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Replication labeling patterns and chromosome territories typical of mammalian nuclei are conserved in the early metazoan Hydra

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Abstract

To investigate the evolutionary conservation of higher order nuclear architecture previously described for mammalian cells we have analyzed the nuclear architecture of the simple polyp Hydra. These diploblastic organisms have large nuclei (8–10 μm) containing about 3×109 bp of DNA organized in 15 chromosome pairs. They belong to the earliest metazoan phylum and are separated from mammals by at least 600 million years. Single and double pulse labeling with halogenated nucleotides (bromodeoxyuridine, iododeoxyuridine and chlorodeoxyuridine) revealed striking similarities to the known sequence of replication labeling patterns in mammalian nuclei. These patterns reflect a persistent nuclear arrangement of early, mid-, and late replicating chromatin foci that could be identified during all stages of interphase over at least 5–10 cell generations. Segregation of labeled chromatids led after several cell divisions to nuclei with single or a few labeled chromosome territories. In such nuclei distinct clusters of labeled chromatin foci were separated by extended nuclear areas with non-labeled chromatin, which is typical of a territorial arrangement of interphase chromosomes. Our results indicate the conservation of fundamental features of higher order chromatin arrangements throughout the evolution of metazoan animals and suggest the existence of conserved mechanism(s) controlling this architecture.

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Abbreviations

CT:

Chromosome territory

BrdU:

Bromodeoxyuridine

IdU:

Iododeoxyuridine

CldU:

Chlorodeoxyuridine

References

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    PubMed  Google Scholar 

  • Campbell RD, David CN (1974) Cell cycle kinetics and development of Hydra attenuata. II. Interstitial cells. J Cell Sci 16:349–358

    CAS  PubMed  Google Scholar 

  • Cohen M, Lee KK, Wilson KL, Gruenbaum Y (2001) Transcriptional repression, apoptosis, human disease and the functional evolution of the nuclear lamina. Trends Biochem Sci 26:41–47

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Cremer T, Kreth G, Koester H, Fink RH, Heintzmann R, Cremer M, Solovei I, Zink D, Cremer C (2000) Chromosome territories, interchromatin domain compartment, and nuclear matrix: an integrated view of the functional nuclear architecture. Crit Rev Eukaryot Gene Expr 10:179–212

    CAS  PubMed  Google Scholar 

  • David CN (1973) A quantative method for maceration of Hydra tissue. Wilhelm Roux Archiv 171:259–268

    Google Scholar 

  • David CN, RD Campbell (1972) Cell cycle kinetics and development of Hydra attenuata. I. Epithelial cells. J Cell Sci 11:557–568

    CAS  PubMed  Google Scholar 

  • David CN, Gierer A (1974) Cell cycle kinetics and development of Hydra attenuata. III. Nerve and nematocyte differentiation. J Cell Sci 16:359–375

    CAS  PubMed  Google Scholar 

  • Dimitrova DS, Berezney R (2002) The spatio-temporal organization of DNA replication sites is identical in primary, immortalized and transformed mammalian cells. J Cell Sci 115:4037–4051

    Article  CAS  PubMed  Google Scholar 

  • Erber A, Riemer D, Hofemeister H, Bovenschulte M, Stick R, Panopoulou G, Lehrach H, Weber K (1999) Characterization of the Hydra lamin and its gene: a molecular phylogeny of metazoan lamins. J Mol Evol 49:260–271

    CAS  PubMed  Google Scholar 

  • Fisher AG, Merkenschlager M (2002) Gene silencing, cell fate and nuclear organisation. Curr Opin Genet Dev 12:193–197

    Article  CAS  PubMed  Google Scholar 

  • Garagna S, Perez-Zapata A, Zuccotti M, Mascheretti S, Marziliano N, Redi CA, Aguilera M, Capanna E (1997) Genome composition in Venezuelan spiny-rats of the genus Proechimys (Rodentia, Echimyidae). I. Genome size, C-heterochromatin and repetitive DNAs in situ hybridization patterns. Cytogenet Cell Genet 78:36–43

    CAS  PubMed  Google Scholar 

  • Gasser SM (2002) Visualizing chromatin dynamics in interphase nuclei. Science 296:1412–1416

    CAS  PubMed  Google Scholar 

  • Gruenbaum Y, Wilson KL, Harel A, Goldberg M, Cohen M (2000) Review: nuclear lamins—structural proteins with fundamental functions. J Struct Biol 129:313–323

    Article  CAS  PubMed  Google Scholar 

  • Gruenbaum Y, Lee KK, Liu J, Cohen M, Wilson KL (2002) The expression, lamin-dependent localization and RNAi depletion phenotype for emerin in C. elegans. J Cell Sci 115:923–929

    CAS  PubMed  Google Scholar 

  • Hoffmann K, Dreger CK, Olins AL, Olins DE, Shultz LD, Lucke B, Karl H, Kaps R, Muller D, Vaya A, Aznar J, Ware RE, Sotelo Cruz N, Lindner TH, Herrmann H, Reis A, Sperling K (2002) Mutations in the gene encoding the lamin B receptor produce an altered nuclear morphology in granulocytes (Pelger-Huet anomaly). Nat Genet 31:410–414

    CAS  PubMed  Google Scholar 

  • Holstein TW, Hobmayer E, David CN (1991) Pattern of epithelial cell cycling in hydra. Dev Biol 148:602–611

    CAS  PubMed  Google Scholar 

  • Lentz TL (1965) The fine structure of differentiating interstitial cells in Hydra. Z Zellforsch Mikrosk Anat 67:547–560

    CAS  PubMed  Google Scholar 

  • Lentz TL (1966) The cell biology of Hydra. North-Holland Publishing Company-Amsterdam, Amsterdam

  • Leonhardt H, Rahn HP, Weinzierl P, Sporbert A, Cremer T, Zink D, Cardoso MC (2000) Dynamics of DNA replication factories in living cells. J Cell Biol 149:271–280

    CAS  PubMed  Google Scholar 

  • Ma H, Samarabandu J, Devdhar RS, Acharya R, Cheng PC, Meng C, Berezney R (1998) Spatial and temporal dynamics of DNA replication sites in mammalian cells. J Cell Biol 143:1415–1425

    CAS  PubMed  Google Scholar 

  • Martou G, De Boni U (2000) Nuclear topology of murine, cerebellar Purkinje neurons: changes as a function of development. Exp Cell Res 256:131–139

    Article  CAS  PubMed  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 11:471–484

    Article  CAS  PubMed  Google Scholar 

  • McNulty AK, Saunders MJ (1992) Purification and immunological detection of pea nuclear intermediate filaments: evidence for plant nuclear lamins. J Cell Sci 103:407–414

    CAS  PubMed  Google Scholar 

  • Minguez A, Moreno Diaz de la Espina S (1993) Immunological characterization of lamins in the nuclear matrix of onion cells. J Cell Sci 106:431–439

    PubMed  Google Scholar 

  • O’Keefe RT, Henderson SC, Spector DL (1992) Dynamic organization of DNA replication in mammalian cell nuclei: spatially and temporally defined replication of chromosome-specific alpha-satellite DNA sequences. J Cell Biol 116:1095–1110

    CAS  PubMed  Google Scholar 

  • Park PC, De Boni U (1992) Spatial rearrangement and enhanced clustering of kinetochores in interphase nuclei of dorsal root ganglion neurons in vitro: association with nucleolar fusion. Exp Cell Res 203:222–229

    CAS  PubMed  Google Scholar 

  • Sadoni N, Langer S, Fauth C, Bernardi G, Cremer T, Turner BM, Zink D (1999) Nuclear organization of mammalian genomes. Polar chromosome territories build up functionally distinct higher order compartments. J Cell Biol 146:1211–1226

    CAS  PubMed  Google Scholar 

  • Scholtyseck E (1979) Fine structure of parasitic protozoa. Springer, Berlin Heidelberg New York

  • Shultz LD, Lyons BL, Burzenski LM, Gott B, Samuels R, Schweitzer PA, Dreger C, Herrmann H, Kalscheuer V, Olins AL, Olins DE, Sperling K, Hoffmann K (2003) Mutations at the mouse ichthyosis locus are within the lamin B receptor gene: a single gene model for human Pelger-Huet anomaly. Hum Mol Genet 12:61–69

    Article  CAS  PubMed  Google Scholar 

  • Solovei I, Grandy N, Knoth R, Volk B, Cremer T (2004) Pericentromere heterochromatin dynamics in postmitotic Purkinje cells during murine cerebellum development. Cytogenet Genome Res (in press)

  • Sparvoli E, Levi M, Rossi E (1994) Replicon clusters may form structurally stable complexes of chromatin and chromosomes. J Cell Sci 107:3097–3103

    CAS  PubMed  Google Scholar 

  • Stuurman N, Heins S, Aebi U (1998) Nuclear lamins: their structure, assembly, and interactions. J Struct Biol 122:42–66

    Article  CAS  PubMed  Google Scholar 

  • Walter J, Schermelleh L, Cremer M, Tashiro S, Cremer T (2003) Chromosome order in HeLa cells changes during mitosis and early G1, but is stably maintained during subsequent interphase stages. J Cell Biol 160:685–697

    Article  CAS  PubMed  Google Scholar 

  • Westphal A (1976) Protozoa. Blackie, London

  • Zaman V, Howe J, Ng M (1998) Ultrastructure of the nucleus of the Iodamoeba butschlii cyst. Parasitol Res 84:421–422

    Article  CAS  PubMed  Google Scholar 

  • Zink D, Cremer T (1998) Cell nucleus: chromosome dynamics in nuclei of living cells. Curr Biol 8:R321–324

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants to T. Cremer and C.N. David from the Deutsche Forschungsgemeinschaft.

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Correspondence to Charles N. David.

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Communicated by E.A. Nigg

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Alexandrova, O., Solovei, I., Cremer, T. et al. Replication labeling patterns and chromosome territories typical of mammalian nuclei are conserved in the early metazoan Hydra . Chromosoma 112, 190–200 (2003). https://doi.org/10.1007/s00412-003-0259-z

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