Protein unfolding rates correlate as strongly as folding rates with native structure

Protein Science

Volumn 24, Issue 4, 2015, Pages 580-587

  Broom, Aron ^a   Gosavi, Shachi ^b   Meiering, Elizabeth M ^a  

^a UNIVERSITY OF WATERLOO   (Canada)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

contact order; folding rate; kinetic stability; long range order; protein design; protein engineering; scaffold selection; structural complexity; topology; unfolding rate

Indexed keywords

PROTEINASE; PROTEIN;

ARTICLE; DISULFIDE BOND; PRIORITY JOURNAL; PROTEIN DENATURATION; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN UNFOLDING; THERMODYNAMICS; CHEMISTRY; KINETICS; METABOLISM; PROTEIN DATABASE;

DATABASES, PROTEIN; KINETICS; PROTEIN ENGINEERING; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN UNFOLDING; PROTEINS; THERMODYNAMICS;

EID: 84948393948     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2606     Document Type: Article

References (61)

1. Daggett V, Fersht A, (2003) The present view of the mechanism of protein folding. Nat Rev Mol Cell Biol 4: 497-502.
2. Sosnick TR, Barrick D, (2011) The folding of single domain proteins-have we reached a consensus? Curr Opin Struct Biol 21: 12-24.
3. Chan HS, Zhang Z, Wallin S, Liu Z, (2011) Cooperativity, local-nonlocal coupling, and nonnative interactions: principles of protein folding from coarse-grained models. Annu Rev Phys Chem 62: 301-326.
4. Dill KA, Ozkan SB, Shell MS, Weikl TR, (2008) The protein folding problem. Annu Rev Biophys 37: 289-316.
5. Onuchic JN, Luthey-Schulten Z, Wolynes PG, (1997) Theory of protein folding: the energy landscape perspective. Annu Rev Phys Chem 48: 545-600.
6. Plaxco KW, Simons KT, Baker D, (1998) Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 277: 985-994.
7. Ivankov DN, Garbuzynskiy SO, Alm E, Plaxco KW, Baker D, Finkelstein AV, (2003) Contact order revisited: influence of protein size on the folding rate. Protein Sci 12: 2057-2062.
8. Lane TJ, Pande VS, (2013) Inferring the rate-length law of protein folding. PLoS One 8: e78606.
9. Gutin A, Abkevich V, Shakhnovich E, (1996) Chain length scaling of protein folding time. Phys Rev Lett 77: 5433-5436.
10. Zwanzig R, Szabo A, Bagchi B, (1992) Levinthal's paradox. Proc Natl Acad Sci USA 89: 20-22.
11. Li MS, Klimov DK, Thirumalai D, (2002) Dependence of folding rates on protein length. J Phys Chem B 106: 8302-8305.
12. Wolynes PG, (1997) Folding funnels and energy landscapes of larger proteins within the capillarity approximation. Proc Natl Acad Sci USA 94: 6170-6175.
13. Naganathan AN, Muñoz V, (2005) Scaling of folding times with protein size. J Am Chem Soc 127: 480-481.
14. Istomin AY, Jacobs DJ, Livesay DR, (2007) On the role of structural class of a protein with two-state folding kinetics in determining correlations between its size, topology, and folding rate. Protein Sci 16: 2564-2569.
15. Rollins GC, Dill KA, (2014) A general mechanism of 2-state protein-folding kinetics. J Am Chem Soc 136: 11420-11427.
16. Paci E, Lindorff-Larsen K, Dobson CM, Karplus M, Vendruscolo M, (2005) Transition state contact orders correlate with protein folding rates. J Mol Biol 352: 495-500.
17. Faísca PFN, Travasso RDM, Parisi A, Rey A, (2012) Why do protein folding rates correlate with metrics of native topology? PLoS One 7: e35599.
18. Sosnick TR, (2008) Kinetic barriers and the role of topology in protein and RNA folding. Protein Sci 17: 1308-1318.
19. Gromiha MM, Selvaraj S, (2001) Comparison between long-range interactions and contact order in determining the folding rate of two-state proteins: application of long-range order to folding rate prediction. J Mol Biol 310: 27-32.
20. Zou T, Ozkan SB, (2011) Local and non-local native topologies reveal the underlying folding landscape of proteins. Phys Biol 8: 066011.
21. Zhou H, Zhou Y, (2002) Folding rate prediction using total contact distance. Biophys J 82: 458-463.
22. Ouyang Z, Liang J, (2008) Predicting protein folding rates from geometric contact and amino acid sequence. Protein Sci 17: 1256-1263.
23. Micheletti C, (2003) Prediction of folding rates and transition-state placement from native-state geometry. Proteins 51: 74-84.
24. Tejera E, Machado A, Rebelo I, Nieto-Villar J, (2009) Fractal protein structure revisited: topological, kinetic and thermodynamic relationships. Phys A Stat Mech Appl 388: 4600-4608.
25. Rustad M, Ghosh K, (2012) Why and how does native topology dictate the folding speed of a protein? J Chem Phys 137: 205104.
26. Su JG, Li CH, Hao R, Chen WZ, Wang CX, (2008) Protein unfolding behavior studied by elastic network model. Biophys J 94: 4586-4596.
27. Jung J, Buglass AJ, Lee E-K, (2010) Topological quantities determining the folding/unfolding rate of two-state folding proteins. J Solut Chem 39: 943-958.
28. Jung J, Lee J, Moon H-T, (2005) Topological determinants of protein unfolding rates. Proteins 58: 389-395.
29. Harihar B, Selvaraj S, (2011) Application of long-range order to predict unfolding rates of two-state proteins. Proteins 79: 880-887.
30. Maxwell KL, Wildes D, Zarrine-Afsar A, De Los Rois MA, Brown AG, Friel CT, Hedberg L, Horng J-C, Bona D, Miller EJ, Vallée-Bélisle A, Main ERG, Bemporad F, Qiu L, Teilum K, Vu N-D, Edwards AM, Ruczinski I, Poulsen FM, Kragelund BB, Michnick SW, Chiti F, Bai Y, Hagen SJ, Serrano L, Oliveberg M, Raleigh DP, Wittung-Stafshede P, Radford SE, Jackson SE, Sosnick TR, Marqusee S, Davidson AR, Plaxco KW, (2005) Protein folding: defining a "standard" set of experimental conditions and a preliminary kinetic data set of two-state proteins. Protein Sci 14: 602-616.
31. Wensley BG, Gärtner M, Choo WX, Batey S, Clarke J, (2009) Different members of a simple three-helix bundle protein family have very different folding rate constants and fold by different mechanisms. J Mol Biol 390: 1074-1085.
32. Ferguson N, Sharpe TD, Schartau PJ, Sato S, Allen MD, Johnson CM, Rutherford TJ, Fersht AR, (2005) Ultra-fast barrier-limited folding in the peripheral subunit-binding domain family. J Mol Biol 353: 427-446.
33. Perl D, Welker C, Schindler T, Schröder K, Marahiel MA, Jaenicke R, Schmid FX, (1998) Conservation of rapid two-state folding in mesophilic, thermophilic and hyperthermophilic cold shock proteins. Nat Struct Biol 5: 229-235.
34. Garbuzynskiy SO, Ivankov DN, Bogatyreva NS, Finkelstein AV, (2013) Golden triangle for folding rates of globular proteins. Proc Natl Acad Sci USA 110: 147-150.
35. Chavez LL, Onuchic JN, Clementi C, (2004) Quantifying the roughness on the free energy landscape: entropic bottlenecks and protein folding rates. J Am Chem Soc 126: 8426-8432.
36. Plaxco KW, Simons KT, Ruczinski I, Baker D, (2000) Topology, stability, sequence, and length: defining the determinants of two-state protein folding kinetics. Biochemistry 39: 11177-11183.
37. Gráczer E, Varga A, Hajdú I, Melnik B, Szilágyi A, Semisotnov G, Závodszky P, Vas M, (2007) Rates of unfolding, rather than refolding, determine thermal stabilities of thermophilic, mesophilic, and psychrotrophic 3-isopropylmalate dehydrogenases. Biochemistry 46: 11536-11549.
38. Dobson CM, (2003) Protein folding and misfolding. Nature 426: 884-890.
39. Matouschek A, (2003) Protein unfolding-an important process in vivo? Curr Opin Struct Biol 13: 98-109.
40. De Sancho D, Muñoz V, (2011) Integrated prediction of protein folding and unfolding rates from only size and structural class. Phys Chem Chem Phys 13: 17030-17043.
41. Fiebig KM, Dill KA, (1993) Protein core assembly processes. J Chem Phys 98: 3475.
42. Nickson AA, Clarke J, (2010) What lessons can be learned from studying the folding of homologous proteins? Methods 52: 38-50.
43. Jackson SE, (1998) How do small single-domain proteins fold? Fold Des 3: R81-R91.
44. Lawrence C, Kuge J, Ahmad K, Plaxco KW, (2010) Investigation of an anomalously accelerating substitution in the folding of a prototypical two-state protein. J Mol Biol 403: 446-458.
45. Naganathan AN, Muñoz V, (2010) Insights into protein folding mechanisms from large scale analysis of mutational effects. Proc Natl Acad Sci USA 107: 8611-8616.
46. Gosavi S, (2013) Understanding the folding-function tradeoff in proteins. PLoS One 8: e61222.
47. Yi Q, Scalley-Kim ML, Alm EJ, Baker D, (2000) NMR characterization of residual structure in the denatured state of protein L. J Mol Biol 299: 1341-1351.
48. Ratcliff K, Marqusee S, (2010) Identification of residual structure in the unfolded state of ribonuclease H1 from the moderately thermophilic Chlorobium tepidum: comparison with thermophilic and mesophilic homologues. Biochemistry 49: 5167-5175.
49. Zarrine-Afsar A, Wallin S, Neculai AM, Neudecker P, Howell PL, Davidson AR, Chan HS, (2008) Theoretical and experimental demonstration of the importance of specific nonnative interactions in protein folding. Proc Natl Acad Sci USA 105: 9999-10004.
50. Shental-Bechor D, Smith MTJ, Mackenzie D, Broom A, Marcovitz A, Ghashut F, Go C, Bralha F, Meiering EM, Levy Y, (2012) Nonnative interactions regulate folding and switching of myristoylated protein. Proc Natl Acad Sci USA 109: 17839-17844.
51. Clementi C, Plotkin SS, (2004) The effects of nonnative interactions on protein folding rates: theory and simulation. Protein Sci 13: 1750-1766.
52. Machius M, Declerck N, Huber R, Wiegand G, (2003) Kinetic stabilization of Bacillus licheniformis alpha-amylase through introduction of hydrophobic residues at the surface. J Biol Chem 278: 11546-11553.
53. Cavagnero S, Debe DA, Zhou ZH, Adams MW, Chan SI, (1998) Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins. Biochemistry 37: 3369-3376.
54. Rodriguez-Larrea D, Minning S, Borchert TV, Sanchez-Ruiz JM, (2006) Role of solvation barriers in protein kinetic stability. J Mol Biol 360: 715-724.
55. Manning M, Colõn W, (2004) Structural basis of protein kinetic stability: resistance to sodium dodecyl sulfate suggests a central role for rigidity and a bias toward beta-sheet structure. Biochemistry 43: 11248-11254.
56. Sanchez-Ruiz JM, (2010) Protein kinetic stability. Biophys Chem 148: 1-15.
57. Bogatyreva NS, Osypov AA, Ivankov DN, (2009) KineticDB: a database of protein folding kinetics. Nucleic Acids Res 37: D342-D346.
58. Smith MTJ, Meissner J, Esmonde S, Wong HJ, Meiering EM, (2010) Energetics and mechanisms of folding and flipping the myristoyl switch in the {beta}-trefoil protein, hisactophilin. Proc Natl Acad Sci USA 107: 20952-20957.
59. Lee J, Blaber SI, Dubey VK, Blaber M, (2011) A polypeptide "building block" for the β-trefoil fold identified by "top-down symmetric deconstruction." J Mol Biol 407: 744-763.
60. Spector S, Raleigh DP, (1999) Submillisecond folding of the peripheral subunit-binding domain. J Mol Biol 293: 763-768.
61. Broom A, Doxey AC, Lobsanov YD, Berthin LG, Rose DR, Howell PL, McConkey BJ, Meiering EM, (2012) Modular evolution and the origins of symmetry: reconstruction of a three-fold symmetric globular protein. Structure 20: 161-171.