Skip to main content
Log in

The stage of chromosome duplication in the cell cycle as revealed by X-ray breakage and 3H-thymidine labeling

  • Published:
Chromosoma Aims and scope Submit manuscript

Abstract

By means of combined experiments of X-irradiation and 3H-thymidine labeling of the chromosomes which are in the phase of synthesis, and the subsequent analysis at metaphase on the autoradiographs of the chromosomal damage induced during interphase, it was shown that in somatic cells from a quasi-diploid Chinese hamster line cultured in vitro the chromosomes change their response to radiation from single (chromosome type aberrations) to double (chromatid type aberrations) in late G1. These results are interpreted to indicate that the chromosome splits into two chromatids in G1, before DNA replication. — By extending the observations at the second metaphase after irradiation, it was also seen that cells irradiated while in G2 or late S when they reach the second post-irradiation mitosis still exhibit, beside chromosome type aberrations, many chromatid exchanges, some of which are labeled. Two hypotheses are suggested to account for this unexpected reappearance of chromatid aberrations at the second post-irradiation division. The first hypothesis is that they arise from half-chromatid aberrations. The second hypothesis, which derives from a new interpretation of the mechanisms of production of chromosome aberrations recently forwarded by Evans, is that they arise from gaps or achromatic lesions which undergo, as the cells go through the next cycle, a two-step repair process culminating in the production of aberrations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alfert, M.: Quantitative cytochemical studies on patterns of nuclear growth. In: Symposium on the Fine Structure of Cells, p. 157–163. Groningen: Noordhoff 1955.

    Google Scholar 

  • Bloch, D. P., and C. G. Godman: A microphotometric study of the syntheses of desoxyribonucleic acid and nuclear histone. J. biophys. biochem. Cytol. 1, 17–28 (1955).

    Google Scholar 

  • Evans, H. J.: Chromosome aberrations induced by ionizing radiations. Int. Rev. Cytol. 13, 221–321 (1962); - Uptake of 3H-thymidine and patterns of DNA replication in nuclei and chromosomes of Vicia faba. Exp. Cell Res. 35, 381–393 (1964);- Repair and recovery from chromosome damage induced by fractionated X-ray exposures. In: Radiation research (G. Silini ed.). Amsterdam: North Holland Publ. Co. 1967.

    Google Scholar 

  • —, and J. R. K. Savage: The relation between DNA synthesis and chromosome structure as resolved by X-ray damage. J. Cell Biol. 18, 525–540 (1963).

    Google Scholar 

  • Gilbert, C. W., S. Muldal, L. G. Lajtha, and J. Rowley: Time sequence of human chromosome duplication. Nature (Lond.) 195, 869–873 (1962).

    Google Scholar 

  • Heddle, J. A., and J. E. Trosko: Is the transition from chromosome to chromatid aberrations the result of the formation of single-stranded DNA? Exp. Cell Res. 42, 171–177 (1966).

    Google Scholar 

  • Hsu, T. C., W. C. Dewey, and R. M. Humphrey: Radiosensitivity of cells of Chinese hamster in vitro in relation to the cell cycle. Exp. Cell Res. 27, 441–452 (1962).

    Google Scholar 

  • —, and M. T. Zenzes: Mammalian chromosomes in vitro. XVII. Idiogram of the Chinese hamster. J. nat. Cancer Inst. 32, 857–869 (1964).

    Google Scholar 

  • LaCour, L. F., and A. Rutishauser: X-ray breakage experiments with endosperm. I. Sub-chromatid breakage. Chromosoma (Berl.) 6, 696–709 (1954).

    Google Scholar 

  • Lima-de-Faria, A.: Differential uptake of tritiated thymidine into hetero- and euchromatin in Melanoplus and Secale. J. biophys. biochem. Cytol. 6, 457–466 (1959); - DNA replication in human chromosomes. A review. In: Mammalian cytogenetics and related problems in radiobiology (C. Pavan et al.), (eds.), p. 31–37. London: Pergamon Press 1964.

    Google Scholar 

  • —, J. Reitalu, and S. Bergman: The pattern of DNA synthesis in the chromosomes of man. Hereditas (Lund) 47, 695–704 (1961).

    Google Scholar 

  • — and M. A. O'sullivan: Replication of autosomal heterochromatin in man. Chromosoma (Berl.) 16, 152–161 (1965).

    Google Scholar 

  • Mattingly, Sister A.: Nuclear protein synthesis in Vicia faba. Exp. Cell Res. 29, 314–326 (1963).

    Google Scholar 

  • McLeish, J.: Comparative microphotometric studies of DNA and arginine in plant nuclei. Chromosoma (Berl.) 10, 686–710 (1959).

    Google Scholar 

  • Mitra, S.: Effects of X-rays on chromosomes of Lilium longiflorum during meiosis. Genetics 43, 771–789 (1958).

    Google Scholar 

  • Monesi, V.: Autoradiographic study of DNA synthesis and the cell cycle in spermatogonia and spermatocytes of mouse testis using tritiated thymidine. J. Cell Biol. 14, 1–18 (1962) - Synthetic activities during spermatogenesis in the mouse. RNA and protein. Exp. Cell Res. 39, 197–224 (1965).

    Google Scholar 

  • —, and M. Crippa: Ribonucleic acid transfer from nucleus to cytoplasm during interphase and mitosis in mouse somatic cells cultured in vitro. Z. Zellforsch. 62, 807–821 (1964); - Osservazioni preliminari sullo stadio della scissione dei cromosomi durante il ciclo cellulare. Boll. Zool. 31, 1267–1270 (1964) (Abstr.).

    Google Scholar 

  • Moorhead, P. S., and V. Defendi: Asynchrony of DNA synthesis in chromosomes of human diploid cells. J. Cell Biol. 16, 202–209 (1963).

    Google Scholar 

  • Moses, M. J., and J. H. Taylor: Deoxypentose nucleic acid synthesis during microgametogenesis in Tradescantia. Exp. Cell Res. 9, 474–488 (1955).

    Google Scholar 

  • Ohno, S., and C. Weiler: Relationship between large Y-chromosome and sideby-side pairing of the XY-bivalent observed in the Chinese hamster, Cricetulus griseus. Chromosoma (Berl.) 13, 106–110 (1962).

    Google Scholar 

  • Painter, R. B., and R. M. Drew: Studies on deoxyribonucleic acid metabolism in human cancer cell cultures (HeLa). I. The temporal relationships of deoxyribonucleic acid synthesis to mitosis and turnover time. Lab. Invest. 8, 278–285 (1959).

    Google Scholar 

  • Puck, T. T., P. I. Marcus, and S. J. Cieciura: Clonal growth of mammalian cells in vitro. Growth characteristics of colonies from single HeLa cells with and without a “feeder” layer. J. exp. Med. 103, 273–284 (1956).

    Google Scholar 

  • Revell, S. H.: The accurate estimation of chromatid exchanges and its relevance to a new interpretation of chromatid aberrations induced by ionizing radiations. Proc. roy. Soc. Lond. B, 150, 563–589 (1959).

    Google Scholar 

  • Sax, K., and E. D. King: An X-ray analysis of chromosome duplication. Proc. nat. Acad. Sci. (Wash.) 41, 150–155 (1955).

    Google Scholar 

  • Setlow, R. B., and W. L. Carrier: The disappearance of thymine dimers from DNA: an error-correcting mechanism. Proc. nat. Acad. Sci. (Wash.) 51, 226–231 (1964).

    Google Scholar 

  • Taylor, J. H.: Autoradiographic detection of incorporation of P32 into chromosomes during meiosis and mitosis. Exp. Cell Res. 4, 164–173 (1953); - The mode of chromosome duplication in Crepis capillaris. Exp. Cell Res. 15, 350–357 (1958);- Asynchronous duplication of chromosomes in cultured cells of Chinese hamster. J. biophys. biochem. Cytol. 7, 455–464 (1960).

    Google Scholar 

  • Taylor, J. H., P. S. Woods, and W. L. Hughes: The organization and duplication of chromosomes as revealed by autoradiographic studies using tritium-labeled thymidine. Proc. nat. Acad. Sci. (Wash.) 43, 122–128 (1957).

    Google Scholar 

  • Thoday, J. M.: Radiation-induced chromosome breakage, deoxyribonucleic acid synthesis and the mitotic cycle in root-meristem cells of Vicia faba. New Phytologist 53, 511–516 (1954).

    Google Scholar 

  • Wimber, D. E.: Asynchronous replication of deoxyribonucleic acid in root tip chromosomes of Tradescantia paludosa. Exp. Cell Res. 23, 402–407 (1961).

    Google Scholar 

  • Wolff, S.: Interpretation of induced chromosome breakage and rejoining. Radiat. Res., Suppl. 1, 453–462 (1959); - Radiation studies on the nature of chromosome breakage. Amer. Naturalist 44, 85–93 (1960).

    Google Scholar 

  • —, and H. E. Luippold: Chromosome splitting as revealed by combined X-ray and labelling experiments. Exp. Cell Res. 34, 548–556 (1964).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

This work was supported in part by grant No. RH-00304 from the Division of Radiological Health, Bureau of State Services, Public Health Service, U.S.A.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Monesi, V., Crippa, M. & Zito-Bignami, R. The stage of chromosome duplication in the cell cycle as revealed by X-ray breakage and 3H-thymidine labeling. Chromosoma 21, 369–386 (1967). https://doi.org/10.1007/BF00336948

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00336948

Keywords

Navigation