Is there an en route folding intermediate for cold shock proteins?

Protein Science

Volumn 21, Issue 5, 2012, Pages 677-685

  Huang, Lei ^a,b   Shakhnovich, Eugene I ^a  

^a HARVARD UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

Author keywords

value analysis; Cold shock protein; Discrete molecular dynamics; Folding dynamics; Folding intermediate; Transition state ensemble

Indexed keywords

COLD SHOCK PROTEIN;

AB INITIO CALCULATION; ARTICLE; ATOM; BACILLUS SUBTILIS; COLD SHOCK RESPONSE; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PHASE TRANSITION; PREDICTION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN UNFOLDING; SIMULATION; THERMOTOGA MARITIMA;

BACTERIAL PROTEINS; COLD SHOCK PROTEINS AND PEPTIDES; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEAT-SHOCK PROTEINS; KINETICS; MOLECULAR DYNAMICS SIMULATION; PROTEIN FOLDING;

EID: 84860143066     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2053     Document Type: Article

References (66)

1. Schindelin H, Marahiel MA, Heinemann U (1993) Universal nucleic acid-binding domain revealed by crystal-structure of the bacillus-subtilis major cold-shock protein. Nature 364:164-168. (Pubitemid 23238202)
2. Horn G, Hofweber R, Kremer W, Kalbitzer HR (2007) Structure and function of bacterial cold shock proteins. Cell Mol Life Sci 64:1457-1470. (Pubitemid 46954148)
3. Perl D, Welker C, Schindler T, Schroder 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. (Pubitemid 28113755)
4. Schindler T, Herrler M, Marahiel MA, Schmid FX (1995) Extremely rapid protein-folding in the absence of intermediates. Nat Struct Biol 2:663-673.
5. Schindler T, Schmid FX (1996) Thermodynamic properties of an extremely rapid protein folding reaction. Biochemistry 35:16833-16842. (Pubitemid 27020529)
6. Jacob M, Holtermann G, Perl D, Reinstein J, Schindler T, Geeves MA, Schmid FX (1999) Microsecond folding of the cold shock protein measured by a pressure-jump technique. Biochemistry 38:2882-2891.
7. Garcia-Mira MM, Boehringer D, Schmid FX (2004) The folding transition state of the cold shock protein is strongly polarized. J Mol Biol 339:555-569. (Pubitemid 38656116)
8. Garcia-Mira MM, Schmid FX (2006) Key role of coulombic interactions for the folding transition state of the cold shock protein. J Mol Biol 364:458-468. (Pubitemid 44715926)
9. Perl D, Holtermann G, Schmid FX (2001) Role of the chain termini for the folding transition state of the cold shock protein. Biochemistry 40:15501-15511. (Pubitemid 34015177)
10. Magg C, Kubelka J, Holtermann G, Haas E, Schmid FX (2006) Specificity of the initial collapse in the folding of the cold shock protein. J Mol Biol 360: 1067-1080. (Pubitemid 44062520)
11. Magg C, Schmid FX (2004) Rapid collapse precedes the fast two-state folding of the cold shock protein. J Mol Biol 335:1309-1323. (Pubitemid 38077248)
12. Reid KL, Rodriguez HM, Hillier BJ, Gregoret LM (1998) Stability and folding properties of a model beta-sheet protein, Escherichia coli CspA. Protein Sci 7:470-479.
13. Rodriguez HM, Vu DM, Gregoret LM (2000) Role of a solvent-exposed aromatic cluster in the folding of Escherichia coli CspA. Protein Sci 9:1993-2000.
14. Leeson DT, Gai F, Rodriguez HM, Gregoret LM, Dyer RB (2000) Protein folding and unfolding on a complex energy landscape. Proc Natl Acad Sci USA 97:2527-2532. (Pubitemid 30159204)
15. Vu DM, Reid KL, Rodriguez HM, Gregoret LM (2001) Examination of the folding of E-coli CspA through tryptophan substitutions. Protein Sci 10:2028-2036. (Pubitemid 32911222)
16. Rodriguez HM, Robertson AD, Gregoret LM (2002) Native state EX2 and EX1 hydrogen exchange of Escherichia coli CspA, a small beta-sheet protein. Biochemistry 41:2140-2148. (Pubitemid 34160873)
17. Rhoades E, Cohen M, Schuler B, Haran G (2004) Two-state folding observed in individual protein molecules. J Am Chem Soc 126:14686-14687. (Pubitemid 39532128)
18. Schuler B, Lipman EA, Eaton WA (2002) Probing the free-energy surface for protein folding with single-molecule fluorescence spectroscopy. Nature 419:743-747. (Pubitemid 35177962)
19. Merchant KA, Best RB, Louis JM, Gopich IV, Eaton WA (2007) Characterizing the unfolded states of proteins using single-molecule FRET spectroscopy and molecular simulations. Proc Natl Acad Sci USA 104:1528-1533. (Pubitemid 46214624)
20. Nettels D, Gopich IV, Hoffmann A, Schuler B (2007) Ultrafast dynamics of protein collapse from single-molecule photon statistics. Proc Natl Acad Sci USA 104:2655-2660. (Pubitemid 46327935)
21. Hoffmann A, Kane A, Nettels D, Hertzog DE, Baumgartel P, Lengefeld J, Reichardt G, Horsley DA, Seckler R, Bakajin O, Schuler B (2007) Mapping protein collapse with single-molecule fluorescence and kinetic synchrotron radiation circular dichroism spectroscopy. Proc Natl Acad Sci USA 104:105-110. (Pubitemid 46067992)
22. Chung HS, Louis JM, Eaton WA (2009) 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: 11837-11844.
23. Fersht AR, Matouschek A, Serrano L (1992) The folding of an enzyme 1. Theory of protein engineering analysis of stability and pathway of protein folding. J Mol Biol 224:771-782.
24. Alm E, Morozov AV, Kortemme T, Baker D (2002) Simple physical models connect theory and experiment in protein folding kinetics. J Mol Biol 322:463-476.
25. Shea JE, Brooks CL (2001) From folding theories to folding proteins: a review and assessment of simulation studies of protein folding and unfolding. Annu Rev Phys Chem 52:499-535.
26. Karanicolas J, Brooks CL (2003) The importance of explicit chain representation in protein folding models: an examination of Ising-like models. Proteins 53: 740-747. (Pubitemid 37352186)
27. Morra G, Hodoscek M, Knapp EW (2003) Unfolding of the cold shock protein studied with biased molecular dynamics. Proteins 53:597-606. (Pubitemid 37352173)
28. Huang XQ, Zhou HX (2006) Similarity and difference in the unfolding of thermophilic and mesophilic cold shock proteins studied by molecular dynamics. Biophys J 91:2451-2463.
29. Shaw DE, Deneroff MM, Dror RO, Kuskin JS, Larson RH, Salmon JK, Young C, Batson B, Bowers KJ, Chao JC, Eastwood MP, Gagliardo J, Grossman JP, Ho CR, Ierardi DJ, Kolossv-ary I, Klepeis JL, Layman T, McLeavey C, Moraes MA, Mueller R, Priest EC, Shan Y, Spengler J, Theobald M, Towles B, Wang SC (2008) Anton, a special-purpose machine for molecular dynamics simulation. Commun ACM 51:91-97.
30. Best RB, Buchete NV, Hummer G (2008) Are current molecular dynamics force fields too helical? Biophys J 95:L7-L9.
31. Yoda T, Sugita Y, Okamoto Y (2004) Comparisons of force fields for proteins by generalized-ensemble simulations. Chem Phys Lett 386:460-467.
32. Freddolino PL, Liu F, Gruebele M, Schulten K (2008) Ten-microsecond molecular dynamics simulation of a fast-folding WW domain. Biophys J 94:L75-L77.
33. Nettels D, Muller-Spath S, Kuster F, Hofmann H, Haenni D, Ruegger S, Reymond L, Hoffmann A, Kubelka J, Heinz B, Gast K, Best RB, Schuler B (2009) Single-molecule spectroscopy of the temperature-induced collapse of unfolded proteins. Proc Natl Acad Sci USA 106:20740-20745.
34. Yang JS, Wallin S, Shakhnovich EI (2008) Universality and diversity of folding mechanics for three-helix bundle proteins. Proc Natl Acad Sci USA 105:895-900. (Pubitemid 351282052)
35. Zhou YQ, Karplus M (1997) Folding thermodynamics of a model three-helix-bundle protein. Proc Natl Acad Sci USA 94:14429-14432.
36. Zhou YQ, Karplus M (1999) Interpreting the folding kinetics of helical proteins. Nature 401:400-403.
37. Linhananta A, Zhou YQ (2002) The role of sidechain packing and native contact interactions in folding: discontinuous molecular dynamics folding simulations of an all-atom G(o)over-bar model of fragment B of Staphylococcal protein A. J Chem Phys 117:8983-8995. (Pubitemid 35457605)
38. Shimada J, Kussell EL, Shakhnovich EI (2001) The folding thermodynamics and kinetics of crambin using an all-atom Monte Carlo simulation. J Mol Biol 308:79-95. (Pubitemid 33027629)
39. Shimada J, Shakhnovich EI (2002) The ensemble folding kinetics of protein G from an all-atom Monte Carlo simulation. Proc Natl Acad Sci USA 99:11175-11180. (Pubitemid 34920898)
40. Clementi C, Nymeyer H, Onuchic JN (2000) Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J Mol Biol 298:937-953.
41. Luo ZL, Ding JD, Zhou YQ (2007) Temperature-dependent folding pathways of pin1 WW domain: an all-atom molecular dynamics simulation of a G(o)over-bar model. Biophys J 93:2152-2161.
42. Luo ZL, Ding JD, Zhou YQ (2008) Folding mechanisms of individual beta-hairpins in a Go model of Pin1 WW domain by all-atom molecular dynamics simulations. J Chem Phys 128:225103.
43. Ding F, Guo WH, Dokholyan NV, Shakhnovich EI, Shea JE (2005) Reconstruction of the src-SH3 protein domain transition state ensemble using multiscale molecular dynamics simulations. J Mol Biol 350: 1035-1050. (Pubitemid 40943460)
44. Hills RD, Brooks CL (2009) Insights from coarse-grained go models for protein folding and dynamics. Int J Mol Sci 10:889-905.
45. Klimov DK, Thirumalai D (2000) Mechanisms and kinetics of beta-hairpin formation. Proc Natl Acad Sci USA 97:2544-2549.
46. 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. (Pubitemid 38917965)
47. Dokholyan NV, Li L, Ding F, Shakhnovich EI (2002) Topological determinants of protein folding. Proc Natl Acad Sci USA 99:8637-8641. (Pubitemid 34693612)
48. Paci E, Vendruscolo M, Karplus M (2002) Validity of Go models: comparison with a solvent-shielded empirical energy decomposition. Biophys J 83:3032-3038. (Pubitemid 36041926)
49. Paci E, Vendruscolo M, Karplus M (2002) Native and non-native interactions along protein folding and unfolding pathways. Proteins 47:379-392. (Pubitemid 34438687)
50. Tsai J, Taylor R, Chothia C, Gerstein M (1999) The packing density in proteins: standard radii and volumes. J Mol Biol 290:253-266. (Pubitemid 29308589)
51. Zhou YQ, Karplus M, Wichert JM, Hall CK (1997) Equilibrium thermodynamics of homopolymers and clusters: molecular dynamics and Monte Carlo simulations of systems with square-well interactions. J Chem Phys 107:10691-10708. (Pubitemid 127627219)
52. Sugita Y, Okamoto Y (1999) Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 314:141-151. (Pubitemid 129556751)
53. Ferrenberg AM, Swendsen RH (1989) Optimized Monte Carlo data-analysis. Phys Rev Lett 63:1195-1198.
54. Frenkel D, Smit B (2001) Understanding Molecular Simulation. 2nd ed. San Diego: Academic Press.
55. Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA (1995) Multidimensional free-energy calculations using the weighted histogram analysis method. J Comput Chem 16:1339-1350.
56. Makhatadze GI, Marahiel MA (1994) Effect of pH and phosphate ions on self-association properties of the major cold-shock protein from Bacillus-Subtilis. Protein Sci 3:2144-2147.
57. Cellmer T, Henry ER, Hofrichter J, Eaton WA (2008) Measuring internal friction of an ultrafast-folding protein. Proc Natl Acad Sci USA 105:18320-18325.
58. O'Brien EP, Ziv G, Haran G, Brooks BR, Thirumalai D (2008) Effects of denaturants and osmolytes on proteins are accurately predicted by the molecular transfer model. Proc Natl Acad Sci USA 105:13403-13408.
59. Nettels D, Hoffmann A, Schuler B (2008) Unfolded protein and peptide dynamics investigated with singlemolecule FRET and correlation spectroscopy from picoseconds to seconds. J Phys Chem B 112:6137-6146.
60. Du R, Pande V, Grosberg A, Tanaka T, Shakhnovich EI (1998) On the transition coordinate for protein folding. J Chem Phys 108:334-350. (Pubitemid 128571237)
61. Shakhnovich EI (2006) Protein folding thermodynamics and dynamics: where physics, chemistry, and biology meet. Chem Rev 106:1559-1588.
62. Muff S, Caflisch A (2009) Identification of the protein folding transition state from molecular dynamics trajectories. J Chem Phys 130:125104.
63. Hubner IA, Shimada J, Shakhnovich EI (2004) Commitment and nucleation in the protein G transition state. J Mol Biol 336:745-761. (Pubitemid 38183026)
64. Xu D, Zhang Y (2009) Generating triangulated macromolecular surfaces by Euclidean distance transform. Plos One 4:e8140.
65. Lipman EA, Schuler B, Bakajin O, Eaton WA (2003) Single-molecule measurement of protein folding kinetics. Science 301:1233-1235. (Pubitemid 37052211)
66. Shakhnovich EI (1997) Theoretical studies of protein-folding thermodynamics and kinetics. Curr Opin Struct Biol 7:29-40.