Environmental effects on glycophorin a folding and structure examined through molecular simulations

Journal of Chemical Theory and Computation

Volumn 1, Issue 3, 2005, Pages 375-388

  Nanda, Hirsh ^a   Sachs, Jonathan N ^c   Petrache, Horia I ^b   Woolf, Thomas B ^a  

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

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 33644841042     PISSN: 15499618     EISSN: 15499626     Source Type: Journal    
DOI: 10.1021/ct049928y     Document Type: Article

References (77)

1. Popot, J. L.; Engelman, D. M. Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem. 2000, 69, 881-922.
2. White, S. H.; Wimley, W. C. Membrane protein folding and stability: Physical principles. Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 319-365.
3. Russ, W. P.; Engelman, D. M. The GxxxG motif: A framework for transmembrane helix-helix association. J. Mol. Biol. 2000, 296(3), 911-919.
4. Senes, A.; Gerstein, M.; Engelman, D. M. Statistical analysis of amino acid patterns in transmembrane helices: The GxxxG motif occurs frequently and in association with betabranched residues at neighboring positions. J. Mol. Biol. 2000, 296(3), 921-936.
5. Ubarretxena-Belandia, I.; Engelman, D. M. Helical membrane proteins: diversity of functions in the context of simple architecture. Curr. Opin. Struct. Biol. 2001, 11(3), 370-376.
6. Curran, A. R.; Engelman, D. M. Sequence motifs, polar interactions and conformational changes in helical membrane proteins. Curr. Opin. Struct. Biol. 2003, 13(4), 412-417.
7. Jayasinghe, S.; Hristova, K.; White, S. H. Energetics, stability, and prediction of transmembrane helices. J. Mol. Biol. 2001, 312(5), 927-934.
8. Krogh, A.; Larsson, B.; von Heijne, G.; Sonnhammer, E. L. L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 2001, 305(3), 567-580.
9. Melen, K.; Krogh, A.; von Heijne, G. Reliability measures for membrane protein topology prediction algorithms. J. Mol. Biol. 2003, 327(3), 735-744.
10. Gouaux, E.; White, S. H. Membranes - Lipids lost, lipids regained - Editorial overview. Curr. Opin. Struct. Biol. 2001, 11(4), 393-396.
11. Gouaux, E.; White, S. H. Membranes - Proteins and membranes - a fusion of new ideas - Editorial overview. Curr. Opin. Struct. Biol. 2003, 13(4), 401-403.
12. Fleming, K. G.; Ackerman, A. L.; Engelman, D. M. The effect of point mutations on the free energy of transmembrane alpha-helix dimerization. J. Mol. Biol. 1997, 272(2), 266-275.
13. Liu, W.; Crocker, E.; Siminovitch, D. J.; Smith, S. O. Role of side-chain conformational entropy in transmembrane helix dimerization of glycophorin A. Biophys. J. 2003, 84(2), 1263-1271.
14. Fisher, L. E.; Engelman, D. M.; Sturgis, J. N. Effect of detergents on the association of the glycophorin A transmembrane helix. Biophys. J. 2003, 85(5), 3097-3105.
15. Lemmon, M. A.; Flanagan, J. M.; Hunt, J. F.; Adair, B. D.; Bormann, B. J.; Dempsey, C. E.; Engelman, D. M. Glycophorin-a Dimerization Is Driven by Specific Interactions between Transmembrane Alpha-Helices. J. Biol. Chem. 1992, 267(11), 7683-7689.
16. Lemmon, M. A.; Flanagan, J. M.; Treutlein, H. R.; Zhang, J.; Engelman, D. M. Sequence Specificity in the Dimerization of Transmembrane Alpha-Helices. Biochemistry-Us 1992, 31(51), 12719-12725.
17. Treutlein, H. R.; Lemmon, M. A.; Engelman, D. M.; Brunger, A. T. The Glycophorin-a Transmembrane Domain Dimer - Sequence-Specific Propensity for a Right-Hanqded Supercoil of Helices. Biochemistry-Us 1992, 31(51), 12726-12733.
18. MacKenzie, K. R.; Prestegard, J. H.; Engelman, D. M. A transmembrane helix dimer: Structure and implications. Science 1997, 276(5309), 131-133.
19. Smith, S. O.; Song, D.; Shekar, S.; Groesbeek, M.; Ziliox, M.; Aimoto, S. Structure of the transmembrane dimer interface of glycophorin A in membrane bilayers. Biochemistry-Us 2001, 40(22), 6553-6558.
20. Lemmon, M. A.; Engelman, D. M. Specificity and Promiscuity in Membrane Helix Interactions. Febs. Lett. 1994, 346(1), 17-20.
21. Adams, P. D.; Engelman, D. M.; Brunger, A. T. Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching. Proteins 1996, 26(3), 257-261.
22. Petrache, H. I.; Grossfield, A.; MacKenzie, K. R.; Engelman, D. M.; Woolf, T. B. Modulation of glycophorin A transmembrane helix interactions by lipid bilayers: Molecular dynamics calculations. J. Mol. Biol. 2000, 302(3), 727-746.
23. Bowie, J. U. Understanding membrane protein structure by design. Nat. Struct. Biol. 2000, 7(2), 91-94.
24. Choma, C.; Gratkowski, H.; Lear, J. D.; DeGrado, W. F. Asparagine-mediated self-association of a model transmembrane helix. Nat. Struct. Biol. 2000, 7(2), 161-166.
25. Zhou, F. X.; Cocco, M. J.; Russ, W. P.; Brunger, A. T.; Engelman, D. M. Interhelical hydrogen bonding drives strong interactions in membrane proteins. Nat. Struct. Biol. 2000, 7(2), 154-160.
26. Zhou, F. X.; Merianos, H. J.; Brunger, A. T.; Engelman, D. M. Polar residues drive association of polyleucine transmembrane helices. Proc. Natl. Acad. Sci. U. S. A. 2001, 98(5), 2250-2255.
27. Brown, M. F. Modulation of Rhodopsin Function by Properties of the Membrane Bilayer. Chem. Phys. Lipids 1994, 73 (1-2), 159-180.
28. Litman, B. J.; Mitchell, D. C. A role for phospholipid polyunsaturation in modulating membrane protein function. Lipids 1996, 31, S193-S197.
29. Bezrukov, S. M.; Rand, R. P.; Vodyanoy, I.; Parsegian, V. A. Lipid packing stress and polypeptide aggregation: alamethicin channel probed by proton titration of lipid charge. Faraday Discuss. 1998, 111, 173-183.
30. Greathouse, D. V.; Hinton, J. F.; Kim, K. S.; Koeppe, R. E. Gramicidin-a Short-Chain Phospholipid Dispersions - Chain-Length Dependence of Gramicidin Conformation and Lipid Organization. Biochemistry-Us 1994, 33(14), 4291-4299.
31. Koeppe, R. E.; Andersen, O. S. Engineering the gramicidin channel. Annu. Rev. Biophys. Biomol. Struct. 1996, 25, 231-258.
32. Fisher, L. E.; Engelman, D. M.; Sturgis, J. N. Detergents modulate dimerization but not helicity, of the glycophorin A transmembrane domain. J. Mol. Biol. 1999, 293(3), 639-651.
33. Wang, W.; Donini, O.; Reyes, C. M.; Kollman, P. A. Biomolecular simulations: Recent developments in force fields, simulations of enzyme catalysis, protein-ligand, protein-protein, and protein-nucleic acid noncovalent interactions. Annu. Rev. Biophys. Biomol. Struct. 2001, 30, 211-243.
34. Novotny, J.; Bruccoleri, R.; Karplus, M. An Analysis of Incorrectly Folded Protein Models - Implications for Structure Predictions. J. Mol. Biol. 1984, 177(4), 787-818.
35. Bond, P. J.; Sansom, M. S. P. Membrane protein dynamics versus environment: Simulations of OmpA in a micelle and in a bilayer. J. Mol. Biol. 2003, 329(5), 1035-1053.
36. Edholm, O.; Berger, O.; Jahnig, F. Structure and Fluctuations of Bacteriorhodopsin in the Purple Membrane - a Molecular-Dynamics Study. J. Mol. Biol. 1995, 250(1), 94-111.
37. Crozier, P. S.; Stevens, M. J.; Forrest, L. R.; Woolf, T. B. Molecular dynamics simulation of dark-adapted rhodopsin in an explicit membrane bilayer: Coupling between local retinal and larger scale conformational change. J. Mol. Biol. 2003, 333(3), 493-514.
38. Woolf, T. B.; Roux, B. Molecular-Dynamics Simulation of the Gramicidin Channel in a Phospholipid-Bilayer. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(24), 11631-11635.
39. Woolf, T. B.; Roux, B. Structure, energetics, and dynamics of lipid-protein interactions: A molecular dynamics study of the gramicidin A channel in a DMPC bilayer. Proteins 1996, 24(1), 92-114.
40. Woolf, T. B.; Roux, B. The binding site of sodium in the gramicidin A channel: Comparison of molecular dynamics with solid-state NMR data. Biophys. J. 1997, 72(5), 1930-1945.
41. Bond, P. J.; Faraldo-Gomez, J. D.; Sansom, M. S. P. OmpA: A pore or not a pore? Simulation and modeling studies. Biophys. J. 2002, 83(2), 763-775.
42. Domene, C.; Sansom, M. S. P. Potassium channel, ions, and water: Simulation studies based on the high-resolution X-ray structure of KcsA. Biophys. J. 2003, 85(5), 2787-2800.
43. Braun, R.; Engelman, D. M.; Schulten K. Molecular dynamics simulations of micelle formation around dimeric glycophorin A transmembrane helices. Biophys. J. 2004, 87(2), 754-763.
44. Popot, J. L.; Engelman, D. M. Membrane-Protein Folding and Oligomerization - the 2-Stage Model. Biochemistry-Us 1990, 29(17), 4031-4037.
45. Brooks, B. R.; Bruccoleri, R. E.; Olafson, B. D.; States, D. J.; Swaminathan, S.; Karplus, M. Charmm - a Program for Macromolecular Energy, Minimization, and Dynamics Calculations. J. Comput. Chem. 1983, 4(2), 187-217.
46. Petrache, H. I.; Tristram-Nagle, S.; Nagle, J. F. Fluid phase structure of EPC and DMPC bilayers. Chem. Phys. Lipids 1998, 95(1), 83-94.
47. Sagui, C.; Darden, T. A. Molecular dynamics simulations of biomolecules: Long-range electrostatic effects. Annu. Rev. Biophys. Biomol. Struct. 1999, 28, 155-179.
48. Feller, S. E.; Pastor, R. W. Constant surface tension simulations of lipid bilayers: The sensitivity of surface areas and compressibilities. J. Chem. Phys. 1999, 111(3), 1281-1287.
49. Vangunsteren, W. F.; Berendsen, H. J. C. Algorithms for Macromolecular Dynamics and Constraint Dynamics. Mol Phys. 1977, 34(5), 1311-1327.
50. Volke, F.; Eisenblatter, S.; Galle, J.; Klose G. Dynamic Properties of Water at Phosphatidylcholine Lipid-Bilayer Surfaces as Seen by Deuterium and Pulsed-Field Gradient Proton Nmr. Chem. Phys. Lipids 1994, 70(2), 121-131.
51. Aman, K.; Lindahl, E.; Edholm, O.; Hakansson, P.; Westlund, P. O. Structure and dynamics of interfacial water in an L-alpha phase lipid bilayer from molecular dynamics simulations. Biophys. J. 2003, 84(1), 102-115.
52. Halle, B.; Wennerstrom, H. Interpretation of Magnetic-Resonance Data from Water Nuclei in Heterogeneous Systems. J. Chem. Phys. 1981, 75(4), 1928-1943.
53. Arnold, K.; Pratsch, L.; Gawrisch K. Effect of Poly (Ethylene Glycol) on Phospholipid Hydration and Polarity of the External Phase. Biochim. Biophys. Acta 1983, 728(1), 121-128.
54. Pratt, L. R.; Pohorille, A. Hydrophobic effects and modeling of biophysical aqueous solution interfaces. Chem. Rev. 2002, 102(8), 2671-2691.
55. Gawrisch, K.; Ruston, D.; Zimmerberg, J.; Parsegian, V. A.; Rand, R. P.; Fuller, N. Membrane Dipole Potentials, Hydration Forces, and the Ordering of Water at Membrane Surfaces. Biophys. J. 1992, 61(5), 1213-1223.
56. Sidhu, K. S.; Goodfellow, J. M.; Turner, J. Z. Effect of molecular shape and electrostatic interactions on the water layer around polar and apolar groups in solution. J. Chem. Phys. 1999, 110(16), 7943-7950.
57. Creighton, T. E. Proteins: Structures and Molecular Properties; W. H. Freeman and Company: Heidelberg, 1996;507 p.
58. Wiener, M. C.; King, G. I.; White, S. H. Structure of a Fluid Dioleoylphosphatidylcholine Bilayer Determined by Joint Refinement of X-ray and Neutron-Diffraction Data. 1. Scaling of Neutron Data and the Distributions of Double-Bonds and Water. Biophys. J. 1991, 60(3), 568-576.
59. Wiener, M. C.; White, S. H. Structure of a Fluid Dioleoylphosphatidylcholine Bilayer Determined by Joint Refinement of X-ray and Neutron-Diffraction Data. 2. Distribution and Packing of Terminal Methyl-Groups. Biophys. J. 1992, 61(2), 428-433.
60. Wiener, M. C.; White, S. H. Structure of a Fluid Dioleoylphosphatidylcholine Bilayer Determined by Joint Refinement of X-ray and Neutron-Diffraction Data. 3. Complete Structure. Biophys. J. 1992, 61(2), 434-447.
61. Nagle, J. F.; Tristram-Nagle, S. Structure of lipid bilayers. BBA-Rev Biomembranes 2000, 1469(3), 159-195.
62. Nagle, J. F.; Tristram-Nagle, S. Lipid bilayer structure. Curr. Opin. Struct. Biol. 2000, 10(4), 474-480.
63. Fodje, M. N.; Al-Karadaghi, S. Occurrence, conformational features and amino acid propensities for the pi-helix. Protein Eng. 2002, 15(5), 353-358.
64. Chakrabartty, A.; Schellman, J. A.; Baldwin, R. L. Large Differences in the Helix Propensities of Alanine and Glycine. Nature 1991, 351(6327), 586-588.
65. Tieleman, D. P.; Sansom, M. S. P.; Berendsen, H. J. C. Alamethicin helices in a bilayer and in solution: Molecular dynamics simulations. Biophys. J. 1999, 76(1), 40-49.
66. Tieleman, D. P.; Woolley, G. A.; Sansom, M. S. P. Alamethicin as model system for ion selectivity: Computational studies. Biophys. J. 2000, 78(1), 174a-174a.
67. Korzhnev, D. M.; Orekhov, V. Y.; Arseniev, A. S.; Gratias, R.; Kessler, H. Mechanism of the unfolding of transmembrane alpha-helical segment (1-36)-bacteriorhodopsin studied by molecular dynamics simulations. J. Phys. Chem. B 1999, 103(33), 7036-7043.
68. Marqusee, S.; Robbins, V. H.; Baldwin, R. L. Unusually Stable Helix Formation in Short Alanine-Based Peptides. Proc. Natl. Acad. Sci. U. S. A. 1989, 86(14), 5286-5290.
69. Scholtz, J. M.; York, E. J.; Stewart, J. M.; Baldwin, R. L. A Neutral, Water-Soluble, Alpha-Helical Peptide - the Effect of Ionic-Strength on the Helix Coil Equilibrium. J. Am. Chem. Soc. 1991, 113(13), 5102-5104.
70. Vila, J. A.; Ripoll, D. R.; Scheraga, H. A. Physical reasons for the unusual alpha-helix stabilization afforded by charged or neutral polar residues in alanine-rich peptides. Proc. Natl. Acad. Sci. U. S. A. 2000, 97(24), 13075-13079.
71. Nilsson, I.; Johnson, A. E.; von Heijne, G. How hydrophobic is alanine? J. Biol. Chem. 2003, 278(32), 29389-29393.
72. Cheng, J. X.; Pautot, S.; Weitz, D. A.; Xie, X. S. Ordering of water molecules between phospholipid bilayers visualized by coherent anti-Stokes Raman scattering microscopy. Proc. Natl. Acad. Sci. U. S. A. 2003, 100(17), 9826-9830.
73. Gawrisch, K.; Richter, W.; Mops, A.; Balgavy, P.; Arnold, K.; Klose, G. The Influence of Water Concentration on the Structure of Egg-Yolk Phospholipid Water Dispersions. Stud. Biophys. 1985, 108(1), 5-16.
74. Petrache, H. I.; Tristram-Nagle, S.; Gawrisch, K.; Harries, D.; Parsegian, V. A.; Nagle, J. F. Structure and fluctuations of charged phosphatidylserine bilayers in the absence of salt. Biophys. J. 2004, 86(3), 1574-1586.
75. Ho, C.; Stubbs, C. D. Hydration at the Membrane Protein-Lipid Interface. Biophys. J. 1992, 63(4), 897-902.
76. Wang, H. B.; Carlson, E.; Henderson, D.; Rowley, R. L. Molecular dynamics simulation of the liquid-liquid interface for immiscible and partially miscible mixtures. Mol. Simulat. 2003, 29(12), 777-785.
77. Tikhonov, A. M.; Schlossman, M. L. Surfactant and water ordering in triacontanol monolayers at the water-hexane interface. J. Phys. Chem. B 2003, 107(15), 3344-3347.