Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules

Molecular Biology of the Cell

Volumn 21, Issue 2, 2010, Pages 334-344

  Qiang, Liang ^a   Yu, Wenqian ^a   Liu, Mei ^a   Solowska, Joanna M ^a   Baas, Peter W ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; KATANIN; MICROTUBULE PROTEIN; SMALL INTERFERING RNA; SPASTIN; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DISSOCIATION; HIPPOCAMPUS; MICROTUBULE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM;

ADENOSINE TRIPHOSPHATASES; ANIMALS; AXONS; BIOLOGICAL TRANSPORT; CELL SHAPE; FIBROBLAST GROWTH FACTOR 2; HIPPOCAMPUS; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; NEURONS; PHOSPHORYLATION; RATS; TAU PROTEINS;

EID: 75649119687     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-09-0834     Document Type: Article

References (48)

1. Ahmad, F. J., He, Y., Myers, K. A., Hasaka, T. P., Francis, F., Black, M. M., and Baas, P. W. (2006). Effects of dynactin disruption and dynein depletion on axonal microtubules. Traffic 7, 524-537.
2. Ahmad, F. J., Yu, W., McNally, F. J., and Baas, P. W. (1999). An essential role for katanin in severing microtubules in the neuron. J. Cell Biol. 145, 305-315.
3. Aletsee, C., Brors, D., Mlynski, R., Ryan, A. F., and Dazert, S. (2003). Branching of spiral ganglion neurites is induced by focal application of fibroblast growth factor-1. Laryngoscope 113, 791-796.
4. Baas, P. W., Deitch, J. S., Black, M. M., and Banker, G. A. (1988). Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. USA 85, 8335-8339.
5. Baas, P. W., Karabay, A., and Qiang, L. (2005). Microtubules cut and run. Trends Cell Biol. 15, 518-524.
6. Baas, P. W., Vidya Nadar, C., and Myers, K. A. (2006). Axonal transport of microtubules: the long and short of it. Traffic 7, 490-498.
7. Berry, R. W., et al. (2004). Tau epitope display in progressive supranuclear palsy and corticobasal degeneration. J. Neurocytol. 33, 287-295.
8. Binder, L. I., Frankfurter, A., and Rebhun, L. I. (1985). The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
9. Claudiani, P., Riano, E., Errico, A., Andolfi, G., and Rugarli, E. I. (2005). Spastin subcellular localization is regulated through usage of different translation start sites and active export from the nucleus. Exp. Cell Res. 309, 358-369.
10. Connell, J. W., Lindon, C., Luzio, J. P., and Reid, E. (2008). Spastin couples microtubule severing to membrane traffic in completion of cytokinesis and secretion. Traffic 10, 42-56.
11. Dawson, H. N., Ferreira, A., Eyster, M. V., Ghoshal, N., Binder, L. I., and Vitek, M. P. (2001). Inhibition of neuronal maturation in primary hippocampal neurons from tau deficient mice. J. Cell Sci. 114, 1179-1187.
12. Dent, E. W., Barnes, A. M., Tang, F., and Kalil, K. (2004). Netrin-1 and semaphorin 3A promote or inhibit cortical axon branching, respectively, by reorganization of the cytoskeleton. J. Neurosci. 24, 3002-3012.
13. Dent, E. W., Callaway, J. L., Szebenyi, G., Baas, P. W., and Kalil, K. (1999). Reorganization and movement of microtubules in axonal growth cones and developing interstitial branches. J. Neurosci. 19, 8894-8908.
14. Dent, E. W., and Kalil, K. (2001). Axon branching requires interactions between dynamic microtubules and actin filaments. J. Neurosci. 21, 9757-9769.
15. Falnikar, A., and Baas, P.W. (2009). Critical roles for microtubules in axonal development and disease. Results Probl. Cell Differ. 48, 47-64.
16. Hartman, J. J., and Vale, R. D. (1999). Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin. Science 286, 782-785.
17. Hasaka, T. P., Myers, K. A., and Baas, P. W. (2004). Role of actin filaments in the axonal transport of microtubules. J. Neurosci. 24, 11291-11301.
18. He, Y., Francis, F., Myers, K. A., Yu, W., Black, M. M., and Baas, P. W. (2005). Role of cytoplasmic dynein in the axonal transport of microtubules and neurofilaments. J. Cell Biol. 168, 697-703.
19. Heidemann, S. R. (1991). Microtubule polarity determination based on formation of protofilament hooks. Methods Enzymol. 196, 469-477.
20. Joshi, H. C., and Baas, P. W. (1993). A new perspective on microtubules and axon growth. J. Cell Biol. 121, 1191-1196.
21. Karabay, A., Yu, W., Solowska, J. M., Baird, D. H., and Baas, P. W. (2004). Axonal growth is sensitive to the levels of katanin, a protein that severs microtubules. J. Neurosci. 24, 5778-5788.
22. Klimaschewski, L., Nindl, W., Feurle, J., Kavakebi, P., and Kostron, H. (2004). Basic fibroblast growth factor isoforms promote axonal elongation and branching of adult sensory neurons in vitro. Neuroscience 126, 347-353.
23. Kornack, D. R., and Giger, R. J. (2005). Probing microtubule +TIPs: regulation of axon branching. Curr. Opin. Neurobiol. 15, 58-66.
24. Lee, H. H., Jan, L. Y., and Jan, Y. N. (2009). Drosophila IKK-related kinase Ik2 and Katanin p60-like 1 regulate dendrite pruning of sensory neuron during metamorphosis. Proc. Natl. Acad. Sci. USA 106, 6363-6368.
25. Mancuso, G., and Rugarli, E. I. (2008). A cryptic promoter in the first exon of the SPG4 gene directs the synthesis of the 60-kDa spastin isoform. BMC Biol. 6, 31.
26. Mandell, J. W., and Banker, G. A. (1996). A spatial gradient of tau protein phosphorylation in nascent axons. J. Neurosci. 16, 5727-5740.
27. McNally, K.P., Bazirgan, O.A., and McNally, F.J. (2000). Two domains of p80 katanin regulate microtubule severing and spindle pole targeting by p60 katanin. J. Cell Sci. 113(Pt 9), 1623-1633.
28. Myers, K. A., and Baas, P. W. (2007). Kinesin-5 regulates the growth of the axon by acting as a brake on its microtubule array. J. Cell Biol. 178, 1081-1091.
29. Myers, K. A., Tint, I., Nadar, C. V., He, Y., Black, M. M., and Baas, P. W. (2006). Antagonistic forces generated by cytoplasmic dynein and myosin-II during growth cone turning and axonal retraction. Traffic 7, 1333-1351.
30. Nadar, V. C., Ketschek, A., Myers, K. A., Gallo, G., and Baas, P. W. (2008). Kinesin-5 is essential for growth-cone turning. Curr. Biol. 18, 1972-1977.
31. Papasozomenos, S. C., and Binder, L. I. (1987). Phosphorylation determines two distinct species of Tau in the central nervous system. Cell Motil. Cytoskelet. 8, 210-226.
32. Pujol, F., Kitabgi, P., and Boudin, H. (2005). The chemokine SDF-1 differentially regulates axonal elongation and branching in hippocampal neurons. J. Cell Sci. 118, 1071-1080.
33. Qiang, L., Yu, W., Andreadis, A., Luo, M., and Baas, P. W. (2006). Tau protects microtubules in the axon from severing by katanin. J. Neurosci. 26, 3120-3129.
34. Riano, E., et al. (2009). Pleiotropic effects of spastin on neurite growth depending on expression levels. J. Neurochem. 108, 1277-1288.
35. Solowska, J. M., Morfini, G., Falnikar, A., Himes, B. T., Brady, S. T., Huang, D., and Baas, P. W. (2008). Quantitative and functional analyses of spastin in the nervous system: implications for hereditary spastic paraplegia. J. Neurosci. 28, 2147-2157.
36. Stepanova, T., Slemmer, J., Hoogenraad, C. C., Lansbergen, G., Dortland, B., De Zeeuw, C. I., Grosveld, F., van Cappellen, G., Akhmanova, A., and Galjart, N. (2003). Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655-2664.
37. Szebenyi, G., Dent, E. W., Callaway, J. L., Seys, C., Lueth, H., and Kalil, K. (2001). Fibroblast growth factor-2 promotes axon branching of cortical neurons by influencing morphology and behavior of the primary growth cone. J. Neurosci. 21, 3932-3941.
38. Tarrade, A., et al. (2006). A mutation of spastin is responsible for swellings and impairment of transport in a region of axon characterized by changes in microtubule composition. Hum. Mol. Genet. 15, 3544-3558.
39. Wang, K. H., Brose, K., Arnott, D., Kidd, T., Goodman, C. S., Henzel, W., and Tessier-Lavigne, M. (1999). Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching. Cell 96, 771-784.
40. Wang, L., and Brown, A. (2002). Rapid movement of microtubules in axons. Curr. Biol. 12, 1496-1501.
41. Wu, X., Xiang, X., and Hammer, J. A., 3rd (2006). Motor proteins at the microtubule plus-end. Trends Cell Biol. 16, 135-143.
42. Yu, W., Ahmad, F. J., and Baas, P. W. (1994). Microtubule fragmentation and partitioning in the axon during collateral branch formation. J. Neurosci. 14, 5872-5884.
43. Yu, W., Qiang, L., and Baas, P. W. (2007). Microtubule-severing in the axon: implications for development, disease, and regeneration after injury. J. Environ. Biomed. 1, 1-7.
44. Yu, W., Qiang, L., Solowska, J. M., Karabay, A., Korulu, S., and Baas, P. W. (2008). The microtubule-severing proteins spastin and katanin participate differently in the formation of axonal branches. Mol. Biol. Cell 19, 1485-1498.
45. Yu, W., Solowska, J. M., Qiang, L., Karabay, A., Baird, D., and Baas, P. W. (2005). Regulation of microtubule severing by katanin subunits during neuronal development. J. Neurosci. 25, 5573-5583.
46. Zakharenko, S., and Popov, S. (1998). Dynamics of axonal microtubules regulate the topology of new membrane insertion into the growing neurites. J. Cell Biol. 143, 1077-1086.
47. Zhang, D., Rogers, G. C., Buster, D. W., and Sharp, D. J. (2007). Three microtubule severing enzymes contribute to the "Pacman-flux" machinery that moves chromosomes. J. Cell Biol. 177, 231-242.
48. Zheng, Y., Wildonger, J., Ye, B., Zhang, Y., Kita, A., Younger, S. H., Zimmerman, S., Jan, L. Y., and Jan, Y. N. (2008). Dynein is required for polarized dendritic transport and uniform microtubule orientation in axons. Nat. Cell Biol. 10, 1172-1180.