Fibrillogenesis of huntingtin and other glutamine containing proteins

Sub-Cellular Biochemistry

Volumn 65, Issue , 2012, Pages 225-251

  Lyubchenko, Yuri L ^a   Krasnoslobodtsev, Alexey V ^a   Luca, Sorin ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

AFM; Amyloids; Atomic Force Microscopy; Fibrillogenesis; Huntington s disease; Self assembly; Solid state NMR

Indexed keywords

AMYLOID; HTT PROTEIN, HUMAN; NERVE PROTEIN;

ANIMAL; ATOMIC FORCE MICROSCOPY; CHEMICAL MODEL; CHEMISTRY; GENETICS; HUMAN; HUNTINGTON CHOREA; KINETICS; METABOLISM; NUCLEAR MAGNETIC RESONANCE; PATHOLOGY; PROTEIN MULTIMERIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEIN STABILITY; REVIEW; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

AMYLOID; ANIMALS; CRYSTALLOGRAPHY, X-RAY; HUMANS; HUNTINGTON DISEASE; KINETICS; MICROSCOPY, ATOMIC FORCE; MODELS, CHEMICAL; NERVE TISSUE PROTEINS; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY;

EID: 84877343700     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-94-007-5416-4_10     Document Type: Article

References (91)

1. Baxa U, Cheng N,Winkler DC, Chiu TK, Davies DR, Sharma D, Inouye H, Kirschner DA,Wickner RB, Steven AC (2005) Filaments of the Ure2p prion protein have a cross-beta core structure. J Struct Biol 150:170-179
2. Baxa U,Wickner RB, Steven AC, Anderson DE, Marekov LN,YauW-M, Tycko R (2007) Characterization of beta-sheet structure in Ure2p1-89 yeast prion fibrils by solid-state nuclear magnetic resonance. Biochemistry 46:13149-13162
3. Bernacki JP, Murphy RM (2009) Model discrimination and mechanistic interpretation of kinetic data in protein aggregation studies. Biophys J 96:2871-2887
4. BhattacharyyaA, ThakurAK, ChellgrenVM, Thiagarajan G,WilliamsAD, ChellgrenBW, Creamer TP,Wetzel R (2006) Oligoproline effects on polyglutamine conformation and aggregation. J Mol Biol 355:524-535
5. Bhattacharyya AM, Thakur AK, Wetzel R (2005) Polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction. Proc Natl Acad Sci USA 102:15400-15405
6. Chan JCC, Oyler NA,YauW-M, Tycko R (2005) Parallel beta-sheets and polar zippers in amyloid fibrils formed by residues 10-39 of the yeast prion protein Ure2p. Biochemistry 44:10669-10680
7. Chen S, Berthelier V, Hamilton JB, O'Nuallain B, Wetzel R (2002a) Amyloid-like features of polyglutamine aggregates and their assembly kinetics. Biochemistry 41:7391-7399
8. Chen S, Ferrone FA,Wetzel R (2002b) Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc Natl Acad Sci USA 99:11884-11889
9. Dahlgren PR, KarymovMA,Bankston J, HoldenT, Thumfort P, IngramVM,LyubchenkoYL (2005) Atomic force microscopy analysis of the Huntington protein nanofibril formation. Nanomedicine 1:52-57
10. De Baere I, Liu L, Moens L, Van Beeumen J, Gielens C, Richelle J, Trotman C, Finch J, Gerstein M, Perutz M (1992) Polar zipper sequence in the high-affinity hemoglobin of Ascaris suum: amino acid sequence and structural interpretation. Proc Natl Acad Sci USA 89:4638-4642
11. Der-Sarkissian A, Jao CC, Chen J, Langen R (2003) Structural organization of alpha-synuclein fibrils studied by site-directed spin labeling. J Biol Chem 278:37530-37535
12. Digambaranath JL, Campbell TV, Chung A, McPhail MJ, Stevenson KE, Zohdy MA, Finke JM (2011) An accurate model of polyglutamine. Proteins 79:1427-1440
13. Dobson CM (1999) Protein misfolding, evolution and disease. Trends Biochem Sci 24:329-332
14. Dobson CM (2004a) Experimental investigation of protein folding and misfolding. Methods 34:4-14
15. Dobson CM (2004b) Principles of protein folding, misfolding and aggregation. Semin. Cell Dev Biol 15:3-16
16. Dong J, Castro CE, Boyce MC, Lang MJ, Lindquist S (2010) Optical trapping with high forces reveals unexpected behaviors of prion fibrils. Nat Struct Mol Biol 17:1422-1430
17. Dougan L, Li J, Badilla CL, Berne BJ, FernandezJM (2009) Single homopolypeptide chains collapse into mechanically rigid conformations. Proc Natl Acad Sci USA 106:12605-12610
18. Ferrone F (1999) Analysis of protein aggregation kinetics. Methods Enzymol 309:256-274
19. Flory P (1953) Principles of Polymer Chemistry. Cornell University Press, NewYork
20. Gatchel JR, Zoghbi HY (2005) Diseases of unstable repeat expansion: mechanisms and common principles. Nat Rev Genetics 6:743-755
21. GillianB (2003) Huntingtin aggregation and toxicity in Huntington's disease. The Lancet 361:1642- 1644
22. Glabe CG (2004) Conformation-dependent antibodies target diseases of protein misfolding. Trends Biochem Sci 29:542-547
23. Graham RK, Deng Y, Slow EJ, Haigh B, Bissada N, Lu G, Pearson J, Shehadeh J, Bertram L, Murphy Z,Warby SC, Doty CN, Roy S,Wellington CL, Leavitt BR, Raymond LA, Nicholson DW, Hayden MR (2006) Cleavage at the caspase-6 site is required for neuronal dysfunction and degeneration due to mutant huntingtin. Cell 125:1179-1191
24. Gusella JF, MacDonald ME (2000) Molecular genetics: unmasking polyglutamine triggers in neurodegenerative disease. Nat rev Neurosci 1:109-115
25. Hofrichter J, Ross PD, EatonWA (1974) Kinetics and mechanism of deoxyhemoglobin S gelation: a new approach to understanding sickle cell disease. Proc Natl Acad Sci USA 71:4864-4868
26. Jarrett JT, Lansbury PT Jr (1993) Seeding "one-dimensional crystallization" of amyloid: a pathogenic mechanism in Alzheimer's disease and scrapie? Cell 73:1055-1058
27. Kajava AV, Baxa U, Wickner RB, Steven AC (2004) A model for Ure2p prion filaments and other amyloids: the parallel superpleated beta-structure. Proc Natl Acad Sci USA 101:7885-7890
28. Kar K, Jayaraman M, Sahoo B, Kodali R,Wetzel R (2011) Critical nucleus size for disease-related polyglutamine aggregation is repeat-length dependent. Nat Struct Mol Biol 18:328-336
29. Karsai A, Nagy A, Kengyel A, Martonfalvi Z, Grama L, Penke B, Kellermayer MS (2005) Effect of lysine-28 side-chain acetylation on the nanomechanical behavior of alzheimer amyloid beta25- 35 fibrils. J Chem Inf Model 45:1641-1646
30. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, CotmanCW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489
31. Kellermayer MS, Grama L, Karsai A, Nagy A, Kahn A, Datki ZL, Penke B (2005) Reversible mechanical unzipping of amyloid beta-fibrils. J Biol Chem 280:8464-8470
32. Kim MW, Chelliah Y, Kim SW, Otwinowski Z, Bezprozvanny I (2009) Secondary structure of Huntingtin amino-terminal region. Structure 17:1205-1212
33. Knowles TP, Buehler MJ (2011) Nanomechanics of functional and pathological amyloid materials. Nature nanotechnology 6:469-479
34. KnowlesTP, FitzpatrickAW, Meehan S, Mott HR,Vendruscolo M, Dobson CM,WellandME (2007) Role of intermolecular forces in defining material properties of protein nanofibrils. Science 318:1900-1903
35. Kryndushkin DS, Wickner RB, Tycko R (2011) The core of Ure2p prion fibrils is formed by the N-terminal segment in a parallel cross-β structure: evidence from solid-state NMR. J. Mol. Biol 409:263-277
36. Krzewska J, Tanaka M, Burston SG, Melki R (2007) Biochemical and functional analysis of the assembly of full-length Sup35p and its prion-forming domain. J Biol Chem 282:1679-1686
37. Lewandowski J.z.R, Van Der Wel PCA, Rigney M, Grigorieff N, Griffin RG (2011) Structural Complexity of a Composite Amyloid Fibril. J Am Chem Soc 133:14686-14698
38. Loquet A, Bousset L, Gardiennet C, SouriguesY, Wasmer C, Habenstein B, Schütz A, Meier BH, Melki R, Böckmann A (2009) Prion fibrils of Ure2p assembled under physiological conditions contain highly ordered, natively folded modules. Journal of Molecular Biology 394:108-118
39. LuY,Weers B, Stellwagen NC (2001) DNA persistence length revisited. Biopolymers 61:261-275
40. Lyubchenko YL, Jacobs BL, Lindsay SM, Stasiak A (1995) Atomic force microscopy of nucleoprotein complexes. Scanning Microsc 9:705-724, discussion 724-707
41. Lyubchenko YL, Sherman S, Shlyakhtenko LS, Uversky VN (2006) Nanoimaging for protein misfolding and related diseases. J Cell Biochem 99:52-70
42. Lyubchenko YL, Kim BH, Krasnoslobodtsev AV,Yu J (2010) Nanoimaging for protein misfolding diseases.Wiley Interdiscip Rev Nanomed Nanobiotechnol 2:526-543
43. Ma B, Nussinov R (2002) Stabilities and conformations of Alzheimer's beta -amyloid peptide oligomers (Abeta 16-22, Abeta 16-35, and Abeta 10-35): Sequence effects. Proc Natl Acad Sci USA 99:14126-14131
44. MacDonald ME, Ambrose CM, Duyao MP, Myers RH, Lin C, Srinidhi L, Barnes G, Taylor SA, James M, Groot N, MacFarlane H, Jenkins B, Anderson MA,Wexler NS, Gusella JF, Bates GP, Baxendale S, Hummerich H, Kirby S, North M,Youngman S, Mott R, Zehetner G, Sedlacek Z, Poustka A, Frischauf A-M, Lehrach H, Buckler AJ, Church D, Doucette-Stamm L, O'Donovan MC, Riba-Ramirez L, Shah M, Stanton VP, Strobel SA, Draths KM, Wales JL, Dervan P, Housman DE, Altherr M, Shiang R, Thompson L, Fielder T, Wasmuth JJ, Tagle D, Valdes J, Elmer L, Allard M, Castilla L, Swaroop M, Blanchard K, Collins FS, Snell R, Holloway T, Gillespie K, Datson N, Shaw D, Harper PS (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell 72:971-983
45. Margittai M, Langen R (2008) Fibrils with parallel in-register structure constitute a major class of amyloid fibrils: molecular insights from electron paramagnetic resonance spectroscopy. Q Rev Biophys 41:265-297
46. McAllister C, Karymov MA, Kawano Y, Lushnikov AY, Mikheikin A, Uversky VN, Lyubchenko YL (2005) Protein interactions and misfolding analyzed byAFM force spectroscopy. J Mol Biol 354:1028-1042
47. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, Koenigsknecht-Talboo J, Holtzman DM, Bacskai BJ, Hyman BT (2008) Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 451:720-724
48. Mostaert A, Crockett R, Kearn G, Cherny I, Gazit E, Serpell L, Jarvis S (2009) Mechanically functional amyloid fibrils in the adhesive of a marine invertebrate as revealed by Raman spectroscopy and atomic force microscopy. Arch Histol Cytol 72:199-207
49. Mostaert AS, Higgins MJ, Fukuma T, Rindi F, Jarvis SP (2006) Nanoscale mechanical characterisation of amyloid fibrils discovered in a natural adhesive. J biol Phys 32:393-401
50. Nelson R, Sawaya MR, Balbirnie M, MadsenAØ, Riekel C, Grothe R, EisenbergD (2005) Structure of the cross-beta spine of amyloid-like fibrils. Nature 435:773-778
51. Ngo S, Gu L, Guo Z (2011) Hierarchical organization in the amyloid core of yeast prion protein ure2. J Biol Chem 286:29691-29699
52. O'Nuallain B, Wetzel R (2002) Conformational Abs recognizing a generic amyloid fibril epitope. Proc Natl Acad Sci USA 99:1485-1490
53. Ogawa H, Nakano M, Watanabe H, Starikov EB, Rothstein SM, Tanaka S (2008) Molecular dynamics simulation study on the structural stabilities of polyglutamine peptides. Comput Biol Chem 32:102-110
54. Perutz MF (1995) Glutamine repeats as polar zippers: their role in inherited neurodegenerative disease. Mol Med 1:718-721
55. Perutz MF, Staden R, Moens L, De Baere I (1993) Polar zippers. Curr Biol 3:249-253
56. Perutz MF, Johnson T, Suzuki M, Finch JT (1994) Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc Natl Acad Sci USA 91:5355-5358
57. Perutz MF,Windle AH (2001) Cause of neural death in neurodegenerative diseases attributable to expansion of glutamine repeats. Nature 412:143-144
58. Perutz MF, Finch JT, Berriman J, Lesk A (2002) Amyloid fibers are water-filled nanotubes. Proc. Natl. Acad. Sci. USA 99:5591-5595
59. PetkovaAT, IshiiY, Balbach JJ,Antzutkin ON, Leapman RD, Delaglio F,TyckoR (2002)Astructural model for Alzheimer's beta -amyloid fibrils based on experimental constraints from solid state NMR. Proc Natl Acad Sci USA 99:16742-16747
60. Petkova AT, Leapman RD, Guo Z, Yau W-M, Mattson MP, Tycko R (2005) Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils. Science 307:262-265
61. Robertson AL, Bate MA, Androulakis SG, Bottomley SP, Buckle AM (2011) PolyQ: a database describing the sequence and domain context of polyglutamine repeats in proteins. Nucleic Acids Res 39:D272-D276
62. Rojas AV, Liwo A, Scheraga HA (2011) A Study of the alpha-Helical Intermediate Preceding the Aggregation of the Amino-Terminal Fragment of the beta Amyloid Peptide (Abeta(1-28)). J Phys Chem B 115:12978-12983
63. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, Apostol MI, Thompson MJ, Balbirnie M,Wiltzius JJW, McFarlane HT, Madsen AØ, Riekel C, Eisenberg D (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447:453-457
64. Scherzinger, E, Sittler A, Schweiger K, Heiser V, Lurz R, Hasenbank R, Bates GP, Lehrach H, Wanker EE (1999) Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc Natl Acad Sci USA 96:4604-4609
65. Schneider R, Schumacher MC, Mueller H, Nand D, Klaukien V, Heise H, Riedel D, Wolf G, Behrmann E, Raunser S, Seidel R, Engelhard M, Baldus M (2011) Structural characterization of polyglutamine fibrils by solid-state NMR spectroscopy. J Mol Biol 412:121-136
66. Serio TR, Cashikar AG, Kowal AS, Sawicki GJ, Moslehi JJ, Serpell L, Arnsdorf MF, Lindquist SL (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant. Science 289:1317-1321
67. Sherman DR, Kloek P, Krishnan BR, Guinn B, Goldberg DE (1992) Ascaris hemoglobin gene: plant-like structure reflects the ancestral globin gene. Proc Natl Acad Sci USA 89:11696-11700
68. Sikorski P, Atkins E (2005) New model for crystalline polyglutamine assemblies and their connection with amyloid fibrils. Biomacromolecules 6:425-432
69. Smith JF, Knowles TP, Dobson CM, Macphee CE, Welland ME (2006) Characterization of the nanoscale properties of individual amyloid fibrils. Proc Natl Acad Sci USA 103:15806-15811
70. Stork M, Giese A, Kretzschmar HA, Tavan P (2005) Molecular dynamics simulations indicate a possible role of parallel beta-helices in seeded aggregation of poly-Gln. Biophys J 88:2442-2451
71. Straub JE, Thirumalai D (2011) Toward a molecular theory of early and late events in monomer to amyloid fibril formation. Ann Rev Phys Chem 62:437-463
72. Stromer T, Serpell LC (2005) Structure and morphology of the Alzheimer's amyloid fibril. Microsc Res Tech 67:210-217
73. Sweers K, Van Der Werf K, Bennink M, Subramaniam V (2011) Nanomechanical properties of alpha-synuclein amyloid fibrils: a comparative study by nanoindentation, harmonic force microscopy, and Peakforce QNM. Nanoscale Res Lett 6:270
74. Tam S, Spiess C, Auyeung W, Joachimiak L, Chen B, Poirier MA, 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
75. Thakur AK, Wetzel R (2002) Mutational analysis of the structural organization of polyglutamine aggregates. Proc Natl Acad Sci USA 99:17014-17019
76. Thakur AK, Jayaraman M, Mishra R, Thakur M, Chellgren VM, Byeon IJ, Anjum DH, Kodali R, Creamer TP, Conway JF, Gronenborn AM, Wetzel R (2009) Polyglutamine disruption of the huntingtin exon 1 N terminus triggers a complex aggregation mechanism. Nature structural & molecular biology 16:380-389
77. Tycko R (2003) Insights into the amyloid folding problem from solid-state NMR. Biochemistry 42:3151-3159
78. Uversky VN, Fink AL (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta 1698:131-153
79. Van DerWel PCA, Lewandowski JR, GriffinRG (2007) Solid-stateNMRstudy of amyloid nanocrystals and fibrils formed by the peptide GNNQQNY from yeast prion protein Sup35p. JAm Chem Soc 129:5117-5130
80. Van DerWel PCA, Lewandowski JR, Griffin RG (2010) Structural characterization of GNNQQNY amyloid fibrils by magic angle spinning NMR. Biochemistry 49:9457-9469
81. Van Melckebeke H,Wasmer C, Lange A, Ab E, Loquet A, Böckmann A, Meier BH (2010) Atomicresolution three-dimensional structure of HET-s(218-289) amyloid fibrils by solid-state NMR spectroscopy. J Am Chem Soc 132:13765-13775
82. Van Den Akker CC, Engel MFM, Velikov KP, Bonn M, Koenderink GH (2011) Morphology and Persistence Length of Amyloid Fibrils Are Correlated to Peptide Molecular Structure. J Am Chem Soc 133:18030-18033
83. Venkatraman J, Shankaramma SC, Balaram P (2001) Design of folded peptides. Chemical reviews 101:3131-3152
84. Vitalis A,Wang X, Pappu RV (2007) Quantitative characterization of intrinsic disorder in polyglutamine: insights from analysis based on polymer theories. Biophysical journal 93:1923-1937
85. Walker FO (2007) Huntington's disease. Lancet 369:218-228
86. Walters RH, Murphy RM (2009) Examining polyglutamine peptide length: a connection between collapsed conformations and increased aggregation. Journal of molecular biology 393:978-992
87. Walters RH, Murphy RM (2011) Aggregation kinetics of interrupted polyglutamine peptides. J Mol Biol 412:505-519
88. Wasmer C, Lange A, Van Melckebeke H, Siemer AB, Riek R, Meier BH (2008) Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core. Science 319:1523-1526
89. Yang L, He HY, Zhang XJ (2002) Increased expression of intranuclearAChE involved in apoptosis of SK-N-SH cells. Neurosci Res 42:261-268
90. Zanuy D, Gunasekaran K, Lesk AM, Nussinov R (2006) Computational study of the fibril organization of polyglutamine repeats reveals a common motif identified in beta-helices. J Mol Biol 358:330-345
91. Zoghbi HY, Orr HT (2000) Glutamine repeats and neurodegeneration. Annu Rev Neurosci 23:217-247