Serine phosphorylation suppresses huntingtin amyloid accumulation by altering protein aggregation properties

Journal of Molecular Biology

Volumn 424, Issue 1-2, 2012, Pages 1-14

  Mishra, Rakesh ^a   Hoop, Cody L ^a   Kodali, Ravindra ^a   Sahoo, Bankanidhi ^a   Van Der Wel, Patrick C A ^a   Wetzel, Ronald ^a  

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

Author keywords

critical concentration; nucleation; phosphomimetic; posttranslational modification; helical oligomers

Indexed keywords

AMYLOID; HUNTINGTIN; SERINE;

ALPHA HELIX; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXON; GENE MUTATION; HUNTINGTON CHOREA; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; THERMODYNAMICS;

MUS;

EID: 84868200854     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.09.011     Document Type: Article

References (47)

1. C. Zuccato, M. Valenza, and E. Cattaneo Molecular mechanisms and potential therapeutical targets in Huntington's disease Physiol. Rev. 90 2010 905 981
2. C.A. Ross, and S.J. Tabrizi Huntington's disease: from molecular pathogenesis to clinical treatment Lancet Neurol. 10 2011 83 98
3. G.P. Bates, and C. Benn The polyglutamine diseases G.P. Bates, P.S. Harper, L. Jones, Huntington's Disease 2002 Oxford University Press Oxford, U.K. 429 472
4. B. Wilburn, D.D. Rudnicki, J. Zhao, T.M. Weitz, Y. Cheng, and X.F. Gu An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice Neuron 70 2011 427 440
5. S.W. Davies, M. Turmaine, B.A. Cozens, M. DiFiglia, A.H. Sharp, and C.A. Ross Formation of neuronal intranuclear inclusions underlies the neurological dysfunction in mice transgenic for the HD mutation Cell 90 1997 537 548
6. M. DiFiglia, E. Sapp, K.O. Chase, S.W. Davies, G.P. Bates, J.P. Vonsattel, and N. Aronin Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain Science 277 1997 1990 1993
7. E. Scherzinger, R. Lurz, M. Turmaine, L. Mangiarini, B. Hollenbach, and R. Hasenbank Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo Cell 90 1997 549 558
8. S. Chen, V. Berthelier, W. Yang, and R. Wetzel Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity J. Mol. Biol. 311 2001 173 182
9. X. Gu, E.R. Greiner, R. Mishra, R. Kodali, A. Osmand, and S. Finkbeiner Serines 13 and 16 are critical determinants of full-length human mutant huntingtin induced disease pathogenesis in HD mice Neuron 64 2009 828 840
10. M. Gray, D.I. Shirasaki, C. Cepeda, V.M. Andre, B. Wilburn, and X.H. Lu Full-length human mutant huntingtin with a stable polyglutamine repeat can elicit progressive and selective neuropathogenesis in BACHD mice J. Neurosci. 28 2008 6182 6195
11. J.S. Steffan, N. Agrawal, J. Pallos, E. Rockabrand, L.C. Trotman, and N. Slepko SUMO modification of Huntingtin and Huntington's disease pathology Science 304 2004 100 104
12. R.S. Atwal, J. Xia, D. Pinchev, J. Taylor, R.M. Epand, and R. Truant Huntingtin has a membrane association signal that can modulate huntingtin aggregation, nuclear entry and toxicity Hum. Mol. Genet. 16 2007 2600 2615
13. E. Rockabrand, N. Slepko, A. Pantalone, V.N. Nukala, A. Kazantsev, and J.L. Marsh The first 17 amino acids of Huntingtin modulate its sub-cellular localization, aggregation and effects on calcium homeostasis Hum. Mol. Genet. 16 2007 61 77
14. L.M. Thompson, C.T. Aiken, L.S. Kaltenbach, N. Agrawal, K. Illes, and A. Khoshnan IKK phosphorylates Huntingtin and targets it for degradation by the proteasome and lysosome J. Cell Biol. 187 2009 1083 1099
15. R.S. Atwal, C.R. Desmond, N. Caron, T. Maiuri, J.R. Xia, S. Sipione, and R. Truant Kinase inhibitors modulate huntingtin cell localization and toxicity Nat. Chem. Biol. 7 2011 453 460
16. S. Chen, F. Ferrone, and R. Wetzel Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation Proc. Natl Acad. Sci. USA 99 2002 11884 11889
17. K. Kar, M. Jayaraman, B. Sahoo, R. Kodali, and R. Wetzel Critical nucleus size for disease-related polyglutamine aggregation is repeat-length dependent Nat. Struct. Mol. Biol. 18 2011 328 336
18. A. Bhattacharyya, A.K. Thakur, V.M. Chellgren, G. Thiagarajan, A.D. Williams, and B.W. Chellgren Oligoproline effects on polyglutamine conformation and aggregation J. Mol. Biol. 355 2006 524 535
19. A.K. Thakur, M. Jayaraman, R. Mishra, M. Thakur, V.M. Chellgren, and I.J. Byeon Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism Nat. Struct. Mol. Biol. 16 2009 380 389
20. M. Jayaraman, R. Kodali, B. Sahoo, A.K. Thakur, A. Mayasundari, and R. Mishra Slow amyloid nucleation via alpha-helix-rich oligomeric intermediates in short polyglutamine-containing huntingtin fragments J. Mol. Biol. 415 2012 881 899
21. R. Mishra, M. Jayaraman, B.P. Roland, E. Landrum, T. Fullam, and R. Kodali Inhibiting the nucleation of amyloid structure in a huntingtin fragment by targeting alpha-helix-rich oligomeric intermediates J. Mol. Biol. 415 2012 900 917
22. R. Wetzel Physical chemistry of polyglutamine: intriguing tales of a monotonous sequence J. Mol. Biol. 421 2012 466 490
23. M. Jayaraman, R. Mishra, R. Kodali, A.K. Thakur, L.M.I. Koharudin, A.M. Gronenborn, and R. Wetzel Kinetically competing huntingtin aggregation pathways control amyloid polymorphism and properties Biochemistry 51 2012 2706 2716
24. A. Thakur, and R. Wetzel Mutational analysis of the structural organization of polyglutamine aggregates Proc. Natl Acad. Sci. USA 99 2002 17014 17019
25. M. Jayaraman, R. Kodali, and R. Wetzel The impact of ataxin-1-like histidine insertions on polyglutamine aggregation Protein Eng. Des. Sel. 22 2009 469 478
26. A.K. Thakur, W. Yang, and R. Wetzel Inhibition of polyglutamine aggregate cytotoxicity by a structure-based elongation inhibitor FASEB J. 18 2004 923 925
27. V.N. Sivanandam, M. Jayaraman, C.L. Hoop, R. Kodali, R. Wetzel, and P.C. van der Wel The aggregation-enhancing huntingtin N-terminus is helical in amyloid fibrils J. Am. Chem. Soc. 133 2011 4558 4566
28. D.S. Wishart, and B.D. Sykes The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data J. Biomol. NMR 4 1994 171 180
29. I. Kheterpal, A. Williams, C. Murphy, B. Bledsoe, and R. Wetzel Structural features of the Ab amyloid fibril elucidated by limited proteolysis Biochem. 40 2001 11757 11767
30. B. O'Nuallain, S. Shivaprasad, I. Kheterpal, and R. Wetzel Thermodynamics of abeta(1-40) amyloid fibril elongation Biochemistry 44 2005 12709 12718
31. A.D. Williams, S. Shivaprasad, and R. Wetzel Alanine scanning mutagenesis of Abeta(1-40) amyloid fibril stability J. Mol. Biol. 357 2006 1283 1294
32. S.G. Julien, N. Dube, S. Hardy, and M.L. Tremblay Inside the human cancer tyrosine phosphatome Nat. Rev. Cancer 11 2011 35 49
33. S. Luo, C. Vacher, J.E. Davies, and D.C. Rubinsztein Cdk5 phosphorylation of huntingtin reduces its cleavage by caspases: implications for mutant huntingtin toxicity J. Cell Biol. 169 2005 647 656
34. B. Schilling, J. Gafni, C. Torcassi, X. Cong, R.H. Row, and M.A. LaFevre-Bernt Huntingtin phosphorylation sites mapped by mass spectrometry. Modulation of cleavage and toxicity J. Biol. Chem. 281 2006 23686 23697
35. R. Pardo, E. Colin, E. Regulier, P. Aebischer, N. Deglon, S. Humbert, and F. Saudou Inhibition of calcineurin by FK506 protects against polyglutamine-huntingtin toxicity through an increase of huntingtin phosphorylation at S421 J. Neurosci. 26 2006 1635 1645
36. C.T. Aiken, J.S. Steffan, C.M. Guerrero, H. Khashwji, T. Lukacsovich, and D. Simmons Phosphorylation of threonine 3: implications for Huntingtin aggregation and neurotoxicity J. Biol. Chem. 284 2009 29427 29436
37. L.S. Havel, C.E. Wang, B. Wade, B.D. Huang, S.H. Li, and X.J. Li Preferential accumulation of N-terminal mutant huntingtin in the nuclei of striatal neurons is regulated by phosphorylation Hum. Mol. Genet. 20 2011 1424 1437
38. J.A. Johnston, C.L. Ward, and R.R. Kopito Aggresomes: a cellular response to misfolded proteins J. Cell Biol. 143 1998 1883 1898
39. S. Waelter, A. Boeddrich, R. Lurz, E. Scherzinger, G. Lueder, H. Lehrach, and E.E. Wanker Accumulation of mutant huntingtin fragments in aggresome-like inclusion bodies as a result of insufficient protein degradation Mol. Biol. Cell 12 2001 1393 1407
40. M. Broncel, J.A. Falenski, S.C. Wagner, C.P. Hackenberger, and B. Koksch How post-translational modifications influence amyloid formation: a systematic study of phosphorylation and glycosylation in model peptides Chemistry 16 2010 7881 7888
41. N.M. Valette, S.E. Radford, S.A. Harris, and S.L. Warriner Phosphorylation as a tool to modulate aggregation propensity and to predict fibril architecture ChemBioChem 13 2012 271 281
42. M. Inoue, T. Konno, K. Tainaka, E. Nakata, H. Yoshida, and T. Morii Positional effects of phosphorylation on the stability and morphology of tau-related amyloid fibrils Biochemistry 51 2012 1396 1406
43. C.W. Bugg, J.M. Isas, T. Fischer, P.H. Patterson, and R. Langen Structural features and domain organization of huntingtin fibrils J. Biol. Chem. 287 2012 31739 31746
44. H.J. Dyson Expanding the proteome: disordered and alternatively folded proteins Q. Rev. Biophys. 44 2011 467 518
45. B. O'Nuallain, A.K. Thakur, A.D. Williams, A.M. Bhattacharyya, S. Chen, G. Thiagarajan, and R. Wetzel Kinetics and thermodynamics of amyloid assembly using a high-performance liquid chromatography-based sedimentation assay Methods Enzymol. 413 2006 34 74
46. M. Jayaraman, A.K. Thakur, K. Kar, R. Kodali, and R. Wetzel Assays for studying nucleated aggregation of polyglutamine proteins Methods 53 2011 246 254
47. N. Sreerama, and R.W. Woody Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287 2000 252 260