Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1983 Sep 1;97(3):877–886. doi: 10.1083/jcb.97.3.877

Control mechanisms of the cell cycle: role of the spatial arrangement of spindle components in the timing of mitotic events

PMCID: PMC2112559  PMID: 6885924

Abstract

To characterize the control mechanisms for mitosis, we studied the relationship between the spatial organization of microtubules in the mitotic spindle and the timing of mitotic events. Spindles of altered geometry were produced in sea urchin eggs by two methods: (a) early prometaphase spindles were cut into half spindles by micromanipulation or (b) mercaptoethanol was used to indirectly induce the formation of spindles with only one pole. Cells with monopolar spindles produced by either method required an average of 3 X longer than control cells to traverse mitosis. By the time the control cells started their next mitosis, the experimental cells were usually just finishing the original mitosis. In all cases, only the time from nuclear envelope breakdown to the start of telophase was prolonged. Once the cells entered telophase, events leading to the next mitosis proceeded with normal timing. Once prolonged, the cell cycle never resynchronized with the controls. Several types of control experiments showed that were not an artifact of the experimental techniques. These results show that the spatial arrangement of spindle components plays an important role in the mechanisms that control the timing of mitotic events and the timing of the cell cycle as a whole.

Full Text

The Full Text of this article is available as a PDF (3.8 MB).

Selected References

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

  1. Bajer A. S. Functional autonomy of monopolar spindle and evidence for oscillatory movement in mitosis. J Cell Biol. 1982 Apr;93(1):33–48. doi: 10.1083/jcb.93.1.33. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Begg D. A., Ellis G. W. Micromanipulation studies of chromosome movement. I. Chromosome-spindle attachment and the mechanical properties of chromosomal spindle fibers. J Cell Biol. 1979 Aug;82(2):528–541. doi: 10.1083/jcb.82.2.528. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Begg D. A., Ellis G. W. Micromanipulation studies of chromosome movement. II. Birefringent chromosomal fibers and the mechanical attachment of chromosomes to the spindle. J Cell Biol. 1979 Aug;82(2):542–554. doi: 10.1083/jcb.82.2.542. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ellis G. W. Piezoelectric Micromanipulators: Electrically operated micromanipulators add automatic high-speed movement to normal manual control. Science. 1962 Oct 12;138(3537):84–91. doi: 10.1126/science.138.3537.84. [DOI] [PubMed] [Google Scholar]
  5. HINEGARDNER R. T., RAO B., FELDMAN D. E. THE DNA SYNTHETIC PERIOD DURING EARLY DEVELOPMENT OF THE SEA URCHIN EGG. Exp Cell Res. 1964 Oct;36:53–61. doi: 10.1016/0014-4827(64)90159-4. [DOI] [PubMed] [Google Scholar]
  6. Johnson R. T., Rao P. N. Nucleo-cytoplasmic interactions in the acheivement of nuclear synchrony in DNA synthesis and mitosis in multinucleate cells. Biol Rev Camb Philos Soc. 1971 Feb;46(1):97–155. doi: 10.1111/j.1469-185x.1971.tb01180.x. [DOI] [PubMed] [Google Scholar]
  7. Kauffman S., Wille J. J. The mitotic oscillator in Physarum polycephalum. J Theor Biol. 1975 Nov;55(1):47–93. doi: 10.1016/s0022-5193(75)80108-1. [DOI] [PubMed] [Google Scholar]
  8. Kinoshita S., Yazaki I. The behaviour and localization of intracellular relaxing system during cleavage in the sea urchin egg. Exp Cell Res. 1967 Sep;47(3):449–458. doi: 10.1016/0014-4827(67)90003-1. [DOI] [PubMed] [Google Scholar]
  9. Mazia D., Paweletz N., Sluder G., Finze E. M. Cooperation of kinetochores and pole in the establishment of monopolar mitotic apparatus. Proc Natl Acad Sci U S A. 1981 Jan;78(1):377–381. doi: 10.1073/pnas.78.1.377. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. REBHUN L. I. Aster-associated particles in the cleavage of marine invertebrate eggs. Ann N Y Acad Sci. 1960 Oct 7;90:357–380. doi: 10.1111/j.1749-6632.1960.tb23257.x. [DOI] [PubMed] [Google Scholar]
  11. Salmon E. D., Ellis G. W. Compensator transducer increases ease, accuracy, and rapidity of measuring changes in specimen birefringence with polarization microscopy. J Microsc. 1976 Jan;106(1):63–69. doi: 10.1111/j.1365-2818.1976.tb02384.x. [DOI] [PubMed] [Google Scholar]
  12. Salmon E. D. Spindle microtubules: thermodynamics of in vivo assembly and role in chromosome movement. Ann N Y Acad Sci. 1975 Jun 30;253:383–406. doi: 10.1111/j.1749-6632.1975.tb19216.x. [DOI] [PubMed] [Google Scholar]
  13. Silver R. B., Cole R. D., Cande W. Z. Isolation of mitotic apparatus containing vesicles with calcium sequestration activity. Cell. 1980 Feb;19(2):505–516. doi: 10.1016/0092-8674(80)90525-5. [DOI] [PubMed] [Google Scholar]
  14. Sluder G. Experimental manipulation of the amount of tubulin available for assembly into the spindle of dividing sea urchin eggs. J Cell Biol. 1976 Jul;70(1):75–85. doi: 10.1083/jcb.70.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Sluder G. Role of spindle microtubules in the control of cell cycle timing. J Cell Biol. 1979 Mar;80(3):674–691. doi: 10.1083/jcb.80.3.674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Wolniak S. M., Hepler P. K., Jackson W. T. Ionic changes in the mitotic apparatus at the metaphase/anaphase transition. J Cell Biol. 1983 Mar;96(3):598–605. doi: 10.1083/jcb.96.3.598. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES