Molecular Dynamics Studies of Membrane Proteins: Outer Membrane Proteins and Transporters

Biophysical Analysis of Membrane Proteins: Investigating Structure and Function

Volumn , Issue , 2008, Pages 159-185

  Khalid, Syma ^a   Holyoake, John ^a   Sansom, Mark S P ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biophysical analysis; Cytoplasmic membrane transport proteins; Molecular dynamics studies; Outer membrane proteins; Transporters

Indexed keywords

EID: 84872586897     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527621224.ch7     Document Type: Chapter

References (111)

1. Koebnik, R., Locher, K. P., and Van Gelder, P. (2000) Structure and function of bacterial outer membrane proteins: barrels in a nutshell. Mol. Microbiol., 37, 239-253.
2. Ash, W. L., Zlomislic, M. R., Oloo, E. O., and Tieleman, D. P. (2004) Computer simulations of membrane proteins. Biochim. Biophys. Acta, 1666, 158-189.
3. Gumbart, J., Wang, Y., Aksimentiev, A., Tajkhorshid, E., and Schulten, K. (2005) Molecular dynamics simulations of proteins in lipid bilayers. Curr. Opin. Struct. Biol., 15, 423-431.
4. Roux, B., and Schulten, K. (2004) Computational studies of membrane channels. Structure, 12, 1343-1351.
5. Noskov, S. Y., and Roux, B. (2006) Ion selectivity in potassium channels. Biophys. Chem., 124, 279-291.
6. Im, W., and Brooks, C. L. (2005) Interfacial folding and membrane insertion of designed peptides studied by molecular dynamics simulations. Proc. Natl. Acad. Sci. USA, 102, 6771-6776.
7. Bond, P. J., and Sansom, M. S. P. (2006) Insertion and assembly of membrane proteins via simulation. J. Am. Chem. Soc., 128, 2697-2704.
8. Bond, P. J., Holyoake, J., Ivetac, A., Khalid, S., and Sansom, M. S. P. (2007) Coarse-grained molecular dynamics simulations of membrane proteins and peptides. J. Struct. Biol., 157, 593-605.
9. Deol, S. S., Bond, P. J., Domene, C., and Sansom, M. S. P. (2004) Lipid-protein interactions of integral membrane proteins: a comparative simulation study. Biophys. J., 87, 3737-3749.
10. Deol, S. S., Domene, C., Bond, P. J., and Sansom, M. S. P. (2006) Anionic phospholipids interactions with the potassium channel KcsA: simulation studies. Biophys. J., 90, 822-830.
11. Karplus, M. J., and McCammon, J. A. (2002) Molecular dynamics simulations of biomolecules. Nature Struct. Biol., 9, 646-652.
12. Adcock, S. A., and McCammon, J. A. (2006) Molecular dynamics: survey of methods for simulating the activity of proteins. Chem. Rev., 106, 1589-1615.
13. Faraldo-Gómez, J. D., Smith, G. R., and Sansom, M. S. P. (2002) Setup and optimisation of membrane protein simulations. Eur. Biophys. J., 31, 217-227.
14. Forrest, L. R., and Sansom, M. S. P. (2000) Membrane simulations: bigger and better? Curr. Opin. Struct. Biol., 10, 174-181.
15. Domene, C., Bond, P., and Sansom, M. S. P. (2003) Membrane protein simulation: ion channels and bacterial outer membrane proteins. Adv. Prot. Chem., 66, 159-193.
16. Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T., Nouwens, A. S., Williams, K. L., and Gooley, A. A. (2000) Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem., 267, 2871-2881.
17. Wimley, W. C. (2002) Toward genomic identification of β-barrel membrane proteins: composition and architecture of known structures. Protein Sci., 11, 301-312.
18. Popot, J. L., and Engelman, D. M. (2000) Helical membrane protein folding, stability, and evolution. Annu. Rev. Biochem., 69, 881-922.
19. Buchanan, S. K. (1999) β-Barrel proteins from bacterial outer membranes: structure, function and refolding. Curr. Opin. Struct. Biol., 9, 455-461.
20. Wimley, W. C. (2003) The versatile β-barrel membrane protein. Curr. Opin. Struct. Biol., 13, 404-411.
21. Doerrler, W. T. (2006) Lipid trafficking to the outer membrane of Gram- negative bacteria. Mol. Microbiol., 60, 542-552.
22. Lins, R. D., and Straatsma, T. P. (2001) Computer simulation of the rough lipopolysaccharide membrane of Pseudomonas aeruginosa. Biophys. J., 81, 1037-1046.
23. Shroll, R. M., and Straatsma, T. P. (2002) Molecular structure of the outer bacterial membrane of Pseudomonas aeruginosa via classical simulation. Biopolymers, 65, 395-407.
24. Schirmer, T. (1998) General and specific porins from bacterial outer membranes. J. Struct. Biol., 121, 101-109.
25. Achouak, W., Heulin, T., and Pages, J. M. (2001) Multiple facets of bacterial porins. FEMS Microbiol. Lett., 199, 1-7.
26. Schirmer, T., Keller, T. A., Wang, Y. F., and Rosenbusch, J. P. (1995) Structural basis for sugar translocation through maltoporin channels at 3.1 Å resolution. Science, 267, 512-514.
27. Forst, D., Welte, W., Wacker, T., and Diederichs, K. (1998) Structure of the sucrose-specific porin ScrY from Salmonella typhimurium and its complex with sucrose. Nature Struct. Biol., 5, 37-46.
28. Moraes, T. F., Bains, M., Hancock, P. E. W., and Strynadka, N. C. J. (2007) An arginine ladder in OprP mediates phosphate-specific transfer across the outer membrane. Nature Struct. Mol. Biol., 14, 85-87.
29. Faraldo-Gómez, J. D., and Sansom, M. S. P. (2003) Acquisition of siderophores in Gram-negative bacteria. Nature Rev. Mol. Cell. Biol., 4, 105-115.
30. Henderson, I. R., Navarro-Garcia, F., Desvaux, M., Fernandez, R. C., and Ala'Aldeen, D. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol. Mol. Biol. Rev., 68, 692-744.
31. Bond, P. J., and Sansom, M. S. P. (2004) The simulation approach to bacterial outer membrane proteins. Mol. Membr. Biol., 21, 151-162.
32. Pautsch, A., and Schulz, G. E. (1998) Structure of the outer membrane protein A transmembrane domain. Nature Struct. Biol., 5, 1013-1017.
33. Pautsch, A., and Schulz, G. E. (2000) High-resolution structure of the OmpA membrane domain. J. Mol. Biol., 298, 273-282.
34. Arora, A., Abildgaard, F., Bushweller, J. H., and Tamm, L. K. (2001) Structure of outer membrane protein A transmembrane domain by NMR spectroscopy. Nature Struct. Biol., 8, 334-338.
35. Fernandez, C., Hilty, C., Bonjour, S., Adeishvili, K., Pervushin, K., and Wüthrich, K. (2001) Solution NMR studies of the integral membrane proteins OmpX and OmpA from Escherichia coli. FEBS Lett., 504, 173-178.
36. Saint, N., De, E., Julien, S., Orange, N., and Molle, G. (1993) Ionophore properties of OmpA of Escherichia coli. Biochim. Biophys. Acta, 1145, 119-123.
37. Sugawara, E., and Nikaido, H. (1992) Pore-forming activity of OmpA protein of Escherichia coli. J. Biol. Chem., 267, 2507-2511.
38. Arora, A., Rinehart, D., Szabo, G., and Tamm, L. K. (2000) Refolded outer membrane protein A of Escherichia coli forms ion channels with two conductance states in planar lipid bilayers. J. Biol. Chem., 275, 1594-1600.
39. Bond, P. J., Faraldo-Gómez, J. D., and Sansom, M. S. P. (2002) OmpA-A pore or not a pore? Simulation and modelling studies. Biophys. J., 83, 763-775.
40. Hong, H., Szabo, G., and Tamm, L. K. (2006) Electrostatic couplings in OmpA ion-channel gating suggest a mechanism for pore opening. Nature Chem. Biol., 2, 627-635.
41. Khalid, S., Bond, P. J., Deol, S. S., and Sansom, M. S. P. (2005) Modelling and simulations of a bacterial outer membrane protein: OprF from Pseudomonas aeruginosa. Proteins: Struct. Funct. Bioinf., 63, 6-15.
42. Carpenter, T., Khalid, S., and Sansom, M. S. P. (2006) A multidomain outer membrane protein from Pasteurella multocida: modelling and simulations studies on PmOmpA. Biochim. Biophys. Acta (submitted).
43. Ramakrishnan, M., Pocanschi, C. L., Kleinschmidt, J. H., and Marsh, D. (2004) Association of spin-labeled lipids with β-barrel proteins from the outer membrane of Escherichia coli. Biochemistry, 43, 11630-11636.
44. Bond, P. J., and Sansom, M. S. P. (2003) Membrane protein dynamics vs. environment: simulations of OmpA in a micelle and in a bilayer. J. Mol. Biol., 329, 1035-1053.
45. Bond, P. J., Faraldo-Gómez, J. D., Deol, S. S., and Sansom, M. S. P. (2006) Membrane protein dynamics and detergent interactions within a crystal: a simulation study of OmpA. Proc. Natl. Acad. Sci. USA, 103, 9518-9523.
46. Fernandez, C., Hilty, C., Wider, G., Güntert, P., and Wüthrich, K. (2004) NMR structure of the integral membrane protein OmpX. J. Mol. Biol., 336, 1211-1221.
47. Hwang, P. M., Choy, W. Y., Lo, E. I., Chen, L., Forman-Kay, J. D., Raetz, C. R. H., Privé, G. G., Bishop, R. E., and Kay, L. E. (2002) Solution structure and dynamics of the outer membrane enzyme PagP by NMR. Proc. Natl. Acad. Sci. USA, 99, 13560-13565.
48. Cox, K., Bond, P. J., Grottesi, A., Baaden, M., and Sansom, M. S. P. (2007) Outer membrane proteins: comparing X-ray and NMR structures by MD simulations in lipid bilayers. Eur. Biophys. J. (submitted).
49. Prince, S. M., Achtman, M., and Derrick, J. P. (2002) Crystal structure of the OpcA integral membrane adhesin from Neisseria meningitides. Proc. Natl. Acad. Sci. USA, 99, 3417-3421.
50. Bond, P. J., Derrick, J. P., and Sansom, M. S. P. (2007) Membrane simulations of OpcA: gating in the loops? Biophys. J., 92, L23-L25.
51. Tieleman, D. P., and Berendsen, H. J. C. (1998) A molecular dynamics study of the pores formed by Escherichia coli OmpF porin in a fully hydrated palmitoyloleoylphosphatidylcholine bilayer. Biophys. J., 74, 2786-2801.
52. Smart, O. S., Breed, J., Smith, G. R., and Sansom, M. S. P. (1997) A novel method for structure-based prediction of ion channel conductance properties. Biophys. J., 72, 1109-1126.
53. Im, W., and Roux, B. (2002) Ions and counterions in a biological channel: A molecular dynamics simulation of OmpF porin from Escherichia coli in an explicit membrane with 1 M KCl aqueous salt solution. J. Mol. Biol., 319, 1177-1197.
54. Im, W., and Roux, B. (2002) Ion permeation and selectivity of OmpF porin: A theoretical study based on molecular dynamics, Brownian dynamics, and continuum electrodiffusion theory. J. Mol. Biol., 322, 851-869.
55. Robertson, K. M., and Tieleman, D. P. (2002) Orientation and interactions of dipolar molecules during transport through OmpF porin. FEBS Lett., 528, 53-57.
56. Varma, S., Chiu, S. W., and Jakobsson, E. (2006) The influence of amino acid protonation states on molecular dynamics simulations of the bacterial porin OmpF. Biophys. J., 90, 112-123.
57. Wiener, M. C. (2005) TonB-dependent outer membrane transport: going for Baroque? Curr. Opin. Struct. Biol., 15, 394-400.
58. Oomen, C. J., van Ulsen, P., van Gelder, P., Feijen, M., Tommassen, J., and Gros, P. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J., 23, 1257-1266.
59. Meng, G., Surana, N. K., St. Geme, J. W., and Waksman, G. (2006) Structure of the outer membrane translocator domain of the Haemophilus influenzae Hia trimeric autotransporter. EMBO J., 25, 2297-2304.
60. Faraldo-Gómez, J. D., Smith, G. R., and Sansom, M. S. P. (2003) Molecular dynamics simulations of the bacterial outer membrane protein FhuA: a comparative study of the ferrichrome- free and bound states. Biophys. J., 85, 1-15.
61. Ferguson, A. D., Chakraborty, R., Smith, B. S., Esser, L., van der Helm, D., and Deisenhofer, J. (2002) Structural basis of gating by the outer membrane transporter FecA. Science, 295, 1715-1719.
62. Yue, W. W., Grizot, S., and Buchanan, S. K. (2003) Structural evidence for iron-free citrate and ferric citrate binding to the TonB-dependent outer membrane transporter FecA. J. Mol. Biol., 332, 353-368.
63. Buchanan, S. K., Smith, B. S., Venkatramani, L., Xia, D., Essar, L., Palnitkar, M., Chakraborty, R., van der Helm, D., and Deisenhofer, J. (1999) Crystal structure of the outer membrane active transporter FepA from Escherichia coli. Nature Struct. Biol., 6, 56-63.
64. Chimento, D. P., Mohanty, A. K., Kadner, R. J., and Wiener, M. C. (2003) Substrate- induced transmembrane signaling in the cobalamin transporter BtuB. Nat. Struct. Biol., 10, 394-401.
65. Cobessi, D., Celia, H., Folschweiller, N., Schalk, I. J., Abdallah, M. A., and Pattus, F. (2005) The crystal structure of the pyoverdine outer membrane receptor FpvA from Pseudomonas aeruginosa at 3.6 angstroms resolution. J. Mol. Biol., 347, 121-134.
66. Ferguson, A. D., Hofmann, E., Coulton, J. W., Diederichs, K., and Welte, W. (1998) Siderophore-mediated iron transport: crystal structure of FhuA with bound lipopolysaccharide. Science, 282, 2215-2220.
67. Baaden, M., and Sansom, M. S. P. (2004) OmpT: molecular dynamics simulations of an outer membrane enzyme. Biophys. J., 87, 2942-2953.
68. Khalid, S., and Sansom, M. S. P. (2006) Molecular dynamics simulations of a bacterial autotransporter: NalP from Neisseria meningitidis. Mol. Membr. Biol., 23, 499-508.
69. Buchanan, S. K. (2001) Type I secretion and multidrug efflux: transport through the TolC channel-tunnel. Trends Biochem. Sci., 26, 3-6.
70. Koronakis, V., Sharff, A., Koronakis, E., Luisi, B., and Hughes, C. (2000) Crystal structure of the bacterial membrane protein TolC central to multidrug efflux and protein export. Nature, 405, 914-919.
71. Akama, H., Kanemaki, M., Tsukihara, T., Nakagawa, A., and Nakae, T. (2004) Crystal structure of the drug discharge outer membrane protein, OprM, of Pseudomonas aeruginosa: dual modes of membrane anchoring and occluded cavity end. J. Biol. Chem., 279, 52816-52819.
72. Federici, L., Du, D., Walas, F., Matsumura, H., Fernandez-Recio, J., McKeegan, K. S., Borges-Walmsley, M. I., Luisi, B. F., and Walmsley, A. R. (2005) The crystal structure of the outer membrane protein VceC from the bacterial pathogen Vibrio cholerae at 1.8 Å resolution. J. Biol. Chem., 280, 15307-15314.
73. Murakami, S., Nakashima, R., Yamashita, E., and Yamaguchi, A. (2002) Crystal structure of bacterial multidrug efflux transporter AcrB. Nature, 419, 587-593.
74. Murakami, S., Nakashima, R., Yamashita, E., Matsumoto, T., and Yamaguchi, A. (2006) Crystal structures of a multidrug transporter reveal a functionally rotating mechanism. Nature, 443, 173-179.
75. Mikolosko, J., Bobyk, K., Zgurskaya, H. I., and Ghosh, P. (2006) Conformational flexibility in the multidrug efflux system protein AcrA. Structure, 14, 577-587.
76. Higgins, M. K., Bokma, E., Koronakis, E., Hughes, C., and Koronakis, V. (2004) The structure of the periplasmic component of a drug efflux pump. Proc. Natl. Acad. Sci. USA, 101, 9994-9999.
77. Akama, H., Matsuura, T., Kashiwagi, S., Yoneyama, H., Tsukihara, T., Nakagawa, A., and Nakae, T. (2004) Crystal structure of the membrane fusion protein, MexA, of the multidrug transporter in Pseudomonas aeruginosa. J. Biol. Chem., 279, 25939-25942.
78. Vaccaro, L., and Sansom, M. S. P. (2007) Gating at both ends and breathing in the middle: conformational dynamics of TolC. Biophys. J. (to be submitted).
79. Yildiz, O., Vinothkumar, K. R., Goswami, P., and Kühlbrandt, W. (2006) Structure of the monomeric outer-membrane porin OmpG in the open and closed conformation. EMBO J., 25, 3702-3713.
80. Saier, M. H., Jr., Beatty, J. T., Goffeau, A., Harley, K. T., Heijne, W. H., Huang, S. C., Jack, D. L., Jahn, P. S., Lew, K., Liu, J., Pao, S. S., Paulsen, I. T., Tseng, T. T., and Virk, P. S. (1999) The major facilitator superfamily. J. Mol. Microbiol. Biotechnol., 1, 257-279.
81. Abramson, J., Kaback, H. R., and Iwata, S. (2004) Structural comparison of lactose permease and the glycerol-3-phosphate antiporter: members of the major facilitator superfamily. Curr. Opin. Struct. Biol., 14, 413-419.
82. Guan, L., and Kaback, H. R. (2006) Lessons from lactose permease. Annu. Rev. Biophys. Biomol. Struct., 35, 67-91.
83. Holland, I. B., Cole, S. P. C., Kuchler, K., and Higgins, C. F. (2003), ABC proteins: From Bacteria to Man, Academic Press, London, UK.
84. Locher, K. P. (2004) Structure and mechanism of ABC transporters. Curr. Opin. Struct. Biol., 14, 426-431.
85. Dawson, R. J., and Locher, K. P. (2006) Structure of a bacterial multidrug ABC transporter. Nature, 443, 180-185.
86. Locher, K. P., Lee, A. T., and Rees, D. C. (2002) The E. coli BtuCD structure: a framework for ABC transporter architecture and mechanism. Science, 296, 1091-1098.
87. Abramson, J., Smirnova, I., Kasho, V., Verner, G., Kaback, H. R., and Iwata, S. (2003) Structure and mechanism of the lactose permease of Escherichia coli. Science, 301, 610-615.
88. Pinkett, H. W., Lee, A. T., Lum, P., Locher, K. P., and Rees, D. C. (2007) An inward-facing conformation of a putative metal-chelate-type ABC transporter. Science, 315, 373-377.
89. Chang, G., Roth, C. B., Reyes, C. L., Pornillos, O., Chen, Y. J., and Chen, A. P. (2006) Retraction. Science, 314, 1875.
90. Oloo, E. O., and Tieleman, D. P. (2004) Conformational transitions induced by the binding of MgATP to the vitamin B12 ATP-binding cassette (ABC) transporter BtuCD. J. Biol. Chem., 279, 45013-45019.
91. Borths, E. L., Locher, K. P., Lee, A. T., and Rees, D. C. (2002) The structure of Escherichia coli BtuF and binding to its cognate ATP binding cassette transporter. Proc. Natl. Acad. Sci. USA, 99, 16642-16647.
92. Ivetac, A., Campbell, J. D., and Sansom, M. S. P. (2007) Dynamics and function in a bacterial ABC transporter: simulation studies of the BtuCDF system and its components. Biochemistry, 46, 2767-2778.
93. Yin, Y., Jensen, M., Tajkhorshid, E., and Schulten, K. (2006) Sugar binding and protein conformational changes in lactose permease. Biophys. J., 91, 3972-3985.
94. Huang, Y., Lemieux, M. J., Song, J., Auer, M., and Wang, D. N. (2003) Structure and mechanism of the glycerol-3-phosphate transporter from Escherichia coli. Science, 301, 616-620.
95. Yin, Y., He, X., Szewczyk, P., Nguyen, T., and Chang, G. (2006) Structure of the multidrug transporter EmrD from Escherichia coli. Science, 312, 741-744.
96. Heymann, J. A., Sarker, R., Hirai, T., Shi, D., Milne, J. L., Maloney, P. C., and Subramaniam, S. (2001) Projection structure and molecular architecture of OxlT, a bacterial membrane transporter. EMBO J., 20, 4408-4413.
97. Guan, L., Smirnova, I. N., Verner, G., Nagamori, S., and Kaback, H. R. (2006) Manipulating phospholipids for crystallization of a membrane transport protein. Proc. Natl. Acad. Sci. USA, 103, 1723-1726.
98. Bennett, M., D'Rozario, R., Sansom, M. S. P., and Yeagle, P. L. (2006) Asymmetric stability among transmembrane helices of lactose permease. Biochemistry, 45, 8088-8095.
99. Holyoake, J., and Sansom, M. S. P. (2007) MD simulations of an MFS protein: LacY. Structure (submitted).
100. Haider, S., Hall, B. A., and Sansom, M. S. P. (2006) Simulations of a protein translocation pore: SecY. Biochemistry, 45, 13018-13024.
101. van den Berg, B., Clemons, W. M., Collinson, I., Modis, Y., Hartmann, E., Harrison, S. C., and Rapoport, T. A. (2004) X-ray structure of a protein- conducting channel. Nature, 427, 36-44.
102. Isralewitz, B., Baudry, J., Gullingsrud, J., Kosztin, D., and Schulten, K. (2001) Steered molecular dynamics investigations of protein function. J. Mol. Graphics Model., 19, 13-25.
103. Gumbart, J., and Schulten, K. (2006) Molecular dynamics studies of the archael translocon. Biophys. J., 90, 2356-2367.
104. Capener, C. E., Shrivastava, I. H., Ranatunga, K. M., Forrest, L. R., Smith, G. R., and Sansom, M. S. P. (2000) Homology modelling and molecular dynamics simulation studies of an inward rectifier potassium channel. Biophys. J., 78, 2929-2942.
105. Haider, S., Khalid, S., Tucker, S., Ashcroft, F. M., and Sansom, M. S. P. (2007) Molecular dynamics simulations of inwardly rectifying (Kir) potassium channels: a comparative study. Biochemistry, 46, 3643-3652.
106. Salas-Burgos, A., Iserovich, P., Zuniga, F., Vera, J. C., and Fischbarg, J. (2004) Predicting the three-dimensional structure of the human facilitative glucose transporter Glut1 by a novel evolutionary homology strategy. Biophys. J., 87, 2990-2999.
107. Vardy, E., Arkin, I. T., Gottschalk, K. E., Kaback, H. R., and Schuldiner, S. (2004) Structural conservation in the major facilitator superfamily as revealed by comparative modeling. Protein Sci., 13, 1832-1840.
108. Holyoake, J., Caulfeild, V., Baldwin, S. A., and Sansom, M. S. P. (2006) Modelling, docking and simulation of the major facilitator superfamily. Biophys. J., 91, L84-L86.
109. Faraldo-Gómez, J. D., Forrest, L. R., Baaden, M., Bond, P. J., Domene, C., Patargias, G., Cuthbertson, J., and Sansom, M. S. P. (2004) Conformational sampling and dynamics of membrane proteins from 10-nanosecond computer simulations. Proteins: Struct. Funct. Bioinf., 57, 783-791.
110. Shrivastava, I. H., and Bahar, I. (2006) Common mechanism of pore opening shared by five different potassium channels. Biophys. J., 90, 3929-3940.
111. Smart, O. S., Neduvelil, J. G., Wang, X., Wallace, B. A., and Sansom, M. S. P. (1996) Hole: A program for the analysis of the pore dimensions of ion channel structural models. J. Mol. Graph., 14, 354-360.