Summary
In 1885 Carl Rabl published his theory on the internal structure of the interphase nucleus. We have tested two predictions of this theory in fibroblasts grown in vitro from a female Chinese hamster, namely (1) the Rabl-orientation of interphase chromosomes and (2) the stability of the chromosome arrangement established in telophase throughout the subsequent interphase. Tests were carried out by premature chromosome condensation (PCC) and laser-UV-microirradiation of the interphase nucleus. Rabl-orientation of chromosomes was observed in G1 PCCs and G2 PCCs. The cell nucleus was microirradiated in G1 at one or two sites and pulse-labelled with 3H-thymidine for 2h. Cells were processed for autoradiography either immediately thereafter or after an additional growth period of 10 to 60h. Autoradiographs show unscheduled DNA synthesis (UDS) in the microirradiated nuclear part(s). The distribution of labelled chromatin was evaluated in autoradiographs from 1035 cells after microirradiation of a single nuclear site and from 253 cells after microirradiation of two sites. After 30 to 60h postincubation the labelled regions still appeared coherent although the average size of the labelled nuclear area fr increased from 14.2% (0h) to 26.5% (60h). The relative distance dr, i.e. the distance between two microirradiated sites divided by the diameter of the whole nucleus, showed a slight decrease with increasing incubation time. Nine metaphase figures were evaluated for UDS-label after microirradiation of the nuclear edge in G1. An average of 4.3 chromosomes per cell were labelled. Several chromosomes showed joint labelling of both distal chromosome arms including the telomeres, while the centromeric region was free from label. This label pattern is interpreted as the result of a V-shaped orientation of these particular chromosomes in the interphase nucleus with their telomeric regions close to each other at the nuclear edge. Our data support the tested predictions of the Rabl-model. Small time-dependent changes of the nuclear space occupied by single chromosomes and of their relative positions in the interphase nucleus seem possible, while the territorial organization of interphase chromosomes and their arrangement in general is maintained during interphase. The present limitations of the methods used for this study are discussed.
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References
Avivi L, Feldman M (1980) Arrangement of chromosomes in the interphase nucleus of plants. Hum Genet 55:281–295
Berezney R, Buchholtz LA (1981) Dynamic association of replicating DNA fragments with the nuclear matrix of regenerating liver. Exp Cell Res 132:1–13
Boveri Th (1888) Zellen Studien. Jena, Z Naturw 22:687–882
Boveri Th (1909) Die Blastomerenkerne von Ascaris megalocephala und die Theorie der Chromosomenindividualität. Arch Zellforsch 3:181–268
Cremer C, Zorn C, Cremer T (1974) An ultraviolet microbeam for 257 nm. Microsc Acta 75:331–337
Cremer C, Cremer T, Zorn C, Schoeller L (1976) Effects of laser-UV-microirradiation (γ=2573 Å) on proliferation of Chinese hamster cells. Radiat Res 66:106–121
Cremer C, Cremer T, Zorn C, Cioreanu V (1979a) Partial irradiation of Chinese hamster cell nuclei and detection of unscheduled DNA synthesis in interphase and metaphase. A tool to investigate the arrangement of interphase chromosomes in mammalian cells. Hoppe Seyler's Z Physiol Chem 360:244–245
Cremer T, Cremer C, Cioreanu V (1979b) Unscheduled DNA synthesis induced by laser-UV-microirradiation of the cell nucleus in G1 and autoradiographic examination of the distribution of microirradiated chromatin in G1 and S-phase. Eur J Cell Biol 20:127–128
Cremer C, Cremer T, Fukuda M, Nakanishi K (1980) Detection of laser-UV-microirradiation induced DNA photolesions by immunofluorescent staining. Hum Genet 54:107–110
Cremer C, Cremer T, Jabbur G (1981) Laser-UV-microirradiation of Chinese hamster cells: The influence of the distribution of photolesions on unscheduled DNA synthesis. Photochem Photobiol 33: 925–928
Comings DE (1968) The rationale for an ordered arrangement of chromatin in the interphase nucleus. Am J Hum Genet 20:440–460
Comings DE (1980) Arrangement of chromatin in the nucleus. Hum Genet 53:131–143
Hager D, Schroeder TM, Vogel F (to be published) Position of chromosomes in the interphase nucleus. An analysis of nonhomologous interchanges in lymphocyte cultures after Trenimon treatment and from two patients with Fanconi's anemia and Bloom's syndrome. Hum Genet
Hens L, Kirsch-Volders M, Susanne C, Galperin-Lemaitre H (1975) Relative position of trypsin banded homologous chromosomes in human metaphase figures. Hum Genet 28:303–311
Hoehn H, Martin GM (1973) Nonrandom arrangement of human chromatin: topography of disomic markers X, Y, and 1h+. Cytogenet Cell Genet 12:443–452
Kirsch-Volders M, Hens L, Susanne C, Galperin-Lemaitre H (1977) Stability of centromere-center distances in normal human metaphases. Cytogenet Cell Genet 18:61–74
Kirsch-Volders M, Hens L, Susanne C (1980) Telomere and centromere association tendencies in the human male metaphase complement. Hum Genet 54:69–77
Moroi Y, Peebles C, Fritzler MJ, Steigerwald J, Tan EM (1980) Auto-antibody to centromere (kinetochore) in scleroderma sera. Proc Natl Acad Sci USA 77:1627–1631
Pardoll DM, Vogelstein B, Coffey DS (1980) A fixed site of DNA replication in eucaryotic cells. Cell 19:527–536
Rabl C (1885) Über Zelltheilung. Morphologisches Jahrbuch. Gegenbaur C (ed) 10:214–330
Schnedl W, Mikelsaar A-V, Breitenbach M, Dann O (1977) DIPI and DAPI: fluorescence banding with only negligible fading. Hum Genet 36:167–172
Sperling K, Rao PN (1974) The phenomenon of premature chromosome condensation: its relevance to basic and applied research. Hum Genet 23:235–258
Sperling K, Luedtke E-K (1981) Arrangement of prematurely condensed chromosomes in cultured cells and lymphocytes of the Indian Muntjac. Chromosoma 83:541–553
Sperling K (1982) Cell cycle and chromosome cycle: morphological and functional aspects. In: Rao PN, Johnson RT, Sperling K (eds) Premature chromosome condensation: application in basic, mutation and clinical research. Academic Press, New York
Vogel F, Schroeder TM (1974) The internal order of the interphase nucleus. Hum Genet 25:265–297
Zang KD, Back E (1968) Quantitative studies of the arrangement of human chromosomes. I. Individual features in the association pattern of acrocentric chromosomes of normal males and females. Cytogenetic 7:455–470
Zankl H, Zang KD (1974) Quantitative studies on the arrangement of human metaphase chromosomes. IV. The association frequerncy of human acrocentric marker chromosomes. Hum Genet 23:259–265
Zorn C, Cremer T, Cremer C, Zimmer J (1976) Laser-UV-microirradiation of interphase nuclei and posttreatment with caffeine: a new approach to establish the arrangement of interphase chromosomes. Hum Genet 35:83–89
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
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Part of this work is included in the doctoral thesis of H. Baumann to be submitted to the Faculty of Biology of the University of Heidelberg
Part of this work is included in the doctoral thesis of V. Teuber to be submitted to the Faculty of Medicine of the University of Freiburg i. Br.
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Cremer, T., Cremer, C., Baumann, H. et al. Rabl's model of the interphase chromosome arrangement tested in Chinise hamster cells by premature chromosome condensation and laser-UV-microbeam experiments. Hum Genet 60, 46–56 (1982). https://doi.org/10.1007/BF00281263
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DOI: https://doi.org/10.1007/BF00281263