Enhanced Sampling of Coarse-Grained Transmembrane-Peptide Structure Formation from Hydrogen-Bond Replica Exchange

Journal of Membrane Biology

Volumn 248, Issue 3, 2015, Pages 395-405

  Bereau, Tristan ^a   Deserno, Markus ^b  

^a MAX PLANCK INSTITUTE FOR POLYMER RESEARCH   (Germany)

^b CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Coarse grained; Folding; Membrane peptide; Simulations; WALP

Indexed keywords

COAT PROTEIN; MEMBRANE PROTEIN; TRANSMEMBRANE PEPTIDE; UNCLASSIFIED DRUG; 1-PALMITOYL-2-OLEOYLPHOSPHATIDYLCHOLINE; PHOSPHATIDYLCHOLINE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIOPHAGE; BILAYER MEMBRANE; COMPUTER SIMULATION; HYDROGEN BOND; MEMBRANE MODEL; MOLECULAR DYNAMICS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SAMPLING; CHEMISTRY; MOLECULAR GENETICS; THERMODYNAMICS;

AMINO ACID SEQUENCE; HYDROGEN BONDING; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; PHOSPHATIDYLCHOLINES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

EID: 84933672419     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-014-9738-9     Document Type: Article

References (66)

1. Affentranger R, Tavernelli I, Di Iorio EE (2006) A novel hamiltonian replica exchange md protocol to enhance protein conformational space sampling. J Chem Theory Comput 2(2):217–228
2. Almeida F, Opella S (1997) fd coat protein structure in membrane environments: structural dynamics of the loop between the hydrophobic trans-membrane helix and the amphipathic in-plane helix. J Mol Biol 270(3):481–495
3. Anglin TC, Brown KL, Conboy JC (2009) Phospholipid flip-flop modulated by transmembrane peptides WALP and Melittin. J Struct Biol 168(1):37–52
4. Baaden M, Marrink SJ (2013) Coarse-grain modelling of protein–protein interactions. Curr Opin Struct Biol 23(6):878–886
5. Bereau T (2011) Unconstrained structure formation in coarse-grained protein simulations. Ph.D. thesis, Carnegie Mellon University
6. Bereau T, Bachmann M, Deserno M (2010) Interplay between secondary and tertiary structure formation in protein folding cooperativity. J Am Chem Soc 132(38):13,129–13,131
7. Bereau T, Deserno M (2009) Generic coarse-grained model for protein folding and aggregation. J Chem Phys 130(23):235,106
8. Bereau T, Deserno M, Bachmann M (2011) Structural basis of folding cooperativity in model proteins: insights from a microcanonical perspective. Biophys J 100(11):2764–2772
9. Bereau T, Globisch C, Deserno M, Peter C (2012) Coarse-grained and atomistic simulations of the salt-stable cowpea chlorotic mottle virus (SS-CCMV) subunit 26–49: $$\beta $$β-barrel stability of the hexamer and pentamer geometries. J Chem Theory Comput 8(10):3750–3758
10. Bereau T, Wang ZJ, Deserno M (2014) More than the sum of its parts: coarse-grained peptide–lipid interactions from a simple cross-parametrization. J Chem Phys 140(11):115,101
11. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977) The protein data bank. Eur J Biochem 80(2):319–324
12. Bunker A, Dünweg B (2000) Parallel excluded volume tempering for polymer melts. Phys Rev E 63(1):016,701
13. Caffrey M (2003) Membrane protein crystallization. J Struct Biol 142(1):108–132
14. DeLucas L (2009) Membrane protein crystallization, vol 63. Academic Press, San Diego
15. de Planque MR, Greathouse DV, Koeppe RE, Schäfer H, Marsh D, Killian JA (1998) Influence of lipid/peptide hydrophobic mismatch on the thickness of diacylphosphatidylcholine bilayers. a 2H NMR and ESR study using designed transmembrane $$\alpha $$α-helical peptides and gramicidin A. Biochemistry 37(26):9333–9345
16. Fattal DR, Ben-Shaul A (1993) A molecular model for lipid–protein interaction in membranes: the role of hydrophobic mismatch. Biophys J 65(5):1795
17. Filipe HA, Moreno MJ, Róg T, Vattulainen I, Loura LM (2014) How to tackle the issues in free energy simulations of long amphiphiles interacting with lipid membranes: convergence and local membrane deformations. J Phys Chem B 118(13):3572–3581
18. Freddolino PL, Harrison CB, Liu Y, Schulten K (2010) Challenges in protein-folding simulations. Nature Phys 6(10):751–758
19. Freddolino PL, Park S, Roux B, Schulten K (2009) Force field bias in protein folding simulations. Biophys J 96(9):3772–3780
20. Frishman D, Argos P (1995) Knowledge-based protein secondary structure assignment. Proteins: Struct Funct Bioinf 23(4):566–579
21. Gapsys V, Seeliger D, de Groot BL (2012) New soft-core potential function for molecular dynamics based alchemical free energy calculations. J Chem Theory Comput 8(7):2373–2382
22. Globisch C, Krishnamani V, Deserno M, Peter C (2013) Optimization of an elastic network augmented coarse grained model to study CCMV capsid deformation. PLoS One 8(4):e60,582
23. Grossfield A, Feller SE, Pitman MC (2007) Convergence of molecular dynamics simulations of membrane proteins. Proteins: Struct Funct Bioinf 67(1):31–40
24. Holt A, Rougier L, Réat V, Jolibois F, Saurel O, Czaplicki J, Killian JA, Milon A (2010) Order parameters of a transmembrane helix in a fluid bilayer: case study of a walp peptide. Biophys J 98(9):1864–1872
25. 3 peptide. Biophys J 107(4):991–997
26. Humphrey W, Dalke A, Schulten K (1996) VMD: visual molecular dynamics. J Mol Graph 14(1):33–38
27. Im W, Brooks CL (2005) Interfacial folding and membrane insertion of designed peptides studied by molecular dynamics simulations. Proc Natl Acad Sci USA 102(19):6771–6776
28. Im W, Brooks CL III (2004) De novo folding of membrane proteins: an exploration of the structure and NMR properties of the fd coat protein. J Mol Biol 337(3):513–519
29. Ingólfsson HI, Lopez CA, Uusitalo JJ, de Jong DH, Gopal SM, Periole X, Marrink SJ (2014) The power of coarse graining in biomolecular simulations. Wiley Interdiscip Rev 4(3):225–248
30. Jiang W, Roux B (2010) Free energy perturbation hamiltonian replica-exchange molecular dynamics (FEP/H-REMD) for absolute ligand binding free energy calculations. J Chem Theory Comput 6(9):2559–2565
31. Kar P, Feig M (2014) Recent advances in transferable coarse-grained modeling of proteins. Adv Protein Chem Struct Biol
32. Kar P, Gopal SM, Cheng YM, Panahi A, Feig M (2014) Transferring the primo coarse-grained force field to the membrane environment: simulations of membrane proteins and helix–helix association. J Chem Theory Comput 10(8):3459–3472
33. Killian JA (2003) Synthetic peptides as models for intrinsic membrane proteins. FEBS Lett 555(1):134–138
34. Kim T, Im W (2010) Revisiting hydrophobic mismatch with free energy simulation studies of transmembrane helix tilt and rotation. Biophys J 99(1):175–183
35. Kolb A, Dünweg B (1999) Optimized constant pressure stochastic dynamics. J Chem Phys 111(10):4453–4459
36. Limbach HJ, Arnold A, Mann BA, Holm C (2006) Espresso: an extensible simulation package for research on soft matter systems. Comput Phys Commun 174(9):704–727
37. Liu P, Huang X, Zhou R, Berne B (2006) Hydrophobic aided replica exchange: an efficient algorithm for protein folding in explicit solvent. J Phys Chem B 110(38):19,018–19,022
38. Liu P, Kim B, Friesner RA, Berne B (2005) Replica exchange with solute tempering: a method for sampling biological systems in explicit water. Proc Natl Acad Sci USA 102(39):13,749–13,754
39. Lundbæk JA, Collingwood SA, Ingólfsson HI, Kapoor R, Andersen OS (2010) Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes. J R Soc Interface 7(44):373–395
40. Lyman E, Ytreberg FM, Zuckerman DM (2006) Resolution exchange simulation. Phys Rev Lett 96(2):028,105
41. MacCallum JL, Bennett W, Tieleman DP (2008) Distribution of amino acids in a lipid bilayer from computer simulations. Biophys J 94(9):3393–3404
42. Marassi FM, Opella SJ (2003) Simultaneous assignment and structure determination of a membrane protein from NMR orientational restraints. Protein Sci 12(3):403–411
43. Monticelli L, Kandasamy SK, Periole X, Larson RG, Tieleman DP, Marrink SJ (2008) The martini coarse-grained force field: extension to proteins. J Chem Theory Comput 4(5):819–834
44. Monticelli L, Tieleman DP, Fuchs PF (2010) Interpretation of $$^2$$2H-NMR experiments on the orientation of the transmembrane helix walp23 by computer simulations. Biophys J 99(5):1455–1464
45. Mori T, Jung J, Sugita Y (2013) Surface-tension replica-exchange molecular dynamics method for enhanced sampling of biological membrane systems. J Chem Theory Comput 9(12):5629–5640
46. Mouritsen OG, Bloom M (1984) Mattress model of lipid–protein interactions in membranes. Biophys J 46(2):141–153
47. Mu Y (2009) Dissociation aided and side chain sampling enhanced hamiltonian replica exchange. J Chem Phys 130(16):164,107
48. Neale C, Bennett WD, Tieleman DP, Pomès R (2011) Statistical convergence of equilibrium properties in simulations of molecular solutes embedded in lipid bilayers. J Chem Theory Comput 7(12):4175–4188
49. Neale C, Madill C, Rauscher S, Pomès R (2013) Accelerating convergence in molecular dynamics simulations of solutes in lipid membranes by conducting a random walk along the bilayer normal. J Chem Theory Comput 9(8):3686–3703
50. Noid W (2013) Perspective: coarse-grained models for biomolecular systems. J Chem Phys 139(9):090,901
51. Nymeyer H, Woolf TB, Garcia AE (2005) Folding is not required for bilayer insertion: replica exchange simulations of an $$\alpha $$α-helical peptide with an explicit lipid bilayer. Proteins Struct Funct Bioinf 59(4):783–790
52. Okabe T, Kawata M, Okamoto Y, Mikami M (2001) Replica-exchange Monte Carlo method for the isobaric–isothermal ensemble. Chem Phys Lett 335(5):435–439
53. Paloncýová M, Berka K, Otyepka M (2012) Convergence of free energy profile of coumarin in lipid bilayer. J Chem Theory Comput 8(4):1200–1211
54. Paschek D, García AE (2004) Reversible temperature and pressure denaturation of a protein fragment: a replica exchange molecular dynamics simulation study. Phys Rev Lett 93(23):238,105
55. Periole X, Cavalli M, Marrink SJ, Ceruso M (2009) Combining an elastic network with a coarse-grained molecular force field: structure, dynamics and intermolecular recognition. J Chem Theory Comput 5:2531–2543
56. Piana S, Lindorff-Larsen K, Shaw DE (2011) How robust are protein folding simulations with respect to force field parameterization? Biophys J 100(9):L47–L49
57. Sugita Y, Okamoto Y (1999) Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 314(1):141–151
58. Swendsen RH, Wang JS (1986) Replica Monte Carlo simulation of spin glasses. Phys Rev Lett 57(21):2607–2609
59. Ulmschneider JP, Doux JP, Killian JA, Smith JC, Ulmschneider MB (2009) Peptide partitioning and folding into lipid bilayers. J Chem Theory Comput 5(9):2202–2205
60. Ulmschneider MB, Doux JP, Killian JA, Smith JC, Ulmschneider JP (2010) Mechanism and kinetics of peptide partitioning into membranes from all-atom simulations of thermostable peptides. J Am Chem Soc 132(10):3452–3460
61. Ulmschneider MB, Ulmschneider JP (2008) Folding peptides into lipid bilayer membranes. J Chem Theory Comput 4(11):1807–1809
62. Venturoli M, Smit B, Sperotto MM (2005) Simulation studies of protein-induced bilayer deformations, and lipid-induced protein tilting, on a mesoscopic model for lipid bilayers with embedded proteins. Biophys J 88(3):1778–1798
63. von Heijne G (2011) Introduction to theme membrane protein folding and insertion. Annu Rev Biochem 80:157–160
64. Wan CK, Han W, Wu YD (2011) Parameterization of pace force field for membrane environment and simulation of helical peptides and helix–helix association. J Chem Theory Comput 8(1):300–313
65. Wang ZJ, Deserno M (2010) Systematic implicit solvent coarse-graining of bilayer membranes: lipid and phase transferability of the force field. New J Phys 12(9):095,004
66. Wang ZJ, Deserno M (2010) A systematically coarse-grained solvent-free model for quantitative phospholipid bilayer simulations. J Phys Chem B 114(34):11,207–11,220