Skip to main content
PMC home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1987 Sep 1;105(3):1267–1271. doi: 10.1083/jcb.105.3.1267

Dynamic shape changes of cytoplasmic organelles translocating along microtubules

PMCID: PMC2114788  PMID: 3654751

Abstract

Transient shape changes of organelles translocating along microtubules are directly visualized in thinly spread cytoplasmic processes of the marine foraminifer. Allogromia laticollaris, by a combination of high- resolution video-enhanced microscopy and fast-freezing electron microscopy. The interacting side of the organelle flattens upon binding to a microtubule, as if to maximize contact with it. Organelles typically assume a teardrop shape while moving, as if they were dragged through a viscous medium. Associated microtubules bend around attachments of the teardrop-shaped organelles, suggesting that they too are acted on by the forces deforming the organelles. An 18-nm gap between the organelles and the microtubules is periodically bridged by 10-nm-thick cross-bridge structures that may be responsible for the binding and motive forces deforming organelles and microtubules.

Full Text

The Full Text of this article is available as a PDF (1.7 MB).

Selected References

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

  1. Adams R. J., Pollard T. D. Propulsion of organelles isolated from Acanthamoeba along actin filaments by myosin-I. Nature. 1986 Aug 21;322(6081):754–756. doi: 10.1038/322754a0. [DOI] [PubMed] [Google Scholar]
  2. Allen R. D., Weiss D. G., Hayden J. H., Brown D. T., Fujiwake H., Simpson M. Gliding movement of and bidirectional transport along single native microtubules from squid axoplasm: evidence for an active role of microtubules in cytoplasmic transport. J Cell Biol. 1985 May;100(5):1736–1752. doi: 10.1083/jcb.100.5.1736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bowser S. S., Israel H. A., McGee-Russell S. M., Rieder C. L. Surface transport properties of reticulopodia: do intracellular and extracellular motility share a common mechanism? Cell Biol Int Rep. 1984 Dec;8(12):1051–1063. doi: 10.1016/0309-1651(84)90092-4. [DOI] [PubMed] [Google Scholar]
  4. Bridgman P. C., Kachar B., Reese T. S. The structure of cytoplasm in directly frozen cultured cells. II. Cytoplasmic domains associated with organelle movements. J Cell Biol. 1986 Apr;102(4):1510–1521. doi: 10.1083/jcb.102.4.1510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bridgman P. C., Reese T. S. The structure of cytoplasm in directly frozen cultured cells. I. Filamentous meshworks and the cytoplasmic ground substance. J Cell Biol. 1984 Nov;99(5):1655–1668. doi: 10.1083/jcb.99.5.1655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dentler W. L., Suprenant K. A. Isolation of microtubule-secretory granule complexes from the anglerfish endocrine pancreas. Ann N Y Acad Sci. 1986;466:813–831. doi: 10.1111/j.1749-6632.1986.tb38465.x. [DOI] [PubMed] [Google Scholar]
  7. Forman D. S., Brown K. J., Promersberger M. W., Adelman M. R. Nucleotide specificity for reactivation of organelle movements in permeabilized axons. Cell Motil. 1984;4(2):121–128. doi: 10.1002/cm.970040205. [DOI] [PubMed] [Google Scholar]
  8. Gilbert S. P., Allen R. D., Sloboda R. D. Translocation of vesicles from squid axoplasm on flagellar microtubules. Nature. 1985 May 16;315(6016):245–248. doi: 10.1038/315245a0. [DOI] [PubMed] [Google Scholar]
  9. Hayden J. H., Allen R. D. Detection of single microtubules in living cells: particle transport can occur in both directions along the same microtubule. J Cell Biol. 1984 Nov;99(5):1785–1793. doi: 10.1083/jcb.99.5.1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. 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]
  11. Inoué S. Video image processing greatly enhances contrast, quality, and speed in polarization-based microscopy. J Cell Biol. 1981 May;89(2):346–356. doi: 10.1083/jcb.89.2.346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kachar B. Direct visualization of organelle movement along actin filaments dissociated from characean algae. Science. 1985 Mar 15;227(4692):1355–1357. doi: 10.1126/science.4038817. [DOI] [PubMed] [Google Scholar]
  13. Koonce M. P., Schliwa M. Bidirectional organelle transport can occur in cell processes that contain single microtubules. J Cell Biol. 1985 Jan;100(1):322–326. doi: 10.1083/jcb.100.1.322. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lasek R. J., Brady S. T. Attachment of transported vesicles to microtubules in axoplasm is facilitated by AMP-PNP. Nature. 1985 Aug 15;316(6029):645–647. doi: 10.1038/316645a0. [DOI] [PubMed] [Google Scholar]
  15. Martz D., Lasek R. J., Brady S. T., Allen R. D. Mitochondrial motility in axons: membranous organelles may interact with the force generating system through multiple surface binding sites. Cell Motil. 1984;4(2):89–101. doi: 10.1002/cm.970040203. [DOI] [PubMed] [Google Scholar]
  16. Miller R. H., Lasek R. J. Cross-bridges mediate anterograde and retrograde vesicle transport along microtubules in squid axoplasm. J Cell Biol. 1985 Dec;101(6):2181–2193. doi: 10.1083/jcb.101.6.2181. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Rebhun L. I. Polarized intracellular particle transport: saltatory movements and cytoplasmic streaming. Int Rev Cytol. 1972;32:93–137. doi: 10.1016/s0074-7696(08)60339-3. [DOI] [PubMed] [Google Scholar]
  18. Schnapp B. J., Vale R. D., Sheetz M. P., Reese T. S. Single microtubules from squid axoplasm support bidirectional movement of organelles. Cell. 1985 Feb;40(2):455–462. doi: 10.1016/0092-8674(85)90160-6. [DOI] [PubMed] [Google Scholar]
  19. Sheetz M. P., Chasan R., Spudich J. A. ATP-dependent movement of myosin in vitro: characterization of a quantitative assay. J Cell Biol. 1984 Nov;99(5):1867–1871. doi: 10.1083/jcb.99.5.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Smith D. S., Järlfors U., Cayer M. L. Structural cross-bridges between microtubules and mitochondria in central axons of an insect (Periplaneta americana). J Cell Sci. 1977;27:255–272. doi: 10.1242/jcs.27.1.255. [DOI] [PubMed] [Google Scholar]
  21. Travis J. L., Allen R. D. Studies on the motility of the foraminifera. I. Ultrastructure of the reticulopodial network of Allogromia laticollaris (Arnold). J Cell Biol. 1981 Jul;90(1):211–221. doi: 10.1083/jcb.90.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Travis J. L., Kenealy J. F., Allen R. D. Studies on the motility of the foraminifera. II. The dynamic microtubular cytoskeleton of the reticulopodial network of Allogromia laticollaris. J Cell Biol. 1983 Dec;97(6):1668–1676. doi: 10.1083/jcb.97.6.1668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Vale R. D., Reese T. S., Sheetz M. P. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell. 1985 Aug;42(1):39–50. doi: 10.1016/s0092-8674(85)80099-4. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Vale R. D., Schnapp B. J., Mitchison T., Steuer E., Reese T. S., Sheetz M. P. Different axoplasmic proteins generate movement in opposite directions along microtubules in vitro. Cell. 1985 Dec;43(3 Pt 2):623–632. doi: 10.1016/0092-8674(85)90234-x. [DOI] [PubMed] [Google Scholar]

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

RESOURCES