Skip to main content
NCBI home page
Biophysical Journal logoLink to Biophysical Journal
. 1995 Oct;69(4):1596–1605. doi: 10.1016/S0006-3495(95)80032-9

Anaphase chromatid motion: involvement of type II DNA topoisomerases.

B Duplantier 1, G Jannink 1, J L Sikorav 1
PMCID: PMC1236390  PMID: 8534830

Abstract

Sister chromatids are topologically intertwined at the onset of anaphase: their segregation during anaphase is known to require strand-passing activity by type II DNA topoisomerase. We propose that the removal of the intertwinings involves at the same time the traction of the mitotic spindle and the activity of topoisomerases. This implies that the velocity of the chromatids is compatible with the kinetic constraints imposed by the enzymatic reaction. We show that the greatest observed velocities (about 0.1 microns s-1) are close to the theoretical upper bound compatible with both the diffusion rate (calculated here within a probabilistic model) and the measured reaction rate of the enzyme.

Full text

PDF
1596

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albery W. J., Knowles J. R. Evolution of enzyme function and the development of catalytic efficiency. Biochemistry. 1976 Dec 14;15(25):5631–5640. doi: 10.1021/bi00670a032. [DOI] [PubMed] [Google Scholar]
  2. Alexander S. P., Rieder C. L. Chromosome motion during attachment to the vertebrate spindle: initial saltatory-like behavior of chromosomes and quantitative analysis of force production by nascent kinetochore fibers. J Cell Biol. 1991 May;113(4):805–815. doi: 10.1083/jcb.113.4.805. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bennett S. P., Halford S. E. Recognition of DNA by type II restriction enzymes. Curr Top Cell Regul. 1989;30:57–104. doi: 10.1016/b978-0-12-152830-0.50005-0. [DOI] [PubMed] [Google Scholar]
  4. Downes C. S., Mullinger A. M., Johnson R. T. Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):8895–8899. doi: 10.1073/pnas.88.20.8895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Drake F. H., Hofmann G. A., Bartus H. F., Mattern M. R., Crooke S. T., Mirabelli C. K. Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry. 1989 Oct 3;28(20):8154–8160. doi: 10.1021/bi00446a029. [DOI] [PubMed] [Google Scholar]
  6. Gasser S. M., Laroche T., Falquet J., Boy de la Tour E., Laemmli U. K. Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol. 1986 Apr 20;188(4):613–629. doi: 10.1016/s0022-2836(86)80010-9. [DOI] [PubMed] [Google Scholar]
  7. Holm C. Coming undone: how to untangle a chromosome. Cell. 1994 Jul 1;77(7):955–957. doi: 10.1016/0092-8674(94)90433-2. [DOI] [PubMed] [Google Scholar]
  8. Holm C., Goto T., Wang J. C., Botstein D. DNA topoisomerase II is required at the time of mitosis in yeast. Cell. 1985 Jun;41(2):553–563. doi: 10.1016/s0092-8674(85)80028-3. [DOI] [PubMed] [Google Scholar]
  9. Holm C., Stearns T., Botstein D. DNA topoisomerase II must act at mitosis to prevent nondisjunction and chromosome breakage. Mol Cell Biol. 1989 Jan;9(1):159–168. doi: 10.1128/mcb.9.1.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hyrien O., Méchali M. Chromosomal replication initiates and terminates at random sequences but at regular intervals in the ribosomal DNA of Xenopus early embryos. EMBO J. 1993 Dec;12(12):4511–4520. doi: 10.1002/j.1460-2075.1993.tb06140.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Krueger S., Zaccai G., Wlodawer A., Langowski J., O'Dea M., Maxwell A., Gellert M. Neutron and light-scattering studies of DNA gyrase and its complex with DNA. J Mol Biol. 1990 Jan 5;211(1):211–220. doi: 10.1016/0022-2836(90)90021-D. [DOI] [PubMed] [Google Scholar]
  12. Lindsley J. E., Wang J. C. On the coupling between ATP usage and DNA transport by yeast DNA topoisomerase II. J Biol Chem. 1993 Apr 15;268(11):8096–8104. [PubMed] [Google Scholar]
  13. McDowall A. W., Smith J. M., Dubochet J. Cryo-electron microscopy of vitrified chromosomes in situ. EMBO J. 1986 Jun;5(6):1395–1402. doi: 10.1002/j.1460-2075.1986.tb04373.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nicklas R. B. The forces that move chromosomes in mitosis. Annu Rev Biophys Biophys Chem. 1988;17:431–449. doi: 10.1146/annurev.bb.17.060188.002243. [DOI] [PubMed] [Google Scholar]
  15. Osheroff N., Shelton E. R., Brutlag D. L. DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J Biol Chem. 1983 Aug 10;258(15):9536–9543. [PubMed] [Google Scholar]
  16. Permana P. A., Ferrer C. A., Snapka R. M. Inverse relationship between catenation and superhelicity in newly replicated simian virus 40 daughter chromosomes. Biochem Biophys Res Commun. 1994 Jun 30;201(3):1510–1517. doi: 10.1006/bbrc.1994.1875. [DOI] [PubMed] [Google Scholar]
  17. Pienta K. J., Coffey D. S. A structural analysis of the role of the nuclear matrix and DNA loops in the organization of the nucleus and chromosome. J Cell Sci Suppl. 1984;1:123–135. doi: 10.1242/jcs.1984.supplement_1.9. [DOI] [PubMed] [Google Scholar]
  18. Rattner J. B., Lin C. C. Radial loops and helical coils coexist in metaphase chromosomes. Cell. 1985 Aug;42(1):291–296. doi: 10.1016/s0092-8674(85)80124-0. [DOI] [PubMed] [Google Scholar]
  19. Saitoh Y., Laemmli U. K. Metaphase chromosome structure: bands arise from a differential folding path of the highly AT-rich scaffold. Cell. 1994 Feb 25;76(4):609–622. doi: 10.1016/0092-8674(94)90502-9. [DOI] [PubMed] [Google Scholar]
  20. Schomburg U., Grosse F. Purification and characterization of DNA topoisomerase II from calf thymus associated with polypeptides of 175 and 150 kDa. Eur J Biochem. 1986 Nov 3;160(3):451–457. doi: 10.1111/j.1432-1033.1986.tb10061.x. [DOI] [PubMed] [Google Scholar]
  21. Shamu C. E., Murray A. W. Sister chromatid separation in frog egg extracts requires DNA topoisomerase II activity during anaphase. J Cell Biol. 1992 Jun;117(5):921–934. doi: 10.1083/jcb.117.5.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Spell R. M., Holm C. Nature and distribution of chromosomal intertwinings in Saccharomyces cerevisiae. Mol Cell Biol. 1994 Feb;14(2):1465–1476. doi: 10.1128/mcb.14.2.1465. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sundin O., Varshavsky A. Arrest of segregation leads to accumulation of highly intertwined catenated dimers: dissection of the final stages of SV40 DNA replication. Cell. 1981 Sep;25(3):659–669. doi: 10.1016/0092-8674(81)90173-2. [DOI] [PubMed] [Google Scholar]
  24. Swedlow J. R., Sedat J. W., Agard D. A. Multiple chromosomal populations of topoisomerase II detected in vivo by time-lapse, three-dimensional wide-field microscopy. Cell. 1993 Apr 9;73(1):97–108. doi: 10.1016/0092-8674(93)90163-k. [DOI] [PubMed] [Google Scholar]
  25. Wang J. C. DNA topoisomerases: why so many? J Biol Chem. 1991 Apr 15;266(11):6659–6662. [PubMed] [Google Scholar]
  26. Wasserman S. A., White J. H., Cozzarelli N. R. The helical repeat of double-stranded DNA varies as a function of catenation and supercoiling. Nature. 1988 Aug 4;334(6181):448–450. doi: 10.1038/334448a0. [DOI] [PubMed] [Google Scholar]
  27. Watt P. M., Louis E. J., Borts R. H., Hickson I. D. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell. 1995 Apr 21;81(2):253–260. doi: 10.1016/0092-8674(95)90335-6. [DOI] [PubMed] [Google Scholar]
  28. Zechiedrich E. L., Osheroff N. Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 1990 Dec;9(13):4555–4562. doi: 10.1002/j.1460-2075.1990.tb07908.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zhu J., Newlon C. S., Huberman J. A. Localization of a DNA replication origin and termination zone on chromosome III of Saccharomyces cerevisiae. Mol Cell Biol. 1992 Oct;12(10):4733–4741. doi: 10.1128/mcb.12.10.4733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zimmerman S. B., Minton A. P. Macromolecular crowding: biochemical, biophysical, and physiological consequences. Annu Rev Biophys Biomol Struct. 1993;22:27–65. doi: 10.1146/annurev.bb.22.060193.000331. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES