MemProtMD: Automated Insertion of Membrane Protein Structures into Explicit Lipid Membranes

Structure

Volumn 23, Issue 7, 2015, Pages 1350-1361

  Stansfeld, Phillip J ^a   Goose, Joseph E ^a,c   Caffrey, Martin ^b   Carpenter, Elisabeth P ^a   Parker, Joanne L ^a   Newstead, Simon ^a   Sansom, Mark S P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b TRINITY COLLEGE DUBLIN   (Ireland)

^c SCHRÖDINGER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; OUTER MEMBRANE PROTEIN; LIPID BILAYER;

AMINO ACID SEQUENCE; ARTICLE; AUTOANALYSIS; BINDING SITE; COARSE GRAINED MOLECULAR DYNAMICS; LIGAND BINDING; LIPID BILAYER; MOLECULAR DYNAMICS; NONHUMAN; OCTOPUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; CHEMICAL PHENOMENA; CHEMISTRY; PROTEIN CONFORMATION;

BINDING SITES; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; LIPID BILAYERS; MEMBRANE PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN CONFORMATION;

EID: 84936845938     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2015.05.006     Document Type: Article

References (76)

1. C. Arnarez, J.P. Mazat, J. Elezgaray, S.J. Marrink, and X. Periole Evidence for cardiolipin binding sites on the membrane-exposed surface of the cytochrome bc1 J. Am. Chem. Soc. 135 2013 3112 3120
2. P. Badola, and C.R. Sanders 2nd Escherichia coli diacylglycerol kinase is an evolutionarily optimized membrane enzyme and catalyzes direct phosphoryl transfer J. Biol. Chem. 272 1997 24176 24182
3. C. Baeza-Delgado, M.A. Marti-Renom, and I. Mingarro Structure-based statistical analysis of transmembrane helices Eur. Biophys. J. 42 2013 199 207
4. M. Bayrhuber, T. Meins, M. Habeck, S. Becker, K. Giller, S. Villinger, C. Vonrhein, C. Griesinger, M. Zweckstetter, and K. Zeth Structure of the human voltage-dependent anion channel Proc. Natl. Acad. Sci. USA 105 2008 15370 15375
5. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucleic Acids Res. 28 2000 235 242
6. P.J. Bond, and M.S.P. Sansom Insertion and assembly of membrane proteins via simulation J. Am. Chem. Soc. 128 2006 2697 2704
7. J.D. Brunner, N.K. Lim, S. Schenck, A. Duerst, and R. Dutzler X-ray structure of a calcium-activated TMEM16 lipid scramblase Nature 516 2014 207 212
8. M. Caffrey A comprehensive review of the lipid cubic phase or in meso method for crystallizing membrane and soluble proteins and complexes Acta Crystallogr. F Struct. Biol. Commun. 71 2015 3 18
9. O.P. Choudhary, A. Paz, J.L. Adelman, J.P. Colletier, J. Abramson, and M. Grabe Structure-guided simulations illuminate the mechanism of ATP transport through VDAC1 Nat. Struct. Mol. Biol. 21 2014 626 632
10. U. Coskun, and K. Simons Cell membranes: the lipid perspective Structure 19 2011 1543 1548
11. T.A. Cross, D.T. Murray, and A. Watts Helical membrane protein conformations and their environment Eur. Biophys. J. 42 2013 731 755
12. F. Cymer, G. von Heijne, and S.H. White Mechanisms of integral membrane protein insertion and folding J. Mol. Biol. 427 2015 999 1022
13. R.J. Dawson, and K.P. Locher Structure of a bacterial multidrug ABC transporter Nature 443 2006 180 185
14. T.J. Dolinsky, P. Czodrowski, H. Li, J.E. Nielsen, J.H. Jensen, G. Klebe, and N.A. Baker PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations Nucleic Acids Res. 35 2007 W522 W525
15. H. Dong, Q. Xiang, Y. Gu, Z. Wang, N.G. Paterson, P.J. Stansfeld, C. He, Y. Zhang, W. Wang, and C. Dong Structural basis for outer membrane lipopolysaccharide insertion Nature 511 2014 52 56
16. N.D. Drachmann, C. Olesen, J.V. Moller, Z. Guo, P. Nissen, and M. Bublitz Comparing crystal structures of Ca(2+)-ATPase in the presence of different lipids FEBS J. 281 2014 4249 4262
17. M. Eilers, S.C. Shekar, T. Shieh, S.O. Smith, and P.J. Fleming Internal packing of helical membrane proteins Proc. Natl. Acad. Sci. USA 97 2000 5796 5801
18. P.J. Franco, and T.H. Wilson Alteration of Na(+)-coupled transport in site-directed mutants of the melibiose carrier of Escherichia coli Biochim. Biophys. Acta 1282 1996 240 248
19. G. Heijne The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology EMBO J. 5 1986 3021 3027
20. B. Hess, C. Kutzner, D. van der Spoel, and E. Lindahl GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulation J. Chem. Theor. Comp. 4 2008 435 447
21. R.K. Hite, Z.L. Li, and T. Walz Principles of membrane protein interactions with annular lipids deduced from aquaporin-0 2D crystals EMBO J. 29 2010 1652 1658
22. H.I. Ingolfsson, M.N. Melo, F.J. van Eerden, C. Arnarez, C.A. Lopez, T.A. Wassenaar, X. Periole, A.H. de Vries, D.P. Tieleman, and S.J. Marrink Lipid organization of the plasma membrane J. Am. Chem. Soc. 136 2014 14554 14559
23. M.S. Jin, M.L. Oldham, Q. Zhang, and J. Chen Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans Nature 490 2012 566 569
24. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern-recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
25. S. Kelm, J. Shi, and C.M. Deane MEDELLER: homology-based coordinate generation for membrane proteins Bioinformatics 26 2010 2833 2840
26. J.A. Killian, and G. von Heijne How proteins adapt to a membrane-water interface Trends Biochem. Sci. 25 2000 429 434
27. H. Koldso, D. Shorthouse, J. Helie, and M.S. Sansom Lipid clustering correlates with membrane curvature as revealed by molecular simulations of complex lipid bilayers PLoS Comput. Biol. 10 2014 e1003911
28. D. Kozma, I. Simon, and G.E. Tusnady PDBTM: Protein Data Bank of transmembrane proteins after 8 years Nucleic Acids Res. 41 2013 D524 D529
29. E. Krissinel, and K. Henrick Inference of macromolecular assemblies from crystalline state J. Mol. Biol. 372 2007 774 797
30. C. Landolt-Marticorena, K.A. Williams, C.M. Deber, and R.A.F. Reithmeier Nonrandom distribution of amino-acids in the transmembrane segments of human type-I single span membrane-proteins J. Mol. Biol. 229 1993 602 608
31. 2+-ATPase structure in the E1 and E2 conformations: mechanism, helix-helix and helix-lipid interactions Biochim. Biophys. Acta 1565 2002 246 266
32. A.G. Lee Biological membranes: the importance of molecular detail Trends Biochem. Sci. 36 2011 493 500
33. D. Li, J.A. Lyons, V.E. Pye, L. Vogeley, D. Aragao, C.P. Kenyon, S.T. Shah, C. Doherty, M. Aherne, and M. Caffrey Crystal structure of the integral membrane diacylglycerol kinase Nature 497 2013 521 524
34. J. Li, K.F. Jaimes, and S.G. Aller Refined structures of mouse P-glycoprotein Protein Sci. 23 2014 34 46
35. M. Liao, E. Cao, D. Julius, and Y. Cheng Single particle electron cryo-microscopy of a mammalian ion channel Curr. Opin. Struct. Biol. 27 2014 1 7
36. X. Liu, Y. Yin, J. Wu, and Z. Liu Structure and mechanism of an intramembrane liponucleotide synthetase central for phospholipid biosynthesis Nat. Commun. 5 2014 4244
37. M.A. Lomize, I.D. Pogozheva, H. Joo, H.I. Mosberg, and A.L. Lomize OPM database and PPM web server: resources for positioning of proteins in membranes Nucleic Acids Res. 40 2012 D370 D376
38. S.J. Marrink, and D.P. Tieleman Perspective on the Martini model Chem. Soc. Rev. 42 2013 6801 6822
39. N. Michaud-Agrawal, E.J. Denning, T.B. Woolf, and O. Beckstein MDAnalysis: a toolkit for the analysis of molecular dynamics simulations J. Comput. Chem. 32 2011 2319 2327
40. S. Mondal, G. Khelashvili, L. Shi, and H. Weinstein The cost of living in the membrane: a case study of hydrophobic mismatch for the multi-segment protein LeuT Chem. Phys. Lipids 169 2013 27 38
41. L. Monticelli, S.K. Kandasamy, X. Periole, R.G. Larson, D.P. Tieleman, and S.J. Marrink The MARTINI coarse grained force field: extension to proteins J. Chem. Theor. Comp. 4 2008 819 834
42. C.P. Moon, and K.G. Fleming Side-chain hydrophobicity scale derived from transmembrane protein folding into lipid bilayers Proc. Natl. Acad. Sci. USA 108 2011 10174 10177
43. T. Nugent, and D.T. Jones Accurate de novo structure prediction of large transmembrane protein domains using fragment-assembly and correlated mutation analysis Proc. Natl. Acad. Sci. USA 109 2012 E1540 E1547
44. T. Nugent, and D.T. Jones Membrane protein orientation and refinement using a knowledge-based statistical potential BMC Bioinformatics 14 2013 276
45. H. Palsdottir, and C. Hunte Lipids in membrane protein structures Biochim. Biophys. Acta 1666 2004 2 18
46. J.L. Parker, and S. Newstead Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1 Nature 507 2014 68 72
47. E. Pebay-Peyroula, C. Dahout-Gonzalez, R. Kahn, V. Trezeguet, G.J. Lauquin, and G. Brandolin Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside Nature 426 2003 39 44
48. X. Periole, A.M. Knepp, T.P. Sakmar, S.J. Marrink, and T. Huber Structural determinants of the supramolecular organization of G protein-coupled receptors in bilayers J. Am. Chem. Soc. 134 2012 10959 10965
49. T.J. Piggot, D.A. Holdbrook, and S. Khalid Electroporation of the E. coli and S. aureus membranes: molecular dynamics simulations of complex bacterial membranes J. Phys. Chem. B 115 2011 13381 13388
50. C.L. Piscitelli, H. Krishnamurthy, and E. Gouaux Neurotransmitter/sodium symporter orthologue LeuT has a single high-affinity substrate site Nature 468 2010 1129 1132
51. I.D. Pogozheva, S. Tristram-Nagle, H.I. Mosberg, and A.L. Lomize Structural adaptations of proteins to different biological membranes Biochim. Biophys. Acta 1828 2013 2592 2608
52. A. Quigley, Y.Y. Dong, A.C. Pike, L. Dong, L. Shrestha, G. Berridge, P.J. Stansfeld, M.S. Sansom, A.M. Edwards, and C. Bountra The structural basis of ZMPSTE24-dependent laminopathies Science 339 2013 1604 1607
53. F. Rodriguez, S.L. Rouse, C.E. Tait, J. Harmer, A. De Riso, C.R. Timmel, M.S. Sansom, B.C. Berks, and J.R. Schnell Structural model for the protein-translocating element of the twin-arginine transport system Proc. Natl. Acad. Sci. USA 110 2013 E1092 E1101
54. S.E. Rollauer, M.J. Tarry, J.E. Graham, M. Jaaskelainen, F. Jager, S. Johnson, M. Krehenbrink, S.M. Liu, M.J. Lukey, and J. Marcoux Structure of the TatC core of the twin-arginine protein transport system Nature 492 2012 210 214
55. D.M. Rosenbaum, V. Cherezov, M.A. Hanson, S.G. Rasmussen, F.S. Thian, T.S. Kobilka, H.J. Choi, X.J. Yao, W.I. Weis, and R.C. Stevens GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function Science 318 2007 1266 1273
56. P. Rotkiewicz, and J. Skolnick Fast procedure for reconstruction of full-atom protein models from reduced representations J. Comput. Chem. 29 2008 1460 1465
57. J.J. Ruprecht, A.M. Hellawell, M. Harding, P.G. Crichton, A.J. McCoy, and E.R. Kunji Structures of yeast mitochondrial ADP/ATP carriers support a domain-based alternating-access transport mechanism Proc. Natl. Acad. Sci. USA 111 2014 E426 E434
58. W.P. Russ, and D.M. Engelman The GxxxG motif: a framework for transmembrane helix-helix association J. Mol. Biol. 296 2000 911 919
59. A. Sali, and T.L. Blundell Comparative protein modeling by satisfaction of spatial restraints J. Mol. Biol. 234 1993 779 815
60. M.R. Schmidt, P.J. Stansfeld, S.J. Tucker, and M.S. Sansom Simulation-based prediction of phosphatidylinositol 4,5-bisphosphate binding to an ion channel Biochemistry 52 2013 279 281
61. K.A. Scott, P.J. Bond, A. Ivetac, A.P. Chetwynd, S. Khalid, and M.S.P. Sansom Coarse-grained MD simulations of membrane protein-bilayer self-assembly Structure 16 2008 621 630
62. C.A. Shintre, A.C. Pike, Q. Li, J.I. Kim, A.J. Barr, S. Goubin, L. Shrestha, J. Yang, G. Berridge, and J. Ross Structures of ABCB10, a human ATP-binding cassette transporter in apo- and nucleotide-bound states Proc. Natl. Acad. Sci. USA 110 2013 9710 9715
63. P.J. Stansfeld, and M.S.P. Sansom From coarse-grained to atomistic: a serial multi-scale approach to membrane protein simulations J. Chem. Theor. Comp. 7 2011 1157 1166
64. 2 binding site in Kir channels: definition by multi-scale biomolecular simulations Biochemistry 48 2009 10926 10933
65. P.J. Stansfeld, E.E. Jefferys, and M.S. Sansom Multiscale simulations reveal conserved patterns of lipid interactions with aquaporins Structure 21 2013 810 819
66. J. Sun, J.R. Bankston, J. Payandeh, T.R. Hinds, W.N. Zagotta, and N. Zheng Crystal structure of the plant dual-affinity nitrate transporter NRT1.1 Nature 507 2014 73 77
67. J. Tan, S.L. Rouse, D. Li, V.E. Pye, L. Vogeley, A.R. Brinth, T. El Arnaout, J.C. Whitney, P.L. Howell, and M.S. Sansom A conformational landscape for alginate secretion across the outer membrane of Pseudomonas aeruginosa Acta Crystallogr. D Biol. Crystallogr. 70 2014 2054 2068
68. G. van Meer, D. Halter, H. Sprong, P. Somerharju, and M.R. Egmond ABC lipid transporters: extruders, flippases, or flopless activators? FEBS Lett. 580 2006 1171 1177
69. H. Viklund, and A. Elofsson OCTOPUS: improving topology prediction by two-track ANN-based preference scores and an extended topological grammar Bioinformatics 24 2008 1662 1668
70. S. Villinger, R. Briones, K. Giller, U. Zachariae, A. Lange, B.L. de Groot, C. Griesinger, S. Becker, and M. Zweckstetter Functional dynamics in the voltage-dependent anion channel Proc. Natl. Acad. Sci. USA 107 2010 22546 22551
71. A.B. Ward, P. Szewczyk, V. Grimard, C.W. Lee, L. Martinez, R. Doshi, A. Caya, M. Villaluz, E. Pardon, and C. Cregger Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain Proc. Natl. Acad. Sci. USA 110 2013 13386 13391
72. S.H. White Biophysical dissection of membrane proteins Nature 459 2009 344 346
73. M.R. Whorton, and R. MacKinnon X-ray structure of the mammalian GIRK2-betagamma G-protein complex Nature 498 2013 190 197
74. V. Yarov-Yarovoy, J. Schonbrun, and D. Baker Multipass membrane protein structure prediction using Rosetta Proteins 62 2006 1010 1025
75. U. Zachariae, R. Schneider, R. Briones, Z. Gattin, J.P. Demers, K. Giller, E. Maier, M. Zweckstetter, C. Griesinger, and S. Becker Beta-barrel mobility underlies closure of the voltage-dependent anion channel Structure 20 2012 1540 1549
76. H. Zaid, S. Abu-Hamad, A. Israelson, I. Nathan, and V. Shoshan-Barmatz The voltage-dependent anion channel-1 modulates apoptotic cell death Cell Death Differ. 12 2005 751 760