromeres, Chromosoma, 118, 113–125.PubMedCrossRefGoogle Scholar
  24. 24.
    Longo, M. S., Carone, D. M., Green, E. D., O’Neill, M. J., and O’Neill, R. J. (2009) Distinct retroelement classes define evolutionary breakpoints demarcating sites of evolutionary novelty, BMC Genomics, 10, 334.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Ruiz-Herrera, A., Farre, M., and Robinson, T. J. (2012) Molecular cytogenetic and genomic insights into chromosomal evolution, Heredity, 108, 28–36.PubMedCrossRefGoogle Scholar
  26. 26.
    Ferreri, G. C., Brown, J. D., Obergfell, C., Jue, N., Finn, C. E., O’Neill, M. J., and O’Neill, R. J. (2011) Recent amplification of the kangaroo endogenous retrovirus, KERV, limited to the centromere, J. Virol., 85, 4761–4771.PubMedGoogle Scholar
  27. 27.
    Brattas, P. L., Jonsson, M. E., Fasching, L., Wahlestedt, J. N., Shahsavani, M., Falk, R., and Jakobsson, J. (2017) TRIM28 controls a gene regulatory network based on endogenous retroviruses in human neural progenitor cells, Cell Rep., 18, 1–11.PubMedCrossRefGoogle Scholar
  28. 28.
    Chuong, E. B., Rumi, M. K., Soares, M. J., and Baker, J. C. (2013) Endogenous retroviruses function as species-specific enhancer elements in the placenta, Nat. Genet., 45, 325–329.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Lynch, V. J., Nnamani, M. C., Kapusta, A., Brayer, K., Plaza, S. L., Mazur, E. C., and Graf, A. (2015) Ancient transposable elements transformed the uterine regulatory landscape and transcriptome during the evolution of mammalian pregnancy, Cell Rep., 10, 551–561.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Roberts, R. M., Green, J. A., and Schulz, L. C. (2016) The evolution of the placenta, Reproduction, 152, 179–189.CrossRefGoogle Scholar
  31. 31.
    Imakawa, K., and Nakagawa, S. (2017) The phylogeny of placental evolution through dynamic integrations of retrotransposons, Prog. Mol. Biol. Transl. Sci., 145, 89–109.PubMedCrossRefGoogle Scholar
  32. 32.
    Mager, D. L., and Stoye, J. P. (2015) Mammalian endogenous retroviruses, Microbiol. Spectrum, 3, No. 1, MDNA3-0009-2014; doi: 10.1128/microbiolspec.MDNA3-0009-2014.Google Scholar
  33. 33.
    Lu, X., Sachs, F., Ramsay, L., Jacques, P. E., Goke, J., Bourque, G., and Ngoh, H. (2014) The retrovirus HERVH is a long noncoding RNA required for human embryonic stem cell identity, Nat. Struct. Mol. Biol., 21, 423–425.PubMedCrossRefGoogle Scholar
  34. 34.
    Goke, J., Lu, X., Chan, Y. S., Ng, H. H., Ly, L. H., Sachs, F., and Szczerbinska, I. (2015) Dynamic transcription of distinct classes of endogenous retroviral elements marks specific populations of early human embryonic cells, Cell Stem Cell, 16, 135–141.PubMedCrossRefGoogle Scholar
  35. 35.
    Schoorlemmer, J., Perez-Palacios, R., Climent, M., Guallar, D., and Muniesa, P. (2014) Regulation of mouse retroelement MuERV-L/MERVL expression by REX1 and epigenetic control of stem cell potency, Front. Oncol., doi: 10.3389/fonc.2014.00014.Google Scholar
  36. 36.
    Robbez-Masson, L., and Rowe, H. M. (2015) Retrotransposons shape species-specific embryonic stem cell gene expression, Retrovirology, 12, 45.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Crichton, J. H., Dunican, D. S., MacLennan, M., Meehan, R. R., and Adams, I. R. (2014) Defending the genome from the enemy within: mechanisms of retrotransposon suppression in the mouse germline, Cell. Mol. Life Sci., 71, 1581–1605.PubMedCrossRefGoogle Scholar
  38. 38.
    Gerdes, P., Richardson, S. R., Mager, D. L., and Faulkner, G. J. (2016) Transposable elements in the mammalian embryo: pioneers surviving through stealth and service, Genome Biol., 17, 100.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Wong, C., Chen, A. A., Behr, B., and Shen, S. (2013) Time-lapse microscopy and image analysis in basic and clinical embryo development research, Reprod. Biomed. Online, 26, 120–129.PubMedCrossRefGoogle Scholar
  40. 40.
    Grow, E. J., Flynn, R. A., Chavez, S. L., Bayless, N. L., Wossidlo, M., Wesche, D. J., and Pera, R. A. R. (2015) Intrinsic retroviral reactivation in human preimplantation embryos and pluripotent cells, Nature, 522, 221–225.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Boyle, A. L., Ballard, S. G., and Ward, D. C. (1990) Differential distribution of long and short interspersed element sequences in the mouse genome: chromosome karyotyping by fluorescence in situ hybridization, Proc. Natl. Acad. Sci. USA, 87, 7757–7761.PubMedPubMedCentralCrossRefGoogle Scholar
  42. 42.
    Waterston, R. H., Lander, E. S., and Sulston, J. E. (2002) On the sequencing of the human genome, Proc. Natl. Acad. Sci. USA, 99, 3712–3716.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Solovei, I., Kreysing, M., Lanctot, C., Kosem, S., Peichl, L., Cremer, T., and Joffe, B. (2009) Nuclear architecture of rod photoreceptor cells adapts to vision in mammalian evolution, Cell, 137, 356–368.PubMedCrossRefGoogle Scholar
  44. 44.
    Podgornaya, O., Gavrilova, E., Stephanova, V., Demin, S., and Komissarov, A. (2013) Large tandem repeats make up the chromosome bar code: a hypothesis, Adv. Protein Chem. Struct. Biol., 90, 1–30.PubMedCrossRefGoogle Scholar
  45. 45.
    Miga, K. H. (2015) Completing the human genome: the progress and challenge of satellite DNA assembly, Chromosome Res., 23, 421–426.PubMedCrossRefGoogle Scholar
  46. 46.
    Kuznetsova, I. S., Ostromyshenskii, D. I., Komissarov, A. S., Prusov, A. N., Waisertreiger, I. S., Gorbunova, A. V., Trifonov, V. A., Ferguson-Smith, M., and Podgornaya, O. I. (2016) LINE-related component of mouse heterochromatin and complex chromocenters’ composition, Chromosome Res., 24, 309–323.PubMedCrossRefGoogle Scholar
  47. 47.
    Ostromyshenskii, D. I., Komissarov, A. S., Kuznetsova, I. S., Chernyaeva, E. N., Vaysertreyger, I. R., and Podgornaya, O. I. (2016) The structure of DNA chromocentres in mouse in silico and in situ. LINE and ERV fragments are an obligatory components of DNA chromocentres besides tandem repeats, Tsitologiya, 58, 389–392.Google Scholar
  48. 48.
    Van de Werken, H. J. G., De Haan, J. C., Feodorova, Y., Bijos, D., Weuts, A., Theunis, K., and Kumar, P. (2017) Small chromosomal regions position themselves autonomously according to their chromatin class, Genome Res., 27, 922–933.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Choo, K. H. (1997) Centromeres, John Wiley & Sons, Ltd.Google Scholar
  50. 50.
    Fadloun, A., Le Gras, S., Jost, B., Ziegler-Birling, C., Takahashi, H., Gorab, E., and Torres-Padilla, M. E. (2013) Chromatin signatures and retrotransposon profiling in mouse embryos reveal regulation of LINE-1 by RNA, Nat. Struct. Mol. Biol., 20, 332–338.PubMedCrossRefGoogle Scholar
  51. 51.
    Hall, L. L., Carone, D. M., Gomez, A. V., Kolpa, H. J., Byron, M., Mehta, N., and Lawrence, J. B. (2014) Stable C0 T-1 repeat RNA is abundant and is associated with euchromatic interphase chromosomes, Cell, 156, 907–919.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Kit, S. (1961) Equilibrium sedimentation in density gradients of DNA preparations from animal tissues, J. Mol. Biol., 3, 711–716.PubMedCrossRefGoogle Scholar
  53. 53.
    Vogt, P. (1990) Potential genetic functions of tandem repeated DNA sequence blocks in the human genome are based on a highly conserved “chromatin folding code”, Hum. Genet., 84, 301–336.PubMedGoogle Scholar
  54. 54.
    Pavlek, M., Gelfand, Y., Plohl, M., and Mestrovic, N. (2015) Genome-wide analysis of tandem repeats in Tribolium castaneum genome reveals abundant and highly dynamic tandem repeat families with satellite DNA features in euchromatic chromosomal arms, DNA Res., 22, 387–401.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Wevrick, R., and Willard, H. F. (1991) Physical map of the centromeric region of human chromosome 7: relationship between two distinct alpha satellite arrays, Nucleic Acids Res., 19, 2295–2301.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Ikeno, M., Masumoto, H., and Okazaki, T. (1994) Distribution of CENP-B boxes reflected in CREST centromere antigenic sites on long-range α-satellite DNA arrays of human chromosome 21, Hum. Mol. Genetics, 3, 1245–1257.CrossRefGoogle Scholar
  57. 57.
    He, D., Zeng, C., Woods, K., Zhong, L., Turner, D., Busch, R. K., and Busch, H. (1998) CENP-G: a new centromeric protein that is associated with the α-1 satellite DNA subfamily, Chromosoma, 107, 189–197.PubMedCrossRefGoogle Scholar
  58. 58.
    Miheev, D. Yu., Podgornaya, O. I., and Ostromyshenskii, D. I. (2015) Large tandem repeats of Mesocricetus auratus in silico and in situ, Tsitologiya, 57, 95–101.Google Scholar
  59. 59.
    Ostromyshenskii, D. I., Kuznetsova, I. S., Komissarov, A. S., Kartavtseva, I. V., and Podgornaya, O. I. (2015) Tandem repeats in rodents genome and their mapping, Tsitologiya, 57, 102–110.Google Scholar
  60. 60.
    Ames, D., Murphy, N., Helentjaris, T., Sun, N., and Chandler, V. (2008) Comparative analyses of human single-and multilocus tandem repeats, Genetics, 179, 1693–1704.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Warburton, P. E., Hasson, D., Guillem, F., Lescale, C., Jin, X., and Abrusan, G. (2008) Analysis of the largest tandemly repeated DNA families in the human genome, BMC Genomics, 9, 533.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Alkan, C., Cardone, M. F., Catacchio, C. R., Antonacci, F., O’Brien, S. J., Ryder, O., and Ventura, M. (2011) Genome-wide characterization of centromeric satellites from multiple mammalian genomes, Genome Res., 21, 137–145.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Capy, P. (2005) Classification and nomenclature of retrotransposable elements, Cytogenet. Genome Res., 110, 457–461.PubMedCrossRefGoogle Scholar
  64. 64.
    Kronmiller, B. A., and Wise, R. P. (2008) Tenest: automated chronological annotation and visualization of nested plant transposable elements, Plant Physiol., 146, 45–59.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Feschotte, C., Keswani, U., Ranganathan, N., Guibotsy, M. L., and Levine, D. (2009) Exploring repetitive DNA landscapes using REPCLASS, a tool that automates the classification of transposable elements in eukaryotic genomes, Genome Biol. Evol., 1, 205–220.PubMedGoogle Scholar
  66. 66.
    Seberg, O., and Petersen, G. (2009) A unified classification system for eukaryotic transposable elements should reflect their phylogeny, Nat. Rev. Genet., 10, 276–276.PubMedCrossRefGoogle Scholar
  67. 67.
    Vassetzky, N. S., and Kramerov, D. A. (2012) SINEBase: a database and tool for SINE analysis, Nucleic Acids Res., 41, 83–89.CrossRefGoogle Scholar
  68. 68.
    Gelfand, Y., Rodriguez, A., and Benson, G. (2006) TRDB–the tandem repeats database, Nucleic Acids Res., 35, 80–87.CrossRefGoogle Scholar
  69. 69.
    Jurka, J., Kapitonov, V. V., Pavlicek, A., Klonowski, P., Kohany, O., and Walichiewicz, J. (2005) Repbase Update, a database of eukaryotic repetitive elements, Cytogenet. Genome Res., 110, 462–467.PubMedCrossRefGoogle Scholar
  70. 70.
    Melters, D. P., Bradnam, K. R., Young, H. A., Telis, N., May, M. R., Ruby, J. G., and Garcia, J. F. (2013) Comparative analysis of tandem repeats from hundreds of species reveals unique insights into centromere evolution, Genome Biol., 14, R10.Google Scholar
  71. 71.
    Kuznetsova, I., Podgornaya, O., and Ferguson-Smith, M. A. (2006) High-resolution organization of mouse centromeric and pericentromeric DNA, Cytogenet. Genome Res., 112, 248–255.PubMedCrossRefGoogle Scholar
  72. 72.
    Lobov, I. B., Tsutsui, K., Mitchell, A. R., and Podgornaya, O. (2000) Specific interaction of mouse major satellite with MAR-binding protein SAF-A, Europ. J. Cell Biol., 79, 839–849.PubMedCrossRefGoogle Scholar
  73. 73.
    Lobov, I. B., Tsutsui, K., Mitchell, A. R., and Podgornaya, O. I. (2001) Specificity of SAF−A and lamin B binding in vitro correlates with the satellite DNA bending state, J. Cell. Biochem., 83, 218–229.PubMedCrossRefGoogle Scholar
  74. 74.
    Enukashvily, N., Donev, R., Sheer, D., and Podgornaya, O. (2005) Satellite DNA binding and cellular localisation of RNA helicase P68, J. Cell Sci., 118, 611–622.PubMedCrossRefGoogle Scholar
  75. 75.
    Podgornaya, O. I., Voronin, A. P., Enukashvily, N., Matveev, I. V., and Lobov, I. B. (2003) Structure-specific DNA-binding proteins as the foundation for three-dimensional chromatin organization, Int. Rev. Cytol., 224, 227–296.PubMedCrossRefGoogle Scholar
  76. 76.
    Fondon, J. W., and Garner, H. R. (2004) Molecular origins of rapid and continuous morphological evolution, Proc. Natl. Acad. Sci. USA, 101, 18058–18063.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Politz, J. C. R., Scalzo, D., and Groudine, M. (2013) Something silent this way forms: the functional organization of the repressive nuclear compartment, Ann. Rev. Cell Develop. Biol., 29, 241–270.CrossRefGoogle Scholar
  78. 78.
    Cremer, M., Solovei, I., Schermelleh, L., and Cremer, T. (2003) Chromosomal arrangement during different phases of the cell cycle, in Nature Encyclopedia of the Human Genome, Macmillan Publishers Ltd., Nature Publishing Group, pp. 451–457.Google Scholar
  79. 79.
    Kuznetsova, I. S., Enukashvily, N. I., Noniashvili, E. M., Shatrova, A. N., Aksenov, N. D., Zenin, V. V., Dyban, A. P., and Podgornaya, O. I. (2007) Evidence for the existence of satellite DNA-containing connection between metaphase chromosomes, J. Cell. Biochem., 101, 1046–1061.PubMedCrossRefGoogle Scholar
  80. 80.
    Wang, L. H.-C., Schwarzbraun, T., Speicher, M. R., and Nigg, E. A. (2008) Persistence of DNA threads in human anaphase cells suggests late completion of sister chromatid decatenation, Chromosoma, 117, 123–135.PubMedCrossRefGoogle Scholar
  81. 81.
    Dreissig, S., Schiml, S., Schindele, P., Weiss, O., Rutten, T., Schubert, V., and Houben, A. (2017) Live cell CRISPR-imaging in plants reveals dynamic telomere movements, Plant J., 91, 565–573.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Cohen, A. K., Huh, T. Y., and Helleiner, C. W. (1973) Transcription of satellite DNA in mouse L-cells, Can. J. Biochem., 51, 529–532.PubMedCrossRefGoogle Scholar
  83. 83.
    Cohen, A. K., Rode, H. N., and Helleiner, C. W. (1972) The time of synthesis of satellite DNA in mouse cells (L cells), Can. J. Biochem., 50, 229–231.PubMedCrossRefGoogle Scholar
  84. 84.
    Seidman, M. M., and Cole, R. D. (1977) Chromatin fractionation related to cell type and chromosome condensation but perhaps not to transcriptional activity, J. Biol. Chem., 252, 2630–2639.PubMedGoogle Scholar
  85. 85.
    Haaf, T., and Ward, D. C. (1996) Inhibition of RNA polymerase II transcription causes chromatin decondensation, loss of nucleolar structure, and dispersion of chromosomal domains, Exp. Cell Res., 224, 163–173.PubMedGoogle Scholar
  86. 86.
    Macgregor, H. C. (1979) In situ hybridization of highly repetitive DNA to chromosomes of Triturus cristatus, Chromosoma, 71, 57–64.PubMedCrossRefGoogle Scholar
  87. 87.
    Varley, J. M., Macgregor, H. C., Nardi, I., Andrews, C., and Erba, H. P. (1980) Cytological evidence of transcription of highly repeated DNA sequences during the lamp-brush stage in Triturus cristatus carnifex, Chromosoma, 80, 289–307.PubMedCrossRefGoogle Scholar
  88. 88.
    Krasikova, A. V., Vasilevskaia, E. V., and Gaginskaia, E. R. (2010) Chicken lampbrush chromosomes: transcription of tandemly repetitive DNA sequences, Genetika, 46, 1329–1334.PubMedGoogle Scholar
  89. 89.
    Rouleux-Bonnin, F., Bigot, S., and Bigot, Y. (2004) Structural and transcriptional features of Bombus terrestris satellite DNA and their potential involvement in the differentiation process, Genome, 47, 877–888.PubMedCrossRefGoogle Scholar
  90. 90.
    Rizzi, N., Denegri, M., Chiodi, I., Corioni, M., Valgardsdottir, R., Cobianchi, F., and Biamonti, G. (2004) Transcriptional activation of a constitutive heterochromatic domain of the human genome in response to heat shock, Mol. Biol. Cell, 15, 543–551.PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Lehnertz, B., Ueda, Y., Derijck, A. A., Braunschweig, U., Perez-Burgos, L., Kubicek, S., and Peters, A. H. (2003) Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin, Curr. Biol., 13, 1192–1200.PubMedCrossRefGoogle Scholar
  92. 92.
    Rudert, F., Bronner, S., Garnier, J. M., and Dolle, P. (1995) Transcripts from opposite strands of gamma satellite DNA are differentially expressed during mouse development, Mamm. Genome, 6, 76–83.PubMedCrossRefGoogle Scholar
  93. 93.
    Lorite, P., Renault, S., Rouleux-Bonnin, F., Bigot, S., Periquet, G., and Palomeque, T. (2002) Genomic organization and transcription of satellite DNA in the ant Aphaenogaster subterranea (Hymenoptera, Formicidae), Genome, 45, 609–616.PubMedCrossRefGoogle Scholar
  94. 94.
    Lee, H. R., Neumann, P., Macas, J., and Jiang, J. (2006) Chromosomal localization, copy number assessment, and transcriptional status of BamHI repeat fractions in water buffalo Bubalus bubalis, Mol. Biol. Evol., 23, 2505–2520.Google Scholar
  95. 95.
    Ting, D. T., Lipson, D., Paul, S., Brannigan, B. W., Akhavanfard, S., Coffman, E. J., and Rivera, M. N. (2011) Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers, Science, 331, 593–596.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Kuznetsova, I. S., Thevasagayam, N. M., Sridatta, P. S., Komissarov, A. S., Saju, J. M., Ngoh, S. Y., Jiang, J., Shen, X., and Orban, L. (2014) Primary analysis of repeat elements of the Asian seabass (Lates calcarifer) transcriptome and genome, Front. Genet., doi: 10.3389/ fgene.2014.00223.Google Scholar
  97. 97.
    Saksouk, N., Simboeck, E., and Dejardin, J. (2015) Constitutive heterochromatin formation and transcription in mammals, Epigenet. Chromatin, doi: 10.1186/1756-8935-8-3.Google Scholar
  98. 98.
    Enukashvily, N. I., and Ponomartsev, N. V. (2013) Mammalian satellite DNA: a speaking dumb, Adv. Protein Chem. Struct. Biol., 90, 31–65.PubMedCrossRefGoogle Scholar
  99. 99.
    Valgardsdottir, R., Chiodi, I., Giordano, M., Rossi, A., Bazzini, S., Ghigna, C., Riva, S., and Biamonti, G. (2008) Transcription of satellite III non-coding RNAs is a general stress response in human cells, Nucleic Acids Res., 36, 423–434.PubMedCrossRefGoogle Scholar
  100. 100.
    Lu, J., and Gilbert, D. M. (2007) Proliferation-dependent and cell cycle-regulated transcription of mouse pericentric heterochromatin, J. Cell Biol., 179, 411–421.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Bersani, F., Leeb, E., Kharchenko, P. V., Xu, A. W., Liu, M., Xega, K., MacKenzie, O. C., Brannigan, B. W., Wittner, B. S., Jung, H., Ramaswamy, S., Park, P. J., Maheswaran, S., Ting, D. T., and Haber, D. A. (2015) Pericentromeric satellite repeat expansions through RNA-derived DNA intermediates in cancer, Proc. Natl. Acad. Sci. USA, 112, 15148–15153.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Kuznetsova, T. V., Enukashvily, N. I., Trofimova, I. L., Gorbunova, A., Vashukova, E. S., and Baranov, V. S. (2012) Localization and transcription of human chromosome 1 pericentromeric heterochromatin in embryonic and extraembryonic tis sues, Med. Genet. (Moscow), 11, 19–24.Google Scholar
  103. 103.
    Trofimova, I. L., Enukashvily, N. I., Kuznetsova, T. V., and Baranov, V. S. (2018) Transcription of satellite DNA in human embryogenesis: literature review and our own data, Med. Genet. (Moscow), 17, 3–7.Google Scholar
  104. 104.
    Suzuki, T., Fujii, M., and Ayusawa, D. (2002) Demethylation of classical satellite 2 and 3 DNA with chromosomal instability in senescent human fibroblasts, Exp. Gerontol., 37, 1005–1014.PubMedCrossRefGoogle Scholar
  105. 105.
    Tessadori, F., Schulkes, R. K., Van Driel, R., and Fransz, P. (2007) Light-regulated large-scale reorganization of chromatin during the floral transition in Arabidopsis, Plant J., 50, 848–857.PubMedCrossRefGoogle Scholar
  106. 106.
    Zhang, P., Kerkela, E., Skottman, H., Levkov, L., Kivinen, K., Lahesmaa, R., and Kere, J. (2007) Distinct sets of developmentally regulated genes that are expressed by human oocytes and human embryonic stem cells, Fertil. Steril., 87, 677–690.PubMedCrossRefGoogle Scholar
  107. 107.
    Gerrard, D. T., Berry, A. A., Jennings, R. E., Hanley, K. P., Bobola, N., and Hanley, N. A. (2016) An integrative transcriptomic atlas of organogenesis in human embryos, Elife, pii: e15657.Google Scholar
  108. 108.
    Santenard, A., Ziegler-Birling, C., Koch, M., Tora, L., Bannister, A. J., and Torres-Padilla, M. E. (2010) Heterochromatin formation in the mouse embryo requires critical residues of the histone variant H3.3, Nat. Cell Biol., 12, 853–862.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Enukashvily, N. I., Malashicheva, A. B., and Waisertreiger, I. S. (2009) Satellite DNA spatial localization and transcriptional activity in mouse embryonic E-14 and IOUD2 stem cells, Cytogenet. Genome Res., 124, 277–287.PubMedCrossRefGoogle Scholar
  110. 110.
    Kuhn, G. C. S. (2015) Satellite DNA transcripts have diverse biological roles in Drosophila, Heredity, 115, 1–2.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Bouzinba-Segard, H., Guais, A., and Francastel, C. (2006) Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function, Proc. Natl. Acad. Sci. USA, 103, 8709–8714.PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Gaubatz, J. W., and Cutler, R. G. (1990) Mouse satellite DNA is transcribed in senescent cardiac muscle, J. Biol. Chem., 265, 17753–17758.PubMedGoogle Scholar
  113. 113.
    Pastor, B. M., and Mostoslavsky, R. (2016) SIRT6: a new guardian of mitosis, Nat. Struct. Mol. Biol., 23, 360–362.PubMedCrossRefGoogle Scholar
  114. 114.
    Chan, D. L., Moralli, D., Khoja, S., and Monaco, Z. L. (2017) Noncoding centromeric RNA expression impairs chromosome stability in human and murine stem cells, Dis. Markers, 7506976.Google Scholar
  115. 115.
    Enukashvily, N. I., Donev, R., Waisertreiger, I. S.-R., and Podgornaya, O. I. (2007) Human chromosome 1 satellite 3 DNA is decondensed, demethylated and transcribed in senescent cells and in A431 epithelial carcinoma cells, Cytogenet. Genome Res., 118, 42–54.PubMedGoogle Scholar
  116. 116.
    De Cecco, M., Criscione, S. W., Peckham, E. J., Hillenmeyer, S., Hamm, E. A., Manivannan, J., Peterson, A. L., Kreiling, J. A., Neretti, N., and Sedivy, J. M. (2013) Genomes of replicatively senescent cells undergo global epigenetic changes leading to gene silencing and activation of transposable elements, Aging Cell, 12, 247–256.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Wong, L. H., Brettingham-Moore, K. H., Chan, L., Quach, J. M., Anderson, M. A., Northrop, E. L., Hannan, R., Saffery, R., Shaw, M. L., Williams, E., and Choo, K. A. (2007) Centromere RNA is a key component for the assembly of nucleoproteins at the nucleolus and centromere, Genome Res., 17, 1146–1160.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Du, Y., Topp, C. N., and Dawe, R. K. (2010) DNA binding of centromere protein C (CENPC) is stabilized by single-stranded RNA, PLoS Genet., 6, e1000835.PubMedPubMedCentralCrossRefGoogle Scholar
  119. 119.
    Eymery, A., Souchier, C., Vourc’h, C., and Jolly, C. (2010) Heat shock factor 1 binds to and transcribes satellite II and III sequences at several pericentromeric regions in heat-shocked cells, Exp. Cell Res., 316, 1845–1855.PubMedCrossRefGoogle Scholar
  120. 120.
    Jolly, C., Metz, A., Govin, J., Vigneron, M., Turner, B. M., Khochbin, S., and Vourc’h, C. (2004) Stress-induced transcription of satellite III repeats, J. Cell. Biol., 164, 25–33.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Col, E., Hoghoughi, N., Dufour, S., Penin, J., Koskas, S., Faure, V., Ouzounova, M., Hernandez-Vargash, H., Reynoird, N., Daujat, S., Folco, E., Vigneron, M., Schneider, R., Verdel, A., Khochbin, S., Herceg, Z., Caron, C., and Vourc’h, C. (2017) Bromodomain factors of BET family are new essential actors of pericentric heterochromatin transcriptional activation in response to heat shock, Nature Sci. Rep., 7, 5418.CrossRefGoogle Scholar
  122. 122.
    Sengupta, S., Parihar, R., and Ganesh, S. (2009) Satellite III non-coding RNAs show distinct and stress-specific patterns of induction, Biochem. Biophys. Res. Commun., 382, 102–107.PubMedCrossRefGoogle Scholar
  123. 123.
    Morozov, V. M., Gavrilova, E. V., Ogryzko, V. V., and Ishov, A. M. (2012) Dualistic function of Dax at centromeric and pericentromeric heterochromatin in normal and stress conditions, Nucleus, 3, 276–285.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Pezer, Z., and Ugarkovic, D. (2012) Satellite DNA-associated siRNAs as mediators of heat shock response in insects, RNA Biol., 9, 587–595.PubMedCrossRefGoogle Scholar
  125. 125.
    Wang, Y., Zhang, Z., Chi, Y., Zhang, Q., Xu, F., Yang, Z., Meng, L., Yang, S., Yan, S., Mao, A., Zhang, J., Yang, Y., Wang, S., Cui, J., Liang, L., Ji, Y., Han, Z.-B., Fang, X., and Han, Z. C. (2013) Long-term cultured mesenchymal stem cells frequently develop genomic mutations but do not undergo malignant transformation, Cell Death Dis., 4, 950.CrossRefGoogle Scholar
  126. 126.
    Ponomartsev, N., Bulavin, D., Enukashvily, N., and Brichkina, A. (2016) Transcription of pericentromeric major satellite DNA in lung cancer, Cytogenet. Genome Res., 148, 146.Google Scholar
  127. 127.
    Ruiz-Herrera, A., Castresana, J., and Robinson, T. J. (2006) Is mammalian chromosomal evolution driven by regions of genome fragility? Genome Biol., 7, 115.CrossRefGoogle Scholar
  128. 128.
    Podgornaya, O. I. (2016) Extracellular DNA for the unsolved evolutionary problems, Tsitologiya, 58, 385–388.Google Scholar
  129. 129.
    Anker, P., Stroun, M., and Maurice, P. A. (1975) Spontaneous release of DNA by human blood lymphocytes as shown in vitro system, Cancer Res., 35, 2375–2382.PubMedGoogle Scholar
  130. 130.
    Vasyukhin, V. I., Lipskaya, L. A., Tsvetkov, A. G., and Podgornaya, O. I. (1991) DNA excreted by human lymphocytes contains sequences homologous to Ck gene, Mol. Biol. (Moscow), 25, 405–412.Google Scholar
  131. 131.
    Vasioukhin, V., Anker, P., Maurice, P., Lyautey, J., Lederrey, C., and Stroun, M. (1994) Point mutations of the N-ras gene in the blood plasma DNA of patients with myelodysplastic syndrome or acute myelogenous leukaemia, Brit. J. Haematol., 86, 774–779.CrossRefGoogle Scholar
  132. 132.
    Thierry, A. R., Mouliere, F., El Messaoudi, S., Mollevi, C., Lopez-Crapez, E., Rolet, F., Gillet, B., Gongora, C., Dechelotte, P., Robert, B., Del Rio, M., Lamy, P.-J., Bibeau, F., Nouaille, M., Loriot, V., Jarrousse, A.-S., Molina, F., Mathonnet, M., Pezet, D., and Ychou, M. (2014) Clinical validation of the detection of KRAS and BRAF mutations from circulating tumor DNA, Nat. Med., 20, 430–435.PubMedCrossRefGoogle Scholar
  133. 133.
    Murtaza, M., Dawson, S. J., Tsui, D. W., Gale, D., Forshew, T., Piskorz, A. M., Parkinson, C., Chin, S.-F., Kingsbury, Z., Wong, A. S. C., Marass, F., Humphray, S., Hadfield, J., Bentley, D., Chin, T. M., Brenton, J. D., Caldas, C., and Rosenfeld, N. (2013) Non-invasive analysis of acquired resistance to cancer therapy by sequencing of plasma DNA, Nature, 497, 108–112.PubMedCrossRefGoogle Scholar
  134. 134.
    Rykova, E. Y., Morozkin, E. S., Ponomaryova, A. A., Loseva, E. M., Zaporozhchenko, I. A., Cherdyntseva, N. V., Vlasov, V. V., and Laktionov, P. P. (2012) Cell-free and cell-bound circulating nucleic acid complexes: mechanisms of generation, concentration and content, Expert. Opin. Biol. Ther., 12, 141–153.CrossRefGoogle Scholar
  135. 135.
    Mittra, I., Khare, N. K., Raghuram, G. V., Chaubal, R., Khambatti, F., Gupta, D., Gaikwad, A., Prasannan, P., Singh, A., Iyer, A., Singh, A., Upadhyay, P., Nair, N. K., Mishra, P. K., and Dutt, A. (2015) Circulating nucleic acids damage DNA of healthy cells by integrating into their genomes, J. Biosci., 40, 91–111.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 136.
    Morozkin, E. S., Loseva, E. M., Morozov, I. V., Kurilshikov, A. M., Bondar, A. A., Rykova, E. Y., Rubtsov, N. B., Vlasov, V. V., and Laktionov, P. P. (2012) A comparative study of cell-free apoptotic and genomic DNA using FISH and massive parallel sequencing, Expert Opin. Biol. Ther., 12, 141–153.CrossRefGoogle Scholar
  137. 137.
    Beck, J., Urnovitz, H. B., Riggert, J., Clerici, M., and Schutz, E. (2009) Profile of the circulating DNA in apparently healthy individuals, Clin. Chem., 55, 730–738.PubMedCrossRefGoogle Scholar
  138. 138.
    Vasil’eva, I. N., Podgornaya, O. I., and Bespalov, V. G. (2015) Nucleosome fraction of extracellular DNA as the index of apoptosis, Tsitologiya, 57, 87–94.Google Scholar
  139. 139.
    Cheng, J., Torkamani, A., Peng, Y., Jones, T. M., and Lerner, R. A. (2012) Plasma membrane associated transcription of cytoplasmic DNA, Proc. Natl. Acad. Sci. USA, 109, 10827–10831.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Youngera, S. T., and Rinna, J. L. (2015) Silent pericentromeric repeats speak out, Proc. Natl. Acad. Sci. USA, 112, 15008–15009.CrossRefGoogle Scholar
  141. 141.
    Podgornaya, O. I., Vasilyeva, I. N., and Bespalov, V. G. (2016) Heterochromatic tandem repeats in the extracellular DNA, in Circulating Nucleic Acids in Serum and Plasma–CNAPS IX, pp. 85–89.CrossRefGoogle Scholar
  142. 142.
    Earnshaw, W. C., Halligan, N., Cooke, C., and Rothfield, N. (1984) The kinetochore is part of the metaphase chromosome scaffold, J. Cell. Biol., 98, 352–357.PubMedCrossRefGoogle Scholar
  143. 143.
    Zasadzinska, E., and Foltz, D. R. (2017) Orchestrating the specific assembly of centromeric nucleosomes, in Centromeres and Kinetochores, Springer, Cham, pp. 165–192.CrossRefGoogle Scholar
  144. 144.
    Van Helden, P. D. (1985) Potential Z-DNA-forming elements in serum DNA from human systemic lupus erythematosus, J. Immunol., 134, 177–179.PubMedGoogle Scholar
  145. 145.
    Herrman, M., Leitmann, W., Krapf, E. F., and Kalden, J. R. (1989) Molecular characterization and in vitro effects of nucleic acids from plasma of patients with systemic lupus erythematosus, in Molecular and Cellular Mechanisms of Human Hypersensitivity and Autoimmunity, Wiley, New York, pp. 147–157.Google Scholar
  146. 146.
    Winter, O., Musiol, S., Schabowsky, M., Cheng, Q., Khodadadi, L., and Hiepe, F. (2015) Analyzing pathogenic (double-stranded (ds) DNA-specific) plasma cells via immunofluorescence microscopy, Arthritis Res. Ther., 17, 293.PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Ostromyshenskii, D. I., Kuznetsova, I. S., Golenishchev, F. N., Malikov, V. G., and Podgornaya, O. I. (2011) Satellite DNA as a phylogenetic marker: case study of three genera of the murine subfamily, Cell Tiss. Biol., 5, 543–550.CrossRefGoogle Scholar
  148. 148.
    Carey, N. (2015) Junk DNA: A Journey through the Dark Matter of the Genome, Icon Books.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2018

Authors and Affiliations

  • O. I. Podgornaya
    • 1
    • 2
    • 3
  • D. I. Ostromyshenskii
    • 1
    • 3
  • N. I. Enukashvily
    • 1
  1. 1.Institute of CytologyRussian Academy of SciencesSt. PetersburgRussia
  2. 2.St. Petersburg State UniversitySt. PetersburgRussia
  3. 3.Far Eastern Federal UniversityVladivostokRussia

Personalised recommendations