Poly-L-glutamine forms cation channels: Relevance to the pathogenesis of the polyglutamine diseases

Biophysical Journal

Volumn 78, Issue 6, 2000, Pages 2892-2899

  Monoi, Hiroshi ^a,b   Futaki, Shiroh ^c   Kugimiya, Shin Ichi ^d   Minakata, Hiroyuki ^e   Yoshihara, Kazuo ^e  

^a Res Inst of Neurodeg Diseases   (Japan)

^b TOHOKU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

^e SUNTORY INSTITUTE FOR BIOORGANIC RESEARCH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CATION CHANNEL; GLUTAMINE; POLYGLUTAMINE;

AMINO ACID SEQUENCE; ARTICLE; CALCULATION; DEGENERATIVE DISEASE; HUNTINGTON CHOREA; LIPID BILAYER; MEMBRANE CONDUCTANCE; MEMBRANE PERMEABILITY; TRINUCLEOTIDE REPEAT;

EID: 0034125918     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(00)76830-5     Document Type: Article

References (45)

1. Andrew, S. E., Y. P. Goldberg, B. Kremer, H. Telenius, J. Theilmann, S. Adam, E. Starr, F. Squitieri, B. Lin, M. A. Kalchman, R. K. Graham, and M. R. Hayden. 1993. The relationship between trinucleotide (CAG) repeat length and clinical features of Huntington's disease. Nature Genet. 4:398-403.
2. Arispe, N., H. B. Pollard, and E. Rojas. 1993a. Giant multilevel cation channels formed by Alzheimer disease amyloid β-protein [AβP-(1-40)] in bilayer membranes. Proc. Natl. Acad. Sci. USA. 90:10573-10577.
3. Arispe, N., E. Rojas, and H. B. Pollard. 1993b. Alzheimer disease amyloid β protein forms calcium channels in bilayer membranes: blockade by tromethamine and aluminum. Proc. Natl. Acad. Sci. USA. 90:567-571.
4. Banfi, S., A. Servadio, M.-Y. Chung, T. J. Kwiatkowski Jr, A. E. McCall, L. A. Duvick, Y. Shen, E. J. Roth, H. T. Orr, and H. Y. Zoghbi. 1994. Identification and characterization of the gene causing type 1 spinocerebellar ataxia. Nature Genet. 7:513-520.
5. Barron, L. H., J. P. Warner, M. Porteous, S. Holloway, S. Simpson, R. Davidson, and D. J. H. Brock. 1993. A study of the Huntington's disease associated trinucleotide repeat in the Scottish population. J. Med. Genet. 30:1003-1007.
6. Cooper, A. J. L., K.-F. R. Sheu, J. R. Burke, O. Onodera, W. J. Strittmatter, A. D. Roses, and J. P. Blass. 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.
7. David, G., N. Abbas, G. Stevanin, A. Dürr, G. Yvert, G. Cancel, C. Weber, G. Imbert, F. Saudou, E. Antoniou, H. Drabkin, R. Gemmill, P. Giunti, A. Benomar, N. Wood, M. Ruberg, Y. Agid, J.-L. Mandel, and A. Brice. 1997. Cloning of the SCA7 gene reveals a highly unstable CAG repeat expansion. Nature Genet. 17:65-70.
8. 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.
9. Duyao, M., C. Ambrose, R. Myers, A. Novelletto, F. Persichetti, M. Frontali, S. Folstein, C. Ross, M. Franz, M. Abbott, J. Gray, P. Conneally, A. Young, J. Penney, Z. Hollingsworth, I. Shoulson, A. Lazzarini, A. Falek, W. Koroshetz, D. Sax, E. Bird, J. Vonsattel, E. Bonilla, J. Alvir, J. B. Conde, J.-H. Cha, L. Dure, F. Gomez, M. Ramos, J. Sanchez-Ramos, S. Snodgrass, M. de Young, N. Wexler, C. Moscowitz, G. Penchaszadeh, H. MacFarlane, M. Anderson, B. Jenkins, J. Srinidhi, G. Barnes, J. Gusella, and M. MacDonald. 1993. Trinucleotide repeat length instability and age of onset in Huntington's disease. Nature Genet. 4:387-392.
10. Forloni, G., N. Angeretti, R. Chiesa, E. Monzani, M. Salmona, O. Bugiani, and F. Tagliavini. 1993. Neurotoxicity of a prion protein fragment. Nature. 362:543-546.
11. Gentile, V., C. Sepe, M. Calvani, M. A. B. Melone, R. Cotrufo, A. J. L. Cooper, J. P. Blass, and G. Peluso. 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.
12. Green, H. 1993. Human genetic diseases due to codon reiteration: relationship to an evolutionary mechanism. Cell. 74:955-956.
13. 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.
14. Ikeda, H., M. Yamaguchi, S. Sugai, Y. Aze, S. Narumiya, and A. Kakizuka. 1996. Expanded polyglutamine in the Machado-Joseph disease protein induces cell death in vitro and in vivo. Nature Genet. 13: 196-202.
15. Imbert, G., F. Saudou, G. Yvert, D. Devys, Y. Trottier, J.-M. Garnier, C. Weber, J.-L. Mandel, G. Cancel, N. Abbas, A. Dürr, O. Didierjean, G. Stevanin, Y. Agid, and A. Brice. 1996. Cloning of the gene for spinocerebellar ataxia 2 reveals a locus with high sensitivity to expanded CAG/glutamine repeats. Nature Genet. 14:285-291.
16. Kahlem, P., H. Green, and P. Djian. 1998. Transglutaminase action imitates Huntington's disease: selective polymerization of huntingtin containing polyglutamine. Mol. Cell. 1:595-601.
17. Kahlem, P., C. Terré, H. Green, and P. Djian. 1996. Peptides containing glutamine repeats as substrates for transglutaminase-catalyzed cross-linking: relevance to diseases of the nervous system. Proc. Natl. Acad. Sci. USA. 93:14580-14585.
18. Kawaguchi, Y., T. Okamoto, M. Taniwaki, M. Aizawa, M. Inoue, S. Katayama, H. Kawakami, S. Nakamura, M. Nishimura, I. Akiguchi, J. Kimura, S. Narumiya, and A. Kakizuka. 1994. CAG expansions in a novel gene for Machado-Joseph disease at chromosome 14q32.1. Nature Genet. 8:221-228.
19. Koide, R., T. Ikeuchi, O. Onodera, H. Tanaka, S. Igarashi, K. Endo, H. Takahashi, R. Kondo, A. Ishikawa, T. Hayashi, M. Saito, A. Tomoda, T. Miike, H. Naito, F. Ikuta, and S. Tsuji. 1994. Unstable expansion of CAG repeat in hereditary dentatorubral-pallidoluysian atrophy (DRPLA). Nature Genet. 6:9-13.
20. Komure, O., A. Sano, N. Nishino, N. Yamauchi, S. Ueno, K. Kondoh, N. Sano, M. Takahashi, N. Murayama, I. Kondo, S. Nagafuchi, M. Yamada, and I. Kanazawa. 1995. DNA analysis in hereditary dentatorubral-pallidoluysian atrophy: correlation between CAG repeat length and phenotypic variation and the molecular basis of anticipation. Neurology. 45:143-149.
21. Kunz, B., E. Sandmeier, and P. Christen. 1999. Neurotoxicity of prion peptide 106-126 not confirmed. FEBS Lett. 458:65-68.
22. La Spada, A. R., E. M. Wilson, D. B. Lubahn, A. E. Harding, and K. H. Fischbeck. 1991. Androgen receptor gene mutations in X-linked spinal and bulbar muscular atrophy. Nature. 352:77-79.
23. Li, S.-H., G. Schilling, W. S. Young, III., X.-J. Li, R. L. Margolis, O. C. Stine, M. V. Wagster, M. H. Abbott, M. L. Franz, N. G. Ranen, S. E. Folstein, J. C. Hedreen, and C. A. Ross. 1993. Huntington's disease gene (IT15) is widely expressed in human and rat tissues. Neuron. 11: 985-993.
24. Lin, M.-C., T. Mirzabekov, and B. L. Kagan. 1997. Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 272:44-47.
25. Monoi, H. 1995. New tubular single-stranded helix of poly-L-amino acids suggested by molecular mechanics calculations. I. Homopolypeptides in isolated environments. Biophys. J. 69:1130-1141.
26. Monoi. H. 1997. The μ helix, a tubular single-stranded helix of poly-L-amino acids. In Progress in Cell Research, Vol. 6. M. Sokabe, A. Auerbach, and F. J. Sigworth, editors. Elsevier Science, Amsterdam. 233-249.
27. Nagafuchi, S., H. Yanagisawa, E. Ohsaki, T. Shirayama, K. Tadokoro, T. Inoue, and M. Yamada. 1994a. Structure and expression of the gene responsible for the triplet repeat disorder, dentatorubral and pallidoluysian atrophy (DRPLA). Nature Genet. 8:177-182.
28. Nagafuchi, S., H. Yanagisawa, K. Sato, T. Shirayama, E. Ohsaki, M. Bundo, T. Takeda, K. Tadokoro, I. Kondo, N. Murayama, Y. Tanaka, H. Kikushima, K. Umino, H. Kurosawa, T. Furukawa, K. Nihei, T. Inoue, A. Sano, O. Komure, M. Takahashi, T. Yoshizawa, I. Kanazawa, and M. Yamada. 1994b. Dentatorubral and pallidoluysian atrophy expansion of an unstable CAG trinucleotide on chromosome 12p. Nature Genet. 6:14-18.
29. Novelletto, A., F. Persichetti, G. Sabbadini, P. Mandich, E. Bellone, F. Ajmar, M. Pergola, L. Del Senno, M. E. MacDonald, J. F. Gusella, and M. Frontali. 1994. Analysis of the trinucleotide repeat expansion in Italian families affected with Huntington's disease. Hum. Mol. Genet. 3:93-98.
30. Orr, H. T., M.-Y. Chung, S. Banfi, T. J. Kwiatkowski, Jr., A. Servadio, A. L. Beaudet, A. E. McCall, L. A. Duvick, L. P. W. Ranum, and H. Y. Zoghbi. 1993. Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1. Nature Genet. 4:221-226.
31. Paulson, H. L., M. K. Perez, Y. Trottier, J. Q. Trojanowski, S. H. Subramony, S. S. Das, P. Vig, J.-L. Mandel, K. H. Fischbeck, and R. N. Pittman. 1997. Intranuclear inclusions of expanded polyglutamine protein in spinocerebellar ataxia type 3. Neuron. 19:333-344.
32. Perutz, M. F., T. Johnson, M. Suzuki, and J. T. Finch. 1994. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc. Natl. Acad. Sci. USA. 91:5355-5358.
33. Ranum, L. P. W., M.-Y. Chung, S. Banfi, A. Bryer, L. J. Schut, R. Ramesar, L. A. Duvick, A. McCall, S. H. Subramony, L. Goldfarb, C. Gomez, L. A. Sandkuijl, H. T. Orr, and H. Y. Zoghbi. 1994. Molecular and clinical correlations in spinocerebellar ataxia type 1: evidence for familial effects on the age of onset. Am. J. Hum. Genet. 55:244-252.
34. Roseman, M. A. 1988. Hydrophobicity of the peptide C=O⋯H-N hydrogen-bonded group. J. Mol. Biol. 201:621-623.
35. Rubinsztein, D. C., J. Leggo, R. Coles, E. Almqvist, V. Biancalana, J.-J. Cassiman, K. Chotai, M. Connarty, D. Craufurd, A. Curtis, D. Curtis, M. J. Davidson, A.-M. Differ, C. Dode, A. Dodge, M. Frontali, N. G. Ranen, O. C. Stine, M. Sherr, M. H. Abbott, M. L. Franz, C. A. Graham, P. S. Harper, J. C. Hedreen, A. Jackson, J.-C. Kaplan, M. Losekoot, J. C. MacMillan, P. Morrison, Y. Trottier, A. Novelletto, S. A. Simpson, J. Theilmann, J. L. Whittaker, S. E. Folstein, C. A. Ross, and M. R. Hayden. 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.
36. Sanpei, K., H. Takano, S. Igarashi, T. Sato, M. Oyake, H. Sasaki, A. Wakisaka, K. Tashiro, Y. Ishida, T. Ikeuchi, R. Koide, M. Saito, A. Sato, T. Tanaka, S. Hanyu, Y. Takiyama, M. Nishizawa, N. Shimizu, Y. Nomura, M. Segawa, K. Iwabuchi, I. Eguchi, H. Tanaka, H. Takahashi, and S. Tsuji. 1996. Identification of the spinocerebellar ataxia type 2 gene using a direct identification of repeat expansion and cloning technique. DIRECT. Nature Genet. 14:277-284.
37. Servadio, A., B. Koshy, D. Armstrong, B. Antalffy, H. T. Orr, and H. Y. Zoghbi. 1995. Expression analysis of the ataxin-1 protein in tissues from normal and spinocerebellar ataxia type 1 individuals. Nature Genet. 10:94-98.
38. Sharp, A. H., S. J. Loev, G. Schilling, S.-H. Li, X.-J. Li, J. Bao, M. V. Wagster, J. A. Kotzuk, J. P. Steiner, A. Lo, J. Hedreen, S. Sisodia, S. H. Snyder, T. M. Dawson, D. K. Ryugo, and C. A. Ross. 1995. Widespread expression of Huntington's disease gene (IT15) protein product. Neuron. 14:1065-1074.
39. Snell, R. G., J. C. MacMillan, J. P. Cheadle, I. Fenton, L. P. Lazarou, P. Davies, M. E. MacDonald, J. F. Gusella, P. S. Harper, and D. J. Shaw. 1993. Relationship between trinucleotide repeat expansion and phenotypic variation in Huntington's disease. Nature Genet. 4:393-397.
40. Stine. O. C., N. Pleasant, M. L. Franz, M. H. Abbott, S. E. Folstein, and C. A. Ross. 1993. Correlation between the onset age of Huntington's disease and length of the trinucleotide repeat in IT-15. Hum. Mol. Genet. 2:1547-1549.
41. Stott, K., J. M. Blackburn, P. J. G. Butler, and M. Perutz, 1995. Incorporation of glutamine repeats makes protein oligomerize: implications for neurodegenerative diseases. Proc. Natl. Acad. Sci. USA. 92:6509-6513.
42. Strong, T. V., D. A. Tagle, J. M. Valdes, L. W. Elmer, K. Boehm, M. Swaroop, K. W. Kaatz, F. S. Collins, and R. L. Albin. 1993. Widespread expression of the human and rat Huntington's disease gene in brain and nonneural tissues. Nature Genet. 5:259-265.
43. Trottier, Y., D. Devys, G. Imbert, F. Saudou, I. An, Y. Lutz, C. Weber, Y. Agid, E. C. Hirsch, and J.-L. Mandel. 1995. Cellular localization of the Huntington's disease protein and discrimination of the normal and mutated form. Nature Genet. 10:104-110.
44. Yazawa, I., N. Nukina, H. Hashida, J. Goto, M. Yamada, and I. Kanazawa. 1995. Abnormal gene product identified in hereditary dentatorubral-pallidoluysian atrophy (DRPLA) brain. Nature Genet. 10:99-103.
45. Zoghbi, H. Y., and H. T. Orr. 1999. Polyglutamine diseases: protein cleavage and aggregation. Curr. Opin. Neurobiol. 9:566-570.