Tau/PTL-1 associates with kinesin-3 KIF1A/UNC-104 and affects the motor's motility characteristics in C. elegans neurons

Neurobiology of Disease

Volumn 43, Issue 2, 2011, Pages 495-506

  Tien, Nai Wen ^a   Wu, Gong Her ^a   Hsu, Chih Chun ^a   Chang, Chien Yu ^a   Wagner, Oliver I ^a  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

Author keywords

Axonal transport; C. elegans; Conventional kinesin 1; Disease model; Dynein; Kinesin 3; Molecular motors; Tauopathies

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; HELMINTH PROTEIN; KINESIN; KINESIN 1; MUTANT PROTEIN; PROTEIN KIF1A; PROTEIN WITH TAU LIKE REPEAT 1; SYNAPTOBREVIN 1; TAU PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; IMMUNOPRECIPITATION; KNOCKOUT GENE; NERVE FIBER TRANSPORT; NERVOUS SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RETROGRADE NERVE FIBER TRANSPORT; TRANSPORT VESICLE;

ANIMALS; AXONAL TRANSPORT; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL LINE, TUMOR; CELLS, CULTURED; HUMANS; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MOLECULAR MOTOR PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PC12 CELLS; RATS;

EID: 79958236828     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.04.023     Document Type: Article

References (65)

1. Ally S., et al. Opposite-polarity motors activate one another to trigger cargo transport in live cells. J. Cell Biol. 2009, 187:1071-1082.
2. Amos L.A., Schlieper D. Microtubules and maps. Adv. Protein Chem. 2005, 71:257-298.
3. Ballatore C., et al. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nat. Rev. Neurosci. 2007, 8:663-672.
4. Barkus R.V., et al. Identification of an axonal kinesin-3 motor for fast anterograde vesicle transport that facilitates retrograde transport of neuropeptides. Mol. Biol. Cell 2008, 19:274-283.
5. Bettencourt da Cruz A., et al. Disruption of the MAP1B-related protein FUTSCH leads to changes in the neuronal cytoskeleton, axonal transport defects, and progressive neurodegeneration in Drosophila. Mol. Biol. Cell 2005, 16:2433-2442.
6. Binder L.I., et al. Tau, tangles, and Alzheimer's disease. Biochim. Biophys. Acta 2005, 1739:216-223.
7. Brandt R., et al. A Caenorhabditis elegans model of tau hyperphosphorylation: induction of developmental defects by transgenic overexpression of Alzheimer's disease-like modified tau. Neurobiol. Aging 2009, 30:22-33.
8. Brenner S. The genetics of Caenorhabditis elegans. Genetics 1974, 77:71-94.
9. Brown A. Axonal transport of membranous and nonmembranous cargoes: a unified perspective. J. Cell Biol. 2003, 160:817-821.
10. Cairns N.J., et al. The cytoskeleton in neurodegenerative diseases. J. Pathol. 2004, 204:438-449.
11. Chalfie M., et al. The neural circuit for touch sensitivity in Caenorhabditis elegans. J. Neurosci. 1985, 5:956-964.
12. Christensen M., et al. A primary culture system for functional analysis of C. elegans neurons and muscle cells. Neuron 2002, 33:503-514.
13. Cuchillo-Ibanez I., et al. Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin. FASEB J. 2008, 22:3186-3195.
14. Dixit R., et al. Differential regulation of dynein and kinesin motor proteins by tau. Science 2008, 319:1086-1089.
15. Dubey M., et al. Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate tau-mediated neurite instability. Cell Motil. Cytoskeleton 2008, 65:89-99.
16. Ebneth A., et al. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 1998, 143:777-794.
17. Ebneth A., et al. Overexpression of tau protein inhibits kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: implications for Alzheimer's disease. J. Cell Biol. 1998, 143:777.
18. Ewald C.Y., Li C. Understanding the molecular basis of Alzheimer's disease using a Caenorhabditis elegans model system. Brain Struct. Funct. 2010, 214:263-283.
19. Fire A. Integrative transformation of Caenorhabditis elegans. EMBO J. 1986, 5:2673-2680.
20. Garcia M.L., Cleveland D.W. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr. Opin. Cell Biol. 2001, 13:41-48.
21. Goedert M. Neurodegenerative tauopathy in the worm. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:9653-9655.
22. Goedert M., et al. PTL-1, a microtubule-associated protein with tau-like repeats from the nematode Caenorhabditis elegans. J. Cell Sci. 1996, 109(Pt 11):2661-2672.
23. Gordon P., et al. The invertebrate microtubule-associated protein PTL-1 functions in mechanosensation and development in Caenorhabditis elegans. Dev. Genes Evol. 2008, 218:541-551.
24. Gotz J., et al. Transgenic animal models of Alzheimer's disease and related disorders: histopathology, behavior and therapy. Mol. Psychiatry 2004, 9:664-683.
25. Gross S.P., et al. Coordination of opposite-polarity microtubule motors. J. Cell Biol. 2002, 156:715-724.
26. Hall D.H., Hedgecock E.M. Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 1991, 65:837-847.
27. Hammond J.W., et al. Mammalian kinesin-3 motors are dimeric in vivo and move by processive motility upon release of autoinhibition. PLoS Biol. 2009, 7:e72.
28. Hendricks A.G., et al. Motor coordination via a tug-of-war mechanism drives bidirectional vesicle transport. Curr. Biol. 2010, 20:697-702.
29. Hsu C.C., et al. Sub-cellular distribution of UNC-104(KIF1A) upon binding to adaptors as UNC-16(JIP3), DNC-1(DCTN1/Glued) and SYD-2(Liprin-alpha) in C. elegans neurons. Neuroscience 2011, 176:39-52.
30. Kocsis E., et al. Image averaging of flexible fibrous macromolecules: the clathrin triskelion has an elastic proximal segment. J. Struct. Biol. 1991, 107:6-14.
31. Koushika S.P., et al. Mutations in Caenorhabditis elegans cytoplasmic dynein components reveal specificity of neuronal retrograde cargo. J. Neurosci. 2004, 24:3907-3916.
32. Kumar J., et al. The Caenorhabditis elegans kinesin-3 motor UNC-104/KIF1A is degraded upon loss of specific binding to cargo. PLoS Genet. 2010, 6:e1001200.
33. LaPointe N.E., et al. The amino terminus of tau inhibits kinesin-dependent axonal transport: implications for filament toxicity. J. Neurosci. Res. 2009, 87:440-451.
34. Lee V.M., et al. Transgenic animal models of tauopathies. Biochim. Biophys. Acta 2005, 1739:251-259.
35. Magnani E., et al. Interaction of tau protein with the dynactin complex. EMBO J. 2007, 26:4546-4554.
36. Mandelkow E.M., et al. MARK/PAR1 kinase is a regulator of microtubule-dependent transport in axons. J. Cell Biol. 2004, 167:99-110.
37. McDermott J.B., et al. ptl-1, a Caenorhabditis elegans gene whose products are homologous to the tau microtubule-associated proteins. Biochemistry 1996, 35:9415-9423.
38. Mello C.C., et al. Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 1991, 10:3959-3970.
39. Metcalfe M.J., Figueiredo-Pereira M.E. Relationship between tau pathology and neuroinflammation in Alzheimer's disease. Mt. Sinai J. Med. 2010, 77:50-58.
40. Miller K.E., Heidemann S.R. What is slow axonal transport?. Exp. Cell Res. 2008, 314:1981-1990.
41. Miyasaka T., et al. Progressive neurodegeneration in C. elegans model of tauopathy. Neurobiol. Dis. 2005, 20:372-383.
42. Morfini G.A., et al. Axonal transport defects in neurodegenerative diseases. J. Neurosci. 2009, 29:12776-12786.
43. Muller M.J., et al. Tug-of-war as a cooperative mechanism for bidirectional cargo transport by molecular motors. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:4609-4614.
44. Reck-Peterson S.L., et al. Single-molecule analysis of dynein processivity and stepping behavior. Cell 2006, 126:335-348.
45. Ross J.L., et al. Processive bidirectional motion of dynein-dynactin complexes in vitro. Nat. Cell Biol. 2006, 8:562-570.
46. Seitz A., et al. Single-molecule investigation of the interference between kinesin, tau and MAP2c. EMBO J. 2002, 21:4896-4905.
47. Shyu Y.J., et al. Visualization of protein interactions in living Caenorhabditis elegans using bimolecular fluorescence complementation analysis. Nat. Protoc. 2008, 3:588-596.
48. Soppina V., et al. Tug-of-war between dissimilar teams of microtubule motors regulates transport and fission of endosomes. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19381-19386.
49. Stamer K., et al. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. J. Cell Biol. 2002, 156:1051.
50. Strange K., et al. Primary culture of Caenorhabditis elegans developing embryo cells for electrophysiological, cell biological and molecular studies. Nat. Protoc. 2007, 2:1003-1012.
51. Telley I.A., et al. Obstacles on the microtubule reduce the processivity of Kinesin-1 in a minimal in vitro system and in cell extract. Biophys. J. 2009, 96:3341-3353.
52. Tokuraku K., et al. An isoform of microtubule-associated protein 4 inhibits kinesin-driven microtubule gliding. J. Biochem. 2007, 141:585-591.
53. Tomishige M., et al. Conversion of Unc104/KIF1A kinesin into a processive motor after dimerization. Science 2002, 297:2263-2267.
54. Trinczek B., et al. Tau regulates the attachment/detachment but not the speed of motors in microtubule-dependent transport of single vesicles and organelles. J. Cell Sci. 1999, 112(Pt 14):2355-2367.
55. Utton M.A., et al. The slow axonal transport of the microtubule-associated protein tau and the transport rates of different isoforms and mutants in cultured neurons. J. Neurosci. 2002, 22:6394-6400.
56. Utton M.A., et al. Molecular motors implicated in the axonal transport of tau and alpha-synuclein. J. Cell Sci. 2005, 118:4645-4654.
57. Vale R.D. The molecular motor toolbox for intracellular transport. Cell 2003, 112:467-480.
58. Vershinin M., et al. Multiple-motor based transport and its regulation by Tau. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:87-92.
59. Vershinin M., et al. Tuning microtubule-based transport through filamentous MAPs: the problem of dynein. Traffic 2008, 9:882-892.
60. Wagner O.I., et al. Synaptic scaffolding protein SYD-2 clusters and activates kinesin-3 UNC-104 in C. elegans. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:19605-19610.
61. Welte M.A. Bidirectional transport along microtubules. Curr. Biol. 2004, 14:R525-R537.
62. Yonekawa Y., et al. Defect in synaptic vesicle precursor transport and neuronal cell death in KIF1A motor protein-deficient mice. J. Cell Biol. 1998, 141:431-441.
63. Yuan A., et al. Axonal transport rates in vivo are unaffected by tau deletion or overexpression in mice. J. Neurosci. 2008, 28:1682-1687.
64. Zal T. Visualization of protein interactions in living cells. Adv. Exp. Med. Biol. 2008, 640:183-197.
65. Zhou H.M., et al. Direct visualization of the movement of the monomeric axonal transport motor UNC-104 along neuronal processes in living Caenorhabditis elegans. J. Neurosci. 2001, 21:3749-3755.