Characterizing the conformational ensemble of monomeric polyglutamine

Proteins: Structure, Function and Genetics

Volumn 63, Issue 2, 2006, Pages 297-311

  Wang, Xiaoling ^a,b   Vitalis, Andreas ^b   Wyczalkowski, Matthew A ^a,b   Pappu, Rohit V ^a,b  

^a WASHINGTON UNIVERSITY IN ST LOUIS   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

sheet; Aggregation; Disorder; Nucleation; Order parameter; Polyglutamine

Indexed keywords

POLYGLUTAMINE;

ARTICLE; BETA SHEET; ENTROPY; GROWTH REGULATION; HYDROGEN BOND; MOLECULAR DYNAMICS; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROBABILITY; PROTEIN CONFORMATION; QUANTITATIVE ANALYSIS; REACTION ANALYSIS; THERMODYNAMICS;

ALGORITHMS; HYDROGEN BONDING; MODELS, MOLECULAR; PEPTIDES; PROBABILITY THEORY; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 33645281939     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.20761     Document Type: Article

References (110)

1. Chen S, Ferrone FA, Wetzel R. Huntington's disease age-of-onset linked to polyglutamine aggregation nucleation. Proc Natl Acad Sci U S A 2002;99:11884-11889.
2. Harper PS. Huntington's disease: a clinical, genetic, and molecular model for polyglutamine repeat disorders. In: Harper PS, Perutz M. editors. Glutamine repeats and neurodegenerative diseases: molecular aspects. Oxford: Oxford University Press; 2001. p 1-9.
3. Wilmot GR, Warren ST. A new mutational basis for disease. In: Wells RD, Warren ST, editors. Genetic instabilities and hereditary neurological diseases. San Diego: Academic Press; 1998. p 3-12.
4. Gusella JF, McDonald ME. Huntingtin: a single bait hooks many species. Curr Opin Neurobiol 1998;8:425-430.
5. Cummings CJ, Zoghbi HY. Fourteen and counting: unraveling trinucleotide repeat diseases. Hum Mol Genet 2000;9:909-916.
6. Bates GP, Benn C. The polyglutamine diseases. In: Bates GP, Harper PS, Jones L, editors. Huntington's disease. Oxford: Oxford University Press; 2002. p 429-472.
7. Scherzinger E, Wanker EE, Mangiarini L, Bates GP. Formation of neuronal intranuclear inclusions (NII) underlies the neurological dysfunction in mice transgenic for the HD mutation. Cell 1997;90:537-548.
8. Becher MW, Kotzuk JA, Sharp AH, Davies SW, Bates GP, Price DL, Ross CA. Intranuclear neuronal inclusions in Huntington's disease and dentatorubral pallidoluysian atrophy: correlation between density of inclusions and IT15 CAG repeat length. Neurobiol Dis 1998;4:387-395.
9. Davies SW, Turmaine M, Cozens BA, Raza AS, Mahal A, Mangiarini L, Bates GP. From neuronal inclusions to neurodegeneration: neuropathological investigation of a transgenic mouse model of Huntington's disease. Philos Trans R Soc London B 1999;354:971-979.
10. Perutz MF, Finch JT, Berriman J, Lesk A. Amyloid fibers are water-filled nanotubes. Proc Natl Acad Sci U S A 2002;99:5591-5595.
11. Ross CA, Poirier MA, Wanker EE, Amzel M. Polyglutamine fibrillogenesis: the pathway unfolds. Proc Natl Acad Sci U S A 2003;100:1-3.
12. Chen S, Berthelier V, Hamilton JB, O'Nuallain B, Wetzel R. Amyloid-like features of polyglutamine aggregates and their assembly kinetics. Biochemistry 2002;41:7391-7399.
13. Yang W, Dunlap JR, Andrews RB, Wetzel R. Aggregated polyglutamine peptides delivered to nuclei are toxic to mammalian cells. Hum Mol Genet 2002;11:2905-2917.
14. Rochet JC, Lansbury PT. Amyloid fibrillogenesis: themes and variations. Curr Opin Struct Biol 2000;10:60-68.
15. Wanker EE. Protein aggregation and pathogenesis of Huntington's disease: mechanisms and correlations. Biol Chem 2000;381:937-942.
16. Ross CA. Polyglutamine pathogenesis: emergence of unifying mechanisms for Huntington's disease and related disorders. Neuron 2002;35:819-822.
17. Sacchettini JC, Kelly JW. Therapeutic strategies for human amyloid diseases. Nature Rev Drug Discovery 2002;1:267-275.
18. Serio TR, Lindquist SL. The yeast prion [PSI+]: molecular insights and functional consequences. Adv Protein Chem 2002;59:391-412.
19. Caughey B, Lansbury PT. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu Rev Neurosci 2003;26:267-298.
20. Huff ME, Balch WE, Kelly JW. Pathological and functional amyloid formation orchestrated by the secretory pathway. Curr Opin Struct Biol 2003;13:674-682.
21. Vendruscolo M, Zurdo J, MacPhee CE, Dobson CM. Protein folding and misfolding: a paradigm of self-assembly and regulation in complex biological systems. Phil Trans Royal Soc A 2003;361:1205-1222.
22. Dobson CM. Protein folding and misfolding. Nature 2003;426:884-890.
23. Dobson CM. Principles of protein folding, misfolding and aggregation. Semin Cell Dev Biol 2004;15:3-16.
24. Ohnishi S, Takano K. Amyloid fibrils from the viewpoint of protein folding. Cell Mol Life Sci 2004;61:511-524.
25. Uversky VN, Fink AL. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim Biophys Acta Proteins Proteomics 2004;1698:131-153.
26. Wetzel R. Protein folding and aggregation in the expanded polyglutamine repeat diseases. In: Buchner J, Kiefhaber T, editors. Protein folding handbook. Weinheim, Germany: Wiley-VCH; 2005. p 1200-1244.
27. Chiti F, Stefani M, Taddei N, Ramponi G, Dobson CM. Rationalization of the effects of mutations on peptide and protein aggregation rates. Nature 2003;424:805-808.
28. Dubay KF, Pawar AP, Chiti F, Dobson CM, Vendruscolo M. Prediction of the absolute aggregation rates of amyloidogenic polypeptide chains. J Mol Biol 2004;341:1317-1326.
29. Marchesi VT. An alternative interpretation of the amyloid A beta hypothesis with regard to the pathogenesis of Alzheimer's disease. Proc Natl Acad Sci U S A 2005;102:9093-9098.
30. Reixach N, Deechongkit S, Jiang X, Kelly JW, Buxbaum JN. Tissue damage in the amyloidoses: transthyretin monomers and nonnative oligomers are the major cytotoxic species in tissue culture. Proc Natl Acad Sci U S A 2004;101:2817-2822.
31. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003;300:486-489.
32. Sanchez I, Mahlke C, Yuan JY. Pivotal role of oligomerization in expanded polyglutamine neurodegenerative disorders. Nature 2003;421:373-379.
33. Poirier MA, Li H, Macosko J, Cai S, Amzel M, Ross CA. Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrillization. J Biol Chem 2002;277:41032-41037.
34. El-Agnaf OMA, Mahil DS, Patel BP, Austen BM. Oligomerization and toxicity of beta-amyloid-42 implicated in Alzheimer's disease. Biochem Biophys Res Commun 2000;273:1003-1007.
35. Pillai VNR, Mutter M. Conformational studies of poly(oxyethylene)-bound peptides and protein sequences. Acc Chem Res 1981;14:122-130.
36. Tuchscherer G, Mutter M. Under the influence of Phi and Psi. J Pept Sci 2005;11:278-282.
37. Scherzinger E, Sittler A, Schweiger K, Heiser V, Lurz R, Hasenbank R, Bates GP, Lehrach H, Wanker EE. Self-assembly of polyglutamine-containing huntingtin fragments into amyloid-like fibrils: implications for Huntington's disease pathology. Proc Natl Acad Sci U S A 1999;96:4604-4609.
38. Bennett MJ, Huey-Tubman KE, Herr AB, West AP, Ross SA, Bjorkman PJ. A linear lattice model for polyglutamine in CAG-expansion diseases. Proc Natl Acad Sci U S A 2002;99:11634-11639.
39. Masino L, Kelly G, Leonard K, Trottier Y, Pastore A. Solution structure of polyglutamine tracts in GST-polyglutamine fusion proteins. FEBS Lett 2002;513:267-272.
40. Wacker JL, Zareie MH, Fong H, Sarikaya M, Muchowski PJ. Hsp70 and Hsp40 attenuate formation of spherical and annular polyglutamine oligomers by partitioning monomer. Nature Struct Molec Biol 2004;11:1215-1222.
41. Perutz MF, Johnson T, Suzuki M, Finch JT. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases. Proc Natl Acad Sci U S A 1994;91:5355-5358.
42. Altschuler EL, Hud NV, Mazrimas JA, Rupp B. Random coil conformation for extended polyglutamine stretches in aqueous soluble monomeric peptides. J Pept Res 1997;50:73-75.
43. Chen S, Berthelier V, Yang W, Wetzel R. Polyglutamine aggregation behavior in vitro supports a recruitment mechanism of cytotoxicity. J Mol Biol 2001;311:173-182.
44. Thakur AK, Wetzel R. Mutational analysis of the structural organization of polyglutamine aggregates. Proc Natl Acad Sci U S A 2002;99:17014-17019.
45. Greenfield N, Fasman GD. Computed circular dichroism spectra for the evaluation of protein conformation. Biochemistry 1969;8:4108-4116.
46. Chen YW. Local protein unfolding and pathogenesis of polyglutamine- expansion diseases. Proteins 2003;51:68-73.
47. Kashchiev, D. Nucleation. Oxford, UK; Butterworth; 2000. Chap 2-5.
48. Guo Z, Brooks III CL, Boczko EM. Exploring the folding free energy surface of a three-helix bundle. Proc Natl Acad Sci U S A 1997;94:10161-10166.
49. Mitsutake A, Okamoto Y. Replica-exchange simulated tempering method for simulations of frustrated systems. Chem Phys Lett 2000;332:131-138.
50. Shirts MR, Pande VS. Mathematical analysis of coupled parallel simulations. Phys Rev Lett 2001;86:4983-4987.
51. Shea JE, Brooks III CL. From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding. Annu Rev Phys Chem 2001;52:499-535.
52. Nymeyer H, Gnanakaran S, García AE. Atomic simulations of protein folding using the replica exchange algorithm. Methods Enyzmol 2004;383:119-149.
53. Sheinerman FB, Brooks III CL. Calculations on folding of segment B1 of streptococcal protein G. J Mol Biol 1998;278:439-456.
54. Ferrara P, Apostolakis J, Caflisch A. Thermodynamics and kinetics of folding of two model peptides investigated by molecular dynamics simulations. J Phys Chem B 2000;104:5000-5010.
55. Hiltpol A, Ferrara P, Gsponer J, Caflisch A. Free energy surface of the helical peptide Y(MEARA)6. J Phys Chem B 2000;104:10080-10086.
56. Pande VS, Baker I, Chapman J, Elmer SP, Khaliq S, Larson SM, Rhee YM, Shirts MR, Snow CD, Sorin EJ, Zagrovic B. Atomistic protein folding simulations on the submillisecond time scale using worldwide distributed computing. Biopolymers 2003;68:91-109.
57. Klimov DK, Thirumalai D. Dissecting the assembly of A beta(16-22) amyloid peptides into antiparallel beta sheets. Structure 2003;11:295-307.
58. Paci E, Gsponer J, Salvatella X, Vendruscolo M. Molecular dynamics studies of the process of amyloid aggregation of peptide fragments of transthyretin. J Mol Biol 2004;340:555-569.
59. Wei GH, Mousseau N, Derreumaux, P. Sampling the self-assembly pathways of KFFE hexamers. Biophys J 2004;87:3648-3656.
60. Melquiond A, Boucher G, Mousseau N, Derreumaux P. Following the aggregation of amyloid-forming peptides by computer simulations. J Chem Phys 2005;122:174904.
61. Tsai H-H, Reches M, Tsai C-J, Gunasekaran K, Gazit E, Nussinov R. Energy landscape of amyloidogenic peptide oligomerization by parallel-tempering molecular dynamics simulation: significant role of Asn ladder. Proc Natl Acad Sci U S A 2005;102:8174-8179.
62. Pappu RV, Srinivasan R, Rose GD. The Flory isolated pair hypothesis is not valid for polypeptide chains: implications for protein folding. Proc Natl Acad Sci U S A 2000;97:12565-12570.
63. Zagrovic B, Pande VS. Structural correspondence between the alpha-helix and the random-flight chain resolves how unfolded proteins can have native-like properties. Nat Struct Biol 2003;10:955-961.
64. Finke JM, Cheung MS, Onuchic JN. A structural model of polyglutamine determined from a host-guest method combining experiments and landscape theory. Biophys J 2004;87:1900-1918.
65. Garcia AE. Characterization of non-alpha helical conformations in Ala peptides. Polymer 2004;45:669-676.
66. Day R, Daggett V. All-atom simulations of protein folding and unfolding. Adv Protein Chem 2003;66:373-403.
67. Zaman MH, Shen M-Y, Berry RS, Freed KF, Sosnick TR. Investigations into sequence and conformational dependence of backbone entropy, inter-basin dynamics and the Flory isolated-pair hypothesis for peptides. J Mol Biol 2003;331:693-711.
68. Tran HT, Wang X, Pappu RV. Reconciling observations of sequence specific conformational propensities with the generic polymeric behavior of denatured proteins. Biochemistry 2005;44:11369-11380.
69. Jorgensen WL, Maxwell DS, Tirado-Rives J. Development and testing of the OPLS all-atom force field on conformational energetics and properties of organic liquids. J Am Chem Soc 1996;117:11225-11236.
70. Jorgensen WL, Tirdao-Rives J. Potential energy functions for atomic-level simulations of water and organic and biomolecular systems. Proc Natl Acad Sci U S A 2005;102:6665-6670.
71. Jorgensen WL, Jenson C. Temperature dependence of TIP3P, SPC, and TIP4P water from NPT Monte Carlo simulations: seeking temperatures of maximum density. J Comput Chem 1998;19:1179-1186.
72. Berendsen HJC, van der Spoel D, van Drunen R. GROMACS: a message-passing parallel molecular dynamics implementation. Comp Phys Commun 1995;91:43-56.
73. Lindahl E, Hess B, van der Spoel D. GROMACS 3.0: a package for molecular simulation and trajectory analysis J Mol Model 2001;7:306-317.
74. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Hauk JR. Molecular dynamics with coupling to an external bath. J Chem Phys 1984;81:3684-3690.
75. Hess B, Bekker H, Berendsen HJC, Fraaije JGEM. LINCS: a linear constraint solver for molecular simulations. J Comput Chem 1997;18:1463-1472.
76. York DM, Wlodawer A, Pedersen LG, Darden TA. Atomic-level accuracy in simulations of large protein crystals. Proc Natl Acad Sci U S A 1994;91:8715-8718.
77. Weber W, Hunenberger PH, McCammon JA. Molecular dynamics simulations of a polyalanine octapeptide under Ewald boundary conditions: influence of artificial periodicity on peptide conformation. J Phys Chem B 2000;104:3668-3675.
78. Drozdov AN, Grossfield A, Pappu RV. The role of solvent in determining conformational preferences of alanine dipeptide in water. J Am Chem Soc 2004;126:2574-2581.
79. Mountain RD, Thirumalai D. Molecular dynamics simulations of end-to-end contact formation in hydrocarbon chains in water and aqueous urea solution. J Am Chem Soc 2003;125:1950-1957.
80. Swope WC, Pitera JW, Suits F. Describing protein folding kinetics by molecular dynamics simulations. 1. Theory. J Phys Chem B 2004;108:6571-6581.
81. Swope WC, Pitera JW, Suits F, Pitman M, Eleftheriou M, Fitch BG, Germain RS, Rayshubski A, Ward TJC, Zhestkov Y, Zhou R. Describing protein folding kinetics by molecular dynamics simulations. 2. Example applications to alanine dipeptide and beta-hairpin peptide. J Phys Chem B 2004;108:6582-6594.
82. Snow CD, Sorin EJ, Rhee YM, Pande VS. How well can simulation predict protein folding kinetics and thermodynamics? Annu Rev Biophys Biomol Struct 2005;34:43-69.
83. Onuchic JN, Luthey-Schulten Z, Wolynes PG. Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 1997;48:545-600.
84. Steinhauser MO. A molecular dynamics study on universal properties of polymer chains in different solvent qualities. Part 1. A review of linear chain properties. J Chem Phys 2005;122:094901.
85. i).
86. Schäfer L. Excluded volume effects in polymer solutions as explained by the renormalization group. Berlin: Springer; 1999. p 305-343.
87. Metropolis N, Rosenbluth AW, Rosenbluth MN, Teller AH, Teller E. Equation of state calculations by fast computing machines. J Chem Phys 1953;21:1087-1092.
88. Rubenstein M, Colby RH. Polymer physics. Oxford: Oxford University Press; 2003. p 97-104.
89. Engh RA, Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Cryst 1991;47:392-400.
90. Allen MP, Tildesley DJ. Computer simulation of liquids. New York: Oxford University Press; 1987. p 185-188.
91. Gentle JE. Elements of computational statistics. New York: Springer-Verlag; 2002. p 69-98.
92. Paci E, Cavalli A, Vendruscolo M, Caflisch A. Analysis of the distributed computing approach applied to the folding a small β peptide. Proc Natl Acad Sci U S A 2003;100:8217-8222.
93. Woody RW. Circular dichroism of unordered polypeptides. Adv Biophys Chem 1992;2:37-79.
94. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N, Dothager RS, Seifert S, Thiyagarajan P, Sosnick TR, Hasan MZ, Pande VS, Ruczinski I, Doniach S, Plaxco KW. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci U S A 2004;101:12491-12496.
95. Chan HS, Dill KA. Polymer principles in protein structure and stability. Annu Rev Biophys Biophys Chem 1991;20:447-490.
96. Lifshitz IM, Grosberg AY, Khokhlov AR. Some problems of the statistical physics of polymer chains with volume interaction. Rev Mod Phys 1978;50:684-713.
97. PROSS: Dihedral angle-based secondary structure assignment. 2005. Available at: http://roselab.jhu.edu/utils/pross/.
98. Ramirez-Santiago G, Jose JV. Critical exponents of the fully frustrated 2-dimensional xy-model. Phys Rev B 1994;49:9567-9582.
99. Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, Prisant MG, Richardson JS, Richardson DC. Structure validation by Calpha geometry: phi, psi and Cbeta deviation. Proteins 2003;50:437-450.
100. Rucker AL, Pager CT, Campbell MN, Qualls JE, Creamer TP. Host-guest scale of left-handed polyproline II helix formation. Proteins 2003;53:68-75.
101. Eberhardt ES, Raines RT. Amide-amide and amide-water hydrogen bonds: implications for protein folding and stability. J Am Chem Soc 1994;116:2149-2150.
102. Ramachandran GN, Sasisekharan V. Conformation of polypeptides and proteins. Adv Protein Chem 1968;23:283-487.
103. Guo C, Cheung MS, Levine H, Kessler DA. Mechanisms of cooperativity underlying sequence-independent β-sheet formation. J Chem Phys 2002;116:4353-4365.
104. Poirier MA, Jiang H, Ross CA. A structure-based analysis of huntingtin mutant polyglutamine aggregation and toxicity: evidence for a compact beta-sheet structure. Hum Mol Genet 2005;14:765-774.
105. Hu H, Elstner M, Hermans J. Comparison of a QM/MM force field and molecular mechanics force fields in simulations of alanine and glycine dipeptides (Ace-Ala-Nme and Ace-Gly-Nme) in water in relation to the problem of modeling the unfolded peptide backbone in solution. Proteins 2003;50:451-463.
106. Sikorski P, Atkins E. New model for crystalline polyglutamine assemblies and their connection with amyloid fibrils. Biomacromolecules 2005;6:425-432.
107. Khare SD, Ding F, Gwanmesia KN, Dokholyan NV. Molecular origin of polyglutamine aggregation in neurodegenerative diseases. PLoS Comp Biol 2005;1:0230-0235.
108. Stork M, Giese A, Kretzschmar HA, Tavan P. Molecular dynamics simulations indicate a possible role of parallel beta-helices in seeded aggregation of poly-gln. Biophys J 2005;88:2442-2451.
109. Finkelstein AV. Rate of β-structure formation in polypeptides. Proteins 1991;9:23-27.
110. Rhee YM, Pande VS. Multiplexed-replica exchange molecular dynamics method for protein folding simulations. Biophys J 2003;84:775-786.