Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1990 Nov 1;111(5):1905–1911. doi: 10.1083/jcb.111.5.1905

Mechanism of the formation of contractile ring in dividing cultured animal cells. II. Cortical movement of microinjected actin filaments

PMCID: PMC2116328  PMID: 2229180

Abstract

The contractile ring in dividing animal cells is formed primarily through the reorganization of existing actin filaments (Cao, L.-G., and Y.-L. Wang. 1990. J. Cell Biol. 110:1089-1096), but it is not clear whether the process involves a random recruitment of diffusible actin filaments from the cytoplasm, or a directional movement of cortically associated filaments toward the equator. We have studied this question by observing the distribution of actin filaments that have been labeled with fluorescent phalloidin and microinjected into dividing normal rat kidney (NRK) cells. The labeled filaments are present primarily in the cytoplasm during prometaphase and early metaphase, but become associated extensively with the cell cortex 10-15 min before the onset of anaphase. This process is manifested both as an increase in cortical fluorescence intensity and as movements of discrete aggregates of actin filaments toward the cortex. The concentration of actin fluorescence in the equatorial region, accompanied by a decrease of fluorescence in polar regions, is detected 2-3 min after the onset of anaphase. By directly tracing the distribution of aggregates of labeled actin filaments, we are able to detect, during anaphase and telophase, movements of cortical actin filaments toward the equator at an average rate of 1.0 micron/min. Our results, combined with previous observations, suggest that the organization of actin filaments during cytokinesis probably involves an association of cytoplasmic filaments with the cortex, a movement of cortical filaments toward the cleavage furrow, and a dissociation of filaments from the equatorial cortex.

Full Text

The Full Text of this article is available as a PDF (1.6 MB).

Selected References

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

  1. Bourguignon L. Y., Bourguignon G. J. Capping and the cytoskeleton. Int Rev Cytol. 1984;87:195–224. doi: 10.1016/s0074-7696(08)62443-2. [DOI] [PubMed] [Google Scholar]
  2. Bray D., White J. G. Cortical flow in animal cells. Science. 1988 Feb 19;239(4842):883–888. doi: 10.1126/science.3277283. [DOI] [PubMed] [Google Scholar]
  3. Cao L. G., Wang Y. L. Mechanism of the formation of contractile ring in dividing cultured animal cells. I. Recruitment of preexisting actin filaments into the cleavage furrow. J Cell Biol. 1990 Apr;110(4):1089–1095. doi: 10.1083/jcb.110.4.1089. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Devore J. J., Conrad G. W., Rappaport R. A model for astral stimulation of cytokinesis in animal cells. J Cell Biol. 1989 Nov;109(5):2225–2232. doi: 10.1083/jcb.109.5.2225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Fujiwara K., Pollard T. D. Fluorescent antibody localization of myosin in the cytoplasm, cleavage furrow, and mitotic spindle of human cells. J Cell Biol. 1976 Dec;71(3):848–875. doi: 10.1083/jcb.71.3.848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Harris A. K., Gewalt S. L. Simulation testing of mechanisms for inducing the formation of the contractile ring in cytokinesis. J Cell Biol. 1989 Nov;109(5):2215–2223. doi: 10.1083/jcb.109.5.2215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kitanishi-Yumura T., Fukui Y. Actomyosin organization during cytokinesis: reversible translocation and differential redistribution in Dictyostelium. Cell Motil Cytoskeleton. 1989;12(2):78–89. doi: 10.1002/cm.970120203. [DOI] [PubMed] [Google Scholar]
  8. Koppel D. E., Oliver J. M., Berlin R. D. Surface functions during mitosis. III. Quantitative analysis of ligand-receptor movement into the cleavage furrow: diffusion vs. flow. J Cell Biol. 1982 Jun;93(3):950–960. doi: 10.1083/jcb.93.3.950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Mabuchi I. Biochemical aspects of cytokinesis. Int Rev Cytol. 1986;101:175–213. doi: 10.1016/s0074-7696(08)60249-1. [DOI] [PubMed] [Google Scholar]
  10. Maupin P., Pollard T. D. Arrangement of actin filaments and myosin-like filaments in the contractile ring and of actin-like filaments in the mitotic spindle of dividing HeLa cells. J Ultrastruct Mol Struct Res. 1986 Jan;94(1):92–103. doi: 10.1016/0889-1605(86)90055-8. [DOI] [PubMed] [Google Scholar]
  11. McCaig C. D., Robinson K. R. The distribution of lectin receptors on the plasma membrane of the fertilized sea urchin egg during first and second cleavage. Dev Biol. 1982 Jul;92(1):197–202. doi: 10.1016/0012-1606(82)90163-4. [DOI] [PubMed] [Google Scholar]
  12. McKenna N. M., Wang Y. L., Konkel M. E. Formation and movement of myosin-containing structures in living fibroblasts. J Cell Biol. 1989 Sep;109(3):1163–1172. doi: 10.1083/jcb.109.3.1163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Mckenna N. M., Wang Y. L. Culturing cells on the microscope stage. Methods Cell Biol. 1989;29:195–205. doi: 10.1016/s0091-679x(08)60195-8. [DOI] [PubMed] [Google Scholar]
  14. Perry M. M., John H. A., Thomas N. S. Actin-like filaments in the cleavage furrow of newt egg. Exp Cell Res. 1971 Mar;65(1):249–253. doi: 10.1016/s0014-4827(71)80075-7. [DOI] [PubMed] [Google Scholar]
  15. Salmon E. D. Cytokinesis in animal cells. Curr Opin Cell Biol. 1989 Jun;1(3):541–547. doi: 10.1016/0955-0674(89)90018-5. [DOI] [PubMed] [Google Scholar]
  16. Sanders M. C., Wang Y. L. Exogenous nucleation sites fail to induce detectable polymerization of actin in living cells. J Cell Biol. 1990 Feb;110(2):359–365. doi: 10.1083/jcb.110.2.359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sanger J. W. Changing patterns of actin localization during cell division. Proc Natl Acad Sci U S A. 1975 May;72(5):1913–1916. doi: 10.1073/pnas.72.5.1913. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Schliwa M., van Blerkom J. Structural interaction of cytoskeletal components. J Cell Biol. 1981 Jul;90(1):222–235. doi: 10.1083/jcb.90.1.222. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Schroeder T. E. The contractile ring. I. Fine structure of dividing mammalian (HeLa) cells and the effects of cytochalasin B. Z Zellforsch Mikrosk Anat. 1970;109(4):431–449. [PubMed] [Google Scholar]
  20. Schroeder T. E. The contractile ring. II. Determining its brief existence, volumetric changes, and vital role in cleaving Arbacia eggs. J Cell Biol. 1972 May;53(2):419–434. doi: 10.1083/jcb.53.2.419. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schroeder T. E. The origin of cleavage forces in dividing eggs. A mechanism in two steps. Exp Cell Res. 1981 Jul;134(1):231–240. doi: 10.1016/0014-4827(81)90480-8. [DOI] [PubMed] [Google Scholar]
  22. Spudich J. A., Watt S. The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J Biol Chem. 1971 Aug 10;246(15):4866–4871. [PubMed] [Google Scholar]
  23. Wadsworth P. Microinjected carboxylated beads move predominantly poleward in sea urchin eggs. Cell Motil Cytoskeleton. 1987;8(4):293–301. doi: 10.1002/cm.970080402. [DOI] [PubMed] [Google Scholar]
  24. White J. G., Borisy G. G. On the mechanisms of cytokinesis in animal cells. J Theor Biol. 1983 Mar 21;101(2):289–316. doi: 10.1016/0022-5193(83)90342-9. [DOI] [PubMed] [Google Scholar]

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

RESOURCES