UNC-51/ATG1 kinase regulates axonal transport by mediating motor-cargo assembly

Genes and Development

Volumn 22, Issue 23, 2008, Pages 3292-3307

  Toda, Hirofumi ^a,b   Mochizuki, Hiroaki ^b   Flores III, Rafael ^a   Josowitz, Rebecca ^c   Krasieva, Tatiana B ^d   LaMorte, Vickie J ^d   Suzuki, Emiko ^e   Gindhart, Joseph G ^c   Furukubo Tokunaga, Katsuo ^b   Tomoda, Toshifumi ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF RICHMOND   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

Axonal transport; Kinesin adaptor; Motor cargo assembly; Phosphorylation; unc 51

Indexed keywords

ADAPTOR PROTEIN; KINESIN; SYNAPTOTAGMIN I; UNC 51; UNC 76; UNCLASSIFIED DRUG;

ARTICLE; CELL ORGANELLE; DROSOPHILA; EMBRYO; GENETICS; HEAVY CHAIN; HUMAN; HUMAN CELL; IN VIVO STUDY; MACROMOLECULE; MICROTUBULE; MOTOR PERFORMANCE; MUTANT; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SYNAPSE VESICLE;

ANIMALS; AXONAL TRANSPORT; CARRIER PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; MUTATION; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; SYNAPTIC VESICLES;

EID: 57749095080     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1734608     Document Type: Article

References (64)

1. Ahantarig, A., Chadwell, L.V., Terrazas, I.B., Garcia, C.T., Nazarian, J.J., Lee, H.K., Lundell, M.J., and Cassill, J.A. 2008. Molecular characterization of Pegarn: A Drosophila homolog of UNC-51 kinase. Mol. Biol. Rep. doi: 10.1007/s11033-008-9314-4.
2. Barkus, R.V., Klyachko, O., Horiuchi, D., Dickson, B.J., and Saxton, W.M. 2008. Identification of an axonal Kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol. Biol. Cell 19: 274-283.
3. Blasius, T.L., Cai, D., Jih, G.T., Toret, C.P., and Verhey, K.J. 2007. Two binding partners cooperate to activate the molecular motor Kinesin-1. J. Cell Biol. 176: 11-17.
4. Bloom, L. and Horvitz, H.R. 1997. The Caenorhabditis elegans gene unc-76 and its human homologs define a new gene family involved in axonal outgrowth and fasciculation. Proc. Natl. Acad. Sci. 94: 3414-3419.
5. Bloom, G.S., Richards, B.W., Leopold, P.L., Ritchey, D.M., and Brady, S.T. 1993. GTP γ S inhibits organelle transport along axonal microtubules. J. Cell Biol. 120: 467-476.
6. Bowman, A.B., Kamal, A., Ritchings, B.W., Philp, A.V., McGrail, M., Gindhart, J.G., and Goldstein, L.S. 2000. Kinesin-dependent axonal transport is mediated by the sunday driver (SYD) protein. Cell 103: 583-594.
7. Brady, S.T. 1991. Molecular motors in the nervous system. Neuron 7: 521-533.
8. Byrd, D.T., Kawasaki, M., Walcoff, M., Hisamoto, N., Matsumoto, K., and Jin, Y. 2001. UNC-16, a JNK-signaling scaffold protein, regulates vesicle transport in C. elegans. Neuron 32: 787-800.
9. Coy, D.L., Hancock, W.O., Wagenbach, M., and Howard, J. 1999. Kinesin's tail domain is an inhibitory regulator of the motor domain. Nat. Cell Biol. 5: 288-292.
10. Dinant, C., van Royen, M.E., Vermeulen, W., and Houtsmuller, A.B. 2008. Fluorescence resonance energy transfer of GFP and YFP by spectral imaging and quantitative acceptor photobleaching. J. Microsc. 231: 97-104.
11. Friedman, D.S. and Vale, R.D. 1999. Single-molecule analysis of kinesin motility reveals regulation by the cargo-binding tail domain. Nat. Cell Biol. 1: 293-297.
12. Gindhart, J.G., Desai, C.J., Beushausen, S., Zinn, K., and Goldstein, L.S. 1998. Kinesin light chains are essential for axonal transport in Drosophila. J. Cell Biol. 141: 443-454.
13. Gindhart, J.G., Chen, J., Faulkner, M., Gandhi, R., Doerner, K., Wisniewski, T., and Nandlestadt, A. 2003. The kinesin-associated protein UNC-76 is required for axonal transport in the Drosophila nervous system. Mol. Biol. Cell 14: 3356-3365.
14. Gruhler, A., Olsen, J.V., Mohammed, S., Mortensen, P., Faergeman, N.J., Mann, M., and Jensen, O.N. 2005. Quantitative phosphoproteomics applied to the yeast pheromone signaling pathway. Mol. Cell. Proteomics 4: 310-327.
15. Guillaud, L., Wong, R., and Hirokawa, N. 2008. Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: A molecular model of kinesin-cargo release. Nat. Cell Biol. 10: 19-29.
16. Guzik, B.W. and Goldstein, L.S. 2004. Microtubule-dependent transport in neurons: Steps towards an understanding of regulation, function and dysfunction. Curr. Opin. Cell Biol. 16: 443-450.
17. Hackney, D.D. and Stock, M.F. 2000. Kinesin's IAK tail domain inhibits initial microtubule-stimulated ADP release. Nat. Cell Biol. 5: 257-260.
18. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., et al. 2006. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441: 885-889.
19. Hauptmann, G. and Gerster, T. 2000. Multicolor whole-mount in situ hybridization. Methods Mol. Biol. 137: 139-148.
20. Hedgecock, E.M., Culotti, J.G., Thomson, J.N., and Perkins, L.A. 1985. Axonal guidance mutants of Caenorhabditis elegans identified by filling sensory neurons with fluorescein dyes. Dev. Biol. 111: 158-170.
21. Hirokawa, N. 1998. Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279: 519-526.
22. Hirokawa, N. and Takemura, R. 2005. Molecular motors and mechanisms of directional transport in neurons. Nat. Rev. Neurosci. 6: 201-214.
23. Hollenbeck, P.J. 1993. Phosphorylation of neuronal kinesin heavy and light chains in vivo. J. Neurochem. 60: 2265-2275.
24. Horiuchi, D., Barkus, R.V., Pilling, A.D., Gassman, A., and Saxton, W.M. 2005. APLIP1, a kinesin binding JIP-1/JNK scaffold protein, influences the axonal transport of both vesicles and mitochondria in Drosophila. Curr. Biol. 15: 2137-2141.
25. Horiuchi, D., Collins, C.A., Bhat, P., Barkus, R.V., Diantonio, A., and Saxton, W.M. 2007. Control of a kinesin-cargo linkage mechanism by JNK pathway kinases. Curr. Biol. 17: 1313-1317.
26. Hurd, D.D. and Saxton, W.M. 1996. Kinesin mutations cause motor neuron disease phenotypes by disrupting fast axonal transport in Drosophila. Genetics 144: 1075-1085.
27. Kamal, A., Almenar-Queralt, A., LeBlanc, J.F., Roberts, E.A., and Goldstein, L.S. 2001. Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP. Nature 414: 643-648.
28. Klionsky, D.J. and Ohsumi, Y. 1999. Vacuolar import of proteins and organelles from the cytoplasm. Annu. Rev. Cell Dev. Biol. 15: 1-32.
29. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., et al. 2006. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441: 880-884.
30. Kuroda, S., Nakagawa, N., Tokunaga, C., Tatematsu, K., and Tanizawa, K. 1999. Mammalian homologue of the Caenorhabditis elegans UNC-76 protein involved in axonal outgrowth is a protein kinase C zeta-interacting protein. J. Cell Biol. 144: 403-411.
31. Kurusu, M., Awasaki, T., Masuda-Nakagawa, L.M., Kawauchi, H., Ito, K., and Furukubo-Tokunaga, K. 2002. Embryonic and larval development of the Drosophila mushroom bodies: Concentric layer subdivisions and the role of fasciclin II. Development 129: 409-419.
32. Lai, T. and Garriga, G. 2004. The conserved kinase UNC-51 acts with VAB-8 and UNC-14 to regulate axon outgrowth in C. elegans. Development 131: 5991-6000.
33. LaMorte, V.J., Krasieva, T.B., and Zoumi, A. 2002. One-photon versus two-photon excited FRET of GFP fusion protein. In Multiphoton microscopy in the biomedical sciences II, Proc. SPIE 4620 (eds. A. Periasamy and P.T. So), pp. 73-78. The International Society for Optical Engineering, San Jose, CA.
34. Lazarov, O., Morfini, G.A., Lee, E.B., Farah, M.H., Szodorai, A., DeBoer, S.R., Koliatsos, V.E., Kins, S., Lee, V.M., Wong, P.C., et al. 2005. Axonal transport, amyloid precursor protein, kinesin-1, and the processing apparatus: Revisited. J. Neurosci. 25: 2386-2395.
35. Liu, Z., Steward, R., and Luo, L. 2000. Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat. Cell Biol. 2: 776-783.
36. Mackler, J.M., Drummond, J.A., Loewen, C.A., Robinson, I.M., and Reist, N.E. 2002. The C(2)B Ca(2+)-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418: 340-344.
37. Martin, M., Iyadurai, S.J., Gassman, A., Gindhart, J.G., Hays, T.S., and Saxton, W.M. 1999. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol. Biol. Cell 10: 3717-3728.
38. Miki, H., Okada, Y., and Hirokawa, N. 2005. Analysis of the kinesin superfamily: Insights into structure and function. Trends Cell Biol. 15: 467-476.
39. Morfini, G., Szebenyi, G., Elluru, R., Ratner, N., and Brady, S.T. 2002. Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility. EMBO J. 21: 281-293.
40. Ogura, K. and Goshima, Y. 2006. The autophagy-related kinase UNC-51 and its binding partner UNC-14 regulate the subcellular localization of the Netrin receptor UNC-5 in Caenorhabditis elegans. Development 133: 3441-3450.
41. Ogura, K., Wicky, C., Magnenat, L., Tobler, H., Mori, I., Muller, F., and Ohshima, Y. 1994. Caenorhabditis elegans unc-51 gene required for axonal elongation encodes a novel serine/ threonine kinase. Genes & Dev. 8: 2389-2400.
42. Ogura, K., Shirakawa, M., Barnes, T.M., Hekimi, S., and Ohshima, Y. 1997. The UNC-14 protein required for axonal elongation and guidance in Caenorhabditis elegans interacts with the serine/threonine kinase UNC-51. Genes & Dev. 11: 1801-1811.
43. Okada, Y., Yamazaki, H., Sekine-Aizawa, Y., and Hirokawa, N. 1995. The neuron-specific kinesin superfamily protein KIF1A is a unique monomeric motor for anterograde axonal transport of synaptic vesicle precursors. Cell 81: 769-780.
44. Pack-Chung, E., Kurshan, P.T., Dickman, D.K., and Schwarz, T.L. 2007. A Drosophila kinesin required for synaptic bouton formation and synaptic vesicle transport. Nat. Neurosci. 10: 980-989.
45. Pulipparacharuvil, S., Akbar, M.A., Ray, S., Sevrioukov, E.A., Haberman, A.S., Rohrer, J., and Krämer, H. 2005. Drosophila Vps16A is required for trafficking to lysosomes and biogenesis of pigment granules. J. Cell Sci. 118: 3663-3673.
46. Sakamoto, R., Byrd, D.T., Brown, H.M., Hisamoto, N., Matsumoto, K., and Jin, Y. 2005. The Caenorhabditis elegans UNC-14 RUN domain protein binds to the kinesin-1 and UNC-16 complex and regulates synaptic vesicle localization. Mol. Biol. Cell 16: 483-496.
47. Sato-Yoshitake, R., Yorifuji, H., Inagaki, M., and Hirokawa, N. 1992. The phosphorylation of kinesin regulates its binding to synaptic vesicles. J. Biol. Chem. 267: 23930-23936.
48. Saxton, W.M., Porter, M.E., Cohn, S.A., Scholey, J.M., Raff, E.C., and McIntosh, J.R. 1988. Drosophila kinesin: Characterization of microtubule motility and ATPase. Proc. Natl. Acad. Sci. 85: 1109-1113.
49. 2-terminal kinase (JNK) interacting protein 1 (JIP1) binds the cytoplasmic domain of the Alzheimer's β-amyloid precursor protein (APP). J. Biol. Chem. 277: 3767-3775.
50. Scott, R.C., Schuldiner, O., and Neufeld, T.P. 2004. Role and regulation of starvation-induced autophagy in the Drosophila fat body. Dev. Cell 7: 167-178.
51. Scott, R.C., Juhasz, G., and Neufeld, T.P. 2007. Direct induction of autophagy by atg1 inhibits cell growth and induces apoptotic cell death. Curr. Biol. 17: 1-11.
52. Stowers, R.S., Megeath, L.J., Gorska-Andrzejak, J., Meinertzhagen, I.A., and Schwarz, T.L. 2002. Axonal transport of mitochondria to synapses depends on milton, a novel Drosophila protein. Neuron 36: 1063-1077.
53. Südhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27: 509-547.
54. Suzuki, E. and Hirosawa, K. 1994. Immunolocalization of a Drosophila phosphatidylinositol transfer protein (rdgB) in normal and rdgA mutant photoreceptor cells with special reference to the subrhabdomeric cisternae. J. Electron Microsc. (Tokyo) 43: 183-189.
55. Tomoda, T., Bhatt, R.S., Kuroyanagi, H., Shirasawa, T., and Hatten, M.E. 1999. A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 24: 833-846.
56. Tomoda, T., Kim, J.-H., Zhan, C., and Hatten, M.E. 2004. Role of Unc51.1 and its binding partners in CNS axon outgrowth. Genes & Dev. 18: 541-558.
57. Torroja, L., Chu, H., Kotovsky, I., and White, K. 1999. Neuronal overexpression of APPL, the Drosophila homologue of the amyloid precursor protein (APP), disrupts axonal transport. Curr. Biol. 9: 489-492.
58. Vale, R.D. 2003. The molecular motor toolbox for intracellular transport. Cell 112: 467-480.
59. Vallee, R.B. and Sheetz, M.P. 1996. Targeting of motor proteins. Science 271: 1539-1544.
60. Van Munster, E.B., Kremers, G.J., Adjobo-Hermans, M.J., and Gadella Jr., T.W. 2005. Fluorescence resonance energy transfer (FRET) measurement by gradual acceptor photobleaching. J. Microsc. 218: 253-262.
61. 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.
62. Zhang, J., Schulze, K.L., Hiesinger, P.R., Suyama, K., Wang, S., Fish, M., Acar, M., Hoskins, R.A., Bellen, H.J., and Scott, M.P. 2007. Thirty-one flavors of Drosophila rab proteins. Genetics 176: 1307-1322.
63. Zhou, X., Babu, J.R., da Silva, S., Shu, Q., Graef, I.A., Oliver, T., Tomoda, T., Tani, T., Wooten, M.W., and Wang, F. 2007. Unc-51-like kinase 1/2-mediated endocytic processes regulate filopodia extension and branching of sensory axons. Proc. Natl. Acad. Sci. 104: 5842-5847.
64. Zinsmaier, K.E., Eberle, K.K., Buchner, E., Walter, N., and Benzer, S. 1994. Paralysis and early death in cysteine string protein mutants of Drosophila. Science 263: 977-980.