Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1987 Nov 1;105(5):2123–2135. doi: 10.1083/jcb.105.5.2123

Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans

PMCID: PMC2114830  PMID: 3680373

Abstract

The establishment of cell division axes was examined in the early embryonic divisions of Caenorhabditis elegans. It has been shown previously that there are two different patterns of cleavage during early embryogenesis. In one set of cells, which undergo predominantly determinative divisions, the division axes are established successively in the same orientation, while division axes in the other set, which divide mainly proliferatively, have an orthogonal pattern of division. We have investigated the establishment of these axes by following the movement of the centrosomes. Centrosome separation follows a reproducible pattern in all cells, and this pattern by itself results in an orthogonal pattern of cleavage. In those cells that divide on the same axis, there is an additional directed rotation of pairs of centrosomes together with the nucleus through well-defined angles. Intact microtubules are required for rotation; rotation is prevented by inhibitors of polymerization and depolymerization of microtubules. We have examined the distribution of microtubules in fixed embryos during rotation. From these and other data we infer that microtubules running from the centrosome to the cortex have a central role in aligning the centrosome-nuclear complex.

Full Text

The Full Text of this article is available as a PDF (3.7 MB).

Selected References

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

  1. Bestor T. H., Schatten G. Anti-tubulin immunofluorescence microscopy of microtubules present during the pronuclear movement of sea urchin fertilization. Dev Biol. 1981 Nov;88(1):80–91. doi: 10.1016/0012-1606(81)90220-7. [DOI] [PubMed] [Google Scholar]
  2. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brinkley B. R., Stubblefield E., Hsu T. C. The effects of colcemid inhibition and reversal on the fine structure of the mitotic apparatus of Chinese hamster cells in vitro. J Ultrastruct Res. 1967 Jul;19(1):1–18. doi: 10.1016/s0022-5320(67)80057-1. [DOI] [PubMed] [Google Scholar]
  4. Cowan A. E., McIntosh J. R. Mapping the distribution of differentiation potential for intestine, muscle, and hypodermis during early development in Caenorhabditis elegans. Cell. 1985 Jul;41(3):923–932. doi: 10.1016/s0092-8674(85)80073-8. [DOI] [PubMed] [Google Scholar]
  5. Euteneuer U., Schliwa M. Evidence for an involvement of actin in the positioning and motility of centrosomes. J Cell Biol. 1985 Jul;101(1):96–103. doi: 10.1083/jcb.101.1.96. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Gould R. R., Borisy G. G. The pericentriolar material in Chinese hamster ovary cells nucleates microtubule formation. J Cell Biol. 1977 Jun;73(3):601–615. doi: 10.1083/jcb.73.3.601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kilmartin J. V., Wright B., Milstein C. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line. J Cell Biol. 1982 Jun;93(3):576–582. doi: 10.1083/jcb.93.3.576. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Laufer J. S., Bazzicalupo P., Wood W. B. Segregation of developmental potential in early embryos of Caenorhabditis elegans. Cell. 1980 Mar;19(3):569–577. doi: 10.1016/s0092-8674(80)80033-x. [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. Mitchison T. J., Kirschner M. W. Properties of the kinetochore in vitro. II. Microtubule capture and ATP-dependent translocation. J Cell Biol. 1985 Sep;101(3):766–777. doi: 10.1083/jcb.101.3.766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Moore P. B., Ownby C. L., Carraway K. L. Interactions of cytoskeletal elements with the plasma membrane of sarcoma180 ascites tumor cells. Exp Cell Res. 1978 Sep;115(2):331–342. doi: 10.1016/0014-4827(78)90287-2. [DOI] [PubMed] [Google Scholar]
  12. Nicklas R. B., Gordon G. W. The total length of spindle microtubules depends on the number of chromosomes present. J Cell Biol. 1985 Jan;100(1):1–7. doi: 10.1083/jcb.100.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Priess J. R., Hirsh D. I. Caenorhabditis elegans morphogenesis: the role of the cytoskeleton in elongation of the embryo. Dev Biol. 1986 Sep;117(1):156–173. doi: 10.1016/0012-1606(86)90358-1. [DOI] [PubMed] [Google Scholar]
  14. Priess J. R., Thomson J. N. Cellular interactions in early C. elegans embryos. Cell. 1987 Jan 30;48(2):241–250. doi: 10.1016/0092-8674(87)90427-2. [DOI] [PubMed] [Google Scholar]
  15. Roos U. P. Light and electron microscopy of rat kangaroo cells in mitosis. I. Formation and breakdown of the mitotic apparatus. Chromosoma. 1973;40(1):43–82. doi: 10.1007/BF00319836. [DOI] [PubMed] [Google Scholar]
  16. Schatten G., Schatten H., Bestor T. H., Balczon R. Taxol inhibits the nuclear movements during fertilization and induces asters in unfertilized sea urchin eggs. J Cell Biol. 1982 Aug;94(2):455–465. doi: 10.1083/jcb.94.2.455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Sluder G., Rieder C. L. Experimental separation of pronuclei in fertilized sea urchin eggs: chromosomes do not organize a spindle in the absence of centrosomes. J Cell Biol. 1985 Mar;100(3):897–903. doi: 10.1083/jcb.100.3.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Strome S., Wood W. B. Generation of asymmetry and segregation of germ-line granules in early C. elegans embryos. Cell. 1983 Nov;35(1):15–25. doi: 10.1016/0092-8674(83)90203-9. [DOI] [PubMed] [Google Scholar]
  19. Sulston J. E., Horvitz H. R. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol. 1977 Mar;56(1):110–156. doi: 10.1016/0012-1606(77)90158-0. [DOI] [PubMed] [Google Scholar]
  20. Sulston J. E., Schierenberg E., White J. G., Thomson J. N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev Biol. 1983 Nov;100(1):64–119. doi: 10.1016/0012-1606(83)90201-4. [DOI] [PubMed] [Google Scholar]
  21. Sulston J. E., White J. G. Regulation and cell autonomy during postembryonic development of Caenorhabditis elegans. Dev Biol. 1980 Aug;78(2):577–597. doi: 10.1016/0012-1606(80)90353-x. [DOI] [PubMed] [Google Scholar]
  22. White J. G., Amos W. B., Fordham M. An evaluation of confocal versus conventional imaging of biological structures by fluorescence light microscopy. J Cell Biol. 1987 Jul;105(1):41–48. doi: 10.1083/jcb.105.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Wolf N., Priess J., Hirsh D. Segregation of germline granules in early embryos of Caenorhabditis elegans: an electron microscopic analysis. J Embryol Exp Morphol. 1983 Feb;73:297–306. [PubMed] [Google Scholar]
  24. Wolf R. The cytaster, a colchicine-sensitive migration organelle of cleavage nuclei in an insect egg. Dev Biol. 1978 Feb;62(2):464–472. doi: 10.1016/0012-1606(78)90228-2. [DOI] [PubMed] [Google Scholar]

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

RESOURCES