Temperature and urea induced denaturation of the TRP-cage mini protein TC5b: A simulation study consistent with experimental observations

Protein Science

Volumn 18, Issue 10, 2009, Pages 2090-2099

  Gattin, Z ^a   Riniker, S ^a   Hore, P J ^b   Mok, K H ^c   Van Gunsteren, W F ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Denaturation; GROMOS; MD; TRP cage; Urea

Indexed keywords

PROTEIN; PROTEIN TC5B; SOLVENT; UNCLASSIFIED DRUG; UREA;

ACCELERATION; AQUEOUS SOLUTION; ARTICLE; CALIBRATION; CONTROLLED STUDY; DENATURATION; DENSITY; ENERGY; MOLECULAR DYNAMICS; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; REPRODUCTION; SIMULATION; TEMPERATURE; TETRATRICOPEPTIDE REPEAT; THERMODYNAMICS;

PEPTIDES; PROTEIN CONFORMATION; PROTEIN DENATURATION; RECOMBINANT PROTEINS; TEMPERATURE; THERMODYNAMICS; UREA;

EID: 70349449895     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.223     Document Type: Article

References (45)

1. Moult J, Fidelis K, Zemla A, Hubbard T. (2001) Critical assessment of methods of protein structure prediction (CASP): round IV. Proteins 45:2-7. (Pubitemid 34113162)
2. Moult J, Fidelis K, Kryshtafovych A, Rost B, Hubbard T, Tramontano A. (2007) Critical assessment of methods of protein structure prediction-round VII. Proteins 69:3-9. (Pubitemid 350210108)
3. Ulmschneider JP, Jorgensen WL. (2004) Polypeptide folding using Monte Carlo sampling, concerted rotation and continuum solvation. J Am Chem Soc 126:1849-1857.
4. Shakhnovich E. (2006) Protein folding thermodynamics and dynamics: where physics, chemistry and biology meet. Chem Rev 106:1559-1588.
5. van Gunsteren WF, Bürgi R, Peter C, Daura X. (2001) The key to solving the protein-folding problem lies in an accurate description of the denatured state. Angew Chem Int Ed 40:351-355. (Pubitemid 32114874)
6. van Gunsteren WF, Gattin Z. Simulation of folding equilibria. In: Hecht S, Huc I. Eds. (2007) Foldamers: structure, properties and applications. Weinheim, Germany: Wiley, pp 173-192.
7. Neidigh JW, Fesinmeyer RM, Andersen NH. (2002) Designing a 20-residue protein. Nat Struct Biol 9:425-430.
8. Iavarone AT, Parks JH. (2005) Conformational change in unsolvated Trp-cage protein probed by fluorescence. J Am Chem Soc 127:8606-8607.
9. Ahmed Z, Beta IA, Mikhonin AV, Asher SA. (2005) UV-resonance Raman thermal unfolding study of Trp-cage shows that it is not a simple two-state miniprotein. J Am Chem Soc 127:10943-10950. (Pubitemid 41129869)
10. Neuweiler H, Doose S, Sauer M (2005) A microscopic view of miniprotein folding: enhanced folding efficiency through formation of an intermediate. Proc Natl Acad Sci USA 102:16650-16655. (Pubitemid 41688831)
11. Qiu L, Pabit SA, Roitberg AE, Hagen SJ. (2002) Smaller and faster: the 20-residue Trp-cage protein folds in 4 ls. J Am Chem Soc 124:12952-12953. (Pubitemid 35247099)
12. Qiu L, Hagen SJ. (2004) A limiting speed for protein folding at low solvent viscosity. J Am Chem Soc 126:3398-3399. (Pubitemid 38366711)
13. Simmerling C, Strockbine B, Roitberg AE. (2002) Allatom structure prediction and folding simulations of a stable protein. J Am Chem Soc 124:11258-11259.
14. Snow CD, Zagrovic B, Pande VS. (2002) The Trp-cage: folding kinetics and unfolded state topology via molecular dynamics simulations. J Am Chem Soc 124:14548-14549. (Pubitemid 35425023)
15. Pitera JW, Swope W. (2003) Understanding folding and design: replica exchange simulations of Trp-cage miniproteins. Proc Natl Acad Sci USA 100:7587-7592.
16. Rao F, Caflisch A. (2003) Replica exchange molecular dynamics simulations of reversible folding. J Chem Phys 119:4035-4042.
17. Zhou R. (2003) Trp-cage: folding free energy landscape in explicit water. Proc Natl Acad Sci USA 100:13280-13285.
18. Chowdhury S, Lee MC, Xiong G, Duan Y. (2003) Ab initio folding simulation of the Trp-cage mini-protein approaches NMR resolution. J Mol Biol 327:711-717. (Pubitemid 36300811)
19. Nikiforovich GV, Andersen NH, Fesinmeyer RM, Frieden C. (2003) Possible locally driven folding pathways of TC5b, a 20-residue protein. Proteins 52:292-302.
20. Chowdhury S, Lee MC, Duan Y. (2004) Characterizing the rate-limiting step of Trp-cage folding by all-atom molecular dynamics simulations. J Phys Chem B 108:13855-13865.
21. Paschek D, Nymeyer H, Garca AE. (2007) Replica exchange simulation of reversible folding/unfolding of the Trp-cage miniprotein in explicit solvent: on the structure and possible role of internal water. J Struct Biol 157:524-533. (Pubitemid 46321518)
22. Daura X, Mark AE, van Gunsteren WF. (1998) Parametrization of aliphatic CHn united atoms of GROMOS96 force field. J Comput Chem 19:535-547. (Pubitemid 128562874)
23. Schuler LD, Daura X, van Gunsteren WF. (2001) An improved GROMOS96 force field for aliphatic hydrocarbons in the condense phase. J Comput Chem 22:1205-1218.
24. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF. (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS forcefield parameter sets 53A5 and 53A6. J Comput Chem 25:1656-1676.
25. Mok KH, Kuhn LT, Goez M, Day IJ, Lin JC, Andersen NH, Hore PJ. (2007) A pre-existing hydrophobic collapse in the unfolded state of an ultrafast folding protein. Nature 447:106-109. (Pubitemid 46685836)
26. van Gunsteren WF, Dolenc J, Mark AE. (2008) Molecular simulation as an aid to experimentalists. Curr Opin Struct Biol 18:149-153.
27. Brünger AT, Adams PD, Clore GM, DeLano WL, Gros P, Grosse-Kunstleve RW, Jiang J-S, Kuszewski J, Nilges M, Pannu NS, Read RJ, Rice LM, Simonson T, Warren GL. (1998) Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Cryst D 54:905-921. (Pubitemid 28443603)
28. Neidigh JW, Fesinmeyer RM, Prickett KS, Andersen NH. (2001) Exendin-4 and glucagon-like-peptide-1: NMR structural comparisons in the solution and micelle-associated states. Biochemistry 40:13188-13200.
29. Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc 117:5179-5197.
30. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N, Dothager RS, Seifert S, Thiyagarajan P, Sosnick TR, Zahid Hasan M, Pande VS, Ruczinski I, Doniach S, Plaxco KW. (2003) Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci USA 101:12491-12496. (Pubitemid 39122051)
31. Caballero-Herrera A, Nordstrand K, Berndt KD, Nilsson L. (2005) Effect of urea on peptide conformation in water: molecular dynamics and experimental characterization. Biophys J 89:842-857. (Pubitemid 41098971)
32. Christen M, Hünenberger PH, Bakowies D, Baron R, Bürgi R, Geerke DP, Heinz TN, Kastenholz MA, Kräutler V, Oostenbrink C, Peter C, Trzesniak D, van Gunsteren WF. (2005) The GROMOS software for biomolecular simulation: GROMOS05. J Comput Chem 26:1719-1751. (Pubitemid 43076183)
33. van Gunsteren WF, Billeter SR, Eising AA, Hünenberger PH, Krüger P, Mark AE, Scott WRP, Tironi IG. (1996) Biomolecular simulation: the GROMOS96 manual and user guide. Zürich, Verlag der Fachvereine.
34. Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J. Interaction models for water in relation to protein hydration. In: Pullman B, Ed. (1981) Intermolecular forces. Dordrecht: Reidel, pp 331-342.
35. Smith LJ, Berendsen HJC, van Gunsteren WF. (2004) Computer simulation of urea-water mixtures: a test of force field parameters for use in biomolecular simulation. J Phys Chem B 108:1065-1071.
36. Berendsen HJC, Postma JPM, van Gunsteren WF, DiNola A, Haak JR. (1984) Molecular dynamics with coupling to an external bath. J Chem Phys 81:3684-3690.
37. Ryckaert JP, Ciccotti G, Berendsen HJC. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23:327-341.
38. Scott WRP, Hünenberger P, Tironi IG, Mark AE, Billeter SR, Fennen J, Torda AE, Huber T, Krüger p, van Gunsteren WF. (1999) The GROMOS biomolecular simulation program package. J Phys Chem A 103:3596-3607.
39. Barker JA, Watts RO. (1973) Monte Carlo studies of the dielectric properties of water-like models. Mol Phys 26:789-792.
40. Tironi IG, Sperb R, Smith PE, van Gunsteren WF. (1995) A generalized reaction field method for molecular dynamics simulations. J Chem Phys 102:5451-5459.
41. Heinz TN, van Gunsteren WF, Hünenberger PH. (2001) Comparison of four methods to compute the dielectric permittivity of liquids from molecular dynamics simulations. J Chem Phys 115:1125-1136.
42. Kabsch W, Sander C. (1983) Dictionary of protein secondary structure-pattern-recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
43. Tropp J. (1980) Dipolar relaxation and nuclear Overhauser effects in nonrigid molecules: the effect of fluctuating internuclear distances. J Chem Phys 72:6035-6043.
44. Daura X, Antes I, van Gunsteren WF, Thiel W, Mark AE. (1999) The effect of motional averaging on the calculation of NMR-derived structural properties. Proteins 36:542-555. (Pubitemid 29387752)
45. Daura X, van Gunsteren WF, Mark AE. (1999) Folding-unfolding thermodynamics of a β-heptapeptide from equilibrium simulations. Proteins 34:269-280. (Pubitemid 29071670)