Post-aggregation oxidation of mutant huntingtin controls the interactions between aggregates

Journal of Biological Chemistry

Volumn 287, Issue 41, 2012, Pages 34764-34775

  Mitomi, Yasushi ^a   Nomura, Takao ^a   Kurosawa, Masaru ^b   Nukina, Nobuyuki ^b   Furukawa, Yoshiaki ^a  

^a KEIO UNIVERSITY   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATED PROTEIN; AGGREGATION MECHANISM; COPPER IONS; HUNTINGTIN; HUNTINGTON DISEASE; IN-VITRO; IN-VIVO; METHIONINE OXIDATION; METHIONINE RESIDUES; MUTANT HUNTINGTIN; NEURODEGENERATIVE DISORDERS; OXIDATIVE MODIFICATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN AGGREGATES; PROTEIN MOLECULES; SOLUBLE PROTEINS; SOLUBLE STATE;

AMINO ACIDS; HYDROGEN PEROXIDE; METAL IONS; NEURODEGENERATIVE DISEASES; OXIDATION; PROTEINS;

AGGREGATES;

COPPER ION; HUNTINGTIN; HYDROGEN PEROXIDE; METHIONINE;

ARTICLE; CONTROLLED STUDY; ELECTRON MICROSCOPY; GEL FILTRATION CHROMATOGRAPHY; HUMAN; HUNTINGTON CHOREA; IN VITRO STUDY; IN VIVO STUDY; LIGHT SCATTERING; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MORPHOLOGY; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN PURIFICATION; WESTERN BLOTTING;

COPPER; HUMANS; HUNTINGTON DISEASE; HYDROGEN PEROXIDE; METHIONINE; MUTATION; NERVE TISSUE PROTEINS; OXIDANTS; OXIDATION-REDUCTION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84867267823     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.387035     Document Type: Article

References (51)

1. Ross, C. A., and Poirier, M. A. (2004) Protein aggregation and neurodegenerative disease. Nat. Med. 10, (Suppl.) S10-S17 (Pubitemid 38901862)
2. Furukawa, Y., Fu, R., Deng, H. X., Siddique, T., and O'Halloran, T. V. (2006) Disulfide cross-linked protein represents a significant fraction of ALS-associated Cu,Zn-superoxide dismutase aggregates in spinal cords of model mice. Proc. Natl. Acad. Sci. U.S.A. 103, 7148-7153
3. Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., and Binder, L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein Tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83, 4913-4917
4. Neumann, M., Sampathu, D. M., Kwong, L. K., Truax, A. C., Micsenyi, M. C., Chou, T. T., Bruce, J., Schuck, T., Grossman, M., Clark, C. M., McCluskey, L. F., Miller, B. L., Masliah, E., Mackenzie, I. R., Feldman, H., Feiden, W., Kretzschmar, H. A., Trojanowski, J. Q., and Lee, V. M. (2006) Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 314, 130-133 (Pubitemid 44547757)
5. Seet, B. T., Dikic, I., Zhou, M. M., and Pawson, T. (2006) Reading protein modifications with interaction domains. Nat. Rev. Mol. Cell Biol. 7, 473-483 (Pubitemid 44036453)
6. Huntington's Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group. Cell 72, 971-983
7. Cattaneo, E., Zuccato, C., and Tartari, M. (2005) Normal huntingtin function. An alternative approach to Huntington's disease. Nat. Rev. Neurosci. 6, 919-930 (Pubitemid 41753086)
8. DiFiglia, M., Sapp, E., Chase, K., Schwarz, C., Meloni, A., Young, C., Martin, E., Vonsattel, J. P., Carraway, R., and Reeves, S. A. (1995) Huntingtin is a cytoplasmic protein associated with vesicles in human and rat brain neurons. Neuron 14, 1075-1081
9. Zoghbi, H. Y., and Orr, H. T. (2000) Glutamine repeats and neurodegeneration. Annu. Rev. Neurosci. 23, 217-247 (Pubitemid 30350043)
10. Browne, S. E., Bowling, A. C., MacGarvey, U., Baik, M. J., Berger, S. C., Muqit, M. M., Bird, E. D., and Beal, M. F. (1997) Oxidative damage and metabolic dysfunction in Huntington's disease. Selective vulnerability of the basal ganglia. Ann. Neurol. 41, 646-653 (Pubitemid 27212659)
11. Fox, J. H., Kama, J. A., Lieberman, G., Chopra, R., Dorsey, K., Chopra, V., Volitakis, I., Cherny, R. A., Bush, A. I., and Hersch, S. (2007) Mechanisms of copper ion mediated Huntington's disease progression. PLoS One 2, e334
12. Fox, J. H., Connor, T., Stiles, M., Kama, J., Lu, Z., Dorsey, K., Liebermann, G., Sapp, E., Cherny, R. A., Banks, M., Volitakis, I., DiFiglia, M., Berezovska, O., Bush, A. I., and Hersch, S. M. (2011) Cysteine oxidation within N-terminal mutant huntingtin promotes oligomerization and delays clearance of soluble protein. J. Biol. Chem. 286, 18320-18330
13. Hands, S., Sajjad, M. U., Newton, M. J., and Wyttenbach, A. (2011) In vitro and in vivo aggregation of a fragment of huntingtin protein directly causes free radical production. J. Biol. Chem. 286, 44512-44520
14. Furukawa, Y., Kaneko, K., Matsumoto, G., Kurosawa, M., and Nukina, N. (2009) Cross-seeding fibrillation of Q/N-rich proteins offers new pathomechanism of polyglutamine diseases. J. Neurosci. 29, 5153-5162
15. 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 (Pubitemid 27347243)
16. 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 (Pubitemid 27347244)
17. Wetzel, R. (2012) Physical chemistry of polyglutamine. Intriguing tales of a monotonous sequence. J. Mol. Biol. 421, 466-490
18. Meyer, R. A., and Brunsting, A. (1975) Light scattering from nucleated biological cells. Biophys. J. 15, 191-203
19. Akiyama, S. (2010) Quality control of protein standards for molecular mass determinations by small-angle X-ray scattering. J. Appl. Crystallogr. 43, 237-243
20. Wischik, C. M., Novak, M., Thøgersen, H. C., Edwards, P. C., Runswick, M. J., Jakes, R., Walker, J. E., Milstein, C., Roth, M., and Klug, A. (1988) Isolation of a fragment of tau derived from the core of the paired helical filament of Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 85, 4506-4510
21. Furukawa, Y., Kaneko, K., Yamanaka, K., and Nukina, N. (2010) Mutation-dependent polymorphism of Cu,Zn-superoxide dismutase aggregates in the familial form of amyotrophic lateral sclerosis. J. Biol. Chem. 285, 22221-22231
22. Aiken, C. T., Steffan, J. S., Guerrero, C. M., Khashwji, H., Lukacsovich, T., Simmons, D., Purcell, J. M., Menhaji, K., Zhu, Y. Z., Green, K., Laferla, F., Huang, L., Thompson, L. M., and Marsh, J. L. (2009) Phosphorylation of threonine 3. Implications for Huntingtin aggregation and neurotoxicity. J. Biol. Chem. 284, 29427-29436
23. 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
24. 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
25. Stadtman, E. R. (1990) Metal ion-catalyzed oxidation of proteins. Biochemical mechanism and biological consequences. Free Radic Biol. Med. 9, 315-325
26. Díaz-Hernández, M., Moreno-Herrero, F., Gómez-Ramos, P., Morán, M. A., Ferrer, I., Baró, A. M., Avila, J., Hernández, F., and Lucas, J. J. (2004) Biochemical, ultrastructural, and reversibility studies on huntingtin filaments isolated from mouse and human brain. J. Neurosci. 24, 9361-9371 (Pubitemid 39426173)
27. Beal, M. F., and Ferrante, R. J. (2004) Experimental therapeutics in transgenic mouse models of Huntington's disease. Nat. Rev. Neurosci. 5, 373-384 (Pubitemid 38568498)
28. Gu, X., Greiner, E. R., Mishra, R., Kodali, R., Osmand, A., Finkbeiner, S., Steffan, J. S., Thompson, L. M., Wetzel, R., and Yang, X. W. (2009) Serines 13 and 16 are critical determinants of full-length human mutant huntingtin induced disease pathogenesis in HD mice. Neuron 64, 828-840
29. Steffan, J. S., Agrawal, N., Pallos, J., Rockabrand, E., Trotman, L. C., Slepko, N., Illes, K., Lukacsovich, T., Zhu, Y. Z., Cattaneo, E., Pandolfi, P. P., Thompson, L. M., and Marsh, J. L. (2004) SUMO modification of Huntingtin and Huntington's disease pathology. Science 304, 100-104 (Pubitemid 38451465)
30. Vogt, W. (1995) Oxidation of methionyl residues in proteins. Tools, targets, and reversal. Free Radic Biol. Med. 18, 93-105
31. Dong, J., Atwood, C. S., Anderson, V. E., Siedlak, S. L., Smith, M. A., Perry, G., and Carey, P. R. (2003) Metal binding and oxidation of amyloid-beta within isolated senile plaque cores. Raman microscopic evidence. Biochemistry 42, 2768-2773 (Pubitemid 36331519)
32. Canello, T., Engelstein, R., Moshel, O., Xanthopoulos, K., Juanes, M. E., Langeveld, J., Sklaviadis, T., Gasset, M., and Gabizon, R. (2008) Methionine sulfoxides on PrPSc. A prion-specific covalent signature. Biochemistry 47, 8866-8873
33. Glaser, C. B., Yamin, G., Uversky, V. N., and Fink, A. L. (2005) Methionine oxidation, alpha-synuclein and Parkinson's disease. Biochim. Biophys. Acta 1703, 157-169 (Pubitemid 40170439)
34. Wolschner, C., Giese, A., Kretzschmar, H. A., Huber, R., Moroder, L., and Budisa, N. (2009) Design of anti- and pro-aggregation variants to assess the effects of methionine oxidation in human prion protein. Proc. Natl. Acad. Sci. U.S.A. 106, 7756-7761
35. Wong, Y. Q., Binger, K. J., Howlett, G. J., and Griffin, M. D. (2010) Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I. Proc. Natl. Acad. Sci. U.S.A. 107, 1977-1982
36. Sawaya, M. R., Sambashivan, S., Nelson, R., Ivanova, M. I., Sievers, S. A., Apostol, M. I., Thompson, M. J., Balbirnie, M., Wiltzius, J. J., McFarlane, H. T., Madsen, A. Ø., Riekel, C., and Eisenberg, D. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447, 453-457 (Pubitemid 46816731)
37. Kim, M. W., Chelliah, Y., Kim, S. W., Otwinowski, Z., and Bezprozvanny, I. (2009) Secondary structure of Huntingtin amino-terminal region. Structure 17, 1205-1212
38. Williamson, T. E., Vitalis, A., Crick, S. L., and Pappu, R. V. (2010) Modulation of polyglutamine conformations and dimer formation by the N-terminus of huntingtin. J. Mol. Biol. 396, 1295-1309
39. Lakhani, V. V., Ding, F., and Dokholyan, N. V. (2010) Polyglutamine induced misfolding of huntingtin exon1 is modulated by the flanking sequences. PLoS Comput. Biol. 6, e1000772
40. Sivanandam, V. N., Jayaraman, M., Hoop, C. L., Kodali, R., Wetzel, R., and van der Wel, P. C. (2011) The aggregation-enhancing huntingtin N-terminus is helical in amyloid fibrils. J. Am. Chem. Soc. 133, 4558-4566
41. Gellman, S. H. (1991) On the role of methionine residues in the sequence-independent recognition of nonpolar protein surfaces. Biochemistry 30, 6633-6636
42. 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 (Pubitemid 39434070)
43. 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
44. Stack, E. C., Kubilus, J. K., Smith, K., Cormier, K., Del Signore, S. J., Guelin, E., Ryu, H., Hersch, S. M., and Ferrante, R. J. (2005) Chronology of behavioral symptoms and neuropathological sequela in R6/2 Huntington's disease transgenic mice. J. Comp. Neurol. 490, 354-370 (Pubitemid 41232558)
45. Weiss, A., Klein, C., Woodman, B., Sathasivam, K., Bibel, M., Régulier, E., Bates, G. P., and Paganetti, P. (2008) Sensitive biochemical aggregate detection reveals aggregation onset before symptom development in cellular and murine models of Huntington's disease. J. Neurochem. 104, 846-858
46. Gutekunst, C. A., Li, S. H., Yi, H., Mulroy, J. S., Kuemmerle, S., Jones, R., Rye, D., Ferrante, R. J., Hersch, S. M., and Li, X. J. (1999) Nuclear and neuropil aggregates in Huntington's disease. Relationship to neuropathology. J. Neurosci. 19, 2522-2534 (Pubitemid 29162401)
47. Ding, F., Furukawa, Y., Nukina, N., and Dokholyan, N. V. (2012) Local unfolding of Cu,Zn superoxide dismutase monomer determines the morphology of fibrillar aggregates. J. Mol. Biol. 421, 548-560
48. Laidman, J., Forse, G. J., and Yeates, T. O. (2006) Conformational change and assembly through edge beta strands in transthyretin and other amyloid proteins. Acc. Chem. Res. 39, 576-583
49. Liu, C., Sawaya, M. R., and Eisenberg, D. (2011) β-microglobulin forms three-dimensional domain-swapped amyloid fibrils with disulfide linkages. Nat. Struct. Mol. Biol. 18, 49-55
50. Angers, R. C., Kang, H. E., Napier, D., Browning, S., Seward, T., Mathiason, C., Balachandran, A., McKenzie, D., Castilla, J., Soto, C., Jewell, J., Graham, C., Hoover, E. A., and Telling, G. C. (2010) Prion strain mutation determined by prion protein conformational compatibility and primary structure. Science 328, 1154-1158
51. Tanaka, M., Chien, P., Naber, N., Cooke, R., and Weissman, J. S. (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428, 323-328 (Pubitemid 38418803)