Biophysical underpinnings of the repeat length dependence of polyglutamine amyloid formation

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10254-10260

  Landrum, Elizabeth ^a   Wetzel, Ronald ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY;

AGGREGATION PROPENSITY; AMYLOID FORMATION; DISEASE RISKS; LENGTH DEPENDENCE; MOLECULAR BASIS; NONLINEAR DEPENDENCE; POLYGLUTAMINE DISEASE; THERAPEUTIC STRATEGY;

BIOLOGY;

AMYLOID; POLYGLUTAMINE;

ARTICLE; BIOPHYSICS; CAG REPEAT; CELL NUCLEUS; MOLECULAR DYNAMICS; NONLINEAR SYSTEM; NUCLEAR SIZE; ONSET AGE; PRIORITY JOURNAL; PROTEIN AGGREGATION; QUANTITATIVE ANALYSIS; RIBOSOME;

AMYLOID; HUNTINGTON DISEASE; KINETICS; NUCLEATION; POLYGLUTAMINE; PROTEIN AGGREGATION; PROTEIN STABILITY; REPEAT LENGTH;

AGE OF ONSET; AMYLOID; BIOPHYSICAL PHENOMENA; HUMANS; HUNTINGTON DISEASE; KINETICS; PEPTIDES; PROTEIN CONFORMATION; TEMPERATURE; TRINUCLEOTIDE REPEATS;

EID: 84898623416     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.C114.552943     Document Type: Article

References (54)

1. van Eyk, C. L., and Richards, R. I. (2012) Dynamic mutations: where are they now? Adv. Exp. Med. Biol. 769, 55-77
2. Bates, G. P., and Benn, C. (2002) The polyglutamine diseases. in Huntington's Disease (Bates, G. P., Harper, P. S., and Jones, L., eds), pp. 429-472, Oxford University Press, Oxford, UK
3. Bates, G., Harper, P. S., and Jones, L. (eds) (2002) Huntington's Disease, Oxford University Press, Oxford, UK
4. Bates, G., Tabrizi, S. J., and Jones, L. (eds) (2014) Huntington's Disease, Oxford University Press, Oxford, UK
5. Gusella, J. F., and MacDonald, M. E. (2000) Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat. Rev. Neurosci. 1, 109-115
6. Andresen, J. M., Gayán, J., Djoussé, L., Roberts, S., Brocklebank, D., Cherny, S. S., US-Venezuela Collaborative Research Group, HD MAPS Collaborative Research Group, Cardon, L. R., Gusella, J. F., MacDonald, M. E., Myers, R. H., Housman, D. E., and Wexler, N. S. (2007) The relationship between CAG repeat length and age of onset differs for Huntington's disease patients with juvenile onset or adult onset. Ann. Hum. Genet. 71, 295-301
7. Dragatsis, I., Goldowitz, D., Del Mar, N., Deng, Y. P., Meade, C. A., Liu, L., Sun, Z., Dietrich, P., Yue, J., and Reiner, A. (2009) CAG repeat lengths≥335 attenuate the phenotype in the R6/2 Huntington's disease transgenic mouse. Neurobiol. Dis. 33, 315-330
8. Zuccato, C., Valenza, M., and Cattaneo, E. (2010) Molecular mechanisms and potential therapeutical targets in Huntington's disease. Physiol. Rev. 90, 905-981
9. Takahashi, T., Katada, S., and Onodera, O. (2010) Polyglutamine Diseases: Where does toxicity come from? What is toxicity? Where are we going? J. Mol. Cell Biol. 2, 180-191
10. Ross, C. A., and Tabrizi, S. J. (2011) Huntington's disease: from molecular pathogenesis to clinical treatment. Lancet neurology 10, 83-98
11. Jimenez-Sanchez, M., Thomson, F., Zavodszky, E., and Rubinsztein, D. C. (2012) Autophagy and polyglutamine diseases. Prog. Neurobiol. 97, 67-82
12. Orr, H. T. (2012) Polyglutamine neurodegeneration: expanded glutamines enhance native functions. Curr. Opin. Genet. Dev. 22, 251-255
13. Blum, E. S., Schwendeman, A. R., and Shaham, S. (2013) PolyQ disease: misfiring of a developmental cell death program? Trends Cell Biol. 23, 168-174
14. Labbadia, J., and Morimoto, R. I. (2013) Huntington's disease: underlying molecular mechanisms and emerging concepts. Trends Biochem. Sci. 38, 378-385
15. Hughes, A., and Jones, L. (2014) Pathogenic mechanisms. in Huntington's Disease (Bates, G., Tabrizi, S. J., and Jones, L. eds), 4th Ed., pp. 323-369, Oxford University Press, Oxford, UK
16. Bates, G. (2003) Huntingtin aggregation and toxicity in Huntington's disease. Lancet 361, 1642-1644
17. Michalik, A., and Van Broeckhoven, C. (2003) Pathogenesis of polyglutamine disorders: aggregation revisited. Hum. Mol. Genet. 12, Suppl. 2, R173-R186
18. Davranche, A., Aviolat, H., Zeder-Lutz, G., Busso, D., Altschuh, D., Trottier, Y., and Klein, F. A. C. (2011) Huntingtin affinity for partners is not changed by polyglutamine length: aggregation itself triggers aberrant interactions. Hum. Mol. Genet. 20, 2795-2806
19. Rudnicki, D. D., Pletnikova, O., Vonsattel, J. P., Ross, C. A., and Margolis, R. L. (2008)Acomparison of Huntington disease and Huntington diseaselike 2 neuropathology. J. Neuropathol. Exp. Neurol. 67, 366-374
20. Wilburn, B., Rudnicki, D. D., Zhao, J., Weitz, T. M., Cheng, Y., Gu, X., Greiner, E., Park, C. S., Wang, N., Sopher, B. L., La Spada, A. R., Osmand, A., Margolis, R. L., Sun, Y. E., and Yang, X. W. (2011) An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice. Neuron 70, 427-440
21. Arrasate, M., Mitra, S., Schweitzer, E. S., Segal, M. R., and Finkbeiner, S. (2004) Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death. Nature 431, 805-810
22. Wetzel, R., and Mishra, R. (2014) Structural biology: Order, disorder, and conformational flux. in Huntington's Disease (Bates, G., Tabrizi, S. J., and Jones, L. eds), pp. 274-322, Oxford University Press, Oxford, UK
23. 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
24. 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
25. 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 1Nterminus triggers a complex aggregation mechanism. Nat. Struct. Mol. Biol. 16, 380-389
26. Legleiter, J., Mitchell, E., Lotz, G. P., Sapp, E., Ng, C., DiFiglia, M., Thompson, L. M., and Muchowski, P. J. (2010) Mutant huntingtin fragments form oligomers in a polyglutamine length-dependent manner in vitro and in vivo. J. Biol. Chem. 285, 14777-14790
27. Takahashi, Y., Okamoto, Y., Popiel, H. A., Fujikake, N., Toda, T., Kinjo, M., and Nagai, Y. (2007) Detection of polyglutamine protein oligomers in cells by fluorescence correlation spectroscopy. J. Biol. Chem. 282, 24039-24048
28. Ossato, G., Digman, M. A., Aiken, C., Lukacsovich, T., Marsh, J. L., and Gratton, E. (2010) A two-step path to inclusion formation of huntingtin peptides revealed by number and brightness analysis. Biophys. J. 98, 3078-3085
29. Sathasivam, K., Lane, A., Legleiter, J., Warley, A., Woodman, B., Finkbeiner, S., Paganetti, P., Muchowski, P. J., Wilson, S., and Bates, G. P. (2010) Identical oligomeric and fibrillar structures captured from the brains of R6/2 and knock-in mouse models of Huntington's disease. Hum. Mol. Genet. 19, 65-78
30. Sahl, S. J., Weiss, L. E., Duim, W. C., Frydman, J., and Moerner, W. E. (2012) Cellular inclusion bodies of mutant huntingtin exon 1 obscure small fibrillar aggregate species. Sci. Rep. 2, 895
31. 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
32. 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
33. Morley, J. F., Brignull, H. R., Weyers, J. J., and Morimoto, R. I. (2002) The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proc. Natl. Acad. Sci. U.S.A. 99, 10417-10422
34. Ellisdon, A. M., Thomas, B., and Bottomley, S. P. (2006) The two-stage pathway of ataxin-3 fibrillogenesis involves a polyglutamine-independent step. J. Biol. Chem. 281, 16888-16896
35. Kar, K., Jayaraman, M., Sahoo, B., Kodali, R., and Wetzel, R. (2011) Critical nucleus size for disease-related polyglutamine aggregation is repeatlength dependent. Nat. Struct. Mol. Biol. 18, 328-336
36. Bhattacharyya, A. M., Thakur, A. K., and Wetzel, R. (2005) Polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction. Proc. Natl. Acad. Sci. U.S.A. 102, 15400-15405
37. 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
38. O'Nuallain, B., Thakur, A. K., Williams, A. D., Bhattacharyya, A. M., Chen, S., Thiagarajan, G., and Wetzel, R. (2006) Kinetics and thermodynamics of amyloid assembly using a high-performance liquid chromatographybased sedimentation assay. Methods Enzymol. 413, 34-74
39. Jayaraman, M., Thakur, A. K., Kar, K., Kodali, R., and Wetzel, R. (2011) Assays for studying nucleated aggregation of polyglutamine proteins. Methods 53, 246-254
40. Chen, S., Ferrone, F. A., and Wetzel, R. (2002) Huntington's disease ageof- onset linked to polyglutamine aggregation nucleation. Proc. Natl. Acad. Sci. U.S.A. 99, 11884-11889
41. Ferrone, F. (1999) Analysis of protein aggregation kinetics. Methods Enzymol. 309, 256-274
42. Cannon, M. J., Williams, A. D., Wetzel, R., and Myszka, D. G. (2004) Kinetic analysis of β-amyloid fibril elongation. Anal. Biochem. 328, 67-75
43. Knowles, T. P., Waudby, C. A., Devlin, G. L., Cohen, S. I., Aguzzi, A., Vendruscolo, M., Terentjev, E. M., Welland, M. E., and Dobson, C. M. (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326, 1533-1537
44. O'Nuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of Aβ (1-40) amyloid fibril elongation. Biochemistry 44, 12709-12718
45. Thakur, A. K., and Wetzel, R. (2002) Mutational analysis of the structural organization of polyglutamine aggregates. Proc. Natl. Acad. Sci. U.S.A. 99, 17014-17019
46. Bhattacharyya, A., Thakur, A. K., Chellgren, V. M., Thiagarajan, G., Williams, A. D., Chellgren, B. W., Creamer, T. P., and Wetzel, R. (2006) Oligoproline effects on polyglutamine conformation and aggregation. J. Mol. Biol. 355, 524-535
47. Slepko, N., Bhattacharyya, A. M., Jackson, G. R., Steffan, J. S., Marsh, J. L., Thompson, L. M., and Wetzel, R. (2006) Normal-repeat-length polyglutamine peptides accelerate aggregation nucleation and cytotoxicity of expanded polyglutamine proteins. Proc. Natl. Acad. Sci. U.S.A. 103, 14367-14372
48. Vitalis, A., and Pappu, R. V. (2011) Assessing the contribution of heterogeneous distributions of oligomers to aggregation mechanisms of polyglutamine peptides. Biophys. Chem. 159, 14-23
49. Williams, A. D., Shivaprasad, S., and Wetzel, R. (2006) Alanine scanning mutagenesis of Aβ(1-40) amyloid fibril stability. J. Mol. Biol. 357, 1283-1294
50. Lee, J., Culyba, E. K., Powers, E. T., and Kelly, J. W. (2011) Amyloid-β forms fibrils by nucleated conformational conversion of oligomers. Nat. Chem. Biol. 7, 602-609
51. Kurouski, D., Kar, K., Wetzel, R., Dukor, R. K., Lednev, I. K., and Nafie, L. A. (2013) Levels of supramolecular chirality of polyglutamine aggregates revealed by vibrational circular dichroism. FEBS Lett. 587, 1638-1643
52. Kar, K., Hoop, C. L., Drombosky, K. W., Baker, M. A., Kodali, R., Arduini, I., van der Wel, P. C., Horne, W. S., and Wetzel, R. (2013)β-Hairpinmediated nucleation of polyglutamine amyloid formation. J. Mol. Biol. 425, 1183-1197
53. Nakano, M., Ebina, K., and Tanaka, S. (2013) Study of the aggregation mechanism of polyglutamine peptides using replica exchange molecular dynamics simulations. J. Mol. Model. 19, 1627-1639
54. Nakano, M., Watanabe, H., Rothstein, S. M., and Tanaka, S. (2010) Comparative characterization of short monomeric polyglutamine peptides by replica exchange molecular dynamics simulation. J. Phys. Chem. B 114, 7056-7061