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Distribution of heterochromatin markers in lampbrush chromosomes in birds

Abstract

Changes in functional gene activity not affecting primary DNA structure can be inherited by a cell and in total represent epigenetic mechanisms of the genome expression regulation. Epigenetic genome modifications include DNA methylation, histone modifications, and binding of the proteins and noncoding RNA. The distribution of heterochromatin markers (such as methylated cytosine, HP1 heterochromatin protein, and modifications of H3, H4, and H2A histones) was analyzed by example of lampbrush chromosomes typical for growing bird oocytes. On the lampbrush chromosomes of domesticated chicken (Gallus gallus domesticus), Japanese quail (Coturnix japonica), and chaffinch (Fringilla coelebs), methylated cytosine was mainly detected in chromomeres, as well as in unextended regions of lateral loop axes. The largest accumulation of methylated cytosine was demonstrated by chromosome W and dense chromomeres of macro- and microchromosomes. The HP1β protein distribution in the lampbrush chromosomes corresponded in general to the distribution of methylated cytosine. Chromomeres of chromosome W as well as centromeric and terminal chromomeres of macro- and microchromosomes accumulated the highest amount of the HP1β protein as compared with the remaining chromomeres. The character of distribution of the H3K9 me3 and H3K27 me3 histone modifications, as well as phosphorylated H4 and H2A histones, was different. Phosphorylated H4 and H2A histones were distributed proportionally to the staining by DNA specific dyes and were accumulated in all chromosomes, while trimethylated H3K9 histone was enriched in the regions of constitutive heterochromatin. We assume that the HP1β heterochromatin protein is involved in compaction and transcriptional inactivation of the chromatin in chromomeres of the lampbrush chromosomes.

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References

  1. 1.

    Peterson, C.L. and Laniel, M.A., Histones and histone modifications, Curr. Biol., 2004, vol. 14, no. 14, pp. 546–551. doi 10.1016/j.cub.2004.07.007

    Article  Google Scholar 

  2. 2.

    Gaginskaya, E.R., Lampbrush chromosomes from amphibian oocytes, Tsitologiya, 1989, vol. 31, no. 11, pp. 1267–1291.

    Google Scholar 

  3. 3.

    Callan, H.G., Lampbrush Chromosomes, Berlin: Springer-Verlag, 1986.

    Book  Google Scholar 

  4. 4.

    Morgan, G.T., Lampbrush chromosomes and associated bodies: new insights into principles of nuclear structure and function, Chromosome Res., 2002, vol. 10, pp. 177–200.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Gaginskaya, E., Kulikova, T., and Krasikova, A., Avian lampbrush chromosomes: a powerful tool for exploration of genome expression, Cytogenet. Genome Res., 2009, vol. 124, pp. 251–267. doi 10.1159/000218130

    CAS  Article  PubMed  Google Scholar 

  6. 6.

    Kropotova, E.V. and Gaginskaya, E.R., Lampbrush chromosomes from Japanese quail oocytes: light and electron microscopy data, Tsitologiya, 1984, vol. 26, pp. 1006–1015.

    Google Scholar 

  7. 7.

    Solovei, I., Gaginskaya, E., Hutchison, N., and Macgregor, H., Avian sex chromosomes in the lampbrush form: the ZW lampbrush bivalents from six species of bird, Chromosome Res., 1993, vol. 1, pp. 153–166.

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Solovei, I.V., Gaginskaya, E.R., and Macgregor, H.C., The arrangement and transcription of telomere DNA sequences at the ends of lampbrush chromosomes of birds, Chromosome Res., 1994, vol. 2, pp. 460–470.

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Sumner, A.T., Chromosomes Organization and Function, Blackwell, 2003.

    Google Scholar 

  10. 10.

    Angelier, N., Bonnanfant-Jais, M.L., Moreau, N., et al., DNA methylation and RNA transcriptional activity in amphibian lampbrush chromsomes, Chromosoma, 1986, vol. 94, pp. 169–182. doi 10.1007/BF00288491

    CAS  Article  Google Scholar 

  11. 11.

    Morgan, G.T., Jones, P., and Bellini, M., Association of modified cytosines and the methylated DNA-binding protein MeCP2 with distinctive structural domains of lampbrush chromatin, Chromosome Res., 2012, vol. 20, pp. 925–942. doi 10.1007/s10577-012-9324-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  12. 12.

    Jones, P.L., Veenstra, G.J., Wade, P.A., et al., Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription, Nat. Genet., 1998, vol. 19, no. 2, pp. 187–191. doi 10.1038/561

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Choo, K.H., Centromerization, Trends Cell Biol., 2000, vol. 10, pp. 182–188.

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Choo, K.H., Domain organization at the centromere and neocentromere, Dev. Cell, 2001, vol. 1, no. 2, pp. 165–177.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Solovei, I.V., Joffe, B.I., Gaginskaya, E.R., and Macgregor, H.C., Transcription on lampbrush chromosomes of a centromerically localized highly repeated DNA in pigeon (Columba) relates to sequence arrangement, Chromosome Res., 1996, vol. 4, pp. 588–603.

    CAS  Article  PubMed  Google Scholar 

  16. 16.

    Saifitdinova, A., Derjusheva, S., Krasikova, A., and Gaginskaya, E., Lampbrush chromosomes of the chaffinch (Fringilla coelebs L.), Chromosome Res., 2003, vol. 11, pp. 99–113.

    CAS  Article  PubMed  Google Scholar 

  17. 17.

    Krasikova, A., Deryusheva, S., Galkina, S., et al., On the positions of centromeres in chicken lampbrush chromosomes, Chromosome Res., 2006, vol. 14, no. 7, pp. 777–789. doi 10.1007/s10577-006-1085-y

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Krasikova, A., Daks, A., Zlotina, A., and Gaginskaya, E., Polymorphic heterochromatic segments in Japanese quail microchromosomes, Cytogenet. Genome Res., 2009, vol. 126, pp. 148–155. doi 10.1159/000245914

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Stewart, M.D., Sommerville, J., and Wong, J., Dynamic regulation of histone modifications in Xenopus oocytes through histone exchange, Mol. Cell Biol., 2006, vol. 26, no. 18, pp. 6890–6901. doi 10.1128/MCB.00948-06

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Zlotina, A., Kulikova, T., Kosyakova, N., et al., Microdissection of lampbrush chromosomes as an approach for generation of locus-specific FISH-probes and samples for high-throughput sequencing, BMC Genomics, 2016, vol. 17, p. 126. doi 10.1186/s12864-016-2437-4

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Barber, C.M., Turner, F.B., Wang, Y., et al., The enhancement of histone H4 and H2A serine 1 phosphorylation during mitosis and S-phase is evolutionarily conserved, Chromosoma, 2004, vol. 112, no. 7, pp. 360–371. doi 10.1007/s00412-004-0281-9

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Zhang, Y., Griffin, K., Mondal, N., and Parvin, J.D., Phosphorylation of histone H2A inhibits transcription on chromatin templates, J. Biol. Chem., 2004, vol. 279, pp. 21866–21872. doi 10.1074/jbc.M400099200

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Hock, R., Moorman, A., Fischer, D., and Scheer, U., Absence of somatic histone H1 in oocytes and preblastula embryos of Xenopus laevis, Dev. Biol., 1993, vol. 158, no. 2, pp. 510–522. doi 10.1006/dbio.1993.1209

    CAS  Article  PubMed  Google Scholar 

  24. 24.

    Maison, C. and Almouzni, G., HP1 and the dynamics of heterochromatin maintenance, Nat. Rev. Mol. Cell Biol., 2004, vol. 5, no. 4, pp. 296–304. doi 10.1038/nrm1355

    CAS  Article  PubMed  Google Scholar 

  25. 25.

    Kimmins, S. and Sassone-Corsi, P., Chromatin remodelling and epigenetic features of germ cells, Nature, 2005, vol. 434, no. 7033, pp. 583–589. doi 10.1038/nature03368

    CAS  Article  PubMed  Google Scholar 

  26. 26.

    Henikoff, S., Heterochromatin function in complex genomes, Biochim. Biophys. Acta, 2000, vol. 1470, pp. O1–O8.

    Google Scholar 

  27. 27.

    Redi, C.A., Garagna, S., Zacharias, H., et al., The other chromatin, Chromosoma, 2001, vol. 110, pp. 136–147.

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Hori, T., Suzuki, Y., Solovei, I., et al., Characterization of DNA sequences constituting the terminal heterochromatin of the chicken Z chromosome, Chromosome Res., 1996, vol. 4, no. 6, pp. 411–426.

    CAS  Article  PubMed  Google Scholar 

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Correspondence to A. V. Krasikova.

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Original Russian Text © A.V. Krasikova, T.V. Kulikova, 2017, published in Genetika, 2017, Vol. 53, No. 9, pp. 1077–1085.

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Krasikova, A.V., Kulikova, T.V. Distribution of heterochromatin markers in lampbrush chromosomes in birds. Russ J Genet 53, 1022–1029 (2017). https://doi.org/10.1134/S1022795417090071

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Keywords

  • heterochromatin
  • euchromatin
  • methylated cytosine
  • histone modifications
  • lampbrush chromosomes