Impaired ubiquitin-proteasome system activity in the synapses of Huntington's disease mice

Journal of Cell Biology

Volumn 180, Issue 6, 2008, Pages 1177-1189

  Wang, Jianjun ^a   Wang, Chuan En ^a   Orr, Adam ^a   Tydlacka, Suzanne ^a   Li, Shi Hua ^a   Li, Xiao Jiang ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEASOME; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; UBIQUITIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GLIA CELL; HUNTINGTON CHOREA; IMMUNOHISTOCHEMISTRY; MOLECULAR WEIGHT; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPSE; WESTERN BLOTTING;

ADENOSINE TRIPHOSPHATE; ANIMALS; BRAIN; CELLS, CULTURED; DISEASE MODELS, ANIMAL; GENES, REPORTER; HUNTINGTON DISEASE; INCLUSION BODIES; MICE; MICE, TRANSGENIC; MUTATION; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NUCLEAR PROTEINS; PRESYNAPTIC TERMINALS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RATS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTOSOMES; TRINUCLEOTIDE REPEAT EXPANSION; UBIQUITIN; UBIQUITINATION;

MUS;

EID: 41549129945     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200709080     Document Type: Article

References (61)

1. Avraham, E., R. Szargel, A. Eyal, R. Rott, and S. Engelender. 2005. Glycogen synthase kinase 3beta modulates synphilin-1 ubiquitylation and cellular inclusion formation by SIAH: implications for proteasomal function and Lewy body formation. J. Biol. Chem. 280:42877-42886.
2. Bence, N.F., R.M. Sampat, and R.R. Kopito. 2001. Impairment of the ubiquitin-proteasome system by protein aggregation. Science. 292:1552-1555.
3. Bennett, E.J., N.F. Bence, R. Jayakumar, and R.R. Kopito. 2005. Global impairment of the ubiquitin-proteasome system by nuclear or cytoplasmic protein aggregates precedes inclusion body formation. Mol. Cell. 17:351-365.
4. Bennett, E.J., T.A. Shaler, B. Woodman, K.Y. Ryu, T.S. Zaitseva, C.H. Becker, G.P. Bates, H. Schulman, and R.R. Kopito. 2007. Global changes to the ubiquitin system in Huntington's disease. Nature. 448:704-708.
5. Bett, J.S., G.M. Goellner, B. Woodman, G. Pratt, M. Rechsteiner, and G.P. Bates. 2006. Proteasome impairment does not contribute to pathogenesis in R6/2 Huntington's disease mice: exclusion of proteasome activator REGgamma as a therapeutic target. Hum. Mol. Genet. 15:33-44.
6. Bossy-Wetzel, E., R. Schwarzenbacher, and S.A. Lipton. 2004. Molecular pathways to neurodegeneration. Nat. Med. 10(Suppl): S2-S9.
7. Bowman, A.B., S.Y. Y oo, N.P. D antuma, and H.Y. Zoghbi. 2005. Neuronal dysfunction in a polyglutamine disease model occurs in the absence of ubiquitin-proteasome system impairment and inversely correlates with the degree of nuclear inclusion formation. Hum. Mol. Genet. 14:679-691.
8. Brooks, P., G. Fuertes, R.Z. Murray, S. Bose, E. Knecht, M.C. Rechsteiner, K.B. Hendil, K. Tanaka, J. Dyson, and J. Rivett. 2000. Subcellular localization of proteasomes and their regulatory complexes in mammalian cells. Biochem. J. 346:155-161.
9. Cepeda, C., M.A. Ariano, C.R. Calvert, J. Flores-Hernandez, S.H. Chandler, B.R. Leavitt, M.R. Hayden, and M.S. Levine. 2001. NMDA receptor function in mouse models of Huntington disease. J. Neurosci. Res. 66:525-539.
10. Chang, D.T., G.L. Rintoul, S. Pandipati, and I.J. Reynolds. 2006. Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Neurobiol. Dis. 22:388-400.
11. Chen, H., S. Polo, P.P. Di Fiore, and P.V. De Camilli. 2003. Rapid Ca2+-dependent decrease of protein ubiquitination at synapses. Proc. Natl. Acad. Sci. USA. 100:14908-14913.
12. Colledge, M., E.M. Snyder, R.A. Crozier, J.A. Soderling, Y. Jin, L.K. Langeberg, H. Lu, M.F. Bear, and J.D. Scott. 2003. Ubiquitination regulates PSD-95 degradation and AMPA receptor surface expression. Neuron. 40:595-607.
13. Cummings, D.M., A.J. Milnerwood, G.M. Dallerac, V. Waights, J.Y. Brown, S.C. Vatsavayai, M.C. Hirst, and K.P. Murphy. 2006. Aberrant cortical synaptic plasticity and dopaminergic dysfunction in a mouse model of Huntington's disease. Hum. Mol. Genet. 15:2856-2868.
14. Davies, S.W., M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, C.A. Ross, E. Scherzinger, E.E. Wanker, L. Mangiarini, and G.P. Bates. 1997. Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell. 90:537-548.
15. Demartino, G.N., and T.G. Gillette. 2007. Proteasomes: machines for all reasons. Cell. 129:659-662.
16. Díaz-Hernández, M., F. Hernández, E. Martín-Aparicio, P. Gómez-Ramos, M.A. Morán, J.G. Castaño, I. Ferrer, J. Avila, and J.J. Lucas. 2003. Neuronal induction of the immunoproteasome in Huntington's disease. J. Neurosci. 23:11653-11661.
17. Díaz-Hernández, M., A.G. Valera, M.A. Morán, P. Gómez-Ramos, B. Alvarez-Castelao, J.G. Castaño, F. Hernández, and J.J. Lucas. 2006. Inhibition of 26S proteasome activity by huntingtin filaments but not inclusion bodies isolated from mouse and human brain. J. Neurochem. 98:1585-1596.
18. DiFiglia, M., E. Sapp, K.O. Chase, S.W. Davies, G.P. Bates, J.P. Vonsattel, and N. Aronin. 1997. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science. 277:1990-1993.
19. Dong, X., J. Liu, H. Zheng, J.W. Glasford, W. Huang, Q.H. Chen, N.R. Harden, F. Li, A.M. Gerdes, and X. Wang. 2004. In situ dynamically monitoring the proteolytic function of the ubiquitin-proteasome system in cultured cardiac myocytes. Am. J. Physiol. Heart Circ. Physiol. 287:H1417-H1425.
20. Ehlers, M.D. 2003. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 6:231-242.
21. Fan, M.M., H.B. Fernandes, L.Y. Zhang, M.R. Hayden, and L.A. Raymond. 2007. Altered NMDA receptor trafficking in a yeast artificial chromosome transgenic mouse model of Huntington's disease. J. Neurosci. 27:3768-3779.
22. Glickman, M.H., and D. Raveh. 2005. Proteasome plasticity. FEBS Lett. 579:3214-3223.
23. Goldberg, A.L. 2003. Protein degradation and protection against misfolded or damaged proteins. Nature. 426:895-899.
24. Gusella, J.F., and M.E. Macdonald. 2006. Huntington's disease: seeing the pathogenic process through a genetic lens. Trends Biochem. Sci. 31:533-540.
25. Gutekunst, C.A., S.H. Li, H. Yi, J.S. Mulroy, S. Kuemmerle, R. Jones, D. Rye, R.J. Ferrante, S.M. Hersch, and X.J. Li. 1999. Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci. 19:2522-2534.
26. Hershko, A., and A. Ciechanover. 1998. The ubiquitin system. Annu. Rev. Biochem. 67:425-479.
27. Klyubin, I., D.M. Walsh, C.A. Lemere, W.K. Cullen, G.M. Shankar, V. Betts, E.T. Spooner, L. Jiang, R. Anwyl, D.J. Selkoe, and M.J. Rowan. 2005. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 11:556-561.
28. Kristiansen, M., P. Deriziotis, D.E. Dimcheff, G.S. Jackson, H. Ovaa, H. Naumann, A.R. Clarke, F.W. van Leeuwen, V. Menendez-Benito, N.P. Dantuma, et al. 2007. Disease-associated prion protein oligomers inhibit the 26S proteasome. Mol. Cell. 26:175-188.
29. Kopito, R.R. 2000. Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10:524-530.
30. Korhonen, L., and D. Lindholm. 2004. The ubiquitin proteasome system in synaptic and axonal degeneration: a new twist to an old cycle. J. Cell Biol. 165:27-30.
31. Lecker, S.H., A.L. Goldberg, and W.E. Mitch. 2006. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J. Am. Soc. Nephrol. 17:1807-1819.
32. Li, H., S.H. Li, A.L. Cheng, L. Mangiarini, G.P. Bates, and X.J. Li. 1999. Ultrastructural localization and progressive formation of neuropil aggregates in Huntington's disease transgenic mice. Hum. Mol. Genet. 8:1227-1236.
33. Li, H., S.H. Li, H. Johnston, P.F. Shelbourne, and X.J. Li. 2000. Amino-terminal fragments of mutant huntingtin show selective accumulation in striatal neurons and synaptic toxicity. Nat. Genet. 25:385-389.
34. Li, H., S.H. Li, Z.X. Yu, P. Shelbourne, and X.J. Li. 2001. Huntingtin aggregate-associated axonal degeneration is an early pathological event in Huntington's disease mice. J. Neurosci. 21:8473-8481.
35. Li, S., and X.J. Li. 2006. Multiple pathways contribute to the pathogenesis of Huntington disease. Mol. Neurodegener. 1:19.
36. Lin, C.H., S. Tallaksen-Greene, W.M. Chien, J.A. Cearley, W.S. Jackson, A.B. Crouse, S. Ren, X.J. Li, R.L. Albin, and P.J. Detloff. 2001. Neurological abnormalities in a knock-in mouse model of Huntington's disease. Hum. Mol. Genet. 10:137-144.
37. Lindsten, K., V. Menendez-Benito, M.G. Masucci, and N.P. Dantuma. 2003. A transgenic mouse model of the ubiquitin/proteasome system. Nat. Biotechnol. 21:897-902.
38. Milakovic, T., and G.V. Johnson. 2005. Mitochondrial respiration and ATP production are significantly impaired instriatal cells expressing mutant huntingtin. J. Biol. Chem. 280:30773-30782.
39. Mitchell, P.J., J.C. Hanson, A.T. Quets-Nguyen, M. Bergeron, and R.C. Smith. 2007. A quantitative method for analysis of in vitro neurite outgrowth. J. Neurosci. Methods. 164:350-362.
40. Moore, D.J., V.L. Dawson, and T.M. Dawson. 2003. Role for the ubiquitin-proteasome system in Parkinson's disease and other neurodegenerative brain amyloidoses. Neuromolecular Med. 4:95-108.
41. Orr, H.T., and H.Y. Zoghbi. 2007. Trinucleotide repeat disorders. Annu. Rev. Neurosci. 30:575-621.
42. Patrick, G.N. 2006. Synapse formation and plasticity: recent insights from the perspective of the ubiquitin proteasome system. Curr. Opin. Neurobiol. 16:90-94.
43. Phillips, G.R., J.K. Huang, Y. Wang, H. Tanaka, L. Shapiro, W. Zhang, W.S. Shan, K. Arndt, M. Frank, R.E. Gordon, et al. 2001. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron. 32:63-77.
44. Pickart, C.M., and R.E. Cohen. 2004. Proteasomes and their kin: proteases in the machine age. Nat. Rev. Mol. Cell Biol. 5:177-187.
45. Ross, C.A., and C.M. Pickart. 2004. The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol. 14:703-711.
46. Sánchez, I., C. Mahlke, and J. Yuan. 2003. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature. 421: 373-379.
47. Seo, H., K.C. Sonntag, and O. Isacson. 2004. Generalized brain and skin proteasome inhibition in Huntington's disease. Ann. Neurol. 56:319-328.
48. Seong, I.S., E. Ivanova, J.M. Lee, Y.S. Choo, E. Fossale, M. Anderson, J.F. Gusella, J.M. Laramie, R.H. Myers, M. Lesort, and M.E. MacDonald. 2005. HD CAG repeat implicates a dominant property of huntingtin in mitochondrial energy metabolism. Hum. Mol. Genet. 14:2871-2880.
49. Shin, J.Y., Z.H. Fang, Z.X. Yu, C.E. Wang, S.H. Li, and X.J. Li. 2005. Expression of mutant huntingtin in glial cells contributes to neuronal excitotoxicity. J. Cell Biol. 171:1001-1012.
50. Smith, R., P. Brundin, and J.Y. Li. 2005. Synaptic dysfunction in Huntington's disease: a new perspective. Cell. Mol. Life Sci. 62:1901-1912.
51. Speese, S.D., N. Trotta, C.K. Rodesch, B. Aravamudan, and K. Broadie. 2003. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr. Biol. 13:899-910.
52. Trushina, E., R.B. Dyer, J.D. Badger II, D. Ure, L. Eide, D.D. Tran, B.T. Vrieze, V. Legendre-Guillemin, P.S. McPherson, B.S. Mandavilli, et al. 2004. Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol. Cell. Biol. 24:8195-8209.
53. Usdin, M.T., P.F. Shelbourne, R.M. Myers, and D.V. Madison. 1999. Impaired synaptic plasticity in mice carrying the Huntington's disease mutation. Hum. Mol. Genet. 8:839-846.
54. Venkatraman, P., R. Wetzel, M. Tanaka, N. Nukina, and A.L. Goldberg. 2004. Eukaryotic proteasomes cannot digest polyglutamine sequences and release them during degradation of polyglutamine-containing proteins. Mol. Cell. 14:95-104.
55. Verhoef, L.G., K. Lindsten, M.G. Masucci, and N.P. Dantuma. 2002. Aggregate formation inhibits proteasomal degradation of polyglutamine proteins. Hum. Mol. Genet. 11:2689-2700.
56. Wilson, S.M., B. Bhattacharyya, R.A. Rachel, V. Coppola, L. Tessarollo, D.B. Householder, C.F. F letcher, R.J. Miller, N.G. Copeland, and N.A. Jenkins. 2002. Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat. Genet. 32:420-425.
57. Wó jcik, C., and G.N. DeMartino. 2003. Intracellular localization of proteasomes. Int. J. Biochem. Cell Biol. 35:579-589.
58. Yi, J.J., and M.D. Ehlers. 2005. Ubiquitin and protein turnover in synapse function. Neuron. 47:629-632.
59. Yu, Z.X., S.H. Li, J. Evans, A. Pillarisetti, H. Li, and X.J. Li. 2003. Mutant huntingtin causes context-dependent neurodegeneration in mice with Huntington's disease. J. Neurosci. 23:2193-2202.
60. Zeron, M.M., O. Hansson, N. Chen, C.L. Wellington, B.R. Leavitt, P. Brundin, M.R. Hayden, and L.A. Raymond. 2002. Increased sensitivity to N-methyl-D-aspartate receptor-mediated excitotoxicity in a mouse model of Huntington's disease. Neuron. 33:849-860.
61. Zhou, H., F. Cao, Z. Wang, Z.X. Yu, H.P. Nguyen, J. Evans, S.H. Li, and X.J. Li. 2003. Huntingtin forms toxic NH2-terminal fragment complexes that are promoted by the age-dependent decrease in proteasome activity. J. Cell Biol. 163:109-118