Folding is not required for bilayer insertion: Replica exchange simulations of an α-helical peptide with an explicit lipid bilayer

Proteins: Structure, Function and Genetics

Volumn 59, Issue 4, 2005, Pages 783-790

  Nymeyer, Hugh ^a   Woolf, Thomas B ^b   Garcia, Angel E ^a  

^a LOS ALAMOS NATIONAL LABORATORY   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Four stage model; Replica exchange molecular dynamics; WALP

Indexed keywords

DIPALMITOYLPHOSPHATIDYLCHOLINE; PEPTIDE; PEPTIDE WALP 16; UNCLASSIFIED DRUG; WATER;

ALGORITHM; ALPHA HELIX; ARTICLE; ENERGY; ENTHALPY; ENTROPY; LIPID BILAYER; MOLECULAR DYNAMICS; MOLECULAR MODEL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; SIMULATION;

1,2-DIPALMITOYLPHOSPHATIDYLCHOLINE; LIPID BILAYERS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; PEPTIDES; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS;

EID: 18844362955     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20460     Document Type: Article

References (66)

1. Popot JL, Engelman, DM. Membrane-protein folding and oligomerization: the 2-stage model. Biochemistry 1990;29:4031-4037.
2. Jacobs RE, White SH. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helices. Biochemistry 1989;28:3421-3437.
3. White SH, Wimley WC. Membrane protein folding and stability: physical principles. Annu Rev Biophys Biomol Struct 1999;28:319-365.
4. Boyd D, Schierle C, Beckwith J. How many membrane proteins are there? Protein Sci 1998;7:201-205.
5. Wallin E, Von Heijne G. Genome-wide analysis of integral membrane proteins from eubacterial, archaean, and eukaryotic organisms. Protein Sci 1998;7:1029-1038.
6. Wimley WC. Toward genomic identification of β-barrel membrane proteins: compositions and architecture of known structure. Protein Sci 2002;11:301-312.
7. Landoltmarticorena C, Williams KA, Deber CM, Reithmeier RAF. Nonrandom distribution of amino acids in the transmembrane segments of human type-I single span membrane-proteins. J Mol Biol 1993;229:602-608.
8. White S. Membrane proteins of known 3D structure, http://blanco.biomol. uci.edu/Membrane_Proteins_xtal.html. Accessed 2004 May 10.
9. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, et al. The Protein Data Bank. Nucleic Acids Res 2000;28:235-242 (see also http://www.rcsb.org/pdb).
10. Popot JL, Engelman DM. Helical membrane protein folding, stability, and evolution. Annu Rev Biochem 2000;69:881-922.
11. Killian JA, et al. Induction of nonbilayer structure in diacylphosphatidylcholine model membranes by transmembrane α-helical peptides: importance of hydrophobic mismatch and proposed role of tryptophans. Biochemistry 1996;35:1037-1045.
12. Killian JA. Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta Rev Biomembr 1998;1376:401-416.
13. De Planque MRR, Killian JA. Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring (review). Mol Membr Biol 2003;20: 271-284.
14. de Planque MRR, et al. Sensitivity of single membrane-spanning α-helical peptides to hydrophobic mismatch with a lipid bilayer: effects on backbone structure, orientation, and extent of membrane incorporation. Biochemistry 2001;40:5000-5010.
15. 2H NMR. Biophys J 2002;83:1479-1488.
16. Rinia HA, et al. Visualization of highly ordered striated domains induced by transmembrane peptides in supported phosphatidylcholine bilayers. Biochemistry 200;39:5852-5858.
17. Rinia HA, et al. Domain formation in phosphatidylcholine bilayers containing transmembrane peptides: specific effects of flanking residues. Biochemistry 2002;41:2814-2824.
18. Demmers JAA, et al. Electrospray ionization Mass Spectrometry as a tool to analyze hydrogen/deuterium exchange kinetics of transmembrane peptides in lipid bilayers. Proc Natl Acad Sci USA 2000;97:3189-3194.
19. Demmers JAA, et al. Interfacial positioning and stability of transmembrane peptides in lipid bilayers studied by combining hydrogen/deuterium exchange and mass spectrometry. J Biol Chem 2001;276:34501-34508.
20. de Planque MRR, et al. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 2003;42:5341-5348.
21. 2H NMR and ESR study using designed transmembrane α-helical peptides and gramicidin A. Biochemistry 1998;37:9333-9345.
22. de Planque MRR, et al. Different membrane anchoring positions of tryptophan and lysine in synthetic transmembrane α-helical peptides. J Biol Chem 1999;274:20839-20846.
23. Morein S, et al. The effect of peptide/lipid hydrophobic mismatch on the phase behavior of model membranes mimicking the lipid composition in Escherichia coli membranes. Biophys J 2000;78: 2475-2485.
24. de Planque MRR, et al. The effects of hydrophobic mismatch between phosphatidycholine bilayers and transmembrane α-helical peptides depend on the nature of interfacially exposed aromatic and charged residues. Biochemistry 2002;41:8396-8404.
25. Morein S, Killian JA, Sperotto MM. Characterization of the thermotropic behavior and lateral organization of lipid-peptide mixtures by a combined experimental and theoretical approach: effects of hydrophobic mismatch and role of flanking residues. Biophys J 2002;82:1405-1417.
26. Morein S, et al. Influence of membrane-spanning α-helical peptides on the phase behavior of the dioleoylphosphatidylcholine/water system. Biophys J 1997;73:3078-3088.
27. Weiss TM, et al. Hydrophobic mismatch between helices and lipid bilayers. Biophys J 2003;84:379-385.
28. Petrache HI, Zuckerman DM, Sachs JN, Killian JA, Koeppe RE, Woolf TB. Hydrophobic matching mechanism investigated by molecular dynamics simulations. Langmuir 2002;18:1340-1351.
29. Hunt JF, Rath P, Rothschild KJ, Engelman DM. Spontaneous, pH-dependent membrane insertion of a transbilayer α-helix. Biochemistry 1997;36:15177-15192.
30. Meijbert W, Booth PJ. The activation energy for insertion of transmembrane α-helices is dependent on membrane composition. J Mol Biol 2002;319:839-853.
31. Yano Y, Matsuzaki K. Membrane insertion and dissociation processes of a model transmembrane helix. Biochemistry 2002;41: 12407-12413.
32. Dongarra JJ, Meuer HW, Strohmaier E. TOP500 supercomputer sites. Supercomputer 1997;13:89-120 (see also http://www.top500.org).
33. Sugita Y, Okamoto Y. Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 1999;314:141-151.
34. Swendsen R, Wang J. Replica Monte Carlo simulation of spin-glasses. Phys Rev Lett 1986;57:2607-2609.
35. Marinari E, Parisi G. Simulated tempering-a new Monte-Carlo scheme. Europhys Lett 1992;19:451-458.
36. Geyer C, Thompson E. Annealing Markov-chain Monte-Carlo with applications to ancestral inference. J Am Stat Assoc 1995;90:909-920.
37. Hukushima K, Nemoto K. Exchange Monte-Carlo simulations and application to spin glass simulations. J Phys Soc Jpn 1996;65:1604-1608.
38. Hansmann, U. Parallel tempering algorithm for conformational studies of biological molecules. Chem Phys Lett 1997;281:140-150.
39. Garcia AE, Sanbonmatsu KY. Exploring the energy landscape of a β hairpin in explicit solvent. Protein Struct Funct Genet 2001;42: 345-354.
40. Sanbonmatsu KY, Garcia AE. Structure of met-enkephalin in explicit aqueous solutions using replica exchange molecular dynamics. Protein Struct Funct Genet 2002;46:225-234.
41. Nymeyer H, Gnanakaran S, Garcia AE. Atomic simulations of protein folding, using the replica exchange algorithm. Methods Enzymol 2004;383:119-149.
42. Garcia AE, Sanbonmatsu KY. Alpha-helical stabilization by side chain shielding of hydrogen bonds. Proc Natl Acad Sci USA 2002;99:2782-2787.
43. Yamamoto R, Kob W. Replica-exchange molecular dynamics simulation for supercooled liquids. Phys Rev E 2000;61:5473-5476.
44. Bedrow D, Smith GD. Exploration of conformational phase space in polymer melts: a comparison of parallel tempering and conventional molecular dynamics simulations. J Chem Phys 2001;115: 1121-1124.
45. Ben-Tal N, Sitkoff D, Topol IA, Yang A-S, et al. Free energy of amide hydrogen bond formation in vacuum, in water, and in liquid alkane solution. J Phys Chem B 1997;101:450-457.
46. Roseman MA. Hydrophobicity of the peptide C=O ⋯ H-N hydrogen-bonded group. J Mol Biol 1998;201:621-623.
47. Wimley WC, Creamer TP, White SH. Solvation energies of amino acid side chains and backbone in a family of host-guest pentapeptides. Biochemistry 1996;35:5109-5124.
48. Ben-Tal N, Ben-Shaul A, Nicholls A, Honig B. Free-energy determinants of α-helix insertion into lipid bilayers. Biophys J 1996;70:1803-1812.
49. Russell CJ, Thorgeirsson TE, Shin Y-K. Temperature dependence of polypeptide partitioning between water and phospholipid bilayers. Biochemistry 1996;35:9526-9532.
50. Jain MK, Rogers J, Simpson L, Gierash LM. Effect of tryptophan derivatives on the phase properties of bilayers. Biochim Biophys Acta 1985;816:153-162.
51. Seelig J, Ganz P. Nonclassical hydrophobic effect in membrane binding equilibria. Biochemistry 1991;30:9354-9359.
52. Katzer M, Stillwell W. Partitioning of ABA into bilayers of di-saturated phosphatidylcholines as measured by DSC. Biophys J 2003;84:314-325.
53. Wimley WC, White SH. Membrane partitioning: distinguishing bilayer effects from the hydrophobic effect. Biochemistry 1993;32: 6307-6312.
54. DeVido DR, Dorsey JG, Chan HS, Dill KA. Oil/water partitioning has a different thermodynamic signature when the oil solvent chains are aligned than when they are amorphous. J Phys Chem B 1998;102:7272-7279.
55. Yau WM, Wimley WC, Gawrisch K, White SH. The preference of tryptophan for membrane interfaces. Biochemistry 1998;37:14713-14718.
56. Wimley WC, White SH. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nat Struct Biol 1996;3:842-848.
57. Wimley WC, Gawrisch K, Creamer TP, White SH. A direct measurement of salt-bridge solvation energies using a peptide model system: implications for protein stability. Proc Natl Acad Sci USA 1996;93:2985-2990.
58. Ladokhin AS, Legmann R, Collier RJ, White SH. Reversible refolding of the diphtheria toxin T-domain on lipid membranes. Biochemistry 2004;43:7451-7458.
59. Ladokhin AS, White SH. Interfacial folding and membrane insertion of a designed helical peptide. Biochemistry 2004;43:5782-5791.
60. Dill KA, Chan HS. From Levinthal to pathways to funnels. Nat Struct Biol 1997;4:10-19.
61. Onuchic JN, Nymeyer H, Garcia AE, Chahine J, Socci ND. The energy landscape theory of protein folding: insights into folding mechanisms and scenarios. Adv Protein Chem 2000;53:87-152.
62. Nagle JF, Tristram-Nagle S. Structure of lipid bilayers. Biochim Biophys Acta Rev Biomembr 2000;1469:159-195.
63. Brooks BR, et al. CHARMM: a program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem 1983;4:187-217.
64. Schlenkrish M, Brickmann J, MacKerell AD Jr, Karplus M. Empirical potential energy function for phospholipids: criteria for parameter optimizaton and applications. In: Merz KM, Roux B, editors. Biological membranes: a molecular perspective from computation and experiment. Boston: Birkhaüser; 1996. p 31-81.
65. Feller SE, Yin D, Pastor RW, MacKerell AD Jr. Molecular dynamics simulation of unsaturated lipid bilayers at low hydration: parameterization and comparison with diffraction studies. Biophys J 1997;73:2269-2279.
66. Feller SE, Pastor RW. Constant surface tension simulations of lipid bilayers: the sensitivity of surface areas and compressibilities. J Chem Phys 1999;111:1281-1287.