Microtubules and axonal growth

Current Opinion in Cell Biology

Volumn 9, Issue 1, 1997, Pages 29-36

  Baas, Peter W ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TUBULIN;

CENTROSOME; MICROTUBULE; MICROTUBULE ASSEMBLY; NERVE FIBER GROWTH; PRIORITY JOURNAL; PROTEIN TRANSPORT; REVIEW;

EID: 0031048886     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(97)80148-2     Document Type: Article

References (32)

1. 1. Baas PW, Yu W: A composite model for establishing the microtubule arrays of axons and dendrites. Mol Neurobiol 1996, 12:145-161.
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10. 10. Sabry J, O'Connor TP, Kirschner MW: Axonal transport of tubulin in Ti1 pioneer neurons in situ. Neuron 1995, 14:1247-1256. A photobleach study of axons of living grasshoppers reveals no evidence for movement of a marked microtubule array. An insightful analysis of the axon lengths and rates of axonal growth at which diffusion would fail to deliver sufficient tubulin subunits to support axonal growth indicates that diffusion would in fact be sufficient in all of the axons studied to date in which photobleach or photoactivation has failed to reveal microtubule movement.
11. 11. Miller KW, Joshi HC: Tubulin transport in neurons. J Cell Biol 1996, 133:1355-1366.
12. 12. Terasaki M, Schmidek A, Golbraith JA, Gallant PE, Reese TS: Transport of cytoskeletal elements in the squid giant axon. Proc Natl Acad Sci USA 1995, 92:11500-11503. Fluorescent, stable microtubule fragments introduced into squid giant axons are observed to move anterogradely at rates similar to those previously reported for tubulin transport down the axon in kinetic analyses. Although more work needs to be done on this new experimental regime, these first efforts provide strong support for the view that tubulin is transported down the axon as polymers.
13. 13. Bamburg JR, Bray D, Chapman K: Assembly of microtubules at the tip of growing axons. Nature 1986, 321:788-790.
14. 14. Yu W, Baas PW: The growth of the axon is not dependent upon the net assembly of microtubules at its distal tip. J Neurosci 1995, 15:6827-6833. Revisitation of the work of Bamburg and colleagues [13] in which antimicrotubule drugs were applied topically to the distal tip of the axon. It is shown that the drug treatments used in the original study stopped axonal growth by inducing large-scale microtubule disassembly, whereas drug treatments that induce lower levels of microtubule diassembly do not inhibit axonal growth.
15. 15. Tanaka E, Ho T, Kirschner MW: The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 1995, 128:139-155. Pharmacological inhibition of microtubule dynamics is shown to compromise the capacity of the axonal tip to navigate properly.
16. 16. Rochlin MW, Wickline KM, Bridgeman PC: Microtubule stability decreases axon elongation but not axoplasmic production. J Neurosci 1996, 16:3236-3248. A pharmacological treatment is shown to suppress dynamic instability of microtubules while not suppressing the increase in microtubule polymer mass that occurs during axonal growth. Under these conditions, the axon is shown to grow more slowly.
17. 17. Baas PW, Ahmad FJ: The transport properties of axonal microtubules establish their polarity orientation. J Cell Biol 1993, 120:1427-1437.
18. 18. Ahmad FJ, Baas PW: Microtubules released from the neuronal centrosome are transported into the axon. J Cell Sci 1995, 108:2761-2769. The results of pharmacological studies provide support for the proposal that microtubules released from the centrosome are transported first to the periphery of the neuronal cell body and then into the axon.
19. 19. Wilson L, Jordan MA: Pharmacological probes of microtubule function. In Microtubules. Edited by Hyams JS, Lloyd CW. New York: Wiley-Liss; 1994:59-83.
20. 20. Li Y, Black MM: Microtubule assembly and turnover in growing axons. J Neurosci 1996, 16:531-544. Injection of biotinylated tubulin into cultured neurons permits the determination of rates of subunit turnover. Both stable and labile polymer are identified, and it is confirmed that the former and latter correspond to polymer that is rich in detyrosinated and tyrosinated α-tubulin, respectively. These analyses also document the movement of the injected free tubulin down the axon, and show that the rate of movement and concentrations of injected tubulin along the axon are consistent with diffusion and not active transport of free tubulin subunits.
21. 21. Okabe S, Hirokawa N: Microtubule dynamics in nerve cells: analysis using microinjection of biotinylated tubulin into PC12 cells. J Cell Biol 1988, 107:651-664.
22. 22. Yu W, Schwei MJ, Baas PW: Microtubule transport and assembly during axon growth. J Cell Biol 1996, 133:151-157. A high-resolution approach is used to reveal that microtubule transport and assembly both contribute to axonal growth.
23. 23. Baas PW, Joshi HC: Gamma-tubulin distribution in the neuron: implications for the origins of neuritic microtubules. J Cell Biol 1992, 119:171-178.
24. 24. Baas PW: The neuronal centrosome as a generator of microtubules for the axon. Curr Top Dev Biol 1996, 33:281-298.
25. 25. Moritz M, Braunfeld MB, Sedat JW, Alberts B, Agard DA: Microtubule nucleation by γ-tubulin-containing rings in the centrosome. Nature 1995, 378:638-640. Immunoelectron microscopy of isolated centrosomes reveals the presence of a γ-tubulin-containing ring structure that appears at the ends of microtubules embedded within the centrosome.
26. 26. Zheng Y, Wong ML, Alberts B, Mitchison T: Nucleation of microtubule assembly by a γ-tubulin-containing ring complex. Nature 1995, 378:578-583. High-resolution electron microscopic analyses reveal that a complex of proteins in the centrosome that contains γ-tubulin has an open ring structure. The complex acts as a microtubule-nucleating structure that constrains the lattice structure of the microtubules that it nucleates.
27. 27. McNally FJ, Okawa K, Iwamatsu A, Vale RD: Katanin, the microtubule-severing ATPase, is concentrated at centrosomes. J Cell Sci 1996, 109:561-567. Katanin, a protein with documented microtubule-severing properties, is shown to localize to a region just outside of the pericentriolar material in sea urchin cells. This localization occurs only when microtubules are present at the centrosome, providing an attractive means by which a centrosome might assemble a burst of microtubules for subsequent release.
28. 28. Wang J, Yu W, Baas PW, Black MM: Microtubule assembly in growing dendrites. J Neurosci 1996, 16:6038-6051. Biotinylated tubulin was introduced into cultured sympathetic neurons that had already elaborated dendrites. Sites of incorporation of the tubulin included the plus ends of microtubules of both orientations in the dendrite. No other nucleating structures in the dendrite were observed. In some injected cells, a burst of microtubules rapidly assembled from a discrete site in the cell body, presumably the centrosome, during the first few minutes after injection.
29. 29. Heald R, Tournebize R, Blank T, Sandaltzopoulos R, Becker P, Hyman A, Karsenti E: Self-organization of microtubules into bipolar spindles around artificial chromosomes in Xenopus egg extracts. Nature 1996, 382:420-425. An in vitro preparation is used to show that microtubules can organize into a bipolar spindle in the presence of a cytoplasmic extract and chromatin without chromosomes or a centrosome. Inactivation or depletion of cytoplasmic dynein from the extract inhibits spindle formation, indicating that motor-driven transport is essential for the microtubules to organize into this formation.
30. 30. Sharp DJ, Kuriyama R, Baas PW: Expression of a kinesin related protein induces Sf9 cells to form dendrite-like processes with nonuniform microtubule polarity orientation. J Neurosci 1996, 16:4370-4375. Expression of the mitotic motor protein CHO1/MKLP1 induces normally round insect ovarian Sf9 cells to extend microtubule-rich processes. The processes have a thick tapering morphology similar to that of neuronal dendrites and establish a pattern of nonuniform microtubule polarity by the same sequence of events that occurs during dendritic development.
31. 31. Dillman JF III, Dabney LP, Pfister KK: Cytoplasmic dynein is associated with slow axonal transport. Proc Natl Acad Sci USA 1996, 93:141-144. Almost 80% of the cytoplasmic dynein that is transported anterogradely down the axon is found to be transported at the slow rate of cytoskeletal elements rather than the fast rate of membranous organelles. A model is proposed in which actin filaments provide the substrate and dynein provides the motor for the active transport of microtubules down the axon.
32. 32. Dillman JF III, Dabney LP, Karki S, Paschal BM, Holzbaur ELF, Pfister KK: Functional analysis of dynactin and cytoplasmic dynein in slow axonal transport. J Neurosci 1996, 16:6742-6752. Like cytoplasmic dynein, most of the dynactin that is transported down the axon is found to be transported at rates similar to that of actin. Pfister's model is extended to include dynactin as an intermediate between actin filaments and the dynein that translocates microtubules down the axon.