Axonal Transport and the Neuronal Cytoskeleton

Abstract

The neuronal cytoskeleton is a system of highly organized polymers that provide architectural support for axons and dendrites, and also provide railways for the transport of various classes of cytoplasmic constituents. Molecular motor proteins use the energy derived from adenosine triphosphate hydrolysis for the transport of organelles along the cytoskeletal polymers and for the transport of the polymers themselves. Axons can traverse exceeding long distances in the body, and hence require sophisticated mechanisms of axonal transport in both the anterograde and the retrograde direction.

Keywords: axon; dendrite; neuron; axonal transport; microtubule; microfilament; motor protein

Figure 1.

Structure of cytoskeletal polymers and molecular motors. One example of each member of the motor families is shown. Other family members vary in their structure.

Figure 2.

Current theories on the mechanisms of organelle transport along microtubules and microfilaments within axons. Organelles that engage cytoplasmic dynein are transported towards minus ends of microtubules in retrograde fashion (from the distal end of axon towards the cell body), while organelles that engage most kinesins are transported towards plus ends of microtubules in anterograde fashion (from the cell body towards the distal end of the axon). Organelles that engage myosins are transported towards plus ends of microfilaments. In general, microtubules act as longer range ‘highways’ for organelle transport, while microfilaments act as shorter ‘streets’.

Figure 3.

Current theories on the mechanisms of cytoskeletal polymer transport within the axon. Microtubules are nucleated by gamma tubulin and released from the centrosome by katanin within the cell body of the neuron, and are then transported by cytoplasmic dynein into the axons with the plus end of the microtubule leading. Most of the microtubule transport occurs in anterograde fashion. There is also evidence that some microtubule transport occurs in retrograde fashion. Kinesin‐related motors may contribute to the transport microtubules in one direction or both. Neurofilaments are conveyed either by their association with microtubules or along the microtubules in a similar fashion to membranous organelles. Microfilaments are transported by myosins, and generate forces by pushing against cortical structures associated with sites where the axon adheres to the extracellular matrix.

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References

Ahmad FJ, Echeverri CJ, Vallee RB and Baas PW (1998) Cytoplasmic dynein and dynactin are required for microtubule transport into the axon. Journal of Cell Biology 140: 391–402.

Arimura N, Menager C, Fukata Y and Kaibuchi N (2004) Role of CRMP‐2 in neuronal polarity. Journal of Neurobiology 58: 34–47.

Baas PW (1999) Microtubules and neuronal polarity: lessons from mitosis. Neuron 22: 23–31.

Baas PW and Buster DW (2004) Slow axonal transport and the genesis of neuronal morphology. Journal of Neurobiology 58: 3–17.

Baas PW, Deitch JS, Black MM and Banker GA (1988) Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proceedings of the National Academy of Sciences of the USA 85: 8335–8339.

Banker GA and Waxman AB (1988) Hippocampal neurons generate natural shapes in cell culture. In: Lasek RJ and Black MM (eds) Intrinsic Determinants of Neuronal Form and Function, pp. 61–82. New York: Alan R Liss.

Brown A (2003) Axonal transport of membranous and non‐membranous cargoes: a unified perspective. Journal of Cell Biology 160: 817–821.

Campbell DS and Holt CE (2001) Chemotropic responses of retinal growth cones mediated by rapid local protein synthesis and degradation. Neuron 32: 1013–1026.

Langford GM (1995) Actin‐ and microtubule‐dependent organelle motors: interrelationships between the two motility systems. Current Opinion in Cell Biology 7: 82–88.

Ledesma MD and Dotti CG (2003) Membrane and cytoskeleton dynamics during axonal elongation and stabilization. Internation Review in Cytology 227: 183–219.

Mimori‐Kiyosue Y and Tsukita S (2003) ‘Search‐and‐capture’ of microtubules through plus‐end‐binding proteins (+TIPs). Journal of Biochemistry 134: 321–326.

Sarmiere PD and Bamburg JR (2004) Regulation of the neuronal actin cytoskeleton by ADF/cofilin. Journal of Neurobiology 58: 103–117.

Sharp DJ, Yu W, Ferhat L et al. (1997) Identification of a motor protein essential for dendritic differentiation. Journal of Cell Biology 138: 833–843.

Wang L and Brown A (2001) Rapid intermittent movement of axonal neurofilaments observed by fluorescence photobleaching. Molecular Biology of the Cell 12: 3257–3267.

Wang L and Brown A (2002) Rapid movement of microtubules in axons. Current Biology 12: 1496–1501.

Weiss PA and Hiscoe HB (1948) Experiments on the mechanism of nerve growth. Journal of Experimental Zoology 107: 315–396.

Further Reading

Brady S, Coleman DR and Brophy P (2002) Subcellular organization of the nervous system: organelles and their function. In: Zigmond MJ, Bloom FE, Landis SC, Roberts JL and Squire LR (eds) Fundamental Neuroscience, pp. 79–115. London: Academic Press

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How to Cite close
Baas, PW, and Karabay, A(Sep 2005) Axonal Transport and the Neuronal Cytoskeleton. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1038/npg.els.0004050]