Trehalose reduces aggregate formation and delays pathology in a transgenic mouse model of oculopharyngeal muscular dystrophy

Human Molecular Genetics

Volumn 15, Issue 1, 2006, Pages 23-31

  Davies, Janet E ^a   Sarkar, Sovan ^a   Rubinsztein, David C ^a  

^a ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

POLYADENYLIC ACID BINDING PROTEIN; POLYGLUTAMINE; TREHALOSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG PROTEIN BINDING; MALE; MOUSE; MUSCLE CELL; MUSCLE WEAKNESS; NICK END LABELING; NONHUMAN; OCULOPHARYNGEAL MUSCULAR DYSTROPHY; PATHOLOGY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LOCALIZATION; SKELETAL MUSCLE; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; COS CELLS; IN SITU NICK-END LABELING; INCLUSION BODIES; MICE; MICE, TRANSGENIC; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, OCULOPHARYNGEAL; MUTATION; POLY(A)-BINDING PROTEIN II; TREHALOSE;

ANIMALIA; MUS MUSCULUS;

EID: 29644437591     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi422     Document Type: Article

References (32)

1. Brown, L.Y. and Brown, S.A. (2004) Alanine tracts: The expanding story of human illness and trinucleotide repeats. Trends Genet., 20, 51-58.
2. Brais, B., Bouchard, J.P., Xie, Y.G., Rochefort, D.L., Chretien, N., Tome, F.M., Lafreniere, R.G., Rommens, J.M., Uyama, E., Nohira, O. et al. (1998) Short GCG expansions in the PABP2 gene cause oculopharyngeal muscular dystrophy. Nat. Genet., 18, 164-167.
3. Tome, F.M, Chateau, D., Helbling-Leclerc, A. and Fardeau, M. (1997) Morphological changes in muscle fibers in oculopharyngeal muscular dystrophy. Neuromuscul. Disord., 7, S63-S69.
4. Uyama, E., Tsukahara T., Goto K., Kurano, Y., Ogawa, M., Kim, Y.J., Uchino, M. and Arahata, K. (2000) Nuclear accumulation of expanded PABP2 gene product in oculopharyngeal muscular dystrophy. Muscle Nerve, 23, 1549-1554.
5. Calado, A., Tome, F.M., Brais, B., Rouleau, G.A., Kuhn, U., Wahle, E. and Carmo-Fonseca, M. (2000) Nuclear inclusions in oculopharyngeal muscular dystrophy consist of poly(A) binding protein 2 aggregates which sequester poly(A) RNA. Hum. Mol. Genet., 9, 2321-2328.
6. Albrecht, A.N., Kornak, U., Boddrich, A., Suring, K., Robinson, P.N., Stiege, A.C., Lurz, R., Stricker, S., Wanker, E.E. and Mundlos, S. (2004) A molecular pathogenesis for transcription factor associated poly-alanine tract expansions. Hum. Mol. Genet., 13, 2351-2359.
7. Bao, Y.P., Cook, L.J., O'Donovan, D., Uyama, E. and Rubinsztein, D.C. (2002) Mammalian, yeast, bacterial, and chemical chaperones reduce aggregate formation and death in a cell model of oculopharyngeal muscular dystrophy. J. Biol. Chem., 277, 12263-12269.
8. Abu-Baker, A., Messaed, C., Laganiere, J., Gaspar, C., Brais, B. and Rouleau, G.A. (2003) Involvement of the ubiquitin-proteasome pathway and molecular chaperones in oculopharyngeal muscular dystrophy. Hum. Mol. Genet., 12, 2609-2623.
9. Bao, Y.P., Sarkar, S., Uyama, E. and Rubinsztein, D.C. (2004) Congo red, doxycycline, and HSP70 overexpression reduce aggregate formation and cell death in cell models of oculopharyngeal muscular dystrophy. J. Med. Genet., 41, 47-51.
10. Davies, J.E., Wang, L., Garcia-Oroz, L., Cook, L.J., Vacher, C., O'Donovan, D.G. and Rubinsztein, D.C. (2005) Doxycycline attenuates and delays toxicity of the oculopharyngeal mutation in transgenic mice. Nat. Med., 11, 672-677.
11. Chen, Q. and Haddad, G.G. (2004) Role of trehalose phosphate synthase and trehalose during hypoxia: From flies to mammals. J. Exp. Biol., 207, 3125-3129.
12. Singer, M. and Lindquist, S. (1998) Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell, 1, 639-648.
13. Arora, A., Ha, C. and Park, C.B. (2004) Inhibition of insulin amyloid formation by small stress molecules. FEBS Lett., 564, 121-125.
14. Welch, W.J. and Brown, R. (1996) Influence of molecular and chemical chaperones on protein folding. Cell Stress Chaperones, 1, 109-115.
15. Tanaka, M., Machida, Y., Niu, S., Ikeda, T., Jana, N.R., Doi, H., Kurosawa, M., Nekooki, M. and Nukina, N. (2004) Trehalose alleviates polyglutamine-mediated pathology in a mouse model of Huntington disease. Nat. Med., 10, 148-154.
16. Oliver, A., Jamil, K., Crowe, J. and Tablin, F. (2004) Loading human mesenchymal stem cells with trehalose by fluid-phase endocytosis. Cell Preserv. Technol., 2, 35-49.
17. Ma, X., Jamil, K., MacRae, T., Clegg, J., Russell, J., Villeneuve, T., Euloth, M., Sun, Y., Crowe, J., Tablin, F. and Oliver, A. (2005) A small stress protein acts synergistically with trehalose to confer desiccation tolerance on mammalian cells. Cryobiology, 51, 15-28.
18. Collins, C. and Clegg, J. (2004) A small heat-shock, p26, from the crustacean Artemia protects mammalian cells (Cos-1) against oxidative damage. Cell Biol. Int., 28, 449-455.
19. Wolkers, W., Walker, N., Tablin, F. and Crowe, J. (2001) Human platelets loaded with trehalose survive freeze-drying. Cryobiology, 42, 79-87.
20. Sanchez, I., Mahlke, C. and Yuan, J. (2003) Pivotal role of oligomerisation in expanded polyglutamine neurodegenerative disorders. Nature, 421, 373-379.
21. Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J-J., Chotai, K., Connarty, M., Craufurd, D., Curtis, A. et al. (1996) Phenotypic characterisation of individuals with 30-40 CAG repeats in the Huntington's disease gene reveals HD cases with 36 repeats and apparently normal elderly individuals with 36-39 repeats. Am. J. Hum. Genet., 59, 16-22.
22. Ravikumar, B., Stewart, A., Kita, H., Kato, K., Duden, R. and Rubinsztein, D.C. (2003) Raised intracellular glucose concentrations reduce aggregation and cell death caused by mutant huntingtin exon 1 by decreasing mTOR phosphorylation and inducing autophagy. Hum. Mol. Genet., 12, 985-994.
23. Ravikumar, B., Duden, R. and Rubinsztein, D.C. (2002) Aggregate-prone proteins with polyglutamine and polyalanine expansions are degraded by autophagy. Hum. Mol. Genet., 11, 1107-1117.
24. Ravikumar, B., Vacher, C., Berger, Z., Davies, J.E., Luo, S., Oroz, L.G., Scaravilli, F., Easton, D.F., Duden, R., O'Kane, C.J. and Rubinsztein, D.C. (2004) Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet., 36, 585-595.
25. Calado, A., Kutay, U., Kuhn, U., Wahle, E. and Carmo-Fonseca, M. (2000) Deciphering the cellular pathway for transport of poly(A)-binding protein II. RNA, 6, 245-256.
26. Forood, B., Perez-Paya, E., Houghten, R.A. and Blondelle, S.E. (1995) Formation of an extremely stable polyalanine beta-sheet macromolecule. Biochem. Biophys. Res. Commun., 211, 7-13.
27. Blondelle, S.E., Forood, B., Houghten, R.A. and Perez-Paya, E. (1997) Polyalanine-based peptides as models for self-associated beta-pleated-sheet complexes. Biochemistry, 36, 8393-8400.
28. Shinchuck, L.M., Sharma, D., Blondelle, S.E., Reixach, N., Inouye, H. and Kirschner, D.A. (2005) Poly-(L-alanine) expansions form core beta-sheets that nucleate amyloid assembly. Proteins, doi: 10.1002/ prot.20536.
29. Richards, A.B., Krakowka, S., Dexter, L.B., Schmid, H., Wolterbeek, A.P., Waalkens-Berendsen, D.H., Shigoyuki, A. and Kurimoto, M. (2002) Trehalose: A review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol., 40, 871-898.
30. Narain, Y., Wyttenbach, A., Rankin, J., Furlong, R.A. and Rubinsztein, D.C. (1999) A molecular investigation of true dominance in Huntington's disease. J. Med. Genet., 36, 739-746.
31. Wyttenbach, A., Swartz, J., Kita, H., Thykjaer, T., Carmichael, J., Bradley, J., Brown, R., Maxwell, M., Schapira, A., Orntoft, T.F. et al. (2001) Polyglutamine expansions cause decreased CRE-mediated transcription and early gene expression changes prior to cell death in an inducible cell model of Huntington's disease. Hum. Mol. Genet., 10, 1829-1845.
32. Rogers, D.C., Fisher, E.M., Brown, S.D., Peters, J., Hunter, A.J. and Martin, J.E. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome, 8, 711-713.