Posttranslational modifications of tubulin and the polarized transport of kinesin-1 in neurons

Molecular Biology of the Cell

Volumn 21, Issue 4, 2010, Pages 572-583

  Hammond, Jennetta W ^a   Huang, Chun Fang ^b   Kaech, Stefanie ^b   Jacobson, Catherine ^b,c   Banker, Gary ^b   Verhey, Kristen J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; KINESIN 1; PACLITAXEL; TUBULIN;

ACETYLATION; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; MICROTUBULE; MOTOR DEVELOPMENT; MOUSE; NERVE CELL; NERVE FIBER; NERVE GROWTH; NEURITE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN STABILITY; PROTEIN TRANSPORT; RAT;

ACETYLATION; ANIMALS; CELL POLARITY; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HIPPOCAMPUS; KINESIN; MICROTUBULES; NEURONS; PACLITAXEL; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RATS; SIGNAL TRANSDUCTION; TUBULIN; TUBULIN MODULATORS;

EID: 76649143069     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-01-0044     Document Type: Article

References (47)

1. Arimura, N., and Kaibuchi, K. (2007). Neuronal polarity: from extracellular signals to intracellular mechanisms. Nat. Rev. Neurosci. 8, 194-205.
2. Baas, P. W., Black, M. M., and Banker, G. A. (1989). Changes in microtubule polarity orientation during the development of hippocampal neurons in culture. J. Cell Biol. 109, 3085-3094.
3. Baas, P. W., Slaughter, T., Brown, A., and Black, M. M. (1991). Microtubule dynamics in axons and dendrites. J. Neurosci. Res. 30, 134-153.
4. Barnes, A. P., Solecki, D., and Polleux, F. (2008). New insights into the molecular mechanisms specifying neuronal polarity in vivo. Curr. Opin. Neurobiol. 18, 44-52.
5. Bielas, S. L., Serneo, F. F., Chechlacz, M., Deerinck, T. J., Perkins, G. A., Allen, P. B., Ellisman, M. H., and Gleeson, J. G. (2007). Spinophilin facilitates dephosphorylation of doublecortin by PP1 to mediate microtubule bundling at the axonal wrist. Cell 129, 579-591.
6. Black, M. M. (1987). Taxol interferes with the interaction of microtubule-associated proteins with microtubules in cultured neurons. J. Neurosci. 7, 3695-3702.
7. Cai, D., McEwen, D. P., Martens, J. R., Meyhofer, E., and Verhey, K. J. (2009). Single molecule imaging reveals differences in microtubule track selection between kinesin motors. PLoS Biol. 7, e1000216.
8. Chang, J., Baloh, R. H., and Milbrandt, J. (2009). The NIMA-family kinase Nek3 regulates microtubule acetylation in neurons. J. Cell Sci. 122, 2274-2282.
9. Creppe, C., et al. (2009). Elongator controls the migration and differentiation of cortical neurons through acetylation of alpha-tubulin. Cell 136, 551-564.
10. Dajas-Bailador, F., Jones, E. V., and Whitmarsh, A. J. (2008). The JIP1 scaffold protein regulates axonal development in cortical neurons. Curr. Biol. 18, 221-226.
11. Dompierre, J. P., Godin, J. D., Charrin, B. C., Cordelieres, F. P., King, S. J., Humbert, S., and Saudou, F. (2007). Histone deacetylase 6 inhibition compensates for the TRANSPORT deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci. 27, 3571-3583.
12. Dotti, C. G., and Banker, G. A. (1987). Experimentally induced alteration in the polarity of developing neurons. Nature 330, 254-256.
13. Dotti, C. G., Sullivan, C. A., and Banker, G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454-1468.
14. Dunn, S., Morrison, E. E., Liverpool, T. B., Molina-Paris, C., Cross, R. A., Alonso, M. C., and Peckham, M. (2008). Differential trafficking of Kif5c on tyrosinated and detyrosinated microtubules in live cells. J. Cell Sci. 121, 1085-1095.
15. Eng, C. H., Huckaba, T. M., and Gundersen, G. G. (2006). The formin mDia regulates GSK3beta through novel PKCs to promote microtubule stabilization but not MTOC reorientation in migrating fibroblasts. Mol. Biol. Cell 17, 5004-5016.
16. Gartner, A., Huang, X., and Hall, A. (2006). Neuronal polarity is regulated by glycogen synthase kinase-3 (GSK-3beta) independently of Akt/PKB serine phosphorylation. J. Cell Sci. 119, 3927-3934.
17. Gomis-Ruth, S., Wierenga, C. J., and Bradke, F. (2008). Plasticity of polarization: changing dendrites into axons in neurons integrated in neuronal circuits. Curr. Biol. 18, 992-1000.
18. Goslin, K., and Banker, G. (1989). Experimental observations on the development of polarity by hippocampal neurons in culture. J. Cell Biol. 108, 1507-1516.
19. Gurskaya, N. G., Verkhusha, V. V., Shcheglov, A. S., Staroverov, D. B., Chepurnykh, T. V., Fradkov, A. F., Lukyanov, S., and Lukyanov, K. A. (2006). Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light. Nat. Biotechnol. 24, 461-465.
20. Haggarty, S. J., Koeller, K. M., Wong, J. C., Grozinger, C. M., and Schreiber, S. L. (2003). Domain-selective small-molecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. USA 100, 4389-4394.
21. Hammond, J. W., Cai, D., and Verhey, K. J. (2008). Tubulin modifications and their cellular functions. Curr. Opin. Cell Biol. 20, 71-76.
22. Hubbert, C., Guardiola, A., Shao, R., Kawaguchi, Y., Ito, A., Nixon, A., Yoshida, M., Wang, X. F., and Yao, T. P. (2002). HDAC6 is a microtubule- associated deacetylase. Nature 417, 455-458.
23. Ikegami, K., et al. (2007). Loss of alpha-tubulin polyglutamylation in ROSA22 mice is associated with abnormal targeting of KIF1A and modulated synaptic function. Proc. Natl. Acad. Sci. USA 104, 3213-3218.
24. Ikegami, K., Mukai, M., Tsuchida, J., Heier, R. L., Macgregor, G. R., and Setou, M. (2006). TTLL7 is a mammalian beta-tubulin polyglutamylase required for growth of MAP2-positive neurites. J. Biol. Chem. 281, 30707-30716.
25. Jacobson, C., Schnapp, B., and Banker, G. A. (2006). A change in the selective translocation of the Kinesin-1 motor domain marks the initial specification of the axon. Neuron 49, 797-804.
26. Janke, C., et al. (2005). Tubulin polyglutamylase enzymes are members of the TTL Domain protein family. Science 308, 1758-1762.
27. Jiang, H., Guo, W., Liang, X., and Rao, Y. (2005). Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 120, 123-135.
28. Jordan, M. A., and Wilson, L. (1998). Use of drugs to study role of microtubule assembly dynamics in living cells. Methods Enzymol. 298, 252-276.
29. Kaech, S., and Banker, G. (2006). Culturing hippocampal neurons. Nat. Protoc. 1, 2406-2415.
30. Kim, W. Y., Zhou, F. Q., Zhou, J., Yokota, Y., Wang, Y. M., Yoshimura, T., Kaibuchi, K., Woodgett, J. R., Anton, E. S., and Snider, W. D. (2006). Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 52, 981-996.
31. Konishi, Y., and Setou, M. (2009). Tubulin tyrosination navigates the kinesin-1 motor domain to axons. Nat. Neurosci. 12, 559-567.
32. Larcher, J. C., Boucher, D., Lazereg, S., Gros, F., and Denoulet, P. (1996). Interaction of kinesin motor domains with alpha- and beta-tubulin subunits at a tau-independent binding site. Regulation by polyglutamylation. J. Biol. Chem. 271, 22117-22124.
33. Liao, G., and Gundersen, G. G. (1998). Kinesin is a candidate for cross-bridging microtubules and intermediate filaments. Selective binding of kinesin to detyrosinated tubulin and vimentin. J. Biol. Chem. 273, 9797-9803.
34. Matsuyama, A., et al. (2002). In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831.
35. Meyer, D., Liu, A., and Margolis, B. (1999). Interaction of c-Jun amino-terminal kinase interacting protein-1 with p190 rhoGEF and its localization in differentiated neurons. J. Biol. Chem. 274, 35113-35118.
36. Nakata, T., and Hirokawa, N. (2003). Microtubules provide directional cues for polarized axonal TRANSPORT through interaction with kinesin motor head. J. Cell Biol. 162, 1045-1055.
37. Ohkawa, N., Sugisaki, S., Tokunaga, E., Fujitani, K., Hayasaka, T., Setou, M., and Inokuchi, K. (2008). N-Acetyltransferase ARD1-NAT1 regulates neuronal dendritic development. Genes Cells 13, 1171-1183.
38. Owen, R., and Gordon-Weeks, P. R. (2003). Inhibition of glycogen synthase kinase 3beta in sensory neurons in culture alters filopodia dynamics and microtubule distribution in growth cones. Mol. Cell. Neurosci. 23, 626-637.
39. Reed, N. A., Cai, D., Blasius, T. L., Jih, G. T., Meyhofer, E., Gaertig, J., and Verhey, K. J. (2006). Microtubule acetylation promotes kinesin-1 binding and transport. Curr. Biol. 16, 2166-2172.
40. Samsonov, A., Yu, J. Z., Rasenick, M., and Popov, S. V. (2004). Tau interaction with microtubules in vivo. J. Cell Sci. 117, 6129-6141.
41. Toriyama, M., Shimada, T., Kim, K. B., Mitsuba, M., Nomura, E., Katsuta, K., Sakumura, Y., Roepstorff, P., and Inagaki, N. (2006). Shootin1, A protein involved in the organization of an asymmetric signal for neuronal polarization. J. Cell Biol. 175, 147-157.
42. van Dijk, J., Rogowski, K., Miro, J., Lacroix, B., Edde, B., and Janke, C. (2007). A targeted multienzyme mechanism for selective microtubule polyglutamylation. Mol. Cell 26, 437-448.
43. Verhey, K. J., and Gaertig, J. (2007). The tubulin code. Cell Cycle 6, 2152-2160.
44. Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A., and Margolis, B. (2001). Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970.
45. Witte, H., Neukirchen, D., and Bradke, F. (2008). Microtubule stabilization specifies initial neuronal polarization. J. Cell Biol. 180, 619-632.
46. Wolff, A., de Nechaud, B., Chillet, D., Mazarguil, H., Desbruyeres, E., Audebert, S., Edde, B., Gros, F., and Denoulet, P. (1992). Distribution of glutamylated alpha and beta-tubulin in mouse tissues using a specific monoclonal antibody, GT335. Eur J. Cell Biol. 59, 425-432.
47. Yoshimura, T., Kawano, Y., Arimura, N., Kawabata, S., Kikuchi, A., and Kaibuchi, K. (2005). GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120, 137-149.