α-synuclein oligomers impair neuronal microtubule-kinesin interplay

Journal of Biological Chemistry

Volumn 288, Issue 30, 2013, Pages 21742-21754

  Prots, Iryna ^a   Veber, Vanesa ^a   Brey, Stefanie ^a   Campioni, Silvia ^b   Buder, Katrin ^c   Riek, Roland ^b   Böhm, Konrad J ^c   Winner, Beate ^a  

^a UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^b ETH ZURICH   (Switzerland)

^c FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AXONAL TRANSPORTS; MICROTUBULE STABILITY; NETWORK MORPHOLOGY; NEURITES; SYNUCLEIN;

OLIGOMERS; PATHOLOGY;

NEURONS;

ALPHA SYNUCLEIN; KINESIN; MICROTUBULE ASSOCIATED PROTEIN 2; MONOMER; OLIGOMER; TAU PROTEIN; TUBULIN;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROTUBULE; MICROTUBULE ASSEMBLY; NERVE CELL LESION; NERVE CELL NECROSIS; NERVE CELL NETWORK; NERVE FIBER TRANSPORT; NEUROFILAMENT; NEUROPATHOLOGY; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SURFACE PROPERTY;

ALPHA-SYNUCLEIN; KINESIN; MICROTUBULES; NEURITE; NEURODEGENERATION; OLIGOMERS; TRANSPORT;

ALPHA-SYNUCLEIN; CELL LINE; CELL SURVIVAL; CYTOSKELETAL PROTEINS; DOPAMINERGIC NEURONS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; HUMANS; KINESIN; MICROSCOPY, FLUORESCENCE; MICROTUBULE-ASSOCIATED PROTEINS; MICROTUBULES; MUTATION; NEURITES; PROTEIN BINDING; PROTEIN MULTIMERIZATION; TAU PROTEINS; TUBULIN;

EID: 84881259462     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.451815     Document Type: Article

References (53)

1. Maroteaux, L., Campanelli, J. T., and Scheller, R. H. (1988) Synuclein. A neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8, 2804-2815
2. Nemani, V. M., Lu, W., Berge, V., Nakamura, K., Onoa, B., Lee, M. K., Chaudhry, F. A., Nicoll, R. A., and Edwards, R. H. (2010) Increased expression of-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65, 66-79
3. Singleton, A. B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R., Lincoln, S., Crawley, A., Hanson, M., Maraganore, D., Adler, C., Cookson, M. R., Muenter, M., Baptista, M., Miller, D., Blancato, J., Hardy, J., and Gwinn-Hardy, K. (2003)-Synuclein locus triplication causes Parkinson's disease. Science 302, 841
4. Polymeropoulos, M. H., Lavedan, C., Leroy, E., Ide, S. E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E. S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W. G., Lazzarini, A. M., Duvoisin, R. C., Di Iorio, G., Golbe, L. I., and Nussbaum, R. L. (1997) Mutation in the-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047
5. Krüger, R., Kuhn, W., Müller, T., Woitalla, D., Graeber, M., Kösel, S., Przuntek, H., Epplen, J. T., Schöls, L., and Riess, O. (1998) Ala30Pro mutation in the gene encoding-synuclein in Parkinson's disease. Nat. Genet. 18, 106-108
6. Zarranz, J. J., Alegre, J., Gómez-Esteban, J. C., Lezcano, E., Ros, R., Ampuero, I., Vidal, L., Hoenicka, J., Rodriguez, O., Atarés, B., Llorens, V., Gomez Tortosa, E., del Ser, T.,Muñoz, D. G., and de Yebenes, J. G. (2004) The new mutation, E46K, of-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55, 164-173
7. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997)-synuclein in Lewy bodies. Nature 388, 839-840
8. Takeda, A., Mallory, M., Sundsmo, M., Honer, W., Hansen, L., and Masliah, E. (1998) Abnormal accumulation of NACP/-synuclein in neurodegenerative disorders. Am. J. Pathol. 152, 367-372
9. Haass, C., and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration. Lessons from the Alzheimer's amyloid-peptide. Nat. Rev. Mol. Cell Biol. 8, 101-112
10. Danzer, K. M., Haasen, D., Karow, A. R., Moussaud, S., Habeck, M., Giese, A., Kretzschmar, H., Hengerer, B., and Kostka, M. (2007) Different species of-synuclein oligomers induce calcium influx and seeding. J. Neurosci. 27, 9220-9232
11. Danzer, K. M., Ruf, W. P., Putcha, P., Joyner, D., Hashimoto, T., Glabe, C., Hyman, B. T., and McLean, P. J. (2011) Heat-shock protein 70 modulates toxic extracellular-synuclein oligomers and rescues trans-synaptic toxicity. FASEB J. 25, 326-336
12. Karpinar, D. P., Balija, M. B., Kügler, S., Opazo, F., Rezaei-Ghaleh, N., Wender, N., Kim, H. Y., Taschenberger, G., Falkenburger, B. H., Heise, H., Kumar, A., Riedel, D., Fichtner, L., Voigt, A., Braus, G. H., Giller, K., Becker, S., Herzig, A., Baldus, M., Jäckle, H., Eimer, S., Schulz, J. B., Griesinger, C., and Zweckstetter, M. (2009) Pre-fibrillar- synuclein variants with impaired-structure increase neurotoxicity in Parkinson's disease models. EMBO J. 28, 3256-3268
13. Winner, B., Jappelli, R., Maji, S. K., Desplats, P. A., Boyer, L., Aigner, S., Hetzer, C., Loher, T., Vilar, M., Campioni, S., Tzitzilonis, C., Soragni, A., Jessberger, S., Mira, H., Consiglio, A., Pham, E., Masliah, E., Gage, F. H., and Riek, R. (2011) In vivo demonstration that-synuclein oligomers are toxic. Proc. Natl. Acad. Sci. U.S.A. 108, 4194-4199
14. Goldstein, A. Y., Wang, X., and Schwarz, T. L. (2008) Axonal transport and the delivery of pre-synaptic components. Curr. Opin. Neurobiol. 18, 495-503
15. Chu, Y., Morfini, G. A., Langhamer, L. B., He, Y., Brady, S. T., and Kordower, J. H. (2012) Alterations in axonal transport motor proteins in sporadic and experimental Parkinson's disease. Brain 135, 2058-2073
16. Alim, M. A., Hossain, M. S., Arima, K., Takeda, K., Izumiyama, Y., Nakamura, M., Kaji, H., Shinoda, T., Hisanaga, S., and Ueda, K. (2002) Tubulin seeds-synuclein fibril formation. J. Biol. Chem. 277, 2112-2117
17. Esteves, A. R., Arduíno, D. M., Swerdlow, R. H., Oliveira, C. R., and Cardoso, S. M. (2010) Microtubule depolymerization potentiates-synuclein oligomerization. Front. Aging Neurosci. 1, 5
18. Kim, M., Jung, W., Lee, I. H., Bhak, G., Paik, S. R., and Hahn, J. S. (2008) Impairment of microtubule system increases-synuclein aggregation and toxicity. Biochem. Biophys. Res. Commun. 365, 628-635
19. Lee, H. J., Khoshaghideh, F., Lee, S., and Lee, S. J. (2006) Impairment of microtubule-dependent trafficking by overexpression of-synuclein. Eur. J. Neurosci. 24, 3153-3162
20. Nakayama, K., Suzuki, Y., and Yazawa, I. (2009) Microtubule depolymerization suppresses-synuclein accumulation in a mouse model of multiple system atrophy. Am. J. Pathol. 174, 1471-1480
21. Nakayama, K., Suzuki, Y., and Yazawa, I. (2012) Binding of neuronal-synuclein to-III tubulin and accumulation in a model of multiple system atrophy. Biochem. Biophys. Res. Commun. 417, 1170-1175
22. Zhou, R. M., Huang, Y. X., Li, X. L., Chen, C., Shi, Q., Wang, G. R., Tian, C., Wang, Z. Y., Jing, Y. Y., Gao, C., and Dong, X. P. (2010) Molecular interaction of-synuclein with tubulin influences on the polymerization of microtubule in vitro and structure of microtubule in cells. Mol. Biol. Rep. 37, 3183-3192
23. Chen, L., Jin, J., Davis, J., Zhou, Y., Wang, Y., Liu, J., Lockhart, P. J., and Zhang, J. (2007) Oligomeric-synuclein inhibits tubulin polymerization. Biochem. Biophys. Res. Commun. 356, 548-553
24. Volles, M. J., and Lansbury, P. T., Jr. (2007) Relationships between the sequence of-synuclein and its membrane affinity, fibrillization propensity, and yeast toxicity. J. Mol. Biol. 366, 1510-1522
25. Kalchishkova, N., and Böhm, K. J. (2008) The role of Kinesin neck linker and neck in velocity regulation. J. Mol. Biol. 382, 127-135
26. Shelanski, M. L., Gaskin, F., and Cantor, C. R. (1973) Microtubule assembly in the absence of added nucleotides. Proc. Natl. Acad. Sci. U.S.A. 70, 765-768
27. Weingarten, M. D., Lockwood, A. H., Hwo, S. Y., and Kirschner, M. W. (1975) A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. U.S.A. 72, 1858-1862
28. Herzog, W., and Weber, K. (1978) Fractionation of brain microtubuleassociated proteins. Isolation of two different proteins which stimulate tubulin polymerization in vitro. Eur. J. Biochem. 92, 1-8
29. Böhm, K. J., Steinmetzer, P., Daniel, A., Baum, M., Vater, W., and Unger, E. (1997) Kinesin-driven microtubule motility in the presence of alkalineearth metal ions. Indication for a calcium ion-dependent motility. Cell Motil. Cytoskeleton 37, 226-231
30. Scholz, D., Pöltl, D., Genewsky, A., Weng, M., Waldmann, T., Schildknecht, S., and Leist, M. (2011) Rapid, complete and large-scale generation of post-mitotic neurons from the humanLUHMEScell line. J. Neurochem. 119, 957-971
31. Sharon, R., Bar-Joseph, I., Frosch, M. P., Walsh, D. M., Hamilton, J. A., and Selkoe, D. J. (2003) The formation of highly soluble oligomers of-synuclein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron 37, 583-595
32. Vilar, M., Chou, H. T., Lührs, T., Maji, S. K., Riek-Loher, D., Verel, R., Manning, G., Stahlberg, H., and Riek, R. (2008) The fold of-synuclein fibrils. Proc. Natl. Acad. Sci. U.S.A. 105, 8637-8642
33. Iwai, A., Masliah, E., Yoshimoto, M., Ge, N., Flanagan, L., de Silva, H. A., Kittel, A., and Saitoh, T. (1995) The precursor protein of non-A component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron 14, 467-475
34. Seo, J. H., Rah, J. C., Choi, S. H., Shin, J. K., Min, K., Kim, H. S., Park, C. H., Kim, S., Kim, E. M., Lee, S. H., Lee, S., Suh, S. W., and Suh, Y. H. (2002)-synuclein regulates neuronal survival via Bcl-2 family expression and PI3/Akt kinase pathway. FASEB J. 16, 1826-1828
35. 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
36. Alim, M. A., Ma, Q. L., Takeda, K., Aizawa, T., Matsubara, M., Nakamura, M., Asada, A., Saito, T., Kaji, H., Yoshii, M., Hisanaga, S., and Uéda, K. (2004) Demonstration of a role for-synuclein as a functional microtubule-associated protein. J. Alzheimer's Dis. 6, 435-442; discussion 443-439
37. Payton, J. E., Perrin, R. J., Clayton, D. F., and George, J. M. (2001) Proteinprotein interactions of-synuclein in brain homogenates and transfected cells. Brain Res. Mol. Brain Res. 95, 138-145
38. Wersinger, C., and Sidhu, A. (2005) Disruption of the interaction of-synuclein with microtubules enhances cell surface recruitment of the dopamine transporter. Biochemistry 44, 13612-13624
39. Esposito, A., Dohm, C. P., Kermer, P., Bähr, M., and Wouters, F. S. (2007)-Synuclein and its disease-related mutants interact differentially with the microtubule protein Tau and associate with the actin cytoskeleton. Neurobiol. Dis. 26, 521-531
40. Jensen, P. H., Hager, H., Nielsen, M. S., Hojrup, P., Gliemann, J., and Jakes, R. (1999)-Synuclein binds to Tau and stimulates the protein kinase A-catalyzed Tau phosphorylation of serine residues 262 and 356. J. Biol. Chem. 274, 25481-25489
41. D'Andrea, M. R., Ilyin, S., and Plata-Salaman, C. R. (2001) Abnormal patterns of microtubule-associated protein-2 (MAP-2) immunolabeling in neuronal nuclei and Lewy bodies in Parkinson's disease substantia nigra brain tissues. Neurosci. Lett. 306, 137-140
42. Utton, M. A., Noble, W. J., Hill, J. E., Anderton, B. H., and Hanger, D. P. (2005) Molecular motors implicated in the axonal transport of Tau and-synuclein. J. Cell Sci. 118, 4645-4654
43. Geddes, J. W. (2005)-Synuclein.Apotent inducer of Tau pathology. Exp. Neurol. 192, 244-250
44. Giasson, B. I., Forman, M. S., Higuchi, M., Golbe, L. I., Graves, C. L., Kotzbauer, P. T., Trojanowski, J. Q., and Lee, V. M. (2003) Initiation and synergistic fibrillization of Tau and-synuclein. Science 300, 636-640
45. Lee, V. M., Giasson, B. I., and Trojanowski, J. Q. (2004) More than just two peas in a pod. Common amyloidogenic properties of Tau and-synuclein in neurodegenerative diseases. Trends Neurosci. 27, 129-134
46. Duka, T., Duka, V., Joyce, J. N., and Sidhu, A. (2009)-Synuclein contributes to GSK-3β-catalyzed Tau phosphorylation in Parkinson's disease models. FASEB J. 23, 2820-2830
47. Sharma, M., Ioannidis, J. P., Aasly, J. O., Annesi, G., Brice, A., Van Broeckhoven, C., Bertram, L., Bozi, M., Crosiers, D., Clarke, C., Facheris, M., Farrer, M., Garraux, G., Gispert, S., Auburger, G., Vilariño-Güell, C., Hadjigeorgiou, G. M., Hicks, A. A., Hattori, N., Jeon, B., Lesage, S., Lill, C. M., Lin, J. J., Lynch, T., Lichtner, P., Lang, A. E., Mok, V., Jasinska-Myga, B., Mellick, G. D., Morrison, K. E., Opala, G., Pramstaller, P. P., Pichler, I., Park, S. S., Quattrone, A., Rogaeva, E., Ross, O. A., Stefanis, L., Stockton, J. D., Satake, W., Silburn, P. A., Theuns, J., Tan, E. K., Toda, T., Tomiyama, H., Uitti, R. J., Wirdefeldt, K., Wszolek, Z., Xiromerisiou, G., Yueh, K. C., Zhao, Y., Gasser, T., Maraganore, D., and Kruger, R. (2012) Large-scale replication and heterogeneity in Parkinson disease genetic loci. Neurology 79, 659-667
48. De Vos, K. J., Grierson, A. J., Ackerley, S., and Miller, C. C. (2008) Role of axonal transport in neurodegenerative diseases. Annu. Rev. Neurosci. 31, 151-173
49. Scott, D. A., Tabarean, I., Tang, Y., Cartier, A., Masliah, E., and Roy, S. (2010) A pathologic cascade leading to synaptic dysfunction in-synuclein-induced neurodegeneration. J. Neurosci. 30, 8083-8095
50. Winner, B., Regensburger, M., Schreglmann, S., Boyer, L., Prots, I., Rockenstein, E., Mante, M., Zhao, C., Winkler, J., Masliah, E., and Gage, F. H. (2012) Role of-synuclein in adult neurogenesis and neuronal maturation in the dentate gyrus. J. Neurosci. 32, 16906-16916
51. Luk, K. C., Song, C., O'Brien, P., Stieber, A., Branch, J. R., Brunden, K. R., Trojanowski, J. Q., and Lee, V. M. (2009) Exogenous-synuclein fibrils seed the formation of Lewy body-like intracellular inclusions in cultured cells. Proc. Natl. Acad. Sci. U.S.A. 106, 20051-20056
52. Chung, C. Y., Koprich, J. B., Siddiqi, H., and Isacson, O. (2009) Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV-synucleinopathy. J. Neurosci. 29, 3365-3373
53. Reynolds, N. P., Soragni, A., Rabe, M., Verdes, D., Liverani, E., Handschin, S., Riek, R., and Seeger, S. (2011) Mechanism of membrane interaction and disruption by-synuclein. J. Am. Chem. Soc. 133, 19366-19375