Amyloid formation by mutant huntingtin: Threshold, progressivity and recruitment of normal polyglutamine proteins

Somatic Cell and Molecular Genetics

Volumn 24, Issue 4, 1998, Pages 217-233

  Huang, C Chris ^a   Faber, Peter W ^a   Persichetti, Francesca ^a   Mittal, Vivek ^b   Vonsattel, Jean Paul ^a   MacDonald, Marcy E ^a   Gusella, James F ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; CONGO RED; GLUTAMINE; HUNTINGTIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CROSS LINKING; EMBRYO DEVELOPMENT; GENE MUTATION; GENE TARGETING; HUMAN; HUMAN TISSUE; HUNTINGTON CHOREA; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; TRINUCLEOTIDE REPEAT;

ADULT; AGED; AGED, 80 AND OVER; AMYLOID; AUTOPSY; BRAIN; CEREBELLUM; DNA-BINDING PROTEINS; FEMALE; GLUTATHIONE TRANSFERASE; HUMANS; HUNTINGTON DISEASE; MALE; MIDDLE AGED; MUTATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PEPTIDES; PREFRONTAL CORTEX; PROTEIN CONFORMATION; RECOMBINANT FUSION PROTEINS; SOLUBILITY; TATA-BOX BINDING PROTEIN; TIME FACTORS; TRANSCRIPTION FACTORS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 0032450856     PISSN: 07407750     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:SCAM.0000007124.19463.e5     Document Type: Article

References (49)

1. Gusella, J.F., Persichetti, F., and MacDonald, M.E. (1997). The genetic defect causing Huntington's disease: repeated in other contexts? Mol. Med. 3:238-246.
2. Holmberg, M., Duyckaerts, C., Durr, A., Cancel, G., Gourfinkel-An, I., Damier, P., Faucheux, B., Trottier, Y., Hirsch, E.C., Agid, Y., and Brice, A. (1998). Spinocerebellar ataxia type 7 (SCA7): a neurodegenerative disorder with neuronal intranuclear inclusions. Hum. Mol. Genet. 7:913-918.
3. Ross, C.A. (1997). Intranuclear neuronal inclusions: a common pathogenic mechanism for glutamine-repeat neurodegenerative diseases? Neuron 19:1147-1150.
4. Huntington's Disease Collaborative Research Group (1993). A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983.
5. Duyao, M.P., Auerbach, A.B., Ryan, A., Persichetti, F., Barnes, G.T., McNeil, S.M., Ge, P., Vonsattel, J.P., Gusella, J.F., Joyner, A.L., and MacDonald, ME. (1995). Inactivation of the mouse Huntington's disease gene homolog Hdh. Science 269:407-410.
6. Zeitlin, S., Liu, J.P., Chapman, D.L., Papaioannou, V.E., and Efstratiadis, A. (1995). Increased apoptosis and early embryonic lethality in mice nullizygous for the Huntington's disease gene homologue. Nat. Genet. 11:155-163.
7. Nasir, J., Floresco, S.B., JA, O.K., Diewert, V.M., Richman, J.M., Zeisler, J., Borowski, A., Marth, J.D., Phillips, A.G., and Hayden, M.R. (1995). Targeted disruption of the Huntington's disease gene results in embryonic lethality and behavioral and morphological changes in heterozygotes. Cell 81:811-823.
8. White, J.K., Auerbach, W., Duyao, M.P., Vonsattel, J.P., Gusella, J.F., Joyner, A.L., and MacDonald, M.E. (1997). Huntingtin is required for neurogenesis and is not impaired by the Huntington's disease CAG expansion. Nat. Genet. 17:404-410.
9. Vonsattel, J.P., and DiFiglia, M. (1998). Huntington disease. J. Neuropathol Exp. Neurol. 57:369-384.
10. McNeil, S.M., Novelletto, A., Srinidhi, J., Barnes, G., Kornbluth, I., Altherr, M.R., Wasmuth, J.J., Gusella, J.F., MacDonald, M.E., and Myers, R.H. (1997). Reduced penetrance of the Huntington's disease mutation. Hum. Mol. Genet. 6:775-779.
11. Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J.J., Chotai, K., Connarty, M., Crauford, D., Curtis, A., Curtis, D., Davidson, M.J., Differ, A.M., Dode, C., Dodge, A., Frontali, M., Ranen, N.G., Stine, O.C., Sherr, M., Abbott, M.H., Franz, M.L., Graham, C.A., Harper, P.S., Hedreen, J.C., Jackson, A., Kaplan, J.C., Losekoot, M., MacMillan, J.C., Morrison, P., Trottier, Y., Novelletto, A., Simpson, S.A., Theilmann, J., Whittaker, J.L., Folstein, S.E., Ross, C.A., and Hayden, M.R. (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.
12. MacDonald, M.E., Barnes, G., Srinidhi, J., Duyao, M.P., Ambrose, C.M., Myers, R.H., Gray, J., Conneally, P.M., Young, A., Penney, J., Shoulson, I., Hollingsworth, Z., Koroshetz, W., Bird, E., Vonsattel, J.P., Bonilla, E., Moskowitz, C., Penchaszadeh, G., Brzustowicz, L., Alvir, J., Bickhem Conde, J., Cha, J-H., Dure, L., Gomez, F., Ramos-Arroyo, M., Sanchez-Ramos, J., Snodgrass, S.R., de Young, M., Waxier, N.S., MacFarlane, H., Anderson, M.A., Jenkins, B., and Gusella, J.F. (1993). Gametic but not somatic instability of CAG repeat length in Huntington's disease. J. Med. Genet. 30:982-986.
13. Cummings, C.J., Mancini, M.A., Antalffy, B., DeFranco, D.B., Orr, H.T., and Zoghbi, H.Y. (1998). Chaperone suppression of aggregation and altered subcellular proteasome localization imply protein misfolding in SCA1. Nat. Genet. 19:148-154.
14. 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.
15. 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 neuntes in brain. Science 277:1990-1993.
16. Merry, D.E., Kobayashi, Y., Bailey, C.K., Taye, A.A., and Fischbeck, K.H. (1998). Cleavage, aggregation and toxicity of the expanded androgen receptor in spinal and bulbar muscular atrophy. Hum. Mol. Genet. 7:693-701.
17. Ordway, J.M., Tallaksen-Greene, S., Gutekunst, C.A., Bernstein, E.M., Cearley, J.A., Wiener, H.W., Dure, L.S.T., Lindsey, R., Hersch, S.M., Jope, R.S., Albin, R.L., and Detloff, P.J. (1997). Ectopically expressed CAG repeats cause intranuclear inclusions and a progressive late onset neurological phenotype in the mouse. Cell 91:753-763.
18. 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.
19. Perutz, M.F., Johnson, T., Suzuki, M., and Finch, J.T. (1994). Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. U.S.A. 91:5355-5358.
20. Green, H. (1993). Human genetic diseases due to codon reiteration: relationship to an evolutionary mechanism. Cell 74:955-956.
21. Cooper, A.J.L., Sheu, K.R., Burke, J.R., Onodera, O., Strittmatter, W.J., Roses, A.D., and Blass, J.P. (1997). Transglutaminase-catalyzed inactivation of glyceraldehyde 3-phosphate dehydrogenase and alpha-ketoglutarate dehydrogenase complex by polyglutamine domains of pathological length. Proc. Natl. Acad. Sci. U.S.A. 94:12604-12609.
22. Cooper, A.J., Sheu, K.F., Burke, J.R., Onodera, O., Strittmatter, W.J., Roses, A.D. and Blass, J.P. (1997). Polyglutamine domains are substrates of tissue transglutaminase: does transglutaminase play a role in expanded CAG/poly-Q neurodegenerative diseases? J. Neurochem. 69:431-434.
23. Gentile, V., Sepe, C., Calvani, M., Melone, M.A., Cotrufo, R., Cooper, A.J., Blass, J.P., and Peluso, G. (1998). Tissue transglutaminase-catalyzed formation of high-molecular-weight aggregates in vitro is favored with long polyglutamine domains: a possible mechanism contributing to CAG-triplet diseases. Arch. Biochem. Biophys. 352:314-321.
24. Kahlem, P., Terre, C., Green, H., and Djian, P. (1996). Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system. Proc. Natl. Acad. Sci. U.S.A. 93:14580-14585.
25. Kahlem, P., Green, H., and Djian, P. (1998). Transglutaminase action imitates Huntington's disease: selective polymerization of Huntingtin containing expanded polyglutamine. Mol. Cell 1:595-601.
26. 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.
27. Huang, C.C., and Herr, W. (1996). Differential control of transcription by homologous homeodomain coregulators. Mol. Cell. Biol. 16:2967-2976.
28. Mittal, V., and Hernandez, N. (1997). Role for the amino-lerminal region of human TBP in U6 snRNA transcription. Science 275:1136-1140.
29. Schende, P.F. (1992). Protein expression. In: Current Protocols in Molecular Biology, Eds: Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (New York: John Wiley and Sons).
30. Lobo, S., Ruppert, S.M., McCulloch, V., Meyer, M., Bautista, C., Falkowski, M., Stunnenberg, H.G., and Hernandez, N. (1996). Monoclonal antibodiesdirected against the amino-terminal domain of human TBP cross-react with TBP from other species. Hybridoma 15:55-68.
31. Aronin, N., Chase, K., Sagar, S.M., Sharp, F.R., and DiFiglia, M. (1991). N-methyl-D-aspartate receptor activation in the neostriatum increases c-fos and fos-related antigens selectively in medium-sized neurons. Neuroscience 44:409-420.
32. Turnell, W.G., and Finch, J.T. (1992). Binding of the dye congo red to the amyloid protein pig insulin reveals a novel homology amongst amyloid-forming peptide sequences. J. Mol. Biol. 227:1205-1223.
33. Gusella, J.F., McNeil, S., Persichetti, F., Srinidhi, J., Novelletto, A., Bird, E., Faber, P., Vonsattel, J.P., Myers, R.H., and MacDonald, M.E. (1996). Huntington's Disease. Cold Spring Harbor Symposia on Quantitative Biology LXI:615-625.
34. Myers, R.H., Leavitt, J., Farrer, L.A., Jagadeesh, J., McFarlane, H., Mastromauro, C.A., Mark, R.J., and Gusella, J.F. (1989). Homozygote for Huntington disease. Am. J. Hum. Genet. 45:615-618.
35. Wexler, N.S., Young, A.B., Tanzi, R.E., Travers, H., Starosta-Rubinstein, S., Penney, J.B., Snodgrass, S.R., Shoulson, I., Gomez, F., Ramos Arroyo, M.A., and et al. (1987). Homozygotes for Huntington's disease. Nature 326:194-197.
36. Trottier, Y., Lutz, Y., Stevanin, G., Imbert, G., Devys, D., Cancel, G., Saudou, F., Weber, C., David, G., Tora, L., Agid, Y., Hirsch, E.C., and Mandel, J-L. (1995). Polyglutamine expansion as a pathological epitope in Huntington's disease and four dominant cerebellar ataxias. Nature 378:403-406.
37. Persichetti, F., Ambrose, C.M., Ge, P., McNeil, S.M., Srinidhi, J., Anderson, M.A., Jenkins, H., Barnes, G.T., Duyao, M.P., Kanaley, L., Waxler, N.S., Myers, R.H., Bird, E.D., Vonsattel, J.P., MacDonald, M.E., and Gusella, J.F. (1995). Normal and expanded Huntington's disease gene alleles produce distinguishable proteins due to translation across the CAG repeat. Mol. Med. 1:374-383.
38. Persichetti, F., Carlee, L., Faber, P.W., McNeil, S.M., Ambrose, C.M., Srinidhi, J., Anderson, M., Barnes, G.T., Gusella, J.F., and MacDonald, M.E. (1996). Differential expression of normal and inutant Huntington's disease gene alleles. Neurobiol. Dis. 3:183-190.
39. Klement, I.A., Skinner, P.J., Kaytor, M.D., Yi, H., Hersch, S.M., Clark, H.B., Zoghbi, H.Y., and Orr, H.T. (1998). Ataxio-1 nuclear localization and aggregation: role in polyglutamine-induced disease in SCA1 transgenic mice. Cell 95:41-53.
40. Wellington, C.L., Ellerby, L.M., Hackam, A.S., Margolis, R.L., Trifiro, M.A., Singaraja, R., McCutcheon, K., Salvesen, G.S., Propp, S.S., Bromm, M., Rowland, K.J., Zhang, T., Rasper, D., Roy, S., Thornberry, N., Pinsky, L., Kakizuka, A., Ross, C.A., Nicholson, D.W., Bredesen, D.E., and Hayden, M.R. (1998). Caspase cleavage of gene products associated with triplet expansion disorders generates truncated fragments containing the polyglutamine tract. J. Biol. Chem. 273:9158-9167.
41. Cooper, J.K., Schilling, G., Peters, M.F., Herring, W.J., Sharp, A.H., Kaminsky, Z., Masone, J., Khan, F.A., Delanoy, M., Borchelt, D.R., Dawson, V.L., Dawson, T.M., and Ross, C.A. (1998). Truncated N-terminal fragments of huntingtin with expanded glutamine repeats form nuclear and cytoplasmic aggregates in cell culture. Hum. Mol. Genet. 7:783-790.
42. Hackam, A.S., Singaraja, R., Wellington, C.L., Metzler, M., McCutcheon, K., Zhang, T., Kalchman, M., and Hayden, M.R. (1998). The influence of huntingtin protein size on nuclear localization and cellular toxicity. J. Cell Biol. 141:1097-1105.
43. Li, S.H., and Li, X.J. (1998). Aggregation of N-terminal huntingtin is dependent on the length of its glutamine repeats. Hum. Mol. Genet. 7:777-782.
44. Liu, Y.F. (1998). Expression of polyglutamineexpanded Huntingtin activates the SEK1-JNK pathway and induces apoptosis in a hippocampal neuronal cell line. J. Biol. Chem. 273:28873-28877.
45. Lunkes, A., and Mandel, J.L. (1998). A cellular model that recapitulates major pathogenic steps of Huntington's disease. Hum. Mol. Genet. 7:1355-1361.
46. Martindale, D., Hackam, A., Wieczorek, A., Ellerby, L., Wellington, C., McCutcheon, K., Singaraja, R., Kazemi-Esfarjani, P., Devon, R., Kim, S.U., Bredesen, D.E., Tufaro, F., and Hayden, M.R. (1998). Length of huntingtin and its polyglutamine tract influences localization and frequency of intracellular aggregates. Nat. Genet. 18:150-154.
47. Saudou, F., Finkbeiner, S., Devys, D., and Greenberg, M.E. (1998). Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions. Cell 95:55-66.
48. Dragatsis, I., Efstratiadis, A., and Zeitlin, A. (1998). Mouse mutant embryos lacking huntingtin are rescued from lethality by wild-type extraembryonic tissues. Development 125:1529-1539.
49. Gusella, J.F., and MacDonald, M.E. (1998). Huntingtin: A single bait hooks many species. Curr. Opin. Neurobiol. 8:425-430.