DNA renaturation activity of the SMC complex implicated in chromosome condensation (original) (raw)

Nature volume 388, pages 798–801 (1997)Cite this article

Abstract

Chromosome condensation occurs in mitosis before the separation of sister chromatids, and requires DNA topoisomerase II (refs 1,2) and a group of proteins called SMCs3,4,5. The resulting condensed chromosomes in metaphase have a complex hierarchical structure6,7. SMCs, the components of condensed chromosomes, are also required for the separation of sister chromatids and gene dosage compensation, and are found in a range of organisms from yeasts to mammals8,9,10,11,12,13. However, the mechanisms by which the SMCs contribute to chromosome condensation are unknown. We have studied chromosomes in fission-yeast SMC mutants cut3-477 and cut14-208 (ref. 9), which remain largely non-condensed during mitosis at the restrictive temperature (36 °C)9. To test their role in DNA condensation, we isolated the proteins Cut3 and Cut14 as an oligomeric complex, and tested their interactions with isolated DNA. The complex efficiently promoted the DNA renaturation reactions (the winding up of single-strand DNAs into double helical DNA) as much as ∼70-fold more efficiently than RecA14, which is a bacterial protein with similar activity. The activity of the mutant complex was heat sensitive. As DNA winding by renaturation is a potential cause of supercoiling, the SMC complex may be implicated in promoting the higher-order DNA coiling found in condensed chromosomes.

This is a preview of subscription content, access via your institution

Access options

Subscribe to this journal

Receive 51 print issues and online access

$199.00 per year

only $3.90 per issue

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Additional access options:

Similar content being viewed by others

References

  1. Swedlow, J. R., Agard, D. A. & Sedat, J. W. Chromosome structure inside the nucleus. Curr. Opin. Cell Biol. 5, 412–416 (1993).
    Article CAS Google Scholar
  2. Swedlow J. R. Agard D. A. & Sedat J. W. Chromosome structure inside the nucleus. Curr. Opin. Cell Biol. 5, 412–416 (1993).
    Article CAS Google Scholar
  3. Hirano, T., Mitchison, T. J. & Swedlow, J. R. The SMC family: from chromosome condensation to dosage compensation. Curr. Opin. Cell Biol. 7, 329–336 (1995).
    Article CAS Google Scholar
  4. Gasser, S. M. Coiling up chromosomes. Curr. Biol. 5, 357–360 (1995).
    Article CAS Google Scholar
  5. Koshland, D. & Strunnikov, A. Mitotic chromosome condensation. Annu. Rev. Cell Dev. Biol. 12, 305–333 (1996).
    Article CAS Google Scholar
  6. Boy de la Tour, E. & Laemmli, U. K. The metaphase scaffold is helically folded: sister chromatids have predominantly opposite helical handedness. Cell 55, 937–944 (1988).
    Article CAS Google Scholar
  7. Belmont, A. S., Sedat, J. W. & Agard, D. A. Athree dimensional approach to mitotic chromosome structure: evidence for a complex hierarchical organization. J. Cell Biol. 105, 77–92 (1987).
    Article CAS Google Scholar
  8. Strunnikov, A. V., Larionov, V. L. & Koshland, D. SMC1: an essential yeast gene encoding a putative head-rod-tail protein is required for nuclear division and defines a new ubiquitous family. J. Cell Biol. 123, 1635–1648 (1993).
    Article CAS Google Scholar
  9. Saka, Y.et al. Fission yeast cut3 and cut14, members of a ubiquitous protein family, are required for chromosome condensation and segregation in mitosis. EMBO J. 13, 4938–4952 (1994).
    Article CAS Google Scholar
  10. Hirano, T. & Mitchison, T. J. Aheteromeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79, 449–458 (1994).
    Article CAS Google Scholar
  11. Saitoh, N., Goldberg, I. G., Wood, E. R. & Earnshaw, W. C. ScII: an abundant chromosome scaffold protein is a member of a family of putative ATPase with an unusual predicted tertiary structure. J. Cell Biol. 127, 303–318 (1994).
    Article CAS Google Scholar
  12. Chuang, P.-T., Albertson, D. G. & Meyer, B. J. DPY-27: a chromosome condensation protein homolog that regulates C. elegans dosage compensation through association with the X chromosome. Cell 79, 459–474 (1994).
    Article CAS Google Scholar
  13. Strunnikov, A. V., Hogan, E. & Koshland, D. SMC2, a Saccharomyces cerevisiae gene essential for chromosome segregation and condensation defines a subgroup within the SMC-family. Genes Dev. 9, 587–599 (1995).
    Article CAS Google Scholar
  14. Bryant, F. R. & Lehman, I. R. On the mechanism of renaturation of complementary DNA strands by the recA protein of Escherichia coli. Proc. Natl Acad. Sci. USA 82, 297–301 (1985).
    Article ADS CAS Google Scholar
  15. Maundrell, K. nmt1 of fission yeast. J. Biol. Chem. 265, 10857–10864 (1990).
    CAS PubMed Google Scholar
  16. Côté, J., Quinn, J., Workman, J. L. & Peterson, C. L. Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SW1/SNF complex. Science 265, 53–60 (1994).
    Article ADS Google Scholar
  17. Funabiki, H.et al. Cut2 proteolysis required for sister-chromatid separation in fission yeast. Nature 381, 438–441 (1996).
    Article ADS CAS Google Scholar
  18. Bryant, F. R., Menge, K. L. & Nguyen, T. T. Kinetic modeling of the RecA protein promoted renaturation of complementary DNA strands. Biochemistry 28, 1062–1069 (1989).
    Article CAS Google Scholar
  19. Jessberger, R., Riwar, B., Baechtold, H. & Akhmedov, A. T. SMC proteins constitute two subunits of the mammalian recombination complex RC-1. EMBO J. 15, 4061–4068 (1996).
    Article CAS Google Scholar
  20. Chikashige, Y.et al. Composite motifs and repeat symmetry in S. pombe centromeres: direct analysis by integration of _Not_I restriction sites. Cell 57, 739–751 (1989).
    Article CAS Google Scholar
  21. Hirano, T., Kobayashi, R. & Hirano, M. Condensins, chromosome condensation protein complexes containing XCAP-C, XCAP-E and a Xenopus homolog of the Drosophila Barren protein. Cell 89, 511–521 (1997).
    Article CAS Google Scholar
  22. Connelly, J. C. & Leach, D. R. F. The sbcC and sbcD genes of Escherichia coli encode a nuclease involved in palindrome inviability and genetic recombination. Genes Cells 1, 285–291 (1996).
    Article CAS Google Scholar
  23. Bhat, M. A., Philp, A. V., Glover, D. M. & Bellen, H. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87, 1103–1114 (1996).
    Article Google Scholar

Download references

Acknowledgements

We thank T. Horii, H. Ogawa and Y. Adachi for help and advice; T. Hirano for data before publication; and T. Hyman for critically reading the manuscript. This work was supported by grants from the Ministry of Education, Science and Culture of Japan, the Japan Science Technology Foundation (CREST), and the Human Frontier Science Promotion Organization. T.S. is the recipient of a Japan Science Promotion Society fellowship.

Author information

Authors and Affiliations

  1. Department of Biophysics, Faculty of Science, Kyoto University, Kitashirakawa-Oiwake, Sakyo-ku, 606, Kyoto, Japan
    Takashi Sutani & Mitsuhiro Yanagida

Authors

  1. Takashi Sutani
    You can also search for this author inPubMed Google Scholar
  2. Mitsuhiro Yanagida
    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Mitsuhiro Yanagida.

Rights and permissions

About this article

Cite this article

Sutani, T., Yanagida, . DNA renaturation activity of the SMC complex implicated in chromosome condensation.Nature 388, 798–801 (1997). https://doi.org/10.1038/42062

Download citation

This article is cited by