Dystonia-associated mutations cause premature degradation of torsinA protein and cell-type-specific mislocalization to the nuclear envelope

Human Molecular Genetics

Volumn 17, Issue 17, 2008, Pages 2712-2722

  Giles, Lisa M ^a   Chen, Jue ^a   Li, Lian ^a   Chin, Lih Shen ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMIC ACID; MUTANT PROTEIN; PROTEASOME; PROTEIN; TORSINA PROTEIN;

ARTICLE; AUTOPHAGY; CELL NUCLEUS MEMBRANE; CELL TYPE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DYSTONIA; GENE DELETION; GENE MUTATION; HUMAN; HUMAN CELL; LYSOSOME; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; TORSION DYSTONIA;

AUTOPHAGY; CELL LINE; DYSTONIA; ENDOPLASMIC RETICULUM; HELA CELLS; HUMANS; MOLECULAR CHAPERONES; NUCLEAR ENVELOPE; PROTEASOME ENDOPEPTIDASE COMPLEX;

EID: 49649120229     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddn173     Document Type: Article

References (67)

1. Bressman, S.B., Fahn, S., Ozelius, L.J., Kramer, P.L. and Risch, N.J. (2001) The DYT1 mutation and nonfamilial primary torsion dystonia. Arch. Neurol., 58, 681-682.
2. 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.
3. Leung, J.C., Klein, C., Friedman, J., Vieregge, P., Jacobs, H., Doheny, D., Kamm, C., DeLeon, D., Pramstaller, P.P., Penney, J.B. et al. (2001) Novel mutation in the TOR1A (DYT1) gene in atypical early onset dystonia and polymorphisms in dystonia and early onset parkinsonism. Neurogenetics, 3, 133-143.
4. Klein, C., Liu, L., Doheny, D., Kock, N., Muller, B., de Carvalho Aguiar, P., Leung, J., de Leon, D., Bressman, S.B., Silverman, J. et al. (2002) Epsilon-sarcoglycan mutations found in combination with other dystonia gene mutations. Ann. Neurol., 52, 675-679.
5. Shashidharan, P., Kramer, B.C., Walker, R.H., Olanow, C.W. and Brin, M.F. (2000) Immunohistochemical localization and distribution of torsinA in normal human and rat brain. Brain Res., 853, 197-206.
6. Liu, Z., Zolkiewska, A. and Zolkiewski, M. (2003) Characterization of human torsinA and its dystonia-associated mutant form. Biochem. J. 374, 117-122.
7. Hewett, J., Ziefer, P., Bergeron, D., Naismith, T., Boston, H., Slater, D., Wilbur, J., Schuback, D., Kamm, C., Smith, N. et al. (2003) TorsinA in PC12 cells: Localization in the endoplasmic reticulum and response to stress. J. Neurosci. Res., 72, 158-168.
8. Xiao, J., Gong, S., Zhao, Y. and LeDoux, M.S. (2004) Developmental expression of rat torsinA transcript and protein. Brain Res. Dev. Brain Res., 152, 47-60.
9. 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.
10. Konakova, M. and Pulst, S.M. (2001) Immunocytochemical characterization of torsin proteins in mouse brain. Brain Res., 922, 1-8.
11. 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.
12. Walker, R.H., Brin, M.F., Sandu, D., Gujjari, P., Hof, P.R., Warren Olanow, C. and Shashidharan, P. (2001) Distribution and immunohistochemical characterization of torsinA immunoreactivity in rat brain. Brain Res., 900, 348-354.
13. Walker, R.H., Brin, M.F., Sandu, D., Good, P.F. and Shashidharan, P. (2002) TorsinA immunoreactivity in brains of patients with DYT1 and non-DYT1 dystonia. Neurology, 58, 120-124.
14. Kustedjo, K., Bracey, M.H. and Cravatt, B.F. (2000) Torsin A and its torsion dystonia-associated mutant forms are lumenal glycoproteins that exhibit distinct subcellular localizations. J. Biol. Chem., 275 27933-26939.
15. O'Farrell, C., Hernandez, D.G., Evey, C., Singleton, A.B. and Cookson, M.R. (2002) Normal localization of deltaF323-Y328 mutant torsinA in transfected human cells. Neurosci. Lett., 327, 75-78.
16. Kustedjo, K., Deechongkit, S., Kelly, J.W. and Cravatt, B.F. (2003) Recombinant expression, purification, and comparative characterization of torsinA and its torsion dystonia-associated variant Delta E-torsinA. Biochemistry, 42, 15333-15341.
17. 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.
18. 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.
19. 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. USA, 101, 847-852.
20. Naismith, T.V., Heuser, J.E., Breakefield, X.O. and Hanson, P.I. (2004) TorsinA in the nuclear envelope. Proc. Natl Acad. Sci. USA, 101 7612-7617.
21. Gerace, L. (2004) TorsinA and torsion dystonia: Unraveling the architecture of the nuclear envelope. Proc. Natl Acad. Sci. USA, 101, 8839-8840.
22. Bragg, D.C., Camp, S.M., Kaufman, C.A., Wilbur, J.D., Boston, H., Schuback, D.E., Hanson, P.I., Sena-Esteves, M. and Breakefield, X.O. (2004) Perinuclear biogenesis of mutant torsin-A inclusions in cultured cells infected with tetracycline-regulated herpes simplex virus type 1 amplicon vectors. Neuroscience, 125, 651-661.
23. 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.
24. Beyer, A. (1997) Sequence analysis of the AAA protein family. Protein Sci., 6, 2043-2058.
25. 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., Jacoby, D. et al. (1998) The gene (DYT1) for early-onset torsion dystonia encodes a novel protein related to the Clp protease/heat shock family. Adv. Neurol., 78, 93-105.
26. Neuwald, A.F., Aravind, L., Spouge, J.L. and Koonin, E.V. (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res., 9, 27-43.
27. Ogura, T. and Wilkinson, A.J. (2001) AAA+ superfamily ATPases: Common structure-diverse function. Genes Cells, 6, 575-597.
28. Dalal, S. and Hanson, P.I. (2001) Membrane traffic: What drives the AAA motor? Cell, 104, 5-8.
29. Lupas, A.N. and Martin, J. (2002) AAA proteins. Curr. Opin. Struct. Biol., 12, 746-753.
30. Vale, R.D. (2000) AAA proteins. Lords of the ring. J. Cell Biol., 150, F13-F19.
31. Hanson, P.I. and Whiteheart, S.W. (2005) AAA+ proteins: Have engine, will work. Nat. Rev. Mol. Cell Biol., 6, 519-529.
32. Maurizi, M.R. and Li, C.C. (2001) AAA proteins: In search of a common molecular basis. International Meeting on Cellular Functions of AAA Proteins. EMBO Rep., 2, 980-985.
33. Patel, S. and Latterich, M. (1998) The AAA team: Related ATPases with diverse functions. Trends Cell Biol., 8, 65-71.
34. 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 {Delta}E-torsinA mutant. Proc. Natl Acad. Sci. USA, 101, 15650-15655.
35. Pham, P., Frei, K.P., Woo, W. and Truong, D.D. (2006) Molecular defects of the dystonia-causing torsinA mutation. Neuroreport, 17, 1725-1728.
36. Ciechanover, A. (2005) Intracellular protein degradation: From a idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ., 12, 1178-1190.
37. Rubinsztein, D.C. (2006) The roles of intracellular protein-degradation pathways in neurodegeneration. Nature, 443, 780-786.
38. Chin, L.S., Li, L. and Greengard, P. (1994) Neuron-specific expression of the synapsin II gene is directed by a specific core promoter and upstream regulatory elements. J. Biol. Chem., 269, 18507-18513.
39. Chin, L.S., Vavalle, J.P. and Li, L. (2002) Staring, a novel E3 ubiquitin-protein ligase that targets syntaxin 1 for degradation. J. Biol. Chem., 277, 35071-35079.
40. Ellenberg, J., Siggia, E.D., Moreira, J.E., Smith, C.L., Presley, J. Worman, H.J. and Lippincott-Schwartz, J. (1997) Nuclear membrane dynamics and reassembly in living cells: Targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol., 138 1193-1206.
41. Meusser, B., Hirsch, C., Jarosch, E. and Sommer, T. (2005) ERAD: The long road to destruction. Nat. Cell Biol., 7, 766-772.
42. Nishikawa, S., Brodsky, J.L. and Nakatsukasa, K. (2005) Roles of molecular chaperones in endoplasmic reticulum (ER) quality control ER-associated degradation (ERAD). J. Biochem., 137, 551-555.
43. Xie, Z. and Klionsky, D.J. (2007) Autophagosome formation: Core machinery and adaptations. Nat. Cell Biol., 9, 1102-1109.
44. Seglen, P.O. and Gordon, P.B. (1982) 3-methyladenine: Specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc. Natl Acad. Sci. USA, 79, 1889-1892.
45. 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.
46. 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.
47. Kock, N., Naismith, T.V., Boston, H.E., Ozelius, L.J., Corey, D. P. Breakefield, X.O. and Hanson, P.I. (2006) Effects of genetic variations in the dystonia protein torsinA: Identification of polymorphism at residue 216 as protein modifier. Hum. Mol. Genet., 15, 1355-1364.
48. Bross, P., Corydon, T.J., Andresen, B.S., Jorgensen, M.M., Bolund, L. and Gregersen, N. (1999) Protein misfolding and degradation in genetic diseases. Hum. Mutat., 14, 186-198.
49. Olzmann, J.A., Brown, K., Wilkinson, K.D., Rees, H.D., Huai, Q., Ke, H., Levey, A.I., Li, L. and Chin, L.S. (2004) Familial Parkinson's disease-associated L166P mutation disrupts DJ-1 protein folding and function. J. Biol. Chem., 279, 8506-8515.
50. 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 alpha-synuclein aggregation. J. Neurochem., 83, 846-854.
51. 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.
52. 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.
53. Ding, W.X. and Yin, X.M. (2008) Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy, 4, 141-150.
54. Kostova, Z., Tsai, Y.C. and Weissman, A.M. (2007) Ubiquitin ligases, critical mediators of endoplasmic reticulum-associated degradation. Semin. Cell Dev. Biol., 18, 770-779.
55. Yorimitsu, T. and Klionsky, D.J. (2007) Endoplasmic reticulum stress: A new pathway to induce autophagy. Autophagy, 3, 160-162.
56. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory, Colspring Harbor, NY.
57. Kirk, E., Chin, L.S. and Li, L. (2006) GRIF1 binds Hrs and is a new regulator of endosomal trafficking. J. Cell Sci., 119, 4689-4701.
58. Chin, L.S., Nugent, R.D., Raynor, M.C., Vavalle, J.P. and Li, L. (2000) SNIP, a novel SNAP-25-interacting protein implicated in regulated exocytosis. J. Biol. Chem., 275, 1191-1200.
59. Rogers, A., Schmuck, G., Scholz, G. and Williams, D.C. (2004) c-fos mRNA expression in rat cortical neurons during glutamate-mediated excitotoxicity. Toxicol. Sci., 82, 562-569.
60. Lee, J.T., Wheeler, T.C., Li, L. and Chin, L.S. (2008) Ubiquitination of alpha-synuclein by Siah-1 promotes alpha-synuclein aggregation and apoptotic cell death. Hum. Mol. Genet., 17, 906-917.
61. Bi, Y., Palmiter, R.D., Wood, K.M. and Ma, Q. (2004) Induction of metallothionein I by phenolic antioxidants requires metal-activated transcription factor 1 (MTF-1) and zinc. Biochem. J., 380, 695-703.
62. Ma, Q., Kinneer, K., Bi, Y., Chan, J.Y. and Kan, Y.W. (2004) Induction of murine NAD(P)H:qUinone oxidoreductase by 2,3,7,8-tetrachlorodibenzo-p-dioxin requires the CNC (cap 'n' collar) basic leucine zipper transcription factor Nrf2 (nuclear factor erythroid 2-related factor 2): Cross-interaction between AhR (aryl hydrocarbon receptor) and Nrf2 signal transduction. Biochem. J., 377, 205-213.
63. Olzmann, J.A., Li, L., Chudaev, M.V., Chen, J., Perez, F.A., Palmiter, R.D. and Chin, L.S. (2007) Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J. Cell Biol., 178, 1025-1038.
64. Volpicelli, L.A., Lah, J.J., Fang, G., Goldenring, J.R. and Levey, A.I. (2002) Rab11a and myosin Vb regulate recycling of the M4 muscarinic acetylcholine receptor. J. Neurosci., 22, 9776-9784.
65. Volpicelli, L.A., Lah, J.J. and Levey, A.I. (2001) Rab5-dependent trafficking of the m4 muscarinic acetylcholine receptor to the plasma membrane, early endosomes, and multivesicular bodies. J. Biol. Chem. 276, 47590-47598.
66. Kim, B.Y., Olzmann, J.A., Barsh, G.S., Chin, L.S. and Li, L. (2007) Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell., 18, 1129-1142.
67. Wheeler, T.C., Chin, L.S., Li, Y., Roudabush, F.L. and Li, L. (2002) Regulation of synaptophysin degradation by mammalian homologues of seven in absentia. J. Biol. Chem., 277, 10273-10282.