Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells

Human Molecular Genetics

Volumn 11, Issue 23, 2002, Pages 2905-2917

  Chan, H Y Edwin ^a,c   Warrick, John M ^a,d   Andriola, Isabella ^b   Merry, Diane ^b   Bonini, Nancy M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^d UNIVERSITY OF RICHMOND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; AMYLOID; CYTOSINE; GUANINE; PEPTIDE DERIVATIVE; POLYGLUTAMINE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DEATH; CELL NUCLEUS; CELL STRAIN; CELL STRAIN COS7; CELL VIABILITY; CELLULAR DISTRIBUTION; CLINICAL OBSERVATION; CONTROLLED STUDY; CYTOPLASM; CYTOTOXICITY; EXPERIMENTAL MODEL; GENETIC TRANSFECTION; HUNTINGTON CHOREA; IN VITRO STUDY; MAMMAL CELL; NEUROLOGIC DISEASE; NONHUMAN; NUCLEOTIDE REPEAT; ONSET AGE; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RAT; RISK ASSESSMENT; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL DEATH; CELL NUCLEUS; COS CELLS; CRICETINAE; HUMANS; L-LACTATE DEHYDROGENASE; MICROSCOPY, CONFOCAL; NUCLEAR LOCALIZATION SIGNALS; PC12 CELLS; PEPTIDE FRAGMENTS; PEPTIDES; RATS; TRINUCLEOTIDE REPEAT EXPANSION;

ANIMALIA; MAMMALIA;

EID: 0036850529     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Cummings, C.J. and Zoghbi, H.Y. (2000) Fourteen and counting: unraveling trinucleotide repeat diseases. Hum. Mol. Genet., 9, 909-916.
2. Myers, R.H., Marans, K.S. and MacDonald, M.E. (1998) Huntington's disease. In Wells, R.D. and Warren, S.T. (eds), Genetic Instabilities and Hereditary Neurological Diseases. Academic Press, San Diego, pp. 301-323.
3. 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.
4. Huang, C.C., Faber, P.W., Persichetti, E., Mittal, V., Vonsattel, J.P., MacDonald, M.E. and Gusella, J.F. (1998) Amyloid formation by mutant huntingtin: threshold, progressivity and recruitment of normal polyglutamine proteins. Somat. Cell. Mol. Genet., 24, 217-233.
5. Chen, S., Berthelier, V, Yang, W and Wetzel, R. (2001) Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity. J. Mol. Biol., 311, 173-182.
6. Masino, L., Kelly, G., Leonard, K., Trottier, Y. and Pastore, A. (2002) Solution structure of polyglutarnine tracts in GST-polyglutamine fusion proteins. FEBS Lett., 513, 267-272.
7. Bennett, M.J., Huey-Tubman, K.E., Herr, A.B., West, A.P., Ross, S.A. and Bjorkman, P.J. (2002) A linear lattice model for poly-glutamine in CAG expansion diseases. Proc. Natl Acad. Sci. USA, 99, 11634-11639.
8. Davies, S.W., Turmaine, M., Cozens, B.A., DiFiglia, M., Sharp, A.H., Ross, C.A., Scherzinger, E., Wanker, E.E., Mangiarini, L. and Bates, G.P. (1997) Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell, 90, 537-548.
9. 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.
10. 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.
11. Zoghbi, H.Y. and Orr, H.T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci., 23, 217-247.
12. Cummings, C.J., Mancini, M.A., Antalffy, B., DeFranco, D.B., Orr, H.T. and Zoghbi, HX (1998) Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet., 19, 148-154.
13. Kazemi-Esfarjani, P. and Benzer, S. (2000) Genetic suppression of polyglutarnine toxicity in Drosophila. Science, 287, 1837-1840.
14. Scherzinger, E., Lurz, R., Turmaine, M., Mangiarini, L., Hollenbach, B., Hasenbank, R., Bates, G.P., Davies, S.W., Lehrach, H. and Wanker, E.E. (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell, 90, 549-558.
15. Scherzinger, E., Sittler, A., Schweiger, K., Heiser, V., Lutz, R., Hasenbank, R., Bates, G.P., Lehrach, H. and Wanker, E.E. (1999) Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc. Natl Acad. Sci. USA, 96, 4604-4609.
16. Chen, S., Ferrone, E and Wetzel, R. (2002) Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc. Natl Acad. Sci. USA, 99, 11884-11889.
17. Zoghbi, H.Y. and Orr, H.T. (1999) Polyglutamine diseases: protein cleavage and aggregation. Curr. Opin. Neurobiol., 9, 566-570.
18. Reddy, PH., Williams, M. and Tagle, D.A. (1999) Recent advances in understanding the pathogenesis of Huntington's disease. Trends Neurosci., 22, 248-255.
19. Tobin, A.J. and Signer, E.R. (2000) Huntington's disease: the challenge for cell biologists. Trends Cell Biol., 10, 531-536.
20. Gutekunst, C.A., Li, S.H., Yi, H., Mulroy, J.S., Kuemmerle, S., Jones, R., Rye, D., Ferrante, R.J., Hersch, S.M. and Li, X.J. (1999) Nuclear and neuropil aggregates in Huntington's disease: relationship to neuropathology. J. Neurosci., 19, 2522-2534.
21. Peters, M.F., Nucifora, F.C., Jr., Kushi, J., Seaman, H.C., Cooper, J.K., Herring, W.J., Dawson, VL., Dawson, T.M. and Ross, C.A. (1999) Nuclear targeting of mutant Huntingtin increases toxicity. Mol. Cell Neurosci., 14, 121-128.
22. Klement, I.A., Skinner, P.J., Kaytor, M.D., Yi, H., Hersch, S.M., Clark, H.B., Zoghbi, H.B. and Orr, H.T. (1998) Ataxin-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell, 95, 41-53.
23. Hackam, A.S., Singaraja, R., Zhang, T., Gan, L. and Hayden, M.R. (1999) In vitro evidence for both the nucleus and cytoplasm as subcellular sites of pathogenesis in Huntington's disease. Hum. Mol. Genet., 8, 25-33.
24. Steffan, J.S., Bodai, L., Pallos, J., Poelman, M., McCampbell, A., Apostol, B.L., Kazantsev, A., Schmidt, E., Zhu, Y.Z., Greenwald, M. et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature, 413, 739-743.
25. Chen, S. and Wetzel, R. (2001) Solubilization and disaggregation of polyglutamine peptides. Protein Sci., 10, 887-891.
26. Chen, S., Berthelier, V, Hamilton, J.B., O'Nuallain, B. and Wetzel, R. (2002) Amyloid-like features of polyglutarnine aggregates and their assembly kinetics. Biochemistry, 41, 7391-7399.
27. Talcott, B. and Moore, M.S. (1999) Getting across the nuclear pore complex. Trends Cell Biol., 9, 312-318.
28. Gross, M., Wilkins, D.K., Pitkeathly, M.C., Chung, E.W, Higham, C., Clark, A. and Dobson, C.M. (1999) Formation of amyloid fibrils by peptides derived from the bacterial cold shock protein CspB. Protein Sci., 8, 1350-1357.
29. Gschwind, M. and Huber, G. (1997) Detection of apoptosis or necrosis death in neuronal cells by morphological, biochemical and molecular analysis. In Poirier, J. (ed.), Neuromethods: Apoptosis Techniques and Protocols. Humana Press, New York, Vol. 29, pp. 13-31.
30. Nucifora, F.C., Jr., Sasaki, M., Peters, M.F., Huang, H., Cooper, J.K., Yamada, M., Takahashi, H., Tsuji, S., Troncoso, J., Dawson, V.L. et al. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science, 291, 2423-2428.
31. McCampbell, A. and Fischbeck, K.H. (2001) Polyglutarnine and CBP: fatal attraction? Nat. Med., 7, 528-530.
32. Gerber, H.R, Seipel, K., Georgiev, O., Hofferer, M., Hug, M., Rusconi, S. and Schaffner, W (1994) Transcriptional activation modulated by homopolymeric glutamine and proline stretches. Science, 263, 808-811.
33. La Spada, A.R., Fu, Y., Sopher, B.L., Libby, R.T., Wang, X., Li, L.Y., Einum, D.D., Huang, J., Possin, D.E., Smith, A.C. et al. (2001) Polyglutamine-expanded ataxin-7 antagonizes crx. function and induces cone-rod dystrophy in a mouse model of sca7. Neuron, 31, 913-927.
34. Okazawa, H., Rich, T., Chang, A., Lin, X., Waragai, M., Kajikawa, M., Enokido, Y., Komuro, A., Kato, S., Shibata, M. et al. (2002) Interaction between mutant ataxin-1 and PQBP-1 affects transcription and cell death. Neuron, 34, 701-713.
35. Humbert, S. and Saudou, F. (2002) Toward cell specificity in SCA1. Neuron, 34, 669-670.
36. Cha, J.H. (2000) Transcriptional dysregulation in Huntington's disease. Trends Neurosci., 23, 387-392.
37. Holmberg, M., Duyckaerts, C., Durr, A., Cancel, G., Gourfinkel-An, I., Damier, P., Faucheux, B., Trottier, Y., Hirsch, E.C., Agid, Y. et al. (1998) Spinocerebellar ataxia type 7 (SCA7): a neurodegenerative disorder with neuronal intranuclear inclusions. Hum. Mol. Genet., 7, 913-918.
38. Aronin, N., Kim, M., Laforet, G. and DiFiglia, M. (1999) Are there multiple pathways in the pathogenesis of Huntington's disease? Phil. Trans. R. Soc. Lond. B Biol. Sci., 354, 995-1003.
39. Huynh, D.P., Figueroa, K., Hoang, N. and Pulst, S.M. (2000) Nuclear localization or inclusion body formation of ataxin-2 are not necessary for SCA2 pathogenesis in mouse or human. Nat. Genet., 26, 44-50.
40. Bucciantini, M., Giannoni, E., Chiti, F., Baroni, F., Formigli, L., Zurdo, J., Taddei, N., Ramponi, G., Dobson, C.M. and Stefani, M. (2002) Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature, 416, 507-511.
41. Arispe, N., Rojas, E. and Pollard, H.B. (1993) Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by trometharmine and aluminum. Proc. Natl Acad. Sci. USA, 90, 567-571.
42. Terzi, E., Holzemann, G. and Seelig, J. (1995) Self-association of β-amyloid peptide (1-40) in solution and binding to lipid membranes. J. Mol. Biol., 252, 633-642.
43. Mirzabekov, T.A., Lin, M.C. and Kagan, B.L. (1996) Pore formation by the cytotoxic islet amyloid peptide amylin. J. Biol. Chem., 271, 1988-1992.
44. Lashuel, H.A., Hartley, D., Petre, B.M., Walz, T. and Lansbury, P.T., Jr (2002) Neurodegenerative disease: amyloid pores from pathogenic mutations. Nature, 418, 291.
45. Ding, T.T., Lee, S.J., Rochet, J.C. and Lansbury, P.T., Jr (2002) Annular α-synuclein protofibrils are produced when spherical protofibrils are incubated in solution or bound to brain-derived membranes. Biochemistry, 41, 10209-10217.
46. Preisinger, E., Jordan, B.M., Kazantsev, A. and Housman, D. (1999) Evidence for a recruitment and sequestration mechanism in Huntington's disease. Phil. Trans. R. Soc. Lond. B Biol. Sci., 354, 1029-1034.
47. Pugsley, A.P. (1989) Protein Targeting. Academic Press, San Diego.
48. Berthelier, V., Hamilton, J.B., Chen, S. and Wetzel, R. (2001) A microtiter plate assay for polyglutarnme aggregate extension. Anal. Biochem., 295, 227-236.
49. Hann, S.R., Dixit, M., Sears, R.C. and Sealy, L. (1994) The alternatively initiated c-Myc proteins differentially regulate transcription through a noncanonical DNA-binding site. Genes. Dev., 8, 2441-2452.
50. Decker, T. and Lohmann-Matthes, M.L. (1988) A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity. J. Immunol. Meth., 115, 61-69.
51. Shearman, M.S. (1999) Toxicity of protein aggregates in PC12 cells: 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay. Meth. Enzymol., 309, 716-733.