Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1980 Nov 1;87(2):404–414. doi: 10.1083/jcb.87.2.404

Structural basis of motility in the microtubular axostyle: implications for cytoplasmic microtubule structure and function

PMCID: PMC2110753  PMID: 6448863

Abstract

The gross morphology of the protozoan microtubule axostyle of Saccinobaculus ambloaxostylus can now be described in macromolecular detail. The left-handed coil of the axostyle is seen to be dependent upon the asymmetry inherent in the constituent microtubules as expressed by the specific array of linkages between microtubules and by a possible tendency for microtubules to coil into left-handed helices. The laminated sheets of microtubules are not aligned parallel to the long axis of the organelle, but become increasingly tilted off-axis as one descends through the sheets of microtubules from the convex to the concave surface of the axostyle. Fine-structural analysis of the axostyle indicates similarities of the linkages to dynein. The potential loci of the force-generating protein(s) are discussed as well as implications of the axostyle's structure on general microtubule function.

Full Text

The Full Text of this article is available as a PDF (2.1 MB).

Selected References

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

  1. Allen C., Borisy G. G. Structural polarity and directional growth of microtubules of Chlamydomonas flagella. J Mol Biol. 1974 Dec 5;90(2):381–402. doi: 10.1016/0022-2836(74)90381-7. [DOI] [PubMed] [Google Scholar]
  2. Amos L., Klug A. Arrangement of subunits in flagellar microtubules. J Cell Sci. 1974 May;14(3):523–549. doi: 10.1242/jcs.14.3.523. [DOI] [PubMed] [Google Scholar]
  3. Binder L. I., Rosenbaum J. L. The in vitro assembly of flagellar outer doublet tubulin. J Cell Biol. 1978 Nov;79(2 Pt 1):500–515. doi: 10.1083/jcb.79.2.500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bloodgood R. A., Miller K. R. Freeze-fracture of microtubules and bridges in motile axostyles. J Cell Biol. 1974 Sep;62(3):660–671. doi: 10.1083/jcb.62.3.660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Borisy G. G. Polarity of microtubules of the mitotic spindle. J Mol Biol. 1978 Sep 25;124(3):565–570. doi: 10.1016/0022-2836(78)90188-2. [DOI] [PubMed] [Google Scholar]
  6. Burns R. G., Pollard T. D. A dynein-like protein from brain. FEBS Lett. 1974 Apr 1;40(2):274–280. doi: 10.1016/0014-5793(74)80243-7. [DOI] [PubMed] [Google Scholar]
  7. GIBBONS I. R., GRIMSTONE A. V. On flagellar structure in certain flagellates. J Biophys Biochem Cytol. 1960 Jul;7:697–716. doi: 10.1083/jcb.7.4.697. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. GRIMSTONE A. V., CLEVELAND L. R. THE FINE STRUCTURE AND FUNCTION OF THE CONTRACTILE AXOSTYLES OF CERTAIN FLAGELLATES. J Cell Biol. 1965 Mar;24:387–400. doi: 10.1083/jcb.24.3.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gaskin F., Kramer S. B., Cantor C. R., Adelstein R., Shelanski M. L. A dynein-like protein associated with neurotubules. FEBS Lett. 1974 Apr 1;40(2):281–286. doi: 10.1016/0014-5793(74)80244-9. [DOI] [PubMed] [Google Scholar]
  10. Gibbons B. H., Gibbons I. R. Flagellar movement and adenosine triphosphatase activity in sea urchin sperm extracted with triton X-100. J Cell Biol. 1972 Jul;54(1):75–97. doi: 10.1083/jcb.54.1.75. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gibbons B. H., Gibbons I. R. Properties of flagellar "rigor waves" formed by abrupt removal of adenosine triphosphate from actively swimming sea urchin sperm. J Cell Biol. 1974 Dec;63(3):970–985. doi: 10.1083/jcb.63.3.970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gibbons I. R., Fronk E. Some properties of bound and soluble dynein from sea urchin sperm flagella. J Cell Biol. 1972 Aug;54(2):365–381. doi: 10.1083/jcb.54.2.365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Haimo L. T., Telzer B. R., Rosenbaum J. L. Dynein binds to and crossbridges cytoplasmic microtubules. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5759–5763. doi: 10.1073/pnas.76.11.5759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Heuser J. E., Reese T. S., Dennis M. J., Jan Y., Jan L., Evans L. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J Cell Biol. 1979 May;81(2):275–300. doi: 10.1083/jcb.81.2.275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kincaid H. L., Jr, Gibbons B. H., Gibbons I. R. The salt-extractable fraction of dynein from sea urchin sperm flagella: an analysis by gel electrophoresis and by adenosine triphosphatase activity. J Supramol Struct. 1973;1(6):461–470. doi: 10.1002/jss.400010603. [DOI] [PubMed] [Google Scholar]
  16. Linck R. W. Chemical and structural differences between cilia and flagella from the lamellibranch mollusc, Aequipecten irradians. J Cell Sci. 1973 May;12(3):951–981. doi: 10.1242/jcs.12.3.951. [DOI] [PubMed] [Google Scholar]
  17. Margolis R. L., Wilson L., Keifer B. I. Mitotic mechanism based on intrinsic microtubule behaviour. Nature. 1978 Mar 30;272(5652):450–452. doi: 10.1038/272450a0. [DOI] [PubMed] [Google Scholar]
  18. McIntosh J. R., Ogata E. S., Landis S. C. The axostyle of Saccinobaculus. I. Structure of the organism and its microtubule bundle. J Cell Biol. 1973 Feb;56(2):304–323. doi: 10.1083/jcb.56.2.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McIntosh J. R. The axostyle of Saccinobaculus. II. Motion of the microtubule bundle and a structural comparison of straight and bent axostyles. J Cell Biol. 1973 Feb;56(2):324–339. doi: 10.1083/jcb.56.2.324. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miki-Noumura T., Kamiya R. Conformational change in the outer doublet microtubules from sea urchin sperm flagella. J Cell Biol. 1979 May;81(2):355–360. doi: 10.1083/jcb.81.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mooseker M. S., Tilney L. G. Isolation and reactivation of the axostyle. Evidence for a dynein-like ATPase in the axostyle. J Cell Biol. 1973 Jan;56(1):13–26. doi: 10.1083/jcb.56.1.13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Murphy D. B., Hiebsch R. R. Purification of microtubule protein from beef brain and comparison of the assembly requirements for neuronal microtubules isolated from beef and hog. Anal Biochem. 1979 Jul 1;96(1):225–235. doi: 10.1016/0003-2697(79)90577-3. [DOI] [PubMed] [Google Scholar]
  23. Pratt M. M., Otter T., Salmon E. D. Dynein-like Mg2+-ATPase in mitotic spindles isolated from sea urchin embryos (Strongylocentrotus droebachiensis). J Cell Biol. 1980 Sep;86(3):738–745. doi: 10.1083/jcb.86.3.738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pratt M. M. The identification of a dynein ATPase in unfertilized sea urchin eggs. Dev Biol. 1980 Feb;74(2):364–378. doi: 10.1016/0012-1606(80)90438-8. [DOI] [PubMed] [Google Scholar]
  25. Sato H., Ellis G. W., Inoué S. Microtubular origin of mitotic spindle form birefringence. Demonstration of the applicability of Wiener's equation. J Cell Biol. 1975 Dec;67(3):501–517. doi: 10.1083/jcb.67.3.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Takahashi M., Tonomura Y. Binding of 30s dynein with the B-tubule of the outer doublet of axonemes from Tetrahymena pyriformis and adenosine triphosphate-induced dissociation of the complex. J Biochem. 1978 Dec;84(6):1339–1355. doi: 10.1093/oxfordjournals.jbchem.a132256. [DOI] [PubMed] [Google Scholar]
  27. Warner F. D., Mitchell D. R., Perkins C. R. Structural conformation of the ciliary ATPase dynein. J Mol Biol. 1977 Aug 15;114(3):367–384. doi: 10.1016/0022-2836(77)90255-8. [DOI] [PubMed] [Google Scholar]
  28. Warner F. D., Mitchell D. R. Structural conformation of ciliary dynein arms and the generation of sliding forces in Tetrahymena cilia. J Cell Biol. 1978 Feb;76(2):261–277. doi: 10.1083/jcb.76.2.261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Zanetti N. C., Mitchell D. R., Warner F. D. Effects of divalent cations on dynein cross bridging and ciliary microtubule sliding. J Cell Biol. 1979 Mar;80(3):573–588. doi: 10.1083/jcb.80.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Zobel C. R. Effect of solution composition and proteolysis on the conformation of axonemal components. J Cell Biol. 1973 Dec;59(3):573–594. doi: 10.1083/jcb.59.3.573. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES