Computer modeling of polyleucine-based coiled coil dimers in a realistic membrane environment: Insight into helix-helix interactions in membrane proteins

Biochemistry

Volumn 43, Issue 28, 2004, Pages 9050-9060

  Ash, Walter L ^a   Stockner, Thomas ^a   MacCallum, Justin L ^a   Tieleman, D Peter ^a  

^a UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; HYDROGEN BONDS; POLYPEPTIDES; SIMULATED ANNEALING; VAN DER WAALS FORCES;

PROTEIN DYNAMICS; TRANSMEMBRANE PEPTIDES;

BIOCHEMISTRY;

ALANINE; ASPARAGINE; DIMER; LEUCINE; MEMBRANE PROTEIN; PHENYLALANINE; THREONINE;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; COMPUTER MODEL; COMPUTER SIMULATION; GEOMETRY; HYDROGEN BOND; MEMBRANE; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN FOLDING; ROTATION; SEQUENCE ANALYSIS;

AMINO ACIDS; COMPUTER SIMULATION; DIMERIZATION; HYDROGEN BONDING; MEMBRANE PROTEINS; MODELS, MOLECULAR; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; TIME FACTORS;

INSERTION SEQUENCES;

EID: 3142706507     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0494572     Document Type: Article

References (79)

1. Gether, U. (2000) Uncovering molecular mechanisms involved in activation of G protein-coupled receptors, Endocr. Rev. 21, 90-113.
2. Bertaccini, E., and Trudell, J. R. (2002) Predicting the transmembrane secondary structure of ligand-gated ion channels, Protein Eng. 15, 443-453.
3. Jiang, Y. X., Lee, A., Chen, J. Y., Ruta, V., Cadene, M., Chait, B. T., and MacKinnon, R. (2003) X-ray structure of a voltage-dependent K+ channel, Nature 423, 33-41.
4. Tate, C. G., Kunji, E. R. S., Lebendiker, M., and Schuldiner, S. (2001) The projection structure of EmrE, a proton-linked multidrug transporter from Escherichia coli, at 7 angstrom resolution, EMBO J. 20, 77-81.
5. Arkin, I. T. (2002) Structural aspects of oligomerization taking place between the transmembrane alpha-helices of bitopic membrane proteins, Biochim. Biophys. Acta-Biomembr. 1565, 347-363.
6. Chamberlain, A. K., Faham, S., Yohannan, S., and Bowie, J. U. (2003) in Membrane Proteins (Rees, D. C., Ed.) pp 19-46, Elsevier Science (USA), San Diego, California.
7. Popot, J. L., and Engelman, D. M. (2000) Helical membrane protein folding, stability, and evolution, Annu. Rev. Biochem. 69, 881-922.
8. von Heijne, G. (1992) Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule, J. Mol. Biol. 225, 487-494.
9. von Heijne, G. (1999) A day in the life of Dr. K. or how I learned to stop worrying and love lysozyme: A tragedy in six acts, J. Mol. Biol. 293, 367-379.
10. Edwards, R. A., and Turner, R. J. (1998) Alpha-periodicity analysis of small multidrug resistance (SMR) efflux transporters, Biochem. Cell. Biol. 76, 791-797.
11. Stevens, T. J., and Arkin, I. T. (2001) Substitution rates in alpha-helical transmembrane proteins, Protein Sci. 10, 2507-2517.
12. Popot, J. L., and Engelman, D. M. (1990) Membrane protein folding and oligomerization: the two-stage model, Biochemistry 29, 4031-4037.
13. Engelman, D. M., Chen, Y., Chin, C.-N., Curran, A. R., Dixon, A. M., Dupuy, A. D., Lee, A. S., Lehnert, U., Matthews, E. E., Reshetnyak, Y. K., Senes, A., and Popot, J. L. (2003) Membrane protein folding: beyond the two stage model, FEBS Lett. 555, 122-125.
14. Sansom, M. S. P., and Weinstein, H. (2000) Hinges, swivels and switches: the role of prolines in signalling via transmembrane alpha-helices, Trends Pharmacol. Sci. 21, 445-451.
15. Sato, H., Takeda, K., Tani, K., Hino, T., Okada, T., Nakasako, M., Kamiya, N., and Kouyama, T. (1999) Specific lipid-protein interactions in a novel honeycomb lattice structure of bacterior-hodopsin, Acta Crystallogr. D55, 1251-1256.
16. White, S. H., and Whimley, W. C. (1999) Membrane Protein Folding and Stability: Physical Principles, Annu. Rev. Biophys. Biomol. Struct. 28, 319-365.
17. Liang, J. (2002) Experimental and computational studies of determinants of membrane-protein folding, Curr. Opin. Chem. Biol. 6, 878-884.
18. Curran, A. R., and Engelman, D. M. (2003) Sequence motifs, polar interactions and conformational changes in helical membrane proteins, Curr. Opin. Struct. Biol. 13, 412-417.
19. Lagüe, P., Zuckermann, M. J., and Roux, B. (2000) Lipid-Mediated Interactions between Intrinsic Membrane Proteins: A Theoretical Study Based on Integral Equations, Biophys. J. 79, 2867-2879.
20. Liu, W., Crocker, E., Siminovitch, D. J., and Smith, S. O. (2003) Role of side-chain conformational entropy in transmembrane helix dimerization of glycophorin A, Biophys. J. 84, 1263-1271.
21. Kralchevsky, P. A., and Nagayama, K. (2000) Capillary interactions between particles bound to interfaces, liquid films and biomembranes, Adv. Colloid Interface Sci. 85, 145-192.
22. Gratkowski, H., Lear, J. D., and DeGrado, W. F. (2001) Polar side chains drive the association of model transmembrane peptides, Proc. Natl. Acad. Sci. U.S.A. 98, 880-885.
23. Zhou, F. X., Merianos, H. J., Brunger, A. T., and Engelman, D. M. (2001) Polar residues drive association of polyleucine transmembrane helices, Proc. Natl. Acad. Sci. U.S.A. 98, 2250-2255.
24. Smith, S. O., Smith, C. S., and Bormann, B. J. (1996) Strong hydrogen bonding interactions involving a buried glutamic acid in the transmembrane sequence of the neu/erbB-2 receptor, Nat. Struct. Biol. 3, 252-258.
25. Bargmann, C. I., Hung, M. C., and Weinberg, R. A. (1986) Multiple independent activations of the neu oncogene by a point mutation altering the transmembrane domain of p 185, Cell 45, 649-657.
26. Partridge, A. W., Melnyk, R. A., and Deber, C. M. (2002) Polar residues in membrane domains of proteins: Molecular basis for helix-helix association in a mutant CFTR transmembrane segment, Biochemistry 41, 3647-3653.
27. Adams, P. D., Engelman, D. M., and Brunger, A. T. (1996) Improved prediction for the structure of the dimeric transmembrane domain of glycophorin A obtained through global searching, Proteins 26, 257-261.
28. Torres, J., Briggs, J. A. G., and Arkin, I. T. (2002) Contribution of energy values to the analysis of global searching molecular dynamics simulations of transmembrane helix bundles, Biophys. J. 2002, 6.
29. Sansom, M. S. P., Sankararamakrishnan, R., and Kerr, I. D. (1995) Modeling membrane proteins using structural restraints, Nat. Struct. Biol. 2, 624-631.
30. Capener, C. E., Proks, P., Ashcroft, F. M., and Sansom, M. S. P. (2003) Filter flexibility in a mammalian K channel: Models and simulations of Kir6.2 mutants, Biophys. J. 84, 2345-2356.
31. Law, R. J., Tieleman, D. P., and Sansom, M. S. P. (2003) Pores formed by the nicotinic receptor M2 delta peptide: A molecular dynamics simulation study, Biophys. J. 84, 14-27.
32. Campbell, J. D., Biggin, P. C., Baaden, M., and Sansom, M. S. P. (2003) Extending the structure of an ABC transporter to atomic resolution: Modeling and simulation studies of MsbA, Biochemistry 42, 3666-3673.
33. Tieleman, D. P., Hess, B., and Sansom, M. S. P. (2002) Analysis and evaluation of channel models: Simulations of alamethicin, Biophys. J. 83, 2393-2407.
34. Fleishman, S. J., and Ben-Tal, N. (2002) A novel scoring function for predicting the conformations of tightly packed pairs of transmembrane alpha-helices, J. Mol. Biol. 321, 363-378.
35. Fleishman, S. J., Schlessinger, J., and Ben-Tal, N. (2002) A putative molecular-activation switch in the transmembrane domain of erbB2, Proc. Natl. Acad. Sci. U.S.A. 99, 15937-15940.
36. Choma, C. T., Tieleman, D. P., Cregut, D., Serrano, L., and Berendsen, H. J. C. (2001) Towards the design and computational characterization of a membrane protein, J. Mol. Graphics Modell. 20, 219-234.
37. DeGrado, W. F., Gratkowski, H., and Lear, J. D. (2003) How do helix-helix interactions help determine the folds of membrane proteins? Perspectives from the study of homo-oligomeric helical bundles, Protein Sci. 12, 647-665.
38. Choma, C., Gratkowski, H., Lear, J. D., and DeGrado, W. F. (2000) Asparagine-mediated self-association of a model transmembrane helix, Nat. Struct. Biol. 7, 161-166.
39. Dawson, J. P., Weinger, J. S., and Engelman, D. M. (2002) Motifs of serine and threonine can drive association of transmembrane helices, J. Mol. Biol. 316, 799-805.
40. de Planque, M. R. R., and Killian, J. A. (2003) Protein-lipid interactions studied with designed transmembrane peptides: role of hydrophobic matching and interfacial anchoring, Mol. Membr. Biol. 20, 271-284.
41. Zhou, F. X., Cocco, M. J., Russ, W. P., Brunger, A. T., and Engelman, D. M. (2000) Interhelical hydrogen bonding drives strong interactions in membrane proteins, Nat. Struct. Biol. 7, 154-160.
42. Gurezka, R., and Langosch, D. (2001) In vitro selection of membrane-spanning leucine zipper protein-protein interaction motifs using POSSYCCAT, J. Biol. Chem. 276, 45580-45587.
43. Davis, J. H., Donna, M. C., Hodges, R. S., and Bloom, M. (1983) Interaction of a Synthetic Amphiphilic Polypeptide and Lipids in a Bilayer Structure, Biochemistry 22, 5298-5305.
44. O'Shea, E. K., Klemm, J. D., Kim, P. S., and Alber, T. (1991) X-ray structure of the GCN4 leucine zipper, a two-stranded, parallel coiled coil, Science 254, 539-544.
45. Crick, F. H. C. (1953) The packing of alpha-helices: simple coiled-coils, Acta Crystallogr. 6, 689-697.
46. Newman, J. R. S., and Keating, A. E. (2003) Comprehensive identification of human bZIP interactions with coiled-coil arrays, Science 300, 2097-2101.
47. Lear, J. D., Gratkowski, H., Adamian, L., Liang, J., and DeGrado, W. F. (2003) Position-dependence of stabilizing polar interactions of asparagine in transmembrane helical bundles, Biochemistry 42, 6400-6407.
48. Gurezka, R., Laage, R., Brosig, B., and Langosch, D. (1999) A heptad motif of leucine residues found in membrane proteins can drive self-assembly of artificial transmembrane segments, J. Biol. Chem. 274, 9265-9270.
49. Walshaw, J., and Woolfson, D. N. (2001) SOCKET: A program for identifying and analysing coiled-coil motifs within protein structures, J. Mol. Biol. 307, 1427-1450.
50. Bywater, R. P., Thomas, D., and Vriend, G. (2001) A sequence and structural study of transmembrane helices, J. Comput.-Aided Mol. Des. 15, 533-552.
51. Nilges, M., and Brunger, A. T. (1993) Successful prediction of the coiled coil geometry of the GCN4 leucine zipper domain by simulated annealing: comparison to the X-ray structure, Proteins 15, 133-146.
52. Petrache, H. I., Grossfield, A., MacKenzie, K. R., Engelman, D. M., and Woolf, T. B. (2000) Modulation of glycophorin A transmembrane helix interactions by lipid bilayers: Molecular dynamics calculations, J. Mol. Biol. 302, 727-746.
53. Smith, S. O., Eilers, M., Song, D., Crocker, E., Ying, W. W., Groesbeek, M., Metz, G., Ziliox, M., and Aimoto, S. (2002) Implications of threonine hydrogen bonding in the glycophorin A transmembrane helix dimer, Biophys. J. 82, 2476-2486.
54. Gernert, K. M., Surles, M. C., Labean, T. H., Richardson, J. S., and Richardson, D. C. (1995) The Alacoil: a very tight, antiparallel coiled-coil of helices, Protein Sci. 4, 2252-2260.
55. Fujita, K., Bunjes, N., Nakajima, K., Hara, M., Sasabe, H., and Knoll, W. (1998) Macrodipole interaction of helical-peptides in a self-assembled monolayer on gold substrate, Langmuir 14, 6167-6172.
56. Smith, S. O., Smith, C., Shekar, S., Peersen, O., Ziliox, M., and Aimoto, S. (2002) Transmembrane interactions in the activation of the Neu receptor tyrosine kinase, Biochemistry 41, 9321-9332.
57. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr. D54, 905-921.
58. Kaminski, G. A., Friesner, R. A., Tirado-Rives, J., and Jorgensen, W. L. (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides, J. Phys. Chem. B 105, 6474-6487.
59. Treutlein, H. R., Lemmon, M. A., Engelman, D. M., and Brunger, A. T. (1992) The glycophorin-A transmembrane domain dimer - sequence-specific propensity for a right-handed supercoil of helices, Biochemistry 31, 12726-12733.
60. Kelly, L. A., Gardner, S. P., and Sutcliffe, M. J. (1996) An automated approach for clustering an ensemble of NMR-derived protein structures into conformationally related subfamilies, Protein Eng. 9, 1063-1065.
61. Strelkov, S. V., and Burkhard, P. (2002) Analysis of alpha-Helical Coiled Coils with the Program TWISTER Reveals a Structural Mechanism for Stutter Compensation, J. Struct. Biol. 137, 54-64.
62. Lindahl, E., Hess, B., and van der Spoel, D. (2001) GROMACS 3.0: a package for molecular simulation and trajectory analysis, J. Mol. Model 7, 306-317.
63. Berger, O., Edholm, O., and Jahnig, F. (1997) Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature, Biophys. J. 72, 2002-2013.
64. van der Spoel, D., van Buuren, A. R., Apol, E., Muelenhoff, P. J., Tieleman, D. P., Sijbers, A. L. T. M., Hess, B., Feenstra, K. A., Lindahl, E., van Drunen, R., and Berendsen, H. J. C. (2002) Gromacs User Manual Version 3.1.1, University of Groningen, Groningen, NL.
65. Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., and Pedersen, L. G. (1995) A smooth particle mesh ewald method, J. Chem. Phys. 103, 8577-8593.
66. Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., and Haak, J. R. (1984) Molecular Dynamics with coupling to an external bath, J. Chem. Phys. 81, 3684-3690.
67. Faraldo-Gomez, J. D., Smith, G. R., and Sansom, M. S. P. (2002) Setting up and optimization of membrane protein simulations, Eur. Biophys. J. Biophy. 31, 217-227.
68. Sanner, M. F., Olson, A. J., and Spehner, J. C. (1996) Reduced surface: An efficient way to compute molecular surfaces, Biopolymers 38, 305-320.
69. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features, Biopolymers 22, 2577-2637.
70. Humphrey, W., Dalke, A., and Schulten, K. (1996) VMD - Visual Molecular Dynamics, J. Mol. Graphics 14, 33-38.
71. Leach, A. R. (2001) Molecular Modelling: Principles and Applications, 2 ed., Pearson Education Limited, Essex, England.
72. Matsumoto, M., and Nishimura, T. (1998) Mersenne Twister: A 623-dimensionally equidistributed uniform psuedorandom number generator, ACM Trans. Modell. Comp. Simul. 8, 3-30.
73. Walther, D., Eisenhaber, F., and Argos, P. (1996) Principles of helix-helix packing in proteins: The helical lattice superposition model, J. Mol. Biol. 255, 536-553.
74. Walther, D., Springer, C., and Cohen, F. E. (1998) Helix-helix packing angle preferences for finite helix axes, Proteins 33, 457-459.
75. Bowie, J. U. (1997) Helix packing angle preferences, Nat. Struct. Biol. 4, 915-917.
76. Dawson, J. P., Melnyk, R. A., Deber, C. M., and Engelman, D. M. (2003) Sequence Context Strongly Modulates Association of Polar Residues in Transmembrane Helices, J. Mol. Biol. 331, 255-262.
77. Stockner, T., Ash, W. L., MacCallum, J. L., and Tieleman, D. P. (2004) Direct simulation of transmembrane helix association: role of asparagines. Biophys. J., in press.
78. Miyazawa, A., Fujiyoshi, Y., and Unwin, M. (2003) Structure and gating mechanism of the acetylcholine receptor pore, Nature 423, 949-955.
79. Kollman, P. (1993) Free-energy calculations - applications to chemical and biochemical phenomena, Chem. Rev. 93, 2395-2417.