The simulation approach to bacterial outer membrane proteins (Review)

References

• Arinaminpathy, Y., Biggin, P. C., Bond, P. J., Domene, C., Pang, A. and Sansom, M. S. P., 2003, Large scale biomolecular simula- tions: current status and future prospects. In Proceedings of the UK e-Science All Hands Meeting 2003. Simon J. Cox, ed. (Nottingham), pp. 901 –907.
   Google Scholar
• Arora, A. and Tamm, L. K., 2001, Biophysical approaches tomembrane protein structure determination. Curr. Opin. Struct. Biol., 11, 540 –547.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• Arora, A., Abildgaard, F., Bushweller, J. H. and Tamm, L. K., 2001,Structure of outer membrane protein A transmembrane domain by NMRspectroscopy. Nat. Struct. Biol., 8, 334 -338.
   Google Scholar
• Baaden, M., Meier, C. and Sansom, M. S. P., 2003, A molecular dynamics investigation of mono and dimeric states of the outer membrane enzyme OMPLA. J. Mol. Biol., 331, 177 –189.Bainbridge, G., Gokce, I. and Lakey, J. H., 1998, Voltage gating is a fundamental feature of porin and toxin beta-barrel membrane channels. FEBS Lett., 431, 305 –308.
   Google Scholar
• Benz, J. and Hofmann, A., 1997, Annexins: from structure tofunction. Biol. Chem., 378, 177 –183.
   PubMedGoogle Scholar
• Bjo¨rkste´n, J., Soares, C. M., Nilsson, O. and Tapia, O., 1994, On the stability and plastic properties of the interior L3 loop in R.capsu- latus porin. A molecular dynamics study. Prot. Eng., 7, 487 –493. Bond, P. and Sansom, M. S. P., 2003, Membrane protein dynamics vs. environment: simulations of OmpA in a micelle and in abilayer. J. Mol. Biol., 329, 1035–1053.
   Google Scholar
• Bond, P., Faraldo-Gome´ z, J. and Sansom, M. S. P., 2002, OmpA * A pore or not a pore? Simulation and modelling studies. Biophys. J., 83, 763 –775.
   Google Scholar
• 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. Nat. Struct. Biol., 6, 56 –63.
   Google Scholar
• Chimento, D. P., Mohanty, A. K., Kadner, R. J. and Wiener, M. C., 2003, Substrate-induced transmembrane signaling in the cobala- min transporter BtuB. Nat. Struct. Biol., 10, 394 –401.
   PubMedGoogle Scholar
• Chowdhury, S., Lee, M. C., Xiong, G. and Duan, Y., 2003, Ab initio folding simulation of the trp-cage mini-protein approaches NMR resolution. J. Mol. Biol., 327, 711 –717.
   PubMed Web of Science ®Google Scholar
• Chung, S. H. and Kuyucak, S., 2002, Ion channels: recent progress and prospects. Eur. Biophys. J., 31, 283 –293.
   Google Scholar
• Danelon, C., Suenaga, A., Winterhalter, M. and Yamato, I., 2003, Molecular origin of the cation selectivity in OmpF porin: single channel conductances vs. free energy calculation. Biophys. Chem., 104, 591 –603.
   PubMed Web of Science ®Google Scholar
• Davis, M. E. and McCammon, J. A., 1990, Electrostatics in biomolecular structure and dynamics. Chem. Rev., 90, 509 –521. Domene, C., Bond, P. and Sansom, M. S. P., 2003a, Membrane protein simulation: ion channels and bacterial outer membrane proteins. Adv. Prot. Chem., 66, 159 -193.
   Google Scholar
• Domene, C., Bond, P. J., Deol, S. S. and Sansom, M. S. P., 2003b, Lipid-protein interactions and the membrane/water interfacial region. J. Amer. Chem. Soc., 125, 14966–14967.
   Google Scholar
• Dutzler, R., Rummel, G., Albertı´, S., Herna´ ndez-Alle´ s, S., Phale, P. S., Rosenbusch, J. P., Benedı´, V. J. and Schirmer, T., 1999, Crystal structure and functional characterization of OmpK36, the osmoporin of Klebsiella pneumoniae. Structure, 7, 425 –434.
   Google Scholar
• Dutzler, R., Schirmer, T., Karplus, M. and Fischer, S., 2002, Translocation mechanism of long sugar chains across the maltoporin membrane channel. Structure, 10, 1273 -1284.
   Google Scholar
• Dutzler, R., Campbell, E. B. and MacKinnon, R., 2003, Gating the selectivity filter in ClC chloride channels. Science, 300, 108 –112. Faraldo-Go´ mez, J. D. and Sansom, M. S. P., 2003, Acquisition of siderophores in gram-negative bacteria. Nat. Rev. Mol. Cell. Biol. ,4, 105 –115.
   Google Scholar
• Faraldo-Go´mez, J., Smith, G. R. and Sansom, M. S. P., 2002, Setup and optimisation of membrane protein simulations. Eur. Biophys. J., 31, 217 –227.
   PubMed Web of Science ®Google Scholar
• Faraldo-Go´mez, J., 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.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Ferguson, A. D., Welte, W., Hofmann, E., Lindner, B., Holst, O., Coulton, J. W. and Diederichs, K., 2000, A conserved structural motif for lipopolysaccharide recognition by procaryotic and eucaryotic proteins. Struct. Fold. Des., 8, 585 –592.
   Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Faraldo-Go´mez, C. and Wu¨ thrich, K., 2003, NMRsolution structure determination of membrane proteins reconstituted in detergent micelles. FEBS Lett., 555, 144 –150.
   Google Scholar
• Forrest, L. R. and Sansom, M. S. P., 2000, Membrane simulations: bigger and better? Curr. Opin. Struct. Biol., 10, 174 –181.
   PubMed Web of Science ®Google Scholar
• Fyfe, P. K., McAuley, K. E., Roszak, A. W., Isaacs, N. W., Codgell, R. J. and Jones, M. R., 2001, Probing the interface between membrane proteins and membrane lipids by X-ray crystallogra- phy. Trends Biochem. Sci., 26, 106 –112.
   Google Scholar
• Halgren, T. A. and Damm, W., 2001, Polarizable force fields. Curr.Opin. Struct. Biol., 11, 236 –242.
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A. and Schulten, K., 1996, VMD *Visual Molecular Dynamics. J. Molec. Graph., 14, 33 -38.
   PubMed Web of Science ®Google Scholar
• Im, W. and Roux, B., 2001, Brownian dynamics simulations of ion channels: a general treatment of electrostatic reaction fields for molecular pores of arbitrary geometry. J. Chem. Phys., 115, 4850–4861.
   Web of Science ®Google Scholar
• Im, W. and Roux, B., 2002a, 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.
   PubMed Web of Science ®Google Scholar
• Im, W. and Roux, B., 2002b, 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.
   PubMed Web of Science ®Google Scholar
• Im, W. and Roux, B., 2002c, 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.
   PubMed Web of Science ®Google Scholar
• Im, W., Seefeld, S. and Roux, B., 2000, Grand canonical Monte Carlo-Brownian dynamics algorithm for simulating ion channels. Biophys. J., 79, 788 –801.
   PubMed Web of Science ®Google Scholar
• Karplus, M. and McCammon, J. A., 2002a, Molecular dynamics simulations of biomolecules. Nat. Struct. Biol., 9, 646 –652.
   PubMedGoogle Scholar
• Karplus, M. J. and McCammon, J. A., 2002b, Molecular dynamics simulations of biomolecules. Nat. Struct. Biol., 9, 646 –652.
   PubMedGoogle Scholar
• Karshikoff, A., Spassov, V., Cowan, S. W., Ladenstein, R. and Schirmer, T., 1994, Electrostatic properties of two porin channels from Escherichia coli. J. <i>Mol. Biol., 240, 372 –384.
   Google Scholar
• Killian, J. A. and von Heijne, G., 2000, How proteins adapt to a membrane-water interface. Trends Biochem. Sci., 25, 429 –434. Koebnik, R., Locher, K. P. and Van Gelder, P., 2000, Structure and function of bacterial outer membrane proteins: barrels in a
   Google Scholar
• nutshell. Mol. Microbiol., 37, 239 -253.
   Google Scholar
• 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.
   Google Scholar
• Lee, A. G., 2003, Lipid-protein interactions in biological membranes: a structural perspective. Biochim. Biophys. Acta, 1612, 1 -40.
   Google Scholar
• Lins, R. D. and Straatsma, T. P., 2001, Computer simulation of the rough lipopolysaccharide membrane of Pseudomonas aerugi- nosa. Biophys. J., 81, 1037 -1046.
   PubMed Web of Science ®Google Scholar
• Locher, K. P., Rees, B., Koebnik, R., Mitschler, A., Moulinier, L., Rosenbusch, J. and Moras, D., 1998, Transmembrane signalling across the ligand-gated FhuA receptor; crystal structures of free and ferrichrome-bound states reveal allosteric changes. Cell, 95, 771 –778.
   PubMed Web of Science ®Google Scholar
• Merz, K. M. and Roux, B., 1996, Biological Membranes: A Molecular Perspective from Computation and Experiment (Birkha¨ user, Boston).
   Google Scholar
• Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T., Nouwens,
   Google Scholar
• A. S., Williams, K. L. and Gooley, A. A., 2000, Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem., 267, 2871 –2881.
   Google Scholar
• Nicholls, A., Sharp, K. A. and Honig, B., 1991, Protein folding and association: insights from the interfacial thermodynamic proper- ties of hydrocarbons. Proteins: Struct. Func. Genet., 11, 281 - 296.
   Google Scholar
• Nikaido, H., 2003, Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Molec. Biol. Rev., 67, 593 –656. Pautsch, A. and Schulz, G. E., 1998, Structure of the outer membrane protein A transmembrane domain. Nat. Struct. Biol., 5, 1013 –1017.
   Google Scholar
• Pautsch, A. and Schulz, G. E., 2000, High-resolution structure of the OmpA membrane domain. J. Mol. Biol., 298, 273 –282.
   PubMed Web of Science ®Google Scholar
• Phale, P. S., Schirmer, T., Prilipov, A., Lou, J.-L., Hardmeyer, A. and Rosenbusch, J. P., 1997, Voltage gating of Escherichia coli porin channels: role of the constriction loop. Proc. Natl Acad. Sci. USA, 94, 6741–6745.
   PubMedGoogle Scholar
• Phale, P. S., Philippsen, A., Widmer, C., Phale, V. P., Rosenbusch, J. P. and Schirmer, T., 2001, Role of charged residues at the OmpF porin channel constriction probed by mutagenesis and simulation. Biochemistry, 40, 6319 -6325.
   Google Scholar
• Prince, S. M., Achtman, M. and Derrick, J. P., 2002, Crystal structure of the OpcA integral membrane adhesin from Neisseria meningi- tidis. Proc. Natl Acad. <i>Sci. USA, 99, 3417 -3421.
   Google Scholar
• Robertson, K. M. and Tieleman, D. P., 2002, Orientation and interactions of dipolar molecules during transport through OmpF porin. FEBS Lett., 528, 53 –57.
   Google Scholar
• Roux, B., Berne` che, S. and Im, W., 2000, Ion channels, permeation and electrostatics: insight into the function of KcsA. Biochemistry, 39, 13295 –13306.
   Google Scholar
• Schirmer, T., 1998, General and specific porins from bacterial outer membranes. J. Struct. Biol., 121, 101 –109.
   PubMedGoogle Scholar
• Schirmer, T. and Phale, P. S., 1999, Brownian dynamics simulation of ion flow through porin channels. J. Mol. Biol., 294, 1159 –1167. Schroll, R. M. and Straatsma, T. P., 2002, Molecular structure of the outer bacterial membrane of Pseudomonas aeruginosa viaclassical simulation. Biopolymers, 65, 395 –407.
   Google Scholar
• Schulz, G. E., 2000, b-Barrel membrane proteins. Curr. Opin. Struct.Biol., 10, 443 –447.
   PubMed Web of Science ®Google Scholar
• Scott, D. C., Newton, S. M. C. and Klebba, P. E., 2002, Surface loop motion in FepA. J. Bacteriol., 184, 4906 -4911.
   Google Scholar
• Simmerling, C., Strockbine, B. and Roitberg, A. E., 2002, All-atom structure prediction and folding simulations of a stable protein. J. Am. Chem. Soc., 124, 11258–11259.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• Snijder, H. J. and Dijkstra, B. W., 2000, Bacterial phospholipase A: structure and function of an integral membrane phospholipase. Biochim. Biophys. Acta, 1488, 91 –101.
   Google Scholar
• Snijder, H. J., Ubarretxena-Belandia, I., Blaauw, M., Kalk, K. H., Verheij, H. M., Egmond, M. R., Dekker, N. and Dijkstra, B. W., 1999, Structural evidence for dimerization-regulated activation of an integral membrane phospholipase. Nature, 401, 717 –721.
   PubMedGoogle Scholar
• Snijder, H. J., Kingma, R. L., Kalk, K. H., Dekker, N., Egmond, M. R. and Dijkstra, B. W., 2001, Structural investigations of calcium binding and its role in activity and activation of outer membrane phospholipase A from Escherichia coli. J. Mol. Biol., 309, 477 - 489.Soares, C. M., Bjo¨ rkste´ n, J. and Tapia, O., 1995, L3 loop-mediated mechanisms of pore closing in porin: a molecular dynamics perturbation approach. Prot. Eng., 8, 5 –12.
   Google Scholar
• Suenaga, A., Komeiji, Y., Uebayasi, M., Meguro, T., Saito, M. and Yamato, I., 1998, Compuation observation of an ion permeation through a channel protein. Biosci. Reports, 18, 39 –48.
   Google Scholar
• Tamm, L. K., Abildgaard, F., Arora, A., Blad, H. and Bushweller, J. H., 2003, Structure, dynamics and function of the outer mem- brane protein A (OmpA) and influenza hemagglutinin fusion domain in detergent micelles by solution NMR. FEBS Lett., 555, 139 –143.
   PubMed Web of Science ®Google Scholar
• 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 bi- layer. Biophys. J., 74, 2786 -2801.
   PubMed Web of Science ®Google Scholar
• Tieleman, D. P., Marrink, S. J. and Berendsen, H. J. C., 1997, A computer perspective of membranes: molecular dynamics studies of lipid bilayer systems. Biochim. Biophys. Acta, 1331, 235 –270. Tieleman, D. P., Forrest, L. R., Berendsen, H. J. C. and Sansom, M. S. P., 1999, Lipid properties and the orientation of aromatic residues in OmpF, influenza M2 and alamethicin systems: molecular dynamics simulations. Biochem., 37, 17554–17561.
   Google Scholar
• Tobias, D. J., Tu, K. C. and Klein, M. L., 1997, Atomic-scale molecular dynamics simulations of lipid membranes. Curr. Opin. Coll. Interface Sci., 2, 15 –26.
   Web of Science ®Google Scholar
• Vandeputte-Rutten, L., Kramer, R. A., Kroon, J., Dekker, N., Egmond, M. R. and Gros, P., 2001a, Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J., 20, 5033 -5039.
   PubMed Web of Science ®Google Scholar
• Vandeputte-Rutten, L., Kramer, R. A., Kroon, J., Dekker, N., Egmond, M. R. and Gros, P., 2001b, Crystal structure of the outer membrane protease OmpT from Escherichia coli suggests a novel catalytic site. EMBO J., 20, 5033 -5039.
   PubMed Web of Science ®Google Scholar
• Watanabe, M., Rosenbusch, J., Schirmer, T. and Karplus, M., 1997, Computer simulations of the OmpF porin from the outer mem- brane of Escherichia coli. Biophys. J., 72, 2094 -2102.
   PubMedGoogle Scholar
• Weiss, M. S., Abele, U., Weckesser, J., Welte, W., Schiltz, E. and Schulz, G. E., 1991, Molecular architecture and electrostatic properties of a bacterial porin. Science, 254, 1627 -1630.
   PubMed Web of Science ®Google Scholar
• Wimley, W. C., 2003, The versatile b-barrel membrane protein. Curr.Opin. Struct. Biol., 13, 404 –411.
   PubMed Web of Science ®Google Scholar
• Yau, W. M., Wimley, W. C., Gawrisch, K. and White, S. H., 1998, The preference of tryptophan for membrane interfaces. Biochem., 37, 14713–14718.
   PubMed Web of Science ®Google Scholar
• Zachariae, U., Koumanov, A., Engelhardt, H. and Karshikoff, A., 2002, Electrostatic properties of the anion selective porin Omp32 from Delftia acidovorans and of the arginine cluster of bacterial porins. Prot. Sci., 11, 1309 -1319.
   Google Scholar
• Zachariae, U., Helms, V. and Engelhardt, H., 2003, Multistep mechanism of chloride translocation in a strongly anion-selective porin channel. Biophys. J., 85, 954 –962.
   Google Scholar