Microtubule-severing protein katanin regulates neuromuscular junction development and dendritic elaboration in Drosophila

Development (Cambridge)

Volumn 141, Issue 5, 2014, Pages 1064-1074

  Mao, Chuan Xi ^a,b   Xiong, Ying ^b   Xiong, Zhaohuan ^a   Wang, Qifu ^b   Zhang, Yong Q ^b   Jin, Shan ^a  

^a HUBEI UNIVERSITY   (China)

^b INSTITUTE OF GENETICS AND DEVELOPMENTAL BIOLOGY   (China)

Author keywords

Drosophila melanogaster; HDAC6; Katanin; Neuromuscular junction; Spastin

Indexed keywords

DROSOPHILA MELANOGASTER; HDAC6; KATANIN; NEUROMUSCULAR JUNCTION; SPASTIN;

ADENOSINE TRIPHOSPHATASES; ANIMALS; DENDRITES; DROSOPHILA; DROSOPHILA PROTEINS; HISTONE DEACETYLASES; MICROTUBULES; NEUROMUSCULAR JUNCTION;

EID: 84894093621     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.097774     Document Type: Article

References (63)

1. 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.
2. Ball, R. W., Warren-Paquin, M., Tsurudome, K., Liao, E. H., Elazzouzi, F., Cavanagh, C., An, B. S., Wang, T. T., White, J. H. and Haghighi, A. P. (2010). Retrograde BMP signaling controls synaptic growth at the NMJ by regulating trio expression in motor neurons. Neuron 66, 536-549.
3. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
4. Blackstone, C., O'Kane, C. J. and Reid, E. (2011). Hereditary spastic paraplegias: membrane traffic and the motor pathway. Nat. Rev. Neurosci. 12, 31-42.
5. Budnik, V., Koh, Y. H., Guan, B., Hartmann, B., Hough, C., Woods, D. and Gorczyca, M. (1996). Regulation of synapse structure and function by the Drosophila tumor suppressor gene dlg. Neuron 17, 627-640.
6. Conde, C. and Cáceres, A. (2009). Microtubule assembly, organization and dynamics in axons and dendrites. Nat. Rev. Neurosci. 10, 319-332.
7. Coyle, I. P., Koh, Y. H., Lee, W. C., Slind, J., Fergestad, T., Littleton, J. T. and Ganetzky, B. (2004). Nervous wreck, an SH3 adaptor protein that interacts with Wsp, regulates synaptic growth in Drosophila. Neuron 41, 521-534.
8. Cummings, C. M., Bentley, C. A., Perdue, S. A., Baas, P. W. and Singer, J. D. (2009). The Cul3/Klhdc5 E3 ligase regulates p60/katanin and is required for normal mitosis in mammalian cells. J. Biol. Chem. 284, 11663-11675.
9. Díaz-Valencia, J. D., Morelli, M. M., Bailey, M., Zhang, D., Sharp, D. J. and Ross, J. L. (2011). Drosophila katanin-60 depolymerizes and severs at microtubule defects. Biophys. J. 100, 2440-2449.
10. Dickman, D. K., Lu, Z., Meinertzhagen, I. A. and Schwarz, T. L. (2006). Altered synaptic development and active zone spacing in endocytosis mutants. Curr. Biol. 16, 591-598.
11. Du, G., Liu, X., Chen, X., Song, M., Yan, Y., Jiao, R. and Wang, C. C. (2010). Drosophila histone deacetylase 6 protects dopaminergic neurons against α-synuclein toxicity by promoting inclusion formation. Mol. Biol. Cell 21, 2128-2137.
12. Feng, Y., Ueda, A. and Wu, C. F. (2004). A modified minimal hemolymph-like solution, HL3.1, for physiological recordings at the neuromuscular junctions of normal and mutant Drosophila larvae. J. Neurogenet. 18, 377-402.
13. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2002). Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878.
14. Grueber, W. B., Jan, L. Y. and Jan, Y. N. (2003). Different levels of the homeodomain protein cut regulate distinct dendrite branching patterns of Drosophila multidendritic neurons. Cell 112, 805-818.
15. Hartman, J. J. and Vale, R. D. (1999). Microtubule disassembly by ATP-dependent oligomerization of the AAA enzyme katanin. Science 286, 782-785.
16. Huang, J., Zhou, W., Watson, A. M., Jan, Y. N. and Hong, Y. (2008). Efficient endsout gene targeting in Drosophila. Genetics 180, 703-707.
17. Huang, J., Zhou, W., Dong, W., Watson, A. M. and Hong, Y. (2009). From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl. Acad. Sci. USA 106, 8284-8289.
18. 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.
19. Hummel, T., Krukkert, K., Roos, J., Davis, G. and Klämbt, C. (2000). Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26, 357-370.
20. Jan, Y. N. and Jan, L. Y. (2010). Branching out: mechanisms of dendritic arborization. Nat. Rev. Neurosci. 11, 316-328.
21. Jaworski, J., Kapitein, L. C., Gouveia, S. M., Dortland, B. R., Wulf, P. S., Grigoriev, I., Camera, P., Spangler, S. A., Di Stefano, P., Demmers, J. et al. (2009). Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100.
22. Jin, S., Pan, L., Liu, Z., Wang, Q., Xu, Z. and Zhang, Y. Q. (2009). Drosophila Tubulin-specific chaperone E functions at neuromuscular synapses and is required for microtubule network formation. Development 136, 1571-1581.
23. Jinushi-Nakao, S., Arvind, R., Amikura, R., Kinameri, E., Liu, A. W. and Moore, A. W. (2007). Knot/Collier and cut control different aspects of dendrite cytoskeleton and synergize to define final arbor shape. Neuron 56, 963-978.
24. 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.
25. 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.
26. Liu, Z., Chen, Y., Wang, D., Wang, S. and Zhang, Y. Q. (2010). Distinct presynaptic and postsynaptic dismantling processes of Drosophila neuromuscular junctions during metamorphosis. J. Neurosci. 30, 11624-11634.
27. Liu, Z., Huang, Y., Zhang, Y., Chen, D. and Zhang, Y. Q. (2011). Drosophila Acyl-CoA synthetase long-chain family member 4 regulates axonal transport of synaptic vesicles and is required for synaptic development and transmission. J. Neurosci. 31, 2052-2063.
28. Loughlin, R., Wilbur, J. D., McNally, F. J., Nédélec, F. J. and Heald, R. (2011). Katanin contributes to interspecies spindle length scaling in Xenopus. Cell 147, 1397-1407.
29. Martin, A. R. (1955). A further study of the statistical composition on the end-plate potential. J. Physiol. 130, 114-122.
30. Matsuyama, A., Shimazu, T., Sumida, Y., Saito, A., Yoshimatsu, Y., Seigneurin-Berny, D., Osada, H., Komatsu, Y., Nishino, N., Khochbin, S. et al. (2002). In vivo destabilization of dynamic microtubules by HDAC6-mediated deacetylation. EMBO J. 21, 6820-6831.
31. Matthews, B. J., Kim, M. E., Flanagan, J. J., Hattori, D., Clemens, J. C., Zipursky, S. L. and Grueber, W. B. (2007). Dendrite self-avoidance is controlled by Dscam. Cell 129, 593-604.
32. McNally, F. J. and Vale, R. D. (1993). Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75, 419-429.
33. Nahm, M., Lee, M. J., Parkinson, W., Lee, M., Kim, H., Kim, Y. J., Kim, S., Cho, Y. S., Min, B. M., Bae, Y. C. et al. (2013). Spartin regulates synaptic growth and neuronal survival by inhibiting BMP-mediated microtubule stabilization. Neuron 77, 680-695.
34. O'Connor-Giles, K. M., Ho, L. L. and Ganetzky, B. (2008). Nervous wreck interacts with thickveins and the endocytic machinery to attenuate retrograde BMP signaling during synaptic growth. Neuron 58, 507-518.
35. Ozdowski, E. F., Gayle, S., Bao, H., Zhang, B. and Sherwood, N. T. (2011). Loss of Drosophila melanogaster p21-activated kinase 3 suppresses defects in synapse structure and function caused by spastin mutations. Genetics 189, 123-135.
36. Penzes, P., Srivastava, D. P. and Woolfrey, K. M. (2009). Not just actin? A role for dynamic microtubules in dendritic spines. Neuron 61, 3-5.
37. 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.
38. Qiang, L., Yu, W., Liu, M., Solowska, J. M. and Baas, P. W. (2010). Basic fibroblast growth factor elicits formation of interstitial axonal branches via enhanced severing of microtubules. Mol. Biol. Cell 21, 334-344.
39. Riano, E., Martignoni, M., Mancuso, G., Cartelli, D., Crippa, F., Toldo, I., Siciliano, G., Di Bella, D., Taroni, F., Bassi, M. T. et al. (2009). Pleiotropic effects of spastin on neurite growth depending on expression levels. J. Neurochem. 108, 1277-1288.
40. Rodal, A. A., Motola-Barnes, R. N. and Littleton, J. T. (2008). Nervous wreck and Cdc42 cooperate to regulate endocytic actin assembly during synaptic growth. J. Neurosci. 28, 8316-8325.
41. Roll-Mecak, A. and McNally, F. J. (2010). Microtubule-severing enzymes. Curr. Opin. Cell Biol. 22, 96-103.
42. Roos, J., Hummel, T., Ng, N., Klämbt, C. and Davis, G. W. (2000). Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26, 371-38.
43. Ruiz-Canada, C., Ashley, J., Moeckel-Cole, S., Drier, E., Yin, J. and Budnik, V. (2004). New synaptic bouton formation is disrupted by misregulation of microtubule stability in aPKC mutants. Neuron 42, 567-580.
44. Sharma, N., Bryant, J., Wloga, D., Donaldson, R., Davis, R. C., Jerka-Dziadosz, M. and Gaertig, J. (2007). Katanin regulates dynamics of microtubules and biogenesis of motile cilia. J. Cell Biol. 178, 1065-1079.
45. Sharp, D. J. and Ross, J. L. (2012). Microtubule-severing enzymes at the cutting edge. J. Cell Sci. 125, 2561-2569.
46. Sherwood, N. T., Sun, Q., Xue, M., Zhang, B. and Zinn, K. (2004). Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2, e429.
47. Shi, W., Chen, Y., Gan, G., Wang, D., Ren, J., Wang, Q., Xu, Z., Xie, W. and Zhang, Y. Q. (2013). Brain tumor regulates neuromuscular synapse growth and endocytosis in Drosophila by suppressing mad expression. J. Neurosci. 33, 12352-12363.
48. Srayko, M., O'Toole, E. T., Hyman, A. A. and Müller-Reichert, T. (2006). Katanin disrupts the microtubule lattice and increases polymer number in C. elegans meiosis. Curr. Biol. 16, 1944-1949.
49. Stewart, A., Tsubouchi, A., Rolls, M. M., Tracey, W. D. and Sherwood, N. T. (2012). Katanin p60-like1 promotes microtubule growth and terminal dendrite stability in the larval class IV sensory neurons of Drosophila. J. Neurosci. 32, 11631-11642.
50. Sudo, H. and Baas, P. W. (2010). Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J. Neurosci. 30, 7215-7226.
51. Trotta, N., Orso, G., Rossetto, M. G., Daga, A. and Broadie, K. (2004). The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr. Biol. 14, 1135-1147.
52. Vale, R. D. (1991). Severing of stable microtubules by a mitotically activated protein in Xenopus egg extracts. Cell 64, 827-839.
53. Valenzuela-Fernández, A., Cabrero, J. R., Serrador, J. M. and Sánchez-Madrid, F. (2008). HDAC6: a key regulator of cytoskeleton, cell migration and cell-cell interactions. Trends Cell Biol. 18, 291-297.
54. Wang, X., Shaw, W. R., Tsang, H. T., Reid, E. and O'Kane, C. J. (2007). Drosophila spichthyin inhibits BMP signaling and regulates synaptic growth and axonal microtubules. Nat. Neurosci. 10, 177-185.
55. Whitehead, E., Heald, R. and Wilbur, J. D. (2013). N-terminal phosphorylation of p60 katanin directly regulates microtubule severing. J. Mol. Biol. 425, 214-221.
56. Xiong, Y., Zhao, K., Wu, J., Xu, Z., Jin, S. and Zhang, Y. Q. (2013). HDAC6 mutations rescue human tau-induced microtubule defects in Drosophila. Proc. Natl. Acad. Sci. USA 110, 4604-4609.
57. Yao, A., Jin, S., Li, X., Liu, Z., Ma, X., Tang, J. and Zhang, Y. Q. (2011). Drosophila FMRP regulates microtubule network formation and axonal transport of mitochondria. Hum. Mol. Genet. 20, 51-63.
58. Ye, B., Kim, J. H., Yang, L., McLachlan, I., Younger, S., Jan, L. Y. and Jan, Y. N. (2011). Differential regulation of dendritic and axonal development by the novel Krüppel-like factor Dar1. J. Neurosci. 31, 3309-3319.
59. 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.
60. Zhang, Y. Q., Bailey, A. M., Matthies, H. J., Renden, R. B., Smith, M. A., Speese, S. D., Rubin, G. M. and Broadie, K. (2001). Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107, 591-603.
61. 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.
62. Zhang, D., Grode, K. D., Stewman, S. F., Diaz-Valencia, J. D., Liebling, E., Rath, U., Riera, T., Currie, J. D., Buster, D. W., Asenjo, A. B. et al. (2011). Drosophila katanin is a microtubule depolymerase that regulates cortical-microtubule plus-end interactions and cell migration. Nat. Cell Biol. 13, 361-369.
63. Zhao, L., Wang, D., Wang, Q., Rodal, A. A. and Zhang, Y. Q. (2013). Drosophila cyfip regulates synaptic development and endocytosis by suppressing filamentous actin assembly. PLoS Genet. 9, e1003450.