Abstract
Efforts to observe the slow axonal transport of cytoskeletal polymers during the past decade have yielded conflicting results, and this has generated considerable controversy. The movement of neurofilaments has now been seen, and it is rapid, infrequent and highly asynchronous. This motile behaviour could explain why slow axonal transport has eluded observation for so long.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$189.00 per year
only $15.75 per issue
Buy this article
- Purchase on Springer Link
- Instant access to full article PDF
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Lasek, R. J., Garner, J. A. & Brady, S. T. Axonal transport of the cytoplasmic matrix. J. Cell Biol. 99, S212–S221 (1984).
Hirokawa, N. Kinesin and dynein superfamily proteins and the mechanism of organelle transport . Science 279, 519–526 (1998).
Lim, S.-S., Sammak, P. J. & Borisy, G. G. Progressive and spatially differentiated stability of microtubules in developing neuronal cells. J. Cell Biol. 109, 253–263 (1989).
Lim, S.-S., Edson, K. J., Letourneau, P. C. & Borisy, G. G. A test of microtubule translocation during neurite elongation. J. Cell Biol. 111, 123–130 (1990).
Okabe, S. & Hirokawa, N. Turnover of fluorescently labelled tubulin and actin in the axon. Nature 343, 479–482 (1990).
Okabe, S., Miyasaka, H. & Hirokawa, N. Dynamics of the neuronal intermediate filaments. J. Cell Biol. 121, 375–386 (1993).
Takeda, S., Okabe, S., Funakoshi, T. & Hirokawa, N. Differential dynamics of neurofilament-H protein and neurofilament-L protein in neurons . J. Cell Biol. 127, 173– 185 (1994).
Sabry, J., O'Connor, T. P. & Kirschner, M. W. Axonal transport of tubulin in Ti1 pioneer neurons in situ. Neuron 14, 1247– 1256 (1995).
Takeda, S., Funakoshi, T. & Hirokawa, N. Tubulin dynamics in neuronal axons of living zebrafish embryos. Neuron 14, 1257– 1264 (1995).
Reinsch, S. S., Mitchison, T. J. & Kirschner, M. W. Microtubule polymer assembly and transport during axonal elongation. J. Cell Biol. 115, 365 –379 (1991).
Okabe, S. & Hirokawa, N. Differential behavior of photoactivated microtubules in growing axons of mouse and frog neurons. J. Cell Biol. 117, 105–120 ( 1992).
Okabe, S. & Hirokawa, N. Do photobleached fluorescent microtubules move? Re-evaluation of fluorescence laser photobleaching both in vitro and in growing Xenopus axons. J. Cell Biol. 120 , 1177–1186 (1993).
Chang, S. H., Rodionov, V. I., Borisy, G. G. & Popov, S. V. Transport and turnover of microtubules in frog neurons depend on the pattern of axonal growth. J. Neurosci. 18, 821– 829 (1998).
Wang, L., Ho, C.-L., Sun, D., Liem, R. K. H. & Brown, A. Rapid movement of axonal neurofilaments interrupted by prolonged pauses. Nature Cell Biol. 2, 137–141 (2000).
Roy, S. et al. Neurofilaments are transported rapidly but intermittently in axons: implications for slow axonal transport. J. Neurosci. 20, 6849–6861 (2000).
Lasek, R. J., Paggi, P. & Katz, M. J. Slow axonal transport mechanisms move neurofilaments relentlessly in mouse optic axons. J. Cell Biol. 117, 607–616 (1992).
Nixon, R. A. & Logvinenko, K. B. Multiple fates of newly synthesized neurofilament proteins: Evidence for a stationary neurofilament network distributed non-uniformly along axons of retinal ganglion cells. J. Cell Biol. 102, 647–659 ( 1986).
Nixon, R. A. Dynamic behavior and organization of cytoskeletal proteins in neurons: reconciling old and new findings. Bioessays 20, 798– 807 (1998).
Lasek, R. J., Paggi, P. & Katz, M. J. The maximum rate of neurofilament transport in axons: a view of molecular transport mechanisms continuously engaged. Brain Res. 616, 58–64 ( 1993).
Black, M. M., Keyser, P. & Sobel, E. Interval between the synthesis and assembly of cytoskeletal proteins in cultured neurons. J. Neurosci. 6, 1004–1012 (1986).
Baas, P. W. & Brown, A. Slow axonal transport: the polymer transport model. Trends Cell Biol. 7, 380 –384 (1997).
Hirokawa, N., Terada, S., Funakoshi, T. & Takeda, S. Slow axonal transport: the subunit transport model. Trends Cell Biol. 7, 384–388 ( 1997).
Terasaki, M., Schmidek, A., Galbraith, J. A., Gallant, P. E. & Reese, T. S. Transport of cytoskeletal elements in the squid giant axon. Proc. Natl Acad. Sci. USA 92, 11500–11503 (1995).
Ahmad, F. J. & Baas, P. W. Microtubules released from the neuronal centrosome are transported into the axon. J. Cell Sci. 108, 2761–2769 (1995).
Yu, W., Schwei, M. J. & Baas, P. W. Microtubule transport and assembly during axon growth . J. Cell Biol. 133, 151– 157 (1996).
Slaughter, T., Wang, J. & Black, M. M. Microtubule transport from the cell body into the axons of growing neurons. J. Neurosci. 17, 5807 –5819 (1997).
Ahmad, F. J., Echeverri, C. J., Vallee, R. B. & Baas, P. W. Cytoplasmic dynein and dynactin are required for the transport of microtubules into the axon. J. Cell Biol. 140, 391– 401 (1998).
Galbraith, J. A., Reese, T. S., Schlief, M. L. & Gallant, P. E. Slow transport of unpolymerized tubulin and polymerized neurofilament in the squid giant axon. Proc. Natl Acad. Sci. USA 96, 11589–11594 (1999).
Terada, S., Nakata, T., Peterson, A. C. & Hirokawa, N. Visualization of slow axonal transport in vivo. Science 273, 784–788 ( 1996).
Funakoshi, T., Takeda, S. & Hirokawa, N. Active transport of photoactivated tubulin molecules in growing axons revealed by new electron microscopic analyses. J. Cell Biol. 133, 1347–1354 (1996).
Miller, K. W. & Joshi, H. C. Tubulin transport in neurons. J. Cell Biol. 133, 1355–1366 (1996).
Yabe, J. T., Pimenta, A. & Shea, T. B. Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J. Cell Sci. 112, 3799–3814 (1999).
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. 110 , 1089–1095 (1990).
Keating, T. J., Peloquin, J. G., Rodionov, V. I., Momcilovic, D. & Borisy, G. G. Microtubule release from the centrosome . Proc. Natl Acad. Sci. USA 94, 5078– 5083 (1997).
Dent, E. W., Callaway, J. L., Szebenyi, G., Baas, P. W. & Kalil, K. Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J. Neurosci. 19, 8894–8908 (1999).
Chang, S., Svitkina, T. M., Borisy, G. G. & Popov, S. V. Speckle microscopic evaluation of microtubule transport in growing nerve processes . Nature Cell Biol. 1, 399– 403 (1999).
Shah, J. V., Flanagan, L. A., Janmey, P. A. & Leterrier, J.-F. Bidirectional translocation of neurofilaments along microtubules mediated in part by dynein/dynactin. Mol. Biol. Cell (In the press).
Prahlad, V., Yoon, M., Moir, R. D., Vale, R. D. & Goldman, R. D. Rapid movements of vimentin on microtubule tracks: Kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 143, 159–170 (1998).
Glass, J. D. & Griffin, J. W. Retrograde transport of radiolabeled cytoskeletal proteins in transected nerves. J. Neurosci. 14, 3915–3921 (1994).
Koehnle, T. J. & Brown, A. Slow axonal transport of neurofilament protein in cultured neurons. J. Cell Biol. 144, 447–458 (1999).
Susalka, S. J., Hancock, W. O. & Pfister, K. K. Distinct cytoplasmic dynein complexes are transported by different mechanisms in axons. Biochim. Biophys. Acta 1496, 76–88 (2000).
Yabe, J. T., Jung, C. W., Chan, W. K. H. & Shea, T. B. Phospho-dependent association of neurofilament proteins with kinesin in situ. Cell Motil. Cytoskeleton 45, 249 –262 (2000).
Elluru, R. G., Bloom, G. S. & Brady, S. T. Fast axonal transport of kinesin in the rat visual system: Functionality of kinesin heavy chain isoforms. Mol. Biol. Cell 6, 21–40 ( 1995).
Dahlstrom, A. B., Czernik, A. J. & Li, J. Y. Organelles in fast axonal transport — what molecules do they carry in anterograde vs retrograde directions, as observed in mammalian systems. Mol. Neurobiol. 6, 157–177 (1992).
Acknowledgements
The author thanks Ray Lasek and Peter Baas for stimulating discussions.
Author information
Authors and Affiliations
Related links
Rights and permissions
About this article
Cite this article
Brown, A. Slow axonal transport: stop and go traffic in the axon. Nat Rev Mol Cell Biol 1, 153–156 (2000). https://doi.org/10.1038/35040102
Issue Date:
DOI: https://doi.org/10.1038/35040102
This article is cited by
-
Quantitative tracking of trans-synaptic nose-to-brain transport of nanoparticles and its modulation by odor, aging, and Parkinson’s disease
Nano Research (2023)
-
Biomolecular condensates undergo a generic shear-mediated liquid-to-solid transition
Nature Nanotechnology (2020)
-
Stochastic Hybrid Systems in Cellular Neuroscience
The Journal of Mathematical Neuroscience (2018)
-
Neurite elongation is highly correlated with bulk forward translocation of microtubules
Scientific Reports (2017)
-
Squid Giant Axon Contains Neurofilament Protein mRNA but does not Synthesize Neurofilament Proteins
Cellular and Molecular Neurobiology (2017)