Meandering Down the Energy Landscape of Protein Folding: Are We There Yet?

Biophysical Journal

Volumn 110, Issue 9, 2016, Pages 1924-1932

  Abaskharon, Rachel M ^a   Gai, Feng ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN FOLDING; SPECTROFLUOROMETRY; THERMODYNAMICS;

PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; THERMODYNAMICS;

EID: 84966393656     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2016.03.030     Document Type: Review

References (89)

1. C.B. Anfinsen, and E. Haber F.H. White Jr. The kinetics of formation of native ribonuclease during oxidation of the reduced polypeptide chain Proc. Natl. Acad. Sci. USA 47 1961 1309 1314
2. C. Levinthal Are there pathways for protein folding J. Chim. Phys. Physico-Chemie Biol. 65 1968 44 45
3. J.D. Bryngelson, and J.N. Onuchic P.G. Wolynes Funnels, pathways, and the energy landscape of protein folding: a synthesis Proteins 21 1995 167 195
4. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nat. Struct. Biol. 4 1997 10 19
5. A. Matouschek, and J.T. Kellis Jr. A.R. Fersht Mapping the transition state and pathway of protein folding by protein engineering Nature 340 1989 122 126
6. S.E. Jackson, and A.R. Fersht Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition Biochemistry 30 1991 10428 10435
7. S. Williams, and T.P. Causgrove R.B. Dyer Fast events in protein folding: helix melting and formation in a small peptide Biochemistry 35 1996 691 697
8. B. Schuler, E.A. Lipman, and W.A. Eaton Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy Nature 419 2002 743 747
9. D. Thirumalai, and E.P. O'Brien C. Hyeon Theoretical perspectives on protein folding Annu. Rev. Biophys. 39 2010 159 183
10. V.N. Uversky, and A.K. Dunker Understanding protein non-folding Biochim. Biophys. Acta 1804 2010 1231 1264
11. G.R. Bowman, V.A. Voelz, and V.S. Pande Taming the complexity of protein folding Curr. Opin. Struct. Biol. 21 2011 4 11
12. A. Gershenson, and L.M. Gierasch Protein folding in the cell: challenges and progress Curr. Opin. Struct. Biol. 21 2011 32 41
13. R.B. Best Atomistic molecular simulations of protein folding Curr. Opin. Struct. Biol. 22 2012 52 61
14. R.O. Dror, and R.M. Dirks D.E. Shaw Biomolecular simulation: a computational microscope for molecular biology Annu. Rev. Biophys. 41 2012 429 452
15. I. Guzman, and M. Gruebele Protein folding dynamics in the cell J. Phys. Chem. B 118 2014 8459 8470
16. J.-L. Popot, and D.M. Engelman Membranes do not tell proteins how to fold Biochemistry 55 2016 5 18
17. P.C. Whitford, and J.N. Onuchic What protein folding teaches us about biological function and molecular machines Curr. Opin. Struct. Biol. 30 2015 57 62
18. E. Sherman, and G. Haran Fluorescence correlation spectroscopy of fast chain dynamics within denatured protein L ChemPhysChem 12 2011 696 703
19. D.P. Teufel, and C.M. Johnson H. Neuweiler Backbone-driven collapse in unfolded protein chains J. Mol. Biol. 409 2011 250 262
20. A. Borgia, and B.G. Wensley B. Schuler Localizing internal friction along the reaction coordinate of protein folding by combining ensemble and single-molecule fluorescence spectroscopy Nat. Commun. 3 2012 1195 1203
21. A. Soranno, and B. Buchli B. Schuler Quantifying internal friction in unfolded and intrinsically disordered proteins with single-molecule spectroscopy Proc. Natl. Acad. Sci. USA 109 2012 17800 17806
22. V.A. Voelz, and M. Jäger V.S. Pande Slow unfolded-state structuring in Acyl-CoA binding protein folding revealed by simulation and experiment J. Am. Chem. Soc. 134 2012 12565 12577
23. H.S. Chung, and S. Piana-Agostinetti W.A. Eaton Structural origin of slow diffusion in protein folding Science 349 2015 1504 1510
24. A. Szabo, K. Schulten, and Z. Schulten First passage time approach to diffusion controlled reactions J. Chem. Phys. 72 1980 4350 4357
25. Y. Zhu, and D.O.V. Alonso F. Gai Ultrafast folding of alpha3D: a de novo designed three-helix bundle protein Proc. Natl. Acad. Sci. USA 100 2003 15486 15491
26. M. Pirchi, and G. Ziv G. Haran Single-molecule fluorescence spectroscopy maps the folding landscape of a large protein Nat. Commun. 2 2011 493 499
27. J. Liu, and L.A. Campos V. Muñoz Exploring one-state downhill protein folding in single molecules Proc. Natl. Acad. Sci. USA 109 2012 179 184
28. D.T. Gruszka, and F. Whelan J. Clarke Cooperative folding of intrinsically disordered domains drives assembly of a strong elongated protein Nat. Commun. 6 2015 7271 7279
29. H.S. Chung, and K. McHale W.A. Eaton Single-molecule fluorescence experiments determine protein folding transition path times Science 335 2012 981 984
30. H.S. Chung, J.M. Louis, and W.A. Eaton Experimental determination of upper bound for transition path times in protein folding from single-molecule photon-by-photon trajectories Proc. Natl. Acad. Sci. USA 106 2009 11837 11844
31. Y. Gao, G. Sirinakis, and Y. Zhang Highly anisotropic stability and folding kinetics of a single coiled coil protein under mechanical tension J. Am. Chem. Soc. 133 2011 12749 12757
32. B. Jagannathan, and P.J. Elms S. Marqusee Direct observation of a force-induced switch in the anisotropic mechanical unfolding pathway of a protein Proc. Natl. Acad. Sci. USA 109 2012 17820 17825
33. E.J. Guinn, B. Jagannathan, and S. Marqusee Single-molecule chemo-mechanical unfolding reveals multiple transition state barriers in a small single-domain protein Nat. Commun. 6 2015 6861 6868
34. C. He, and G.Z. Genchev H. Li Mechanically untying a protein slipknot: multiple pathways revealed by force spectroscopy and steered molecular dynamics simulations J. Am. Chem. Soc. 134 2012 10428 10435
35. J. Stigler, and F. Ziegler M. Rief The complex folding network of single calmodulin molecules Science 334 2011 512 516
36. R. Berkovich, and S. Garcia-Manyes J.M. Fernandez Collapse dynamics of single proteins extended by force Biophys. J. 98 2010 2692 2701
37. S. Garcia-Manyes, T.-L. Kuo, and J.M. Fernández Contrasting the individual reactive pathways in protein unfolding and disulfide bond reduction observed within a single protein J. Am. Chem. Soc. 133 2011 3104 3113
38. H. Yu, and A.N. Gupta M.T. Woodside Energy landscape analysis of native folding of the prion protein yields the diffusion constant, transition path time, and rates Proc. Natl. Acad. Sci. USA 109 2012 14452 14457
39. S.A. Waldauer, O. Bakajin, and L.J. Lapidus Extremely slow intramolecular diffusion in unfolded protein L Proc. Natl. Acad. Sci. USA 107 2010 13713 13717
40. M. Xu, and O. Beresneva H. Roder Microsecond folding dynamics of apomyoglobin at acidic pH J. Phys. Chem. B 116 2012 7014 7025
41. T. Aksel, and D. Barrick Direct observation of parallel folding pathways revealed using a symmetric repeat protein system Biophys. J. 107 2014 220 232
42. B.N. Markiewicz, R.M. Culik, and F. Gai Tightening up the structure, lighting up the pathway: application of molecular constraints and light to manipulate protein folding, self-assembly and function Sci. China Chem. 57 2014 1615 1624
43. A.A. Deeg, and M.S. Rampp W. Zinth Isomerization- and temperature-jump-induced dynamics of a photoswitchable β-hairpin Chemistry 20 2014 694 703
44. J. Bredenbeck, and J. Helbing P. Hamm Alpha-helix formation in a photoswitchable peptide tracked from picoseconds to microseconds by time-resolved IR spectroscopy Proc. Natl. Acad. Sci. USA 102 2005 2379 2384
45. J.A. Ihalainen, and B. Paoli P. Hamm Alpha-Helix folding in the presence of structural constraints Proc. Natl. Acad. Sci. USA 105 2008 9588 9593
46. E. Chen, and J.R. Kumita D.S. Kliger The kinetics of helix unfolding of an azobenzene cross-linked peptide probed by nanosecond time-resolved optical rotatory dispersion J. Am. Chem. Soc. 125 2003 12443 12449
47. R.M. Abaskharon, and R.M. Culik F. Gai Tuning the attempt frequency of protein folding dynamics via transition-state rigidification: application to Trp-cage J. Phys. Chem. Lett. 6 2015 521 526
48. H.S.M. Lu, and M. Volk W.F. DeGrado Aminothiotyrosine disulfide, an optical trigger for initiation of protein folding J. Am. Chem. Soc. 119 1997 7173 7180
49. L. Milanesi, and J.P. Waltho M. Volk Measurement of energy landscape roughness of folded and unfolded proteins Proc. Natl. Acad. Sci. USA 109 2012 19563 19568
50. N. Regner, and T.T. Herzog W. Zinth Light-switchable hemithioindigo-hemistilbene-containing peptides: ultrafast spectroscopy of the Z → E isomerization of the chromophore and the structural dynamics of the peptide moiety J. Phys. Chem. B 116 2012 4181 4191
51. S.P. Brown, and A.B. Smith 3rd Peptide/protein stapling and unstapling: introduction of s-tetrazine, photochemical release, and regeneration of the peptide/protein J. Am. Chem. Soc. 137 2015 4034 4037
52. M.J. Tucker, and J.R. Courter R.M. Hochstrasser Tetrazine phototriggers: probes for peptide dynamics Angew. Chem. Int. Ed. Engl. 49 2010 3612 3616
53. M.J. Tucker, and M. Abdo R.M. Hochstrasser Nonequilibrium dynamics of helix reorganization observed by transient 2D IR spectroscopy Proc. Natl. Acad. Sci. USA 110 2013 17314 17319
54. M.M. Lin, and O.F. Mohammed A.H. Zewail Speed limit of protein folding evidenced in secondary structure dynamics Proc. Natl. Acad. Sci. USA 108 2011 16622 16627
55. B.N. Markiewicz, and H. Jo F. Gai Assessment of local friction in protein folding dynamics using a helix cross-linker J. Phys. Chem. B 117 2013 14688 14696
56. R.P. Nobrega, and K. Arora C.R. Matthews Modulation of frustration in folding by sequence permutation Proc. Natl. Acad. Sci. USA 111 2014 10562 10567
57. M.R. Hilaire, R.M. Abaskharon, and F. Gai Biomolecular crowding arising from small molecules, molecular constraints, surface packing, and nano-confinement J. Phys. Chem. Lett. 6 2015 2546 2553
58. D.E. Sagnella, J.E. Straub, and D. Thirumalai Time scales and pathways for kinetic energy relaxation in solvated proteins: application to carbonmonoxy myoglobin J. Chem. Phys. 113 2000 7702 7711
59. B.N. Markiewicz, and L. Yang F. Gai How quickly can a β-hairpin fold from its transition state? J. Phys. Chem. B 118 2014 3317 3325
60. A.T. Shandiz, M.C. Baxa, and T.R. Sosnick A "Link-Psi" strategy using cross-linking indicates that the folding transition state of ubiquitin is not very malleable Protein Sci. 21 2012 819 827
61. A.L. Serrano, M.M. Waegele, and F. Gai Spectroscopic studies of protein folding: linear and nonlinear methods Protein Sci. 21 2012 157 170
62. R.M. Culik, and A.L. Serrano F. Gai Achieving secondary structural resolution in kinetic measurements of protein folding: a case study of the folding mechanism of Trp-cage Angew. Chem. Int. Ed. Engl. 50 2011 10884 10887
63. H. Chi, and W.R.W. Welch T.A. Keiderling Insight into the packing pattern of β2 fibrils: a model study of glutamic acid rich oligomers with 13C isotopic edited vibrational spectroscopy Biomacromolecules 14 2013 3880 3891
64. H.S. Chung, and M. Khalil A. Tokmakoff Transient two-dimensional IR spectrometer for probing nanosecond temperature-jump kinetics Rev. Sci. Instrum. 78 2007 063101
65. K.C. Jones, C.S. Peng, and A. Tokmakoff Folding of a heterogeneous β-hairpin peptide from temperature-jump 2D IR spectroscopy Proc. Natl. Acad. Sci. USA 110 2013 2828 2833
66. S.D. Moran, and A.M. Woys M.T. Zanni Two-dimensional IR spectroscopy and segmental 13C labeling reveals the domain structure of human γD-crystallin amyloid fibrils Proc. Natl. Acad. Sci. USA 109 2012 3329 3334
67. A. Remorino, and I.V. Korendovych R.M. Hochstrasser Residue-specific vibrational echoes yield 3D structures of a transmembrane helix dimer Science 332 2011 1206 1209
68. J.M.G. Rogers, L.G. Lippert, and F. Gai Non-natural amino acid fluorophores for one- and two-step fluorescence resonance energy transfer applications Anal. Biochem. 399 2010 182 189
69. J.M. Goldberg, and R.F. Wissner E.J. Petersson Thioamide quenching of intrinsic protein fluorescence Chem. Commun. (Camb.) 48 2012 1550 1552
70. M.R. Mintzer, T. Troxler, and F. Gai p-Cyanophenylalanine and selenomethionine constitute a useful fluorophore-quencher pair for short distance measurements: application to polyproline peptides Phys. Chem. Chem. Phys. 17 2015 7881 7887
71. I. Peran, and M.D. Watson D.P. Raleigh Selenomethionine, p-cyanophenylalanine pairs provide a convenient, sensitive, non-perturbing fluorescent probe of local helical structure Chem. Commun. (Camb.) 52 2016 2055 2058
72. M.B. Prigozhin, and S.-H. Chao M. Gruebele Mapping fast protein folding with multiple-site fluorescent probes Proc. Natl. Acad. Sci. USA 112 2015 7966 7971
73. J. Ma, and I.M. Pazos F. Gai Site-specific infrared probes of proteins Annu. Rev. Phys. Chem. 66 2015 357 377
74. C.M. Davis, and R.B. Dyer The role of electrostatic interactions in folding of β-proteins J. Am. Chem. Soc. 138 2016 1456 1464
75. S. Nagarajan, and H. Taskent-Sezgin R.B. Dyer Differential ordering of the protein backbone and side chains during protein folding revealed by site-specific recombinant infrared probes J. Am. Chem. Soc. 133 2011 20335 20340
76. A. Bachmann, and D. Wildemann T. Kiefhaber Mapping backbone and side-chain interactions in the transition state of a coupled protein folding and binding reaction Proc. Natl. Acad. Sci. USA 108 2011 3952 3957
77. R.M. Culik, and H. Jo F. Gai Using thioamides to site-specifically interrogate the dynamics of hydrogen bond formation in β-sheet folding J. Am. Chem. Soc. 134 2012 8026 8029
78. C. Sanchez-Medina, and A. Sekhar L.E. Kay Probing the free energy landscape of the fast-folding gpW protein by relaxation dispersion NMR J. Am. Chem. Soc. 136 2014 7444 7451
79. Z.-Y. Kan, and B.T. Walters S.W. Englander Protein hydrogen exchange at residue resolution by proteolytic fragmentation mass spectrometry analysis Proc. Natl. Acad. Sci. USA 110 2013 16438 16443
80. A.N. Calabrese, and J.R. Ault A.E. Ashcroft Using hydroxyl radical footprinting to explore the free energy landscape of protein folding Methods 89 2015 38 44
81. D.E. Shaw, and J.C. Chao K.J. Bowers Anton, a special-purpose machine for molecular dynamics simulation Commun. ACM 51 2008 91 97
82. D.E. Shaw, and P. Maragakis W. Wriggers Atomic-level characterization of the structural dynamics of proteins Science 330 2010 341 346
83. K. Lindorff-Larsen, and S. Piana D.E. Shaw How fast-folding proteins fold Science 334 2011 517 520
84. V.S. Pande, K. Beauchamp, and G.R. Bowman Everything you wanted to know about Markov State Models but were afraid to ask Methods 52 2010 99 105
85. V.A. Voelz, and G.R. Bowman V.S. Pande Molecular simulation of ab initio protein folding for a millisecond folder NTL9(1-39) J. Am. Chem. Soc. 132 2010 1526 1528
86. 2) dihedral angles J. Chem. Theory Comput. 8 2012 3257 3273
87. R.B. Best, W. Zheng, and J. Mittal Balanced protein-water interactions improve properties of disordered proteins and non-specific protein association J. Chem. Theory Comput. 10 2014 5113 5124
88. H.S. Cho, and N. Dashdorj P. Anfinrud Protein structural dynamics in solution unveiled via 100-ps time-resolved x-ray scattering Proc. Natl. Acad. Sci. USA 107 2010 7281 7286
89. J.G. Kim, and T.W. Kim H. Ihee Protein structural dynamics revealed by time-resolved x-ray solution scattering Acc. Chem. Res. 48 2015 2200 2208