Sequence- and Temperature-Dependent Properties of Unfolded and Disordered Proteins from Atomistic Simulations

Journal of Physical Chemistry B

Volumn 119, Issue 46, 2015, Pages 14622-14630

  Zerze, Gül H ^a   Best, Robert B ^b   Mittal, Jeetain ^a  

^a Lehigh University   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAINS; FREE ENERGY; SOLVATION; SOLVENTS; TEMPERATURE DISTRIBUTION;

ATOMISTIC SIMULATIONS; ENVIRONMENTAL CONDITIONS; INTRINSICALLY DISORDERED PROTEINS; SOLVATION FREE ENERGIES; SOLVENT ACCESSIBLE SURFACE AREAS; TEMPERATURE DEPENDENCE; TEMPERATURE DEPENDENT; TEMPERATURE-DEPENDENT PROPERTIES;

PROTEINS;

PROTEIN;

CHEMISTRY; PROTEIN SECONDARY STRUCTURE; TEMPERATURE;

PROTEIN STRUCTURE, SECONDARY; PROTEINS; TEMPERATURE;

EID: 84947998006     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b08619     Document Type: Article

References (83)

1. Wright, P. E.; Dyson, H. J. Intrinsically unstructured proteins: Re-assessing the protein structure-function paradigm J. Mol. Biol. 1999, 293, 321-331 10.1006/jmbi.1999.3110
2. Eliezer, D.; Kutluay, E.; Bussell, R.; Browne, G. Conformational properties of α-synuclein in its free and lipid-associated states J. Mol. Biol. 2001, 307, 1061-1073 10.1006/jmbi.2001.4538
3. Linding, R.; Schymkowitz, J.; Rousseau, F.; Diella, F.; Serrano, L. A comparative study of the relationship between protein structure and β-aggregation in globular and intrinsically disordered proteins J. Mol. Biol. 2004, 342, 345-353 10.1016/j.jmb.2004.06.088
4. Dedmon, M. M.; Lindorff-Larsen, K.; Christodoulou, J.; Vendruscolo, M.; Dobson, C. M. Mapping long-range interactions in α-synuclein using spin-label NMR and ensemble molecular dynamics simulations J. Am. Chem. Soc. 2005, 127, 476-477 10.1021/ja044834j
5. Von Bergen, M.; Barghorn, S.; Biernat, J.; Mandelkow, E.-M.; Mandelkow, E. Tau aggregation is driven by a transition from random coil to beta sheet structure Biochim. Biophys. Acta, Mol. Basis Dis. 2005, 1739, 158-166 10.1016/j.bbadis.2004.09.010
6. Halfmann, R.; Alberti, S.; Krishnan, R.; Lyle, N.; ODonnell, C. W.; King, O. D.; Berger, B.; Pappu, R. V.; Lindquist, S. Opposing effects of glutamine and asparagine govern prion formation by intrinsically disordered proteins Mol. Cell 2011, 43, 72-84 10.1016/j.molcel.2011.05.013
7. Miller, C.; Zerze, G. H.; Mittal, J. Molecular simulations indicate marked differences in the structure of amylin mutants, correlated with known aggregation propensity J. Phys. Chem. B 2013, 117, 16066-16075 10.1021/jp409755y
8. Crick, S. L.; Ruff, K. M.; Garai, K.; Frieden, C.; Pappu, R. V. Unmasking the roles of N-and C-terminal flanking sequences from exon 1 of huntingtin as modulators of polyglutamine aggregation Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 20075-20080 10.1073/pnas.1320626110
9. Hagen, S. J.; Hofrichter, J.; Szabo, A.; Eaton, W. A. Diffusion-limited contact formation in unfolded cytochrome c: Estimating the maximum rate of protein folding Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 11615-11617 10.1073/pnas.93.21.11615
10. Schuler, B.; Lipman, E. A.; Eaton, W. A. Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Nature 2002, 419, 743-747 10.1038/nature01060
11. Uzawa, T.; Akiyama, S.; Kimura, T.; Takahashi, S.; Ishimori, K.; Morishima, I.; Fujisawa, T. Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of α-helical content and compactness Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 1171-1176 10.1073/pnas.0305376101
12. Krieger, F.; Fierz, B.; Bieri, O.; Drewello, M.; Kiefhaber, T. Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding J. Mol. Biol. 2003, 332, 265-274 10.1016/S0022-2836(03)00892-1
13. Sadqi, M.; Lapidus, L. J.; Munoz, V. How fast is protein hydrophobic collapse? Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 12117-22 10.1073/pnas.2033863100
14. Kohn, J. E.; Millett, I. S.; Jacob, J.; Zagrovic, B.; Dillon, T. M.; Cingel, N.; Dothager, R. S.; Seifert, S.; Thiyagarajan, P.; Sosnick, T. R. et al. Random-coil behavior and the dimensions of chemically unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 12491-12496 10.1073/pnas.0403643101
15. Möglich, A.; Joder, K.; Kiefhaber, T. End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 12394-12399 10.1073/pnas.0604748103
16. Sherman, E.; Haran, G. Coil-globule transition in the denatured state of a small protein Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 11539-11543 10.1073/pnas.0601395103
17. Merchant, K. A.; Best, R. B.; Louis, J. M.; Gopich, I. V.; Eaton, W. A. Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 1528-33 10.1073/pnas.0607097104
18. Jacob, J.; Dothager, R. S.; Thiyagarajan, P.; Sosnick, T. R. Fully reduced ribonuclease A does not expand at high denaturant concentration or temperature J. Mol. Biol. 2007, 367, 609-615 10.1016/j.jmb.2007.01.012
19. Hoffmann, A.; Kane, A.; Nettels, D.; Hertzog, D. E.; Baumgärtel, P.; Lengefeld, J.; Reichardt, G.; Horsley, D. A.; Seckler, R.; Bakajin, O. et al. Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 105-110 10.1073/pnas.0604353104
20. Arai, M.; Kondrashkina, E.; Kayatekin, C.; Matthews, C. R.; Iwakura, M.; Bilsel, O. Microsecond hydrophobic collapse in the folding of Escherichia coli dihydrofolate reductase, an α/β-type protein J. Mol. Biol. 2007, 368, 219-229 10.1016/j.jmb.2007.01.085
21. Wang, Y.; Trewhella, J.; Goldenberg, D. P. Small-angle X-ray scattering of reduced ribonuclease A: Effects of solution conditions and comparisons with a computational model of unfolded proteins J. Mol. Biol. 2008, 377, 1576-1592 10.1016/j.jmb.2008.02.009
22. Nettels, D.; Müller-Späth, S.; Küster, F.; Hofmann, H.; Haenni, D.; Rüegger, S.; Reymond, L.; Hoffmann, A.; Kubelka, J.; Heinz, B.; Gast, K.; Best, R. B.; Schuler, B. Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins Proc. Natl. Acad. Sci. U.S.A. 2009, 106, 20740-5 10.1073/pnas.0900622106
23. Ziv, G.; Haran, G. Protein folding, protein collapse, and tanfords transfer model: Lessons from single-molecule FRET J. Am. Chem. Soc. 2009, 131, 2942-7 10.1021/ja808305u
24. Müller-Späth, S.; Soranno, A.; Hirschfeld, V.; Hofmann, H.; Rüegger, S.; Reymond, L.; Nettels, D.; Schuler, B. Charge interactions can dominate the dimensions of intrinsically disordered proteins Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 14609-14614 10.1073/pnas.1001743107
25. Hofmann, H.; Soranno, A.; Borgia, A.; Gast, K.; Nettels, D.; Schuler, B. Polymer scaling laws of unfolded and intrinsically disordered proteins quantified with single-molecule spectroscopy Proc. Natl. Acad. Sci. U.S.A. 2012, 109, 16155-16160 10.1073/pnas.1207719109
26. Lindorff-Larsen, K.; Trbovic, N.; Maragakis, P.; Piana, S.; Shaw, D. E. Structure and dynamics of an unfolded protein examined by molecular dynamics simulation J. Am. Chem. Soc. 2012, 134, 3787-3791 10.1021/ja209931w
27. McParland, V. J.; Kad, N. M.; Kalverda, A. P.; Brown, A.; Kirwin-Jones, P.; Hunter, M. G.; Sunde, M.; Radford, S. E. Partially unfolded states of β2-microglobulin and amyloid formation in vitro Biochemistry 2000, 39, 8735-8746 10.1021/bi000276j
28. Dobson, C. M. Protein folding and misfolding Nature 2003, 426, 884-890 10.1038/nature02261
29. Zheng, W.; Schafer, N. P.; Wolynes, P. G. Free energy landscapes for initiation and branching of protein aggregation Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 20515-20520 10.1073/pnas.1320483110
30. Kozlov, A. G.; Weiland, E.; Mittal, A.; Waldman, V.; Antony, E.; Fazio, N.; Pappu, R. V.; Lohman, T. M. Intrinsically disordered C-terminal tails of E. coli single-stranded DNA binding protein regulate cooperative binding to single-stranded DNA J. Mol. Biol. 2015, 427, 763-774 10.1016/j.jmb.2014.12.020
31. Buske, P. J.; Mittal, A.; Pappu, R. V.; Levin, P. A. An intrinsically disordered linker plays a critical role in bacterial cell division Semin. Cell Dev. Biol. 2015, 37, 3-10 10.1016/j.semcdb.2014.09.017
32. Uversky, V. N. Natively unfolded proteins: a point where biology waits for physics Protein Sci. 2002, 11, 739-756 10.1110/ps.4210102
33. Ashbaugh, H. A.; Hatch, H. Natively unfolded protein stability as a coil-to-globule transition in charge/hydropathy space J. Am. Chem. Soc. 2008, 130, 9536-9542 10.1021/ja802124e
34. Das, R. K.; Pappu, R. V. Conformations of intrinsically disordered proteins are influenced by linear sequence distributions of oppositely charged residues Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 13392-13397 10.1073/pnas.1304749110
35. Mao, A. H.; Crick, S. L.; Vitalis, A.; Chicoine, C. L.; Pappu, R. V. Net charge per residue modulates conformational ensembles of intrinsically disordered proteins Proc. Natl. Acad. Sci. U.S.A. 2010, 107, 8183-8188 10.1073/pnas.0911107107
36. Langridge, T. D.; Tarver, M. J.; Whitten, S. T. Temperature effects on the hydrodynamic radius of the intrinsically disordered N-terminal region of the p53 protein Proteins: Struct., Funct., Genet. 2014, 82, 668-678 10.1002/prot.24449
37. Wuttke, R.; Hofmann, H.; Nettels, D.; Borgia, M. B.; Mittal, J.; Best, R. B.; Schuler, B. Temperature-dependent solvation modulates the dimensions of disordered proteins Proc. Natl. Acad. Sci. U. S. A. 2014, 111, 5213-5218 10.1073/pnas.1313006111
38. Baldwin, R. L.; Zimm, B. H. Are denatured proteins ever random coils? Proc. Natl. Acad. Sci. U.S.A. 2000, 97, 12391-12392 10.1073/pnas.97.23.12391
39. Pappu, R. V.; Srinivasan, R.; Rose, G. D. 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 10.1073/pnas.97.23.12565
40. Plaxco, K. W.; Gross, M. Unfolded, yes, but random? Never! Nat. Struct. Biol. 2001, 8, 659-660 10.1038/90349
41. Chan, H. S.; Dill, K. A. Origins of structure in globular proteins Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 6388-6392 10.1073/pnas.87.16.6388
42. Dobson, C. M. Unfolded proteins, compact states and molten globules Curr. Opin. Struct. Biol. 1992, 2, 6-12 10.1016/0959-440X(92)90169-8
43. Wong, K.-B.; Clarke, J.; Bond, C. J.; Neira, J. L.; Freund, S. M.; Fersht, A. R.; Daggett, V. Towards a complete description of the structural and dynamic properties of the denatured state of barnase and the role of residual structure in folding J. Mol. Biol. 2000, 296, 1257-1282 10.1006/jmbi.2000.3523
44. Shortle, D.; Ackerman, M. S. Persistence of native-like topology in a denatured protein in 8 M urea Science 2001, 293, 487-489 10.1126/science.1060438
45. Jane Dyson, H.; Ewright, P. Insights into the structure and dynamics of unfolded proteins from nuclear magnetic resonance Adv. Protein Chem. 2002, 62, 311-340 10.1016/S0065-3233(02)62012-1
46. Cho, J.-H.; Sato, S.; Raleigh, D. P. Thermodynamics and kinetics of non-native interactions in protein folding: a single point mutant significantly stabilizes the N-terminal domain of L9 by modulating non-native interactions in the denatured state J. Mol. Biol. 2004, 338, 827-837 10.1016/j.jmb.2004.02.073
47. Saxena, A. M.; Udgaonkar, J. B.; Krishnamoorthy, G. Characterization of intra-molecular distances and site-specific dynamics in chemically unfolded barstar: Evidence for denaturant-dependent non-random structure J. Mol. Biol. 2006, 359, 174-89 10.1016/j.jmb.2006.03.013
48. Jensen, M. R.; Markwick, P. R.; Meier, S.; Griesinger, C.; Zweckstetter, M.; Grzesiek, S.; Bernado, P.; Blackledge, M. Quantitative determination of the conformational properties of partially folded and intrinsically disordered proteins using NMR dipolar couplings Structure 2009, 17, 1169-1185 10.1016/j.str.2009.08.001
49. Eliezer, D. Biophysical characterization of intrinsically disordered proteins Curr. Opin. Struct. Biol. 2009, 19, 23-30 10.1016/j.sbi.2008.12.004
50. Zhang, W.; Ganguly, D.; Chen, J. Residual structures, conformational fluctuations, and electrostatic interactions in the synergistic folding of two intrinsically disordered proteins PLoS Comput. Biol. 2012, 8, e1002353 10.1371/journal.pcbi.1002353
51. Meng, W.; Lyle, N.; Luan, B.; Raleigh, D. P.; Pappu, R. V. Experiments and simulations show how long-range contacts can form in expanded unfolded proteins with negligible secondary structure Proc. Natl. Acad. Sci. U.S.A. 2013, 110, 2123-8 10.1073/pnas.1216979110
52. Keppel, T. R.; Weis, D. D. Mapping residual structure in intrinsically disordered proteins at residue resolution using millisecond hydrogen/deuterium exchange and residue averaging J. Am. Soc. Mass Spectrom. 2015, 26, 547-554 10.1007/s13361-014-1033-6
53. Salmon, L.; Nodet, G.; Ozenne, V.; Yin, G.; Jensen, M. R.; Zweckstetter, M.; Blackledge, M. NMR characterization of long-range order in intrinsically disordered proteins J. Am. Chem. Soc. 2010, 132, 8407-8418 10.1021/ja101645g
54. Creamer, T. P.; Srinivasan, R.; Rose, G. D. Modeling unfolded states of peptides and proteins Biochemistry 1995, 34, 16245-16250 10.1021/bi00050a003
55. Creamer, T. P.; Srinivasan, R.; Rose, G. D. Modeling unfolded states of proteins and peptides. II. Backbone solvent accessibility Biochemistry 1997, 36, 2832-2835 10.1021/bi962819o
56. Bernadó, P.; Blackledge, M.; Sancho, J. Sequence-specific solvent accessibilities of protein residues in unfolded protein ensembles Biophys. J. 2006, 91, 4536-4543 10.1529/biophysj.106.087528
57. Gong, H.; Rose, G. D. Assessing the solvent-dependent surface area of unfolded proteins using an ensemble model Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 3321-3326 10.1073/pnas.0712240105
58. Best, R. B.; Mittal, J. Protein simulations with an optimized water model: Cooperative helix formation and temperature-induced unfolded state collapse J. Phys. Chem. B 2010, 114, 14916-14923 10.1021/jp108618d
59. Rubinstein, M.; Colby, R. H. Polymer Physics; OUP: Oxford, 2003.
60. Nettels, D.; Hoffmann, A.; Schuler, B. Unfolded protein and peptide dynamics investigated with single-molecule FRET and correlation spectroscopy from picoseconds to seconds J. Phys. Chem. B 2008, 112, 6137-6146 10.1021/jp076971j
61. Kyte, J.; Doolittle, R. F. A simple method for displaying the hydropathic character of a protein J. Mol. Biol. 1982, 157, 105-132 10.1016/0022-2836(82)90515-0
62. Sugita, Y.; Okamoto, Y. Replica-exchange molecular dynamics method for protein folding Chem. Phys. Lett. 1999, 314, 141-151 10.1016/S0009-2614(99)01123-9
63. Flory, P. J. The configuration of real polymer chains J. Chem. Phys. 1949, 17, 303 10.1063/1.1747243
64. Tran, H. T.; Mao, A.; Pappu, R. V. Role of Backbone-solvent Interactions in determining conformational equilibria of intrinsically disordered proteins J. Am. Chem. Soc. 2008, 130, 7380-7392 10.1021/ja710446s
65. Marsh, J. A.; Forman-Kay, J. D. Sequence determinants of compaction in intrinsically disordered proteins Biophys. J. 2010, 98, 2383-2390 10.1016/j.bpj.2010.02.006
66. Yoo, T. Y.; Meisburger, S. P.; Hinshaw, J.; Pollack, L.; Haran, G.; Sosnick, T. R.; Plaxco, K. Small-angle X-ray scattering and single-molecule FRET spectroscopy produce highly divergent views of the low-denaturant unfolded state J. Mol. Biol. 2012, 418, 226-236 10.1016/j.jmb.2012.01.016
67. Best, R. B.; Zheng, W.; Mittal, J. Balanced protein-water interactions improve properties of disordered proteins and non-specific protein association J. Chem. Theory Comput. 2014, 10, 5113-5124 10.1021/ct500569b
68. Piana, S.; Donchev, A. G.; Robustelli, P.; Shaw, D. E. Water dispersion interactions strongly influence simulated structural properties of disordered protein states J. Phys. Chem. B 2015, 119, 5113-5123 10.1021/jp508971m
69. Kabsch, W.; Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features Biopolymers 1983, 22, 2577-2637 10.1002/bip.360221211
70. Yang, W. Y.; Larios, E.; Gruebele, M. On the extended β-conformation propensity of polypeptides at high temperature J. Am. Chem. Soc. 2003, 125, 16220-16227 10.1021/ja0360081
71. Kimura, T.; Uzawa, T.; Ishimori, K.; Morishima, I.; Takahashi, S.; Konno, T.; Akiyama, S.; Fujisawa, T. Specific collapse followed by slow hydrogen-bond formation of β-sheet in the folding of single-chain monellin Proc. Natl. Acad. Sci. U.S.A. 2005, 102, 2748-2753 10.1073/pnas.0407982102
72. Doniach, S.; Garel, T.; Orland, H. Phase diagram of a semiflexible polymer chain in a θsolvent: application to protein folding J. Chem. Phys. 1996, 105, 1601-1608 10.1063/1.472031
73. Nettels, D.; Gopich, I. V.; Hoffmann, A.; Schuler, B. Ultrafast dynamics of protein collapse from single-molecule photon statistics Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 2655-2660 10.1073/pnas.0611093104
74. Zerze, G. H.; Best, R. B.; Mittal, J. Modest influence of FRET chromophores on the properties of unfolded proteins Biophys. J. 2014, 107, 1654-1660 10.1016/j.bpj.2014.07.071
75. Miller, S.; Janin, J.; Lesk, A. M.; Chothia, C. Interior and surface of monomeric proteins J. Mol. Biol. 1987, 196, 641-656 10.1016/0022-2836(87)90038-6
76. Chandler, D. Interfaces and the driving force of hydrophobic assembly Nature 2005, 437, 640-647 10.1038/nature04162
77. Ozenne, V.; Schneider, R.; Yao, M.; Huang, J.-r.; Salmon, L.; Zweckstetter, M.; Jensen, M. R.; Blackledge, M. Mapping the potential energy landscape of intrinsically disordered proteins at amino acid resolution J. Am. Chem. Soc. 2012, 134, 15138-15148 10.1021/ja306905s
78. Iešmantavičius, V.; Dogan, J.; Jemth, P.; Teilum, K.; Kjaergaard, M. Helical propensity in an intrinsically disordered protein accelerates ligand binding Angew. Chem., Int. Ed. 2014, 53, 1548-1551 10.1002/anie.201307712
79. Abascal, J. L.; Vega, C. A general purpose model for the condensed phases of water: TIP4P/2005 J. Chem. Phys. 2005, 123, 234505 10.1063/1.2121687
80. Hess, B.; Kutzner, C.; Van Der Spoel, D.; Lindahl, E. GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
81. Krieger, J. M.; Fusco, G.; Lewitzky, M.; Simister, P. C.; Marchant, J.; Camilloni, C.; Feller, S. M.; De Simone, A. Conformational recognition of an intrinsically disordered protein Biophys. J. 2014, 106, 1771-1779 10.1016/j.bpj.2014.03.004
82. Knott, M.; Best, R. B. A preformed binding interface in the unbound ensemble of an intrinsically disordered protein: evidence from molecular simulations PLoS Comput. Biol. 2012, 8, e1002605 10.1371/journal.pcbi.1002605
83. Mittal, J.; Yoo, T. H.; Georgiou, G.; Truskett, T. M. Structural ensemble of an intrinsically disordered polypeptide J. Phys. Chem. B 2013, 117, 118-124 10.1021/jp308984e