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The changes in chromosome 6 spatial organization during chromatin polytenization in the Calliphora erythrocephala Mg. (Diptera: Calliphoridae) nurse cells

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Abstract

Localization of Calliphora erythrocephala chromosome 6 in a 3D nuclear space at different stages of nurse cell chromatin polytenization was analyzed by fluorescence in situ hybridization and 3D microscopy. The obtained results suggest a large-scale chromatin relocation in the C. erythrocephala nurse cell nuclei, which is accompanied by a change in the chromosome territory of chromosome 6 associated with the change in expression activity of the nucleus and formation of reticular chromatin structure. It was revealed that the relocation of chromosome 6 (nucleolus organizer chromosome) is accompanied by fragmentation of the single large nucleolus into micronucleoli, which are spread over the entire nuclear space being associated with their nucleolar organizer regions. Presumably, the chromosome 6 material during transition to a highly polytenized structure is redistributed in the nucleus so that the inactive pericentromeric regions are displaced to the nuclear periphery, while the chromosome regions carrying rDNA sequences loop out beyond the chromosome territory. Being dispersed over the entire nuclear space, rDNA sequences are likely to be amplified, thereby providing numerous small signals from the chromosome 6-specific DNA probe. Micronucleoli are formed around the actively transcribed nucleolar organizer regions.

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References

  • Aizenshtadt TB, Baranov VS, Borovkov AYU (1977) Modern problems in ontogenesis. Nauka, Leningrad

    Google Scholar 

  • Alexandrova O, Solovei I, Cremer T, David CN (2003) Replication labeling patterns and chromosome territories typical of mammalian nuclei are conserved in the early metazoan Hydra. Chromosoma 112:190–200

    Article  PubMed  CAS  Google Scholar 

  • Amano T, Sagai T, Tanabe H, Mizushina Y, Nakazawa H, Shiroishi T (2009) Chromosomal dynamics at the Shh locus: limb bud-specific differential regulation of competence and active transcription. Dev Cell 16:47–57

    Article  PubMed  CAS  Google Scholar 

  • Anan’ina TV, Kokhanenko AA, Khodzhanov AE, Stegniy VN (2007) Specific features in the structure of the egg tubes in the Calliphora erythrocephala (Mg.) (Diptera: Calliphoridae) ovaries. Vestn Tomsk Gos Univ 297:175–180

    Google Scholar 

  • Bantignies F, Grimaud CH, Cavalli G (2007) Two-colour fluorescent in situ DNA hybridization on whole mount Drosophila embryos and larval imaginal discs. IOP Publishing epigenesys. http://mescaline.igh.cnrs.fr/EpiGeneSys/www/images/protopdf/p5.pdf. Accessed 24 November 2011

  • Bolzer A, Kreth G, Solovei I, Köhler D, Saracoglu K, Fauth C, Müller S, Eils R, Cremer C, Speicher MR, Cremer T (2005) Three-dimensional maps of all chromosome positions demonstrate aprobabilistic order in human male fibroblast nuclei and prometaphase rosettes. PLoS Biol 3(5):e157

    Article  PubMed  Google Scholar 

  • Boyes JW, Shewell GE (1975) Cytotaxonomy of Calliphoridae (Diptera). Genetica 45:435–488

    Article  Google Scholar 

  • Cremer T, Cremer C (2001) Chromosome territories, nuclear architecture and gene regulation in mammalian cells. Genetics 2:292–301

    PubMed  CAS  Google Scholar 

  • Cremer T, Cremer C (2006) Rise, fall and resurrection of chromosome territories: a historical perspective. Part II. Fall and resurrection of chromosome territories during the 1950s to 1980s. Part III. Chromosome territories and the functional nuclear architecture: experiments and models from the 1990’s, to the present. Eur J Histochem 50:223–272

    PubMed  CAS  Google Scholar 

  • Cremer T, Cremer M (2010) Chromosome territories. Cold Spring Harbor Laboratory Press. doi:10.1101/cshperspect.a003889

  • Cremer T, Dietzel S, Eils R, Lichter P, Cremer C (1995) Chromosome territories, nuclear matrix filaments and interchromatin channels: a topological view on nuclear architecture and function. Kew Chromosome Conference IV (P.E. Brandham, and M.D. Benett) Royal Botanic Gardens. Kew 63–81

    Google Scholar 

  • Cremer M, Heintzmann R, Brero A (2000) Chromosome territories of small and large chromosomes are differently distributed in human lymphocyte nuclei. Medgen 12:95

    Google Scholar 

  • Cremer M, Grasser F, Lanctot C, Muller S, Neusser M et al (2008) Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods Mol Biol 463:205–239

    Article  PubMed  CAS  Google Scholar 

  • Croft JA, Bridger JM, Boyle S, Perry P, Teague P et al (1999) Differences in the localization and morphology of chromosomes in the human nucleus. J Cell Biol 145:1119–1131

    Article  PubMed  CAS  Google Scholar 

  • Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendur J, Fields S, Blau CA, Noble WS (2010) A three-dimensional model of the yeast genome. Nature 465:363–367

    Article  PubMed  CAS  Google Scholar 

  • Gondor A, Ohlsson R (2009) Chromosome crosstalk in three dimensions. Nature 461:212–217

    Article  PubMed  Google Scholar 

  • Habermann FA, Cremer M, Walter J, Kreth G, von Hase J, Bauer K, Wienberg J, Cremer C, Cremer T, Solovei I (2001) Arrangements of macro- and microchromosomes in chicken cells. Chromosome Res 9:569–584

    Article  PubMed  CAS  Google Scholar 

  • Karupu VY (1984) Electron microscopy. Vishcha Shkola, Kiev

    Google Scholar 

  • Koehler D, Zakhartchenko V, Froenicke L, Stone G, Stanyo R, Wolf E, Cremer T, Brero A (2009) Changes of higher order chromatin arrangements during major genom activation in bovine preimplantation embryos. Exp Cell Res 315:2053–2063

    Article  PubMed  CAS  Google Scholar 

  • Kokhanenko AA, Anan’ina TV, Stegniy VN (2010) Intranuclear dynamics of chromosome 6 in nurse cells of Calliphora erythrocephala Mg. (Diptera: Calliphoridae). Russ J Genet 46(9):1045–1047

    Article  CAS  Google Scholar 

  • Lichter P, Ledbetter SA, Ledbetter DH, Ward DC (1990) Fluorescence in situ hybridization with Alu and L1 polymerase chain reaction probes for rapid characterization of human chromosomes in hybrid cell lines. Proc Natl Acad Sci USA 87(17):6634–6638

    Article  PubMed  CAS  Google Scholar 

  • Matarazzo MR (2007) Chromosome territory reorganization in a human disease with altered DNA methylation. PNAS 42:16546–16551

    Article  Google Scholar 

  • Mateos-Langerak J, Bohn M, de Leeuw W, Giromus O, Manders EM, Verschure PJ et al (2009) Spatially confined folding of chromatin in the interphase nucleus. Proc Natl Acad Sci USA 106:3812–3817

    Article  PubMed  CAS  Google Scholar 

  • Mayr C, Jasencakova Z, Meister A, Schubert I, Zink D (2003) Comparative analysis of the functional genome architecture of animal and plant cell nuclei. Chromosome Res 11(5):471–484

    Article  PubMed  CAS  Google Scholar 

  • Németh A, Conesa A, Santoyo-Lopez J, Medina I, Montaner D, Péterfia B, Solovei I, Cremer T, Dopazo J, Längst G (2010) Initial genomics of the human nucleolus. PLoS Genet. doi:10.1371/journal.pgen.1000889

  • Neusser M, Schubel V, Koch A, Cremer T, Muller S (2007) Evolutionarily conserved, cell type and species-specific higher order chromatin arrangements in interphase nuclei of primates. Chromosoma 116:307–320

    Article  PubMed  Google Scholar 

  • Parada L, Misteli T (2002) Chromosome positioning in the interphase nucleus. Trends Cell Biol 12:425–432

    Article  PubMed  CAS  Google Scholar 

  • Postberg J, Alexandrova O, Cremer T, Lipps HJ (2005) Exploiting nuclear duality of ciliates to analyse topological requirements for DNA replication and transcription. J Cell Sci 118:3973–3983

    Article  PubMed  CAS  Google Scholar 

  • Ribbert D (1979) Chromosomes and puffing in experimentally induced polytene chromosomes of Calliphora erythrocephala. Chromosoma (Berl) 74:269–298

    Article  CAS  Google Scholar 

  • Ribbert D, Bier K (1969) Multiple nucleoli and enhanced nucleolar activity in the nurse cells of the insect ovary. Chromosoma (Berl) 27:178–197

    Article  CAS  Google Scholar 

  • Rouquette J, Genoud C, Vazquez-Nin GH, Kraus B, Cremer T, 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

    Article  PubMed  CAS  Google Scholar 

  • Rubtsov NB (2006) Methods for work with mammalian chromosomes. Novosibirsk Gos. Universitet, Novosibirsk

  • Rubtsov NB, Alekseenko AA, Belyaeva ES (1999) Microcloning and characteristics of DNA from regions of the centromeric heterochromatin of Drosophila melanogaster polytene chromosomes. Russ J Genet 1:55–61

    Google Scholar 

  • Stadler S, Schnapp V, Mayer R, Stein S, Cremer C, Bonifer C, Cremer T, Dietzel S (2004) The architecture of chicken chromosome territories changes during differentiation. BMC Cell Biol 5(1):44

    Article  PubMed  Google Scholar 

  • Stegniy VN, Vasserlauf IE, Anan’ina TV (1999) Identification, mutual arrangement, and development of primary polytene chromosomes in the Calliphora erythrocephala (Diptera: Calliphoridae) nurse cell nuclei. Genetika 7:912–918

    Google Scholar 

  • Swedlow JR, Lamond A (2001) Nuclear dynamics: where genes are how they got there. Genome Biol 3:1–7

    Google Scholar 

  • Thiry M (1992) New data concerning the functional organization of the mammalian cell nucleolus: detection of RNA and rRNA by in situ molecular immunocytochemistry. Nucleic Acids Res 20(23):6195–6200

    Article  PubMed  CAS  Google Scholar 

  • van Koningsbruggen S, Gierlinski M, Schofield P, Martin D, Barton GJ, Ariyurek Y, den Dunnen JT, Lamond AI (2010) High resolution whole-genome sequencing reveals that specific chromatin domains from most human chromosomes associate with nucleoli. Mol Biol Cell 21:3735–3748

    Article  PubMed  Google Scholar 

  • Vasserlauf IE, Anan’ina TV, Unger MF, Karamysheva TV, Mel’nikova NN, Rubtsov NB, Stegniĭ VN (2003) Organization and differential staining of the chromosomes of Calliphora erythrocephala (Diptera: Calliphoridae) nurse cell endomitotic nuclei. Genetika 39(9):1193–1202

    PubMed  CAS  Google Scholar 

  • Vinogradova LB (1984) Bluebottle Blowfly (Calliphora vicina): a model object of ecological and physiological studies. Nauka, Leningrad

    Google Scholar 

  • Visser AE, Jaunin F, Fakan S, Aten JA (2000) High resolution analysis of interphase chromosome domains. J Cell Sci 113:2585–2593

    PubMed  CAS  Google Scholar 

  • Volpi EV, Chevret E, Jones T, Vatcheva R, Williamson J et al (2000) Large-scale chromatin organization of the major histocompatibility complex and other regions of human chromosome 6 and its response to interferon in interphase nuclei. J Cell Sci 113:1565–1576

    PubMed  CAS  Google Scholar 

  • Wickly B, Polyakov YuV (1975) Electron microscopy for the beginners. Mir, Moscow

    Google Scholar 

  • Zharskaya OO, Zatsepina OV (2007) The dynamics and mechanisms of nucleolus reorganization in mitosis. Tsitologiya 5:355–369

    Google Scholar 

  • Zorn C, Cremer C, Cremer T, Zimmer J (1979) Unscheduled DNA synthesis after partial UV irradiation of the cell nucleus. Distribution in interphase and metaphase. Exp Cell Res 124:111–119

    Article  PubMed  CAS  Google Scholar 

  • Zybina EV (1986) Cytology of the nurse cell. Nauka, Leningrad

    Google Scholar 

Download references

Acknowledgments

We thank Dr. A.A. Miller for the helpful in electron microscopical study and Dr. S.I. Baiborodin for the helpful in confocal microscopical analysis. The work was supported by the Russian Foundation for Basic Research (grant no. 10-04-01059a).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Tomsk State University, 36 Lenin Prospekt, Tomsk, 634050, Russia

    Alina A. Kokhanenko, Tatyana V. Anan’ina & Vladimir N. Stegniy

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  1. Alina A. Kokhanenko
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  2. Tatyana V. Anan’ina
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  3. Vladimir N. Stegniy
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Correspondence to Alina A. Kokhanenko.

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Kokhanenko, A.A., Anan’ina, T.V. & Stegniy, V.N. The changes in chromosome 6 spatial organization during chromatin polytenization in the Calliphora erythrocephala Mg. (Diptera: Calliphoridae) nurse cells. Protoplasma 250, 141–149 (2013). https://doi.org/10.1007/s00709-012-0385-7

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