Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases

Human Molecular Genetics

Volumn 13, Issue 16, 2004, Pages 1803-1813

  de Pril, Remko ^a   Fischer, David F ^a   Maat Schieman, Marion L C ^b   Hobo, Barbara ^a   de Vos, Rob A I ^c   Brunt, Ewout R ^d   Hol, Elly M ^a   Roos, Raymund A C ^b   van Leeuwen, Fred W ^a  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Laboratory for Pathology East Netherlands   (Netherlands)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

POLYGLUTAMINE; PROTEASOME; UBIQUITIN;

ADULT; AGED; APOPTOSIS; ARTICLE; BIOACCUMULATION; BRAIN; CELL AGGREGATION; CELL DEATH; CELL LINE; CONTROLLED STUDY; CYTOPLASM; DISORDERS OF AMINO ACID AND PROTEIN METABOLISM; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; HUNTINGTON CHOREA; MALE; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; PRIORITY JOURNAL; PROTEIN FUNCTION; SCHOOL CHILD; SPINOCEREBELLAR DEGENERATION;

APOPTOSIS; BLOTTING, WESTERN; BRAIN; CELL SURVIVAL; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FLUORESCENT ANTIBODY TECHNIQUE; HEREDODEGENERATIVE DISORDERS, NERVOUS SYSTEM; HUMANS; IMMUNOHISTOCHEMISTRY; INCLUSION BODIES; PEPTIDES; PLASMIDS; TRANSFECTION; TUMOR CELLS, CULTURED; UBIQUITIN;

ATAXIA;

EID: 4444274236     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddh188     Document Type: Article

References (47)

1. Zoghbi, H.Y. and Orr, H.T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci., 23, 217-247.
2. Nakamura, K., Jeong, S.Y., Uchihara, T., Anno, M., Nagashima, K., Nagashima, T., Ikeda, S., Tsuji, S. and Kanazawa, I. (2001) SCA17, a novel autosomal dominant cerebellar ataxia caused by an expanded polyglutamine in TATA-binding protein. Hum. Mol. Genet., 10, 1441-1448.
3. Zhuchenko, O., Bailey, J., Bonnen, P., Ashizawa, T., Stockton, D.W., Amos, C., Dobyns, W.B., Subramony, S.H., Zoghbi, H.Y. and Lee, C.C. (1997) Autosomal dominant cerebellar ataxia (SCA6) associated with small polyglutamine expansions in the alpha 1A-voltage-dependent calcium channel. Nat. Genet., 15, 62-69.
4. DiFiglia, M., Sapp, E., Chase, K.O., Davies, S.W., Bates, G.P., Vonsattel, J.P. and Aronin, N. (1997) Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science, 277, 1990-1993.
5. Zhou, H., Cao, F., Wang, Z., Yu, Z.X., Nguyen, H.P., Evans, J., Li, S.H. and Li, X.J. (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.
6. Sieradzan, K.A., Mechan, A.O., Jones, L., Wanker, E.E., Nukina, N. and Mann, D.M. (1999) Huntington's disease intranuclear inclusions contain truncated, ubiquitinated huntingtin protein. Exp Neurol., 156, 92-99.
7. Maat-Schieman, M.L., Dorsman, J.C., Smoor, M.A., Siesling, S., Van Duinen, S.G., Verschuuren, J.J., den Dunnen, J.T., Van Ommen, G.J. and Roos, R.A. (1999) Distribution of inclusions in neuronal nuclei and dystrophic neurites in Huntington disease brain. J. Neuropathol. Exp. Neurol., 58, 129-137.
8. Halliday, G.M., McRitchie, D.A., Macdonald, V., Double, K.L., Trent, R.J. and McCusker, E. (1998) Regional specificity of brain atrophy in Huntington's disease. Exp. Neurol., 154, 663-672.
9. Takiyama, Y., Oyanagi, S., Kawashima, S., Sakamoto, H., Saito, K., Yoshida, M., Tsuji, S., Mizuno, Y. and Nishizawa, M. (1994) A clinical and pathologic study of a large Japanese family with Machado-Joseph disease tightly linked to the DNA markers on chromosome 14q. Neurology, 44, 1302-1308.
10. Willingham, S., Outeiro, T.F., DeVit, M.J., Lindquist, S.L. and Muchowski, P.J. (2003) Yeast genes that enhance the toxicity of a mutant huntingtin fragment or alpha-synuclein. Science, 302, 1769-1772.
11. Chan, H.Y.E., Warrick, J.M., Andriola, I., Merry, D. and Bonini, N.M. (2002) Genetic modulation of polyglutamine toxicity by protein conjugation pathways in Drosophila. Hum. Mol. Genet., 11, 2895-2904.
12. Wexler, N.S., Lorimer, J., Porter, J., Gomez, F., Moskowitz, C., Shackell, E., Marder, K., Penchaszadeh, G., Roberts, S.A., Gayan, J. et al. (2004) Venezuelan kindreds reveal that genetic and environmental factors modulate Huntington's disease age of onset. Proc. Natl Acad. Sci. USA, 101, 3498-3503.
13. Paulson, H.L., Perez, M.K., Trottier, Y., Trojanowski, J.Q., Subramony, S.H., Das, S.S., Vig, P., Mandel, J.L., Fischbeck, K.H. and Pittman, R.N. (1997) Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron, 19, 333-344.
14. Bence, N.F., Sampat, R.M. and Kopito, R.R. (2001) Impairment of the ubiquitin-proteasome system by protein aggregation. Science, 292, 1552-1555.
15. Verhoef, L.G., Lindsten, K., Masucci, M.G. and Dantuma, N.P. (2002) Aggregate formation inhibits proteasomal degradation of polyglutamine proteins. Hum. Mol. Genet., 11, 2689-2700.
16. Chai, Y., Koppenhafer, S.L., Shoesmith, S.J., Perez, M.K. and Paulson, H.L. (1999) Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Genet., 8, 673-682.
17. Schmidt, T., Lindenberg, K.S., Krebs, A., Schols, L., Laccone, F., Herms, J., Rechsteiner, M., Riess, O. and Landwehrmeyer, G.B. (2002) Protein surveillance machinery in brains with spinocerebellar ataxia type 3: redistribution and differential recruitment of 26S proteasome subunits and chaperones to neuronal intranuclear inclusions. Ann. Neurol., 51, 302-310.
18. Cummings, C.J., Reinstein, E., Sun, Y., Antalffy, B., Jiang, Y., Ciechanover, A., Orr, H.T., Beaudet, A.L. and Zoghbi, H.Y. (1999) Mutation of the E6-AP ubiquitin ligase reduces nuclear inclusion frequency while accelerating polyglutamine-induced pathology in SCA1 mice. Neuron, 24, 879-892.
19. Ciechanover, A. and Brundin, P. (2003) The ubiquitin proteasome system in neurodegenerative diseases. Sometimes the chicken, sometimes the egg. Neuron, 40, 427-446.
20. van Leeuwen, F.W., de Kleijn, D.P., van den Hurk, H.H., Neubauer, A., Sonnemans, M.A., Sluijs, J.A., Koycu, S., Ramdjielal, R.D., Salehi, A., Martens, G.J. et al. (1998) Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science, 279, 242-247.
21. Fischer, D.F., de Vos, R.A.I., van Dijk, R., de Vrij, F.M.S., Proper, E.A., Sonnemans, M.A.F., Verhage, M.C., Sluijs, J.A., Hobo, B., Zouambia, M. et al. (2003) Disease-specific accumulation of mutant ubiquitin as a marker for proteasomal dysfunction in the brain. FASEB J., 17, 2014-2024.
22. Lindsten, K., de Vrij, F.M., Verhoef, L.G., Fischer, D.F., van Leeuwen, F.W., Hol, E.M., Masucci, M.G. and Dantuma, N.P. (2002) Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J. Cell Biol., 157, 417-427.
23. De Vrij, F.M., Sluijs, J.A., Gregori, L., Fischer, D.F., Hermens, W.T., Goldgaber, D., Verhaagen, J., Van Leeuwen, F.W. and Hol, E.M. (2001) Mutant ubiquitin expressed in Alzheimer's disease causes neuronal death. FASEB J., 15, 2680-2688.
24. Lam, Y.A., Pickart, C.M., Alban, A., Landon, M., Jamieson, C., Ramage, R., Mayer, R.J. and Layfield, R. (2000) Inhibition of the ubiquitin-proteasome system in Alzheimer's disease. Proc. Natl Acad. Sci. USA, 97, 9902-9906.
25. Song, S., Kim, S.Y., Hong, Y.M., Jo, D.G., Lee, J.Y., Shim, S.M., Chung, C.W., Seo, S.J., Yoo, Y.J., Koh, J.Y. et al. (2003) Essential role of E2-25K/Hip-2 in mediating amyloid-beta neurotoxicity. Mol. Cell, 12, 553-563.
26. Keller, J.N., Hanni, K.B. and Markesbery, W.R. (2000) Impaired proteasome function in Alzheimer's disease. J. Neurochem., 75, 436-439.
27. Keck, S., Nitsch, R., Grune, T. and Ullrich, O. (2003) Proteasome inhibition by paired helical filament-tau in brains of patients with Alzheimer's disease. J. Neurochem., 85, 115-122.
28. de Cristofaro, T., Affaitati, A., Cariello, L., Avvedimento, E.V. and Varrone, S. (1999) The length of polyglutamine tract, its level of expression, the rate of degradation, and the transglutaminase activity influence the formation of intracellular aggregates. Biochem. Biophys. Res. Commun., 260, 150-158.
29. Hackam, A.S., Hodgson, J.G., Singaraja, R., Zhang, T., Gan, L., Gutekunst, C.A., Hersch, S.M. and Hayden, M.R. (1999) Evidence for both the nucleus and cytoplasm as subcellular sites of pathogenesis in Huntington's disease in cell culture and in transgenic mice expressing mutant huntingtin. Philos. Trans R. Soc. Lond. B, Biol. Sci., 354, 1047-1055.
30. Lunkes, A. and Mandel, J. (1998) A cellular model that recapitulates major pathogenic steps of Huntington's disease. Hum. Mol. Genet., 7, 1355-1361.
31. Encinas, M., Iglesias, M., Liu, Y., Wang, H., Muhaisen, A., Cena, V., Gallego, C. and Comella, J.X. (2000) Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J. Neurochem., 75, 991-1003.
32. Yoshizawa, T., Yoshida, H. and Shoji, S. (2001) Differential susceptibility of cultured cell lines to aggregate formation and cell death produced by the truncated Machado-Joseph disease gene product with an expanded polyglutamine stretch. Brain Res. Bull., 56, 349-352.
33. Carrard, G., Bulteau, A.L., Petropoulos, I. and Friguet, B. (2002) Impairment of proteasome structure and function in aging. Int. J. Biochem.Cell. Biol., 34, 1461-1474.
34. Furukawa, Y., Vigouroux, S., Wong, H., Guttman, M., Rajput, A.H., Ang, L., Briand, M., Kish, S.J. and Briand, Y. (2002) Brain proteasomal function in sporadic Parkinson's disease and related disorders. Ann. Neurol., 51, 779-782.
35. Ishikawa, K., Fujigasaki, H., Saegusa, H., Ohwada, K., Fujita, T., Iwamoto, H., Komatsuzaki, Y., Toru, S., Toriyama, H., Watanabe, M. et al. (1999) Abundant expression and cytoplasmic aggregations of [alpha]1A voltage-dependent calcium channel protein associated with neurodegeneration in spinocerebellar ataxia type 6. Hum. Mol. Genet., 8, 1185-1193.
36. Lam, Y.A., Lawson, T.G., Velayutham, M., Zweier, J.L. and Pickart, C.M. (2002) A proteasomal ATPase subunit recognizes the polyubiquitin degradation signal. Nature, 416, 763-767.
37. Michalik, A. and Van Broeckhoven, C. (2003) Pathogenesis of polyglutamine disorders: aggregation revisited. Hum. Mol. Genet., 12, 173R-186R.
38. Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J.J., Chotai, K., Connarty, M., Crauford, D., Curtis, A. et al. (1996) Phenotypic characterization of individuals with 30-40 CAG repeats in the Huntington disease (HD) gene reveals HD cases with 36 repeats and apparently normal elderly individuals with 36-39 repeats. Am. J. Hum. Genet., 59, 16-22.
39. McNeil, S., Novelletto, A., Srinidhi, J., Barnes, G., Kornbluth, I., Altherr, M., Wasmuth, J., Gusella, J., MacDonald, M. and Myers, R. (1997) Reduced penetrance of the Huntington's disease mutation. Hum. Mol. Genet., 6, 775-779.
40. Li, J.L., Hayden, M.R., Almqvist, E.W., Brinkman, R.R., Durr, A., Dode, C., Morrison, P.J., Suchowersky, O., Ross, C.A., Margolis, R.L. et al. (2003) A genome scan for modifiers of age at onset in Huntington disease: The HD MAPS study. Am. J. Hum. Genet., 73, 682-687.
41. Trottier, Y., Lutz, Y., Stevanin, G., Imbert, G., Devys, D., Cancel, G., Saudou, F., Weber, C., David, G., Tora, L. et al. (1995) Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature, 378, 403-406.
42. Paulson, H.L., Das, S.S., Crino, P.B., Perez, M.K., Patel, S.C., Gotsdiner, D., Fischbeck, K.H. and Pittman, R.N. (1997) Machado-Joseph disease gene product is a cytoplasmic protein widely expressed in brain. Ann. Neurol., 41, 453-462.
43. Hol, E.M., Roelofs, R.F., Moraal, E., Sonnemans, M.A., Sluijs, J.A., Proper, E.A., de Graan, P.N., Fischer, D.F. and van Leeuwen, F.W. (2003) Neuronal expression of GFAP in patients with Alzheimer pathology and identification of novel GFAP splice forms. Mol. Psychiat., 8, 786-796.
44. Neumann, M. and Gabel, D. (2002) Simple method for reduction of autofluorescence in fluorescence microscopy. J. Histochem. Cytochem., 50, 437-439.
45. Kerstens, H.M., Poddighe, P.J. and Hanselaar, A.G. (1995) A novel in situ hybridization signal amplification method based on the deposition of biotinylated tyramine. J. Histochem. Cytochem., 43, 347-352.
46. Naldini, L., Blomer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F.H., Verma, I.M. and Trono, D. (1996) In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science, 272, 263-267.
47. Field, J., Nikawa, J., Brock, D., MacDonald, B., Rodgers, L., Wilson, I.A., Lerner, R.A. and Wigler, M. (1988) Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol. Cell. Biol., 8, 2159-2165.