Natural osmolytes remodel the aggregation pathway of mutant huntingtin exon 1

Biochemistry

Volumn 50, Issue 12, 2011, Pages 2048-2060

  Borwankar, Tejas ^a   Röthlein, Christoph ^a   Zhang, Gong ^a   Techen, Anne ^a   Dosche, Carsten ^a   Ignatova, Zoya ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATE FORMATION; AGGREGATE SPECIES; AMYLOIDOGENESIS; ATTRACTIVE STRATEGIES; CELL TYPES; CELLULAR PROTEINS; COMPLEX INTERACTION; DELETERIOUS EFFECTS; ENVIRONMENTAL CHANGE; FIBRILLIZATION; FIBRILLOGENESIS; HUNTINGTIN; HUNTINGTON'S DISEASE; IN-VITRO; IN-VIVO; MOLECULAR MECHANISM; MUTANT HUNTINGTIN; NATIVE STATE; NEURODEGENERATIVE; OSMOLYTES; OSMOPROTECTANTS; SOLVENT QUALITY; SURFACE AREA; TRIMETHYLAMINE N OXIDES;

AMINO ACIDS; GLYCOPROTEINS; PROTEINS;

AGGREGATES;

AMYLOID; BETAINE; COLLAGEN FIBRIL; GLYCINE; HUNTINGTIN; HUNTINGTIN EXON 1; ORGANIC COMPOUND; OSMOLYTE; PROLINE; TRIMETHYLAMINE OXIDE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; SOLUBILIZATION;

ANIMALS; BETAINE; BIOLOGICAL AGENTS; EXONS; METHYLAMINES; MUTANT PROTEINS; MUTATION; NERVE TISSUE PROTEINS; OSMOSIS; PEPTIDES; PROLINE; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, QUATERNARY; SOLUBILITY;

EID: 79952923961     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1018368     Document Type: Article

References (70)

1. Diamant, S., Eliahu, N., Rosenthal, D., and Goloubinoff, P. (2001) Chemical chaperones regulate molecular chaperones in vitro and in cells under combined salt and heat stresses J. Biol. Chem. 276, 39586-39591
2. Bolen, D. W. and Rose, G. D. (2008) Structure and energetics of the hydrogen-bonded backbone in protein folding Annu. Rev. Biochem. 77, 339-362
3. Hoffmann, E. K., Lambert, I. H., and Pedersen, S. F. (2009) Physiology of cell volume regulation in vertebrates Physiol. Rev. 89, 193-277
4. Yancey, P. H. (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses J. Exp. Biol. 208, 2819-2830 (Pubitemid 41265173)
5. Street, T. O., Bolen, D. W., and Rose, G. D. (2006) A molecular mechanism for osmolyte-induced protein stability Proc. Natl. Acad. Sci. U.S.A. 103, 13997-14002 (Pubitemid 44488414)
6. Lamitina, T., Huang, C. G., and Strange, K. (2006) Genome-wide RNAi screening identifies protein damage as a regulator of osmoprotective gene expression Proc. Natl. Acad. Sci. U.S.A. 103, 12173-12178 (Pubitemid 44215830)
7. Wood, J. M. (1999) Osmosensing by bacteria: signals and membrane-based sensors Microbiol. Mol. Biol. Rev. 63, 230-262 (Pubitemid 29116093)
8. Cayley, S. and Record, M. T., Jr. (2003) Roles of cytoplasmic osmolytes, water, and crowding in the response of Escherichia coli to osmotic stress: biophysical basis of osmoprotection by glycine betaine Biochemistry 42, 12596-12609 (Pubitemid 37337550)
9. Koo, S. P., Higgins, C. F., and Booth, I. R. (1991) Regulation of compatible solute accumulation in Salmonella typhimurium: evidence for a glycine betaine efflux system J. Gen. Microbiol. 137, 2617-2625
10. Ross, C. A. and Poirier, M. A. (2004) Protein aggregation and neurodegenerative disease Nat. Med. 10 (Suppl.) S10-S17
11. Poirier, M. A., Li, H., Macosko, J., Cai, S., Amzel, M., and Ross, C. A. (2002) Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrilization J. Biol. Chem. 277, 41032-41037 (Pubitemid 35215693)
12. Thakur, A. K., Jayaraman, M., Mishra, R., Thakur, M., Chellgren, V. M., Byeon, I. J., Anjum, D. H., Kodali, R., Creamer, T. P., Conway, J. F., Gronenborn, A. M., and Wetzel, R. (2009) Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism Nat. Struct. Mol. Biol. 16, 380-389
13. Behrends, C., Langer, C. A., Boteva, R., Bottcher, U. M., Stemp, M. J., Schaffar, G., Rao, B. V., Giese, A., Kretzschmar, H., Siegers, K., and Hartl, F. U. (2006) Chaperonin TRiC promotes the assembly of polyQ expansion proteins into nontoxic oligomers Mol. Cell 23, 887-897 (Pubitemid 44363048)
14. Kim, S., Nollen, E. A., Kitagawa, K., Bindokas, V. P., and Morimoto, R. I. (2002) Polyglutamine protein aggregates are dynamic Nat. Cell Biol. 4, 826-831
15. Cowan, K. J., Diamond, M. I., and Welch, W. J. (2003) Polyglutamine protein aggregation and toxicity are linked to the cellular stress response Hum. Mol. Genet. 12, 1377-1391 (Pubitemid 36758451)
16. Chun, W., Lesort, M., Lee, M., and Johnson, G. V. (2002) Transient osmotic stress facilitates mutant huntingtin aggregation Neuroreport 13, 2543-2546 (Pubitemid 36143559)
17. Miyata, R., Hayashi, M., Tanuma, N., Shioda, K., Fukatsu, R., and Mizutani, S. (2008) Oxidative stress in neurodegeneration in dentatorubral-pallidoluysian atrophy J. Neurol. Sci. 264, 133-139 (Pubitemid 350184086)
18. Reina, C. P., Zhong, X., and Pittman, R. N. (2010) Proteotoxic stress increases nuclear localization of ataxin-3 Hum. Mol. Genet. 19, 235-249
19. Duennwald, M. L., Jagadish, S., Muchowski, P. J., and Lindquist, S. (2006) Flanking sequences profoundly alter polyglutamine toxicity in yeast Proc. Natl. Acad. Sci. U.S.A. 103, 11045-11050 (Pubitemid 44148415)
20. Tam, S., Spiess, C., Auyeung, W., Joachimiak, L., Chen, B., Poirier, M. A., and Frydman, J. (2009) The chaperonin TRiC blocks a huntingtin sequence element that promotes the conformational switch to aggregation Nat. Struct. Mol. Biol. 16, 1279-1285
21. Bevivino, A. E. and Loll, P. J. (2001) An expanded glutamine repeat destabilizes native ataxin-3 structure and mediates formation of parallel beta -fibrils Proc. Natl. Acad. Sci. U.S.A. 98, 11955-11960 (Pubitemid 32959808)
22. Ignatova, Z. and Gierasch, L. M. (2006) Extended polyglutamine tracts cause aggregation and structural perturbation of an adjacent beta barrel protein J. Biol. Chem. 281, 12959-12967 (Pubitemid 43855389)
23. Auton, M. and Bolen, D. W. (2005) Predicting the energetics of osmolyte-induced protein folding/unfolding Proc. Natl. Acad. Sci. U.S.A. 102, 15065-15068 (Pubitemid 41513335)
24. 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 (Pubitemid 38524884)
25. Furusho, K., Yoshizawa, T., and Shoji, S. (2005) Ectoine alters subcellular localization of inclusions and reduces apoptotic cell death induced by the truncated Machado-Joseph disease gene product with an expanded polyglutamine stretch Neurobiol. Dis. 20, 170-178 (Pubitemid 41219213)
26. Sarkar, S., Davies, J. E., Huang, Z., Tunnacliffe, A., and Rubinsztein, D. C. (2007) Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and alpha-synuclein J. Biol. Chem. 282, 5641-5652 (Pubitemid 47093730)
27. Racher, K. I., Culham, D. E., and Wood, J. M. (2001) Requirements for osmosensing and osmotic activation of transporter ProP from Escherichia coli Biochemistry 40, 7324-7333 (Pubitemid 32554058)
28. Lippincott-Schwartz, J., Snapp, E., and Kenworthy, A. (2001) Studying protein dynamics in living cells Nat. Rev. Mol. Cell. Biol. 2, 444-456 (Pubitemid 33680583)
29. Stenoien, D. L., Mielke, M., and Mancini, M. A. (2002) Intranuclear ataxin1 inclusions contain both fast- and slow-exchanging components Nat. Cell Biol. 4, 806-810 (Pubitemid 35214775)
30. Wanker, E. E., Scherzinger, E., Heiser, V., Sittler, A., Eickhoff, H., and Lehrach, H. (1999) Membrane filter assay for detection of amyloid-like polyglutamine-containing protein aggregates Methods Enzymol. 309, 375-386 (Pubitemid 29446461)
31. Ko, J., Ou, S., and Patterson, P. H. (2001) New anti-huntingtin monoclonal antibodies: implications for huntingtin conformation and its binding proteins Brain Res. Bull. 56, 319-329 (Pubitemid 33062356)
32. Scherzinger, E., Sittler, A., Schweiger, K., Heiser, V., Lurz, 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. U.S.A. 96, 4604-4609 (Pubitemid 29190383)
33. Chien, P., DePace, A. H., Collins, S. R., and Weissman, J. S. (2003) Generation of prion transmission barriers by mutational control of amyloid conformations Nature 424, 948-951 (Pubitemid 37051686)
34. Nekooki-Machida, Y., Kurosawa, M., Nukina, N., Ito, K., Oda, T., and Tanaka, M. (2009) Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity Proc. Natl. Acad. Sci. U.S.A. 106, 9679-9684
35. Legleiter, J., Lotz, G. P., Miller, J., Ko, J., Ng, C., Williams, G. L., Finkbeiner, S., Patterson, P. H., and Muchowski, P. J. (2009) Monoclonal antibodies recognize distinct conformational epitopes formed by polyglutamine in a mutant huntingtin fragment J. Biol. Chem. 284, 21647-21658
36. Munishkina, L. A., Phelan, C., Uversky, V. N., and Fink, A. L. (2003) Conformational behavior and aggregation of alpha-synuclein in organic solvents: modeling the effects of membranes Biochemistry 42, 2720-2730 (Pubitemid 36330626)
37. Ignatova, Z., Thakur, A. K., Wetzel, R., and Gierasch, L. M. (2007) In-cell aggregation of a polyglutamine-containing chimera is a multistep process initiated by the flanking sequence J. Biol. Chem. 282, 36736-36743
38. Chen, H., Farkas, E. R., and Webb, W. W. (2008) Chapter 1: in vivo applications of fluorescence correlation spectroscopy Methods Cell Biol. 89, 3-35
39. Li, X. J., Li, S. H., Sharp, A. H., Nucifora, F. C., Jr., Schilling, G., Lanahan, A., Worley, P., Snyder, S. H., and Ross, C. A. (1995) A huntingtin-associated protein enriched in brain with implications for pathology Nature 378, 398-402
40. de Groot, N. S., Sabate, R., and Ventura, S. (2009) Amyloids in bacterial inclusion bodies Trends Biochem. Sci. 34, 408-416
41. Jebbar, M., Talibart, R., Gloux, K., Bernard, T., and Blanco, C. (1992) Osmoprotection of Escherichia coli by ectoine: uptake and accumulation characteristics J. Bacteriol. 174, 5027-5035
42. Dinnbier, U., Limpinsel, E., Schmid, R., and Bakker, E. P. (1988) Transient accumulation of potassium glutamate and its replacement by trehalose during adaptation of growing cells of Escherichia coli K-12 to elevated sodium chloride concentrations Arch. Microbiol. 150, 348-357
43. Burg, M. B. and Ferraris, J. D. (2008) Intracellular organic osmolytes: function and regulation J. Biol. Chem. 283, 7309-7313
44. Chien, P. and Weissman, J. S. (2001) Conformational diversity in a yeast prion dictates its seeding specificity Nature 410, 223-227 (Pubitemid 32216596)
45. Ross, C. A. and Poirier, M. A. (2005) Opinion: what is the role of protein aggregation in neurodegeneration? Nat. Rev. Mol. Cell Biol. 6, 891-898 (Pubitemid 41568738)
46. 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 (Pubitemid 34288846)
47. Ren, P. H., Lauckner, J. E., Kachirskaia, I., Heuser, J. E., Melki, R., and Kopito, R. R. (2009) Cytoplasmic penetration and persistent infection of mammalian cells by polyglutamine aggregates Nat. Cell Biol. 11, 219-225
48. Shearman, M. S. (1999) Toxicity of protein aggregates in PC12 cells: 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide assay Methods Enzymol. 309, 716-723 (Pubitemid 29446482)
49. Colby, D. W., Chu, Y., Cassady, J. P., Duennwald, M., Zazulak, H., Webster, J. M., Messer, A., Lindquist, S., Ingram, V. M., and Wittrup, K. D. (2004) Potent inhibition of huntingtin aggregation and cytotoxicity by a disulfide bond-free single-domain intracellular antibody Proc. Natl. Acad. Sci. U.S.A. 101, 17616-17621 (Pubitemid 40051935)
50. Tsirigotis, M., Baldwin, R. M., Tang, M. Y., Lorimer, I. A., and Gray, D. A. (2008) Activation of p38MAPK contributes to expanded polyglutamine-induced cytotoxicity PLoS One 3, e2130
51. Cairney, J., Booth, I. R., and Higgins, C. F. (1985) Osmoregulation of gene expression in Salmonella typhimurium: proU encodes an osmotically induced betaine transport system J. Bacteriol. 164, 1224-1232 (Pubitemid 16207267)
52. Cairney, J., Booth, I. R., and Higgins, C. F. (1985) Salmonella typhimurium proP gene encodes a transport system for the osmoprotectant betaine J. Bacteriol. 164, 1218-1223 (Pubitemid 16207266)
53. Record, M. T., Jr., Courtenay, E. S., Cayley, S., and Guttman, H. J. (1998) Biophysical compensation mechanisms buffering E. coli protein-nucleic acid interactions against changing environments Trends Biochem. Sci. 23, 190-194 (Pubitemid 28261038)
54. Natalello, A., Liu, J., Ami, D., Doglia, S. M., and de Marco, A. (2009) The osmolyte betaine promotes protein misfolding and disruption of protein aggregates Proteins 75, 509-517
55. Chen, S., Ferrone, F. A., and Wetzel, R. (2002) Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation Proc. Natl. Acad. Sci. U.S.A. 99, 11884-11889 (Pubitemid 34994493)
56. Uversky, V. N., Li, J., and Fink, A. L. (2001) Trimethylamine-N-oxide- induced folding of alpha-synuclein FEBS Lett. 509, 31-35
57. Scaramozzino, F., Peterson, D. W., Farmer, P., Gerig, J. T., Graves, D. J., and Lew, J. (2006) TMAO promotes fibrillization and microtubule assembly activity in the C-terminal repeat region of tau Biochemistry 45, 3684-3691
58. Kita, Y., Arakawa, T., Lin, T. Y., and Timasheff, S. N. (1994) Contribution of the surface free energy perturbation to protein-solvent interactions Biochemistry 33, 15178-15189
59. Dobson, C. M. (2003) Protein folding and misfolding Nature 426, 884-890 (Pubitemid 38056880)
60. Auton, M. and Bolen, D. W. (2004) Additive transfer free energies of the peptide backbone unit that are independent of the model compound and the choice of concentration scale Biochemistry 43, 1329-1342 (Pubitemid 38176532)
61. Auton, M., Bolen, D. W., and Rosgen, J. (2008) Structural thermodynamics of protein preferential solvation: osmolyte solvation of proteins, amino acids, and peptides Proteins 73, 802-813
62. Fowler, D. M., Koulov, A. V., Alory-Jost, C., Marks, M. S., Balch, W. E., and Kelly, J. W. (2006) Functional amyloid formation within mammalian tissue PLoS Biol. 4, e6
63. Bodner, R. A., Outeiro, T. F., Altmann, S., Maxwell, M. M., Cho, S. H., Hyman, B. T., McLean, P. J., Young, A. B., Housman, D. E., and Kazantsev, A. G. (2006) Pharmacological promotion of inclusion formation: a therapeutic approach for Huntington's and Parkinson's diseases Proc. Natl. Acad. Sci. U.S.A. 103, 4246-4251
64. Cohen, F. E. and Kelly, J. W. (2003) Therapeutic approaches to protein-misfolding diseases Nature 426, 905-909 (Pubitemid 38056884)
65. Muchowski, P. J. and Wacker, J. L. (2005) Modulation of neurodegeneration by molecular chaperones Nat. Rev. Neurosci. 6, 11-22 (Pubitemid 40052135)
66. Arakawa, T., Ejima, D., Kita, Y., and Tsumoto, K. (2006) Small molecule pharmacological chaperones: From thermodynamic stabilization to pharmaceutical drugs Biochim. Biophys. Acta 1764, 1677-1687 (Pubitemid 46053854)
67. Desai, U. A., Pallos, J., Ma, A. A., Stockwell, B. R., Thompson, L. M., Marsh, J. L., and Diamond, M. I. (2006) Biologically active molecules that reduce polyglutamine aggregation and toxicity Hum. Mol. Genet. 15, 2114-2124 (Pubitemid 43923401)
68. Ehrnhoefer, D. E., Duennwald, M., Markovic, P., Wacker, J. L., Engemann, S., Roark, M., Legleiter, J., Marsh, J. L., Thompson, L. M., Lindquist, S., Muchowski, P. J., and Wanker, E. E. (2006) Green tea (-)-epigallocatechin- gallate modulates early events in huntingtin misfolding and reduces toxicity in Huntington's disease models Hum. Mol. Genet. 15, 2743-2751 (Pubitemid 44400401)
69. Clark, P. L. (2004) Protein folding in the cell: reshaping the folding funnel Trends Biochem. Sci. 29, 527-534 (Pubitemid 39265169)
70. Jahn, T. R. and Radford, S. E. (2005) The Yin and Yang of protein folding FEBS J. 272, 5962-5970 (Pubitemid 41713688)