TorsinA and DYT1 dystonia: A synaptopathy?

Biochemical Society Transactions

Volumn 38, Issue 2, 2010, Pages 452-456

  Warner, Thomas T ^a   Granata, Alassandra ^a   Schiavo, Giampietro ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

ATPase associated with various cellular activities chaperone (AAA+ chaperone); Dopaminergic pathway; Dystonia; DYT1; Synaptic vesicle (SV); TorsinA

Indexed keywords

CELL PROTEIN; CELL PROTEIN TA; CHAPERONE; UNCLASSIFIED DRUG; MUTANT PROTEIN; TOR1A PROTEIN, HUMAN;

CELL FUNCTION; CELL POLARITY; CYTOSKELETON; DYSTONIA; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; REVIEW; SECRETORY PATHWAY; SYNAPSE VESICLE; CHEMISTRY; CLASSIFICATION; CONFORMATION; DYSTONIC DISORDER; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN BINDING; STRUCTURE ACTIVITY RELATION; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION; TORSION DYSTONIA;

DYSTONIA MUSCULORUM DEFORMANS; DYSTONIC DISORDERS; HUMANS; MOLECULAR CHAPERONES; MOLECULAR CONFORMATION; MUTANT PROTEINS; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TISSUE DISTRIBUTION;

EID: 77953264427     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST0380452     Document Type: Review

References (46)

1. Fahn, S., Bressman, S.B. and Marsden, C.D. (1998) Classification of dystonia. Adv. Neurol. 78, 1-10
2. Muller, U. (2009) The monogenic primary dystonias. Brain 132, 2005-2032
3. Risch, N.J., Bressman, S.B., Senthil, G. and Ozelius, L.J. (2007) Intragenic cis and trans modification of genetic susceptibility in DYT1 torsion dystonia. Am. J. Hum. Genet. 80, 1188-1193
4. Bressman, S.B. (2004) Dystonia genotypes, phenotypes, and classification. Adv. Neurol. 94, 101-107
5. Ozelius, L.J., Hewett, J.W., Page, C.E., Bressman, S.B., Kramer, P.L., Shalish, C., de Leon, D., Brin, M.F., Raymond, D., Corey, D.P. et al. (1997) The early-onset torsion dystonia gene (DYT1) encodes an ATP-binding protein. Nat. Genet. 17, 40-48
6. Klein, C., Liu, L., Doheny, D., Kock, N., Muller, B., De Carvalho, A.P., Leung, J., de Leon, D., Bressman, S.B., Silverman, J. et al. (2002) ε-Sarcoglycan mutations found in combination with other dystonia gene mutations. Ann. Neurol. 52, 675-679
7. Perlmutter, J.S. and Mink, J.W. (2004) Dysfunction of dopaminergic pathways in dystonia. Adv. Neurol. 94, 163-170
8. Augood, S.J., Hollingsworth, Z., Albers, D.S., Yang, L., Leung, J.C., Muller, B., Klein, C., Breakefield, X.O. and Standaert, D.G. (2002) Dopamine transmission in DYT1 dystonia: a biochemical and autoradiographical study. Neurology 59, 445-448
9. Ozelius, L.J., Page, C.E., Klein, C., Hewett, J.W., Mineta, M., Leung, J., Shalish, C., Bressman, S.B., de Leon, D., Brin, M.F. et al. (1999) The TOR1A (DYT1) gene family and its role in early onset torsion dystonia. Genomics 62, 377-384
10. Vale, R.D. (2000) AAA proteins: lords of the ring. J. Cell Biol. 150, F13-F19
11. Iyer, L.M., Leipe, D.D., Koonin, E.V. and Aravind, L. (2004) Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146, 11-31
12. Ogura, T. and Wilkinson, A.J. (2001) AAA+ superfamily ATPases: common structure - diverse function. Genes Cells 6, 575-597
13. Naismith, T.V., Heuser, J.E., Breakefield, X.O. and Hanson, P.I. (2004) TorsinA in the nuclear envelope. Proc. Natl. Acad. Sci. U.S.A. 101, 7612-7617
14. Callan, A.C., Bunning, S., Jones, O.T., High, S. and Swanton, E. (2007) Biosynthesis of the dystonia-associated AAA+ ATPase torsinA at the endoplasmic reticulum. Biochem. J. 401, 607-612
15. Augood, S.J., Penney, Jr, J.B., Friberg, I.K., Breakefield, X.O., Young, A.B., Ozelius, L.J. and Standaert, D.G. (1998) Expression of the early-onset torsion dystonia gene (DYT1) in human brain. Ann. Neurol. 43, 669-673
16. Rostasy, K., Augood, S.J., Hewett, J.W., Leung, J.C., Sasaki, H., Ozelius, L.J., Ramesh, V., Standaert, D.G., Breakefield, X.O. and Hedreen, J.C. (2003) TorsinA protein and neuropathology in early onset generalized dystonia with GAG deletion. Neurobiol. Dis. 12, 11-24
17. Xiao, J., Gong, S., Zhao, Y. and LeDoux, M.S. (2004) Developmental expression of rat torsinA transcript and protein. Dev. Brain Res. 152, 47-60
18. Augood, S.J., Keller-McGandy, C.E., Siriani, A., Hewett, J., Ramesh, V., Sapp, E., DiFiglia, M., Breakefield, X.O. and Standaert, D.G. (2003) Distribution and ultrastructural localization of torsinA immunoreactivity in the human brain. Brain Res. 986, 12-21
19. Hewett, J., Gonzalez-Agosti, C., Slater, D., Ziefer, P., Li, S., Bergeron, D., Jacoby, D.J., Ozelius, L.J., Ramesh, V. and Breakefield, X.O. (2000) Mutant torsinA, responsible for early-onset torsion dystonia, forms membrane inclusions in cultured neural cells. Hum. Mol. Genet. 9, 1403-1413
20. Gonzalez-Alegre, P. and Paulson, H.L. (2004) Aberrant cellular behavior of mutant torsinA implicates nuclear envelope dysfunction in DYT1 dystonia. J. Neurosci. 24, 2593-2601
21. Kamm, C., Boston, H., Hewett, J., Wilbur, J., Corey, D.P., Hanson, P.I., Ramesh, V. and Breakefield, X.O. (2004) The early onset dystonia protein torsinA interacts with kinesin light chain 1. J. Biol. Chem. 279, 19882-19892
22. Goodchild, R.E. and Dauer, W.T. (2005) The AAA+ protein torsinA interacts with a conserved domain present in LAP1 and a novel ER protein. J. Cell Biol. 168, 855-862
23. Granata, A., Watson, R., Collinson, L.M., Schiavo, G. and Warner, T.T. (2008) The dystonia-associated protein torsinA modulates synaptic vesicle recycling. J. Biol. Chem. 283, 7568-7579
24. Ferrari-Toninelli, G., Paccioretti, S., Francisconi, S., Uberti, D. and Memo, M. (2004) TorsinA negatively controls neurite outgrowth of SH-SY5Y human neuronal cell line. Brain Res. 1012, 75-81
25. Hewett, J.W., Zeng, J., Niland, B.P., Bragg, D.C. and Breakefield, X.O. (2006) Dystonia-causing mutant torsinA inhibits cell adhesion and neurite extension through interference with cytoskeletal dynamics. Neurobiol. Dis. 22, 98-111
26. Nery, F.C., Zenge, J., Niland, B.P., Hewett, J., Farley, J., Irwin, P., Li, Y., Wicke, G., Sommenby, A. and Breakefield, X.O. (2008) TorsinA binds the KASH domain of nesprin-3 and participates in linkage between nuclear envelope and cytosol. J Cell Sci. 121, 3476-3486
27. Basham, S.E. and Rose, L.S. (2001) The Caenorhabditis elegans polarity gene ooc-5 encodes a Torsin-related protein of the AAA ATPase superfamily. Development 128, 4645-4656
28. Ferrari, T.G., Spano, P. and Memo, M. (2003) TorsinA, microtubules and cell polarity. Funct. Neurol. 18, 7-10
29. Goodchild, R.E., Kim, C.E. and Dauer, W.T. (2005) Loss of the dystonia-associated protein torsinA selectively disrupts the neuronal nuclear envelope. Neuron 48, 923-932
30. Goodchild, R.E. and Dauer, W.T. (2004) Mislocalization to the nuclear envelope: an effect of the dystonia-causing torsinA mutation. Proc. Natl. Acad. Sci. U.S.A. 101, 847-852
31. Shashidharan, P., Good, P.F., Hsu, A., Perl, D.P., Brin, M.F. and Olanow, C.W. (2000) TorsinA accumulation in Lewy bodies in sporadic Parkinson's disease. Brain Res. 877, 379-381
32. McLean, P.J., Kawamata, H., Shariff, S., Hewett, J., Sharma, N., Ueda, K., Breakefield, X.O. and Hyman, B.T. (2002) TorsinA and heat shock proteins act as molecular chaperones: suppression of α-synuclein aggregation. J. Neurochem. 83, 846-854
33. Caldwell, G.A., Cao, S., Sexton, E.G., Gelwix, C.C., Bevel, J.P. and Caldwell, K.A. (2003) Suppression of polyglutamine-induced protein aggregation in Caenorhabditis elegans by torsin proteins. Hum. Mol. Genet. 12, 307-319
34. Bragg, D.C., Kaufman, C.A., Kock, N. and Breakefield, X.O. (2004) Inhibition of N-linked glycosylation prevents inclusion formation by the dystonia-related mutant form of torsinA. Mol. Cell. Neurosci. 27, 417-426
35. Torres, G.E., Sweeney, A.L., Beaulieu, J.M., Shashidharan, P. and Caron, M.G. (2004) Effect of torsinA on membrane proteins reveals a loss of function and a dominant-negative phenotype of the dystonia-associated ΔE - torsinA mutant. Proc. Natl. Acad. Sci. U.S.A. 101, 15650-15655
36. Esapa, C.T., Waite, A., Locke, M., Benson, M.A., Kraus, M., McIlhinney, R.A., Sillitoe, R.V., Beesley, P.W. and Blake, D.J. (2007) SGCE missense mutations that cause myoclonus-dystonia syndrome impair epsilon-sarcoglycan trafficking to the plasma membrane: modulation by ubiquitination and torsinA. Hum. Mol. Genet. 16, 327-342
37. Hewett, J.W., Nery, F.C., Niland, B., Ge, P., Tan, P., Hadwiger, P., Tannous, B.A., Sah, D.W. and Breakefield, X.O. (2008) siRNA knock-down of mutant torsinA restores processing through secretory pathway in DYT1 dystonia cells. Hum. Mol. Genet. 17, 1436-1445
38. Misbahuddin, A., Placzek, M.R., Taanman, J.W., Gschmeissner, S., Schiavo, G., Cooper, J.M. and Warner, T.T. (2005) Mutant torsinA, which causes early-onset primary torsion dystonia, is redistributed to membranous structures enriched in vesicular monoamine transporter in cultured human SH-SY5Y cells. Mov. Disord. 20, 432-440
39. Muraro, N.I. and Moffat, K.G. (2006) Down-regulation of torp4a, encoding the Drosophila homologue of torsinA, results in increased neuronal degeneration. J. Neurobiol. 66, 1338-1353
40. Ilardi, J.M., Mochida, S. and Sheng, Z.H. (1999) Snapin: a SNARE-associated protein implicated in synaptic transmission. Nat. Neurosci. 2, 119-124
41. Pan, P.-Y., Tian, J.-H. and Sheng, Z.-H. (2009) Snapin facilitates the synchronisation of synaptic vesicle fusion. Neuron 61, 412-424
42. Sharma, N., Baxter, M.G., Petravicz, J., Bragg, D.C., Schienda, A., Standaert, D.G. and Breakefield, X.O. (2005) Impaired motor learning in mice expressing torsinA with the DYT1 dystonia mutation. J. Neurosci. 25, 5351-5355
43. Balcioglu, A., Kim, M.O., Sharma, N., Cha, J.H., Breakefield, X.O. and Standaert, D.G. (2007) Dopamine release is impaired in a mouse model of DYT1 dystonia. J. Neurochem. 102, 783-788
44. 2 receptor activation and N-type calcium currents in striatal cholinergic interneurons in a mouse model of DYT1 dystonia. Neurobiol. Dis. 24, 318-325
45. Giles, L.M., Chen, J., Li, L. and Chin, L.S. (2008) Dystonia-associated mutations cause premature degradation of torsinA protein and cell-type-specific mislocalization to the nuclear envelope. Hum. Mol. Genet. 17, 2712-2722
46. Naismith, T.V., Dalal, S. and Hanson, P.I. (2009) Interaction of torsinA with its major binding partner is impaired by the dystonia associated GAG deletion. J. Biol. Chem. 284, 27866-27874