Simulating Gram-Negative Bacterial Outer Membrane: A Coarse Grain Model

Journal of Physical Chemistry B

Volumn 119, Issue 46, 2015, Pages 14668-14682

  Ma, Huilin ^a   Irudayanathan, Flaviyan Jerome ^a   Jiang, Wenjuan ^a   Nangia, Shikha ^a  

^a Syracuse University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMICROBIAL AGENTS; BACTERIA; BIOINFORMATICS; BIOLOGICAL MEMBRANES; CYTOLOGY; MACROMOLECULES; MICROORGANISMS; PHOSPHOLIPIDS; PHYSIOLOGY; PROTEINS;

ANTIMICROBIAL PEPTIDE; ATOMISTIC SIMULATIONS; COARSE-GRAINED FORCE FIELDS; GRAM-NEGATIVE BACTERIA; LIQUID CRYSTALLINE PHASE TRANSITION; MEMBRANE COMPOSITION; O-ANTIGEN POLYSACCHARIDES; TIME-SCALE SIMULATION;

MEMBRANES;

BIOLOGICAL MODEL; CELL MEMBRANE; GRAM NEGATIVE BACTERIUM; METABOLISM;

CELL MEMBRANE; GRAM-NEGATIVE BACTERIA; MODELS, BIOLOGICAL;

EID: 84947998007     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/acs.jpcb.5b07122     Document Type: Article

References (80)

1. Poole, K.; Krebes, K.; McNally, C.; Neshat, S. Multiple Antibiotic-Resistance in Pseudomonas-Aeruginosa-Evidence for Involvement of an Efflux Operon J. Bacteriol. 1993, 175, 7363-7372
2. Mah, T. F.; Pitts, B.; Pellock, B.; Walker, G. C.; Stewart, P. S.; OToole, G. A. A Genetic Basis for Pseudomonas Aeruginosa Biofilm Antibiotic Resistance Nature 2003, 426, 306-310 10.1038/nature02122
3. Fisher, J. F.; Meroueh, S. O.; Mobashery, S. Bacterial Resistance to Beta-Lactam Antibiotics: Compelling Opportunism, Compelling Opportunity Chem. Rev. 2005, 105, 395-424 10.1021/cr030102i
4. Thomson, J. M.; Bonomo, R. A. The Threat of Antibiotic Resistance in Gram-Negative Pathogenic Bacteria: Beta-Lactams in Peril! Curr. Opin. Microbiol. 2005, 8, 518-524 10.1016/j.mib.2005.08.014
5. Allen, H. K.; Donato, J.; Wang, H. H.; Cloud-Hansen, K. A.; Davies, J.; Handelsman, J. Call of the Wild: Antibiotic Resistance Genes in Natural Environments Nat. Rev. Microbiol. 2010, 8, 251-259 10.1038/nrmicro2312
6. Andersson, D. I.; Hughes, D. Antibiotic Resistance and Its Cost: Is It Possible to Reverse Resistance? Nat. Rev. Microbiol. 2010, 8, 260-271 10.1038/nrmicro2319
7. Hoiby, N.; Bjarnsholt, T.; Givskov, M.; Molin, S.; Ciofu, O. Antibiotic Resistance of Bacterial Biofilms Int. J. Antimicrob. Agents 2010, 35, 322-332 10.1016/j.ijantimicag.2009.12.011
8. Woodford, N.; Turton, J. F.; Livermore, D. M. Multiresistant Gram-Negative Bacteria: The Role of High-Risk Clones in the Dissemination of Antibiotic Resistance FEMS Microbiol. Rev. 2011, 35, 736-755 10.1111/j.1574-6976.2011.00268.x
9. Wellington, E. M. H.; Boxall, A. B. A.; Cross, P.; Feil, E. J.; Gaze, W. H.; Hawkey, P. M.; Johnson-Rollings, A. S.; Jones, D. L.; Lee, N. M.; Otten, W. et al. The Role of the Natural Environment in the Emergence of Antibiotic Resistance in Gram-Negative Bacteria Lancet Infect. Dis. 2013, 13, 155-165 10.1016/S1473-3099(12)70317-1
10. Graves, N.; Weinhold, D.; Tong, E.; Birrell, F.; Doidge, S.; Ramritu, P.; Halton, K.; Lairson, D.; Whitby, M. Effect of Healthcare-Acquired Infection on Length of Hospital Stay and Cost Infect. Control Hosp. Epidemiol. 2007, 28, 280-292 10.1086/512642
11. Roberts, R. R.; Scott, R. D., II; Hota, B.; Kampe, L. M.; Abbasi, F.; Schabowski, S.; Ahmad, I.; Ciavarella, G. G.; Cordell, R.; Solomon, S. L. et al. Costs Attributable to Healthcare-Acquired Infection in Hospitalized Adults and a Comparison of Economic Methods Med. Care 2010, 48, 1026-1035 10.1097/MLR.0b013e3181ef60a2
12. Delcour, A. H. Outer Membrane Permeability and Antibiotic Resistance Biochim. Biophys. Acta, Proteins Proteomics 2009, 1794, 808-816 10.1016/j.bbapap.2008.11.005
13. Costerton, J. W.; Ingram, J. M.; Cheng, K.-J. Structure and Function of the Cell Envelope of Gram-Negative Bacteria Bacteriol. Rev. 1974, 38, 87-110
14. Lugtenberg, B.; Vanalphen, L. Molecular Architecture and Functioning of the Outer-Membrane of Escherichia-Coli and Other Gram-Negative Bacteria Biochim. Biophys. Acta, Rev. Biomembr. 1983, 737, 51-115 10.1016/0304-4157(83)90014-X
15. Decad, G. M.; Nikaido, H. Outer Membrane of Gram-Negative Bacteria. XII. Molecular-Sieving Function of Cell-Wall J. Bacteriol. 1976, 128, 325-336
16. Benz, R.; Bauer, K. Permeation of Hydrophilic Molecules through the Outer-Membrane of Gram-Negative Bacteria-Review on Bacterial Porins Eur. J. Biochem. 1988, 176, 1-19 10.1111/j.1432-1033.1988.tb14245.x
17. Nikaido, H. Porins and Specific Channels of Bacterial Outer Membranes Mol. Microbiol. 1992, 6, 435-442 10.1111/j.1365-2958.1992.tb01487.x
18. Nikaido, H. Porins and Specific Diffusion Channels in Bacterial Outer Membranes J. Biol. Chem. 1994, 269, 3905-3908
19. Koebnik, R.; Locher, K. P.; Van Gelder, P. Structure and Function of Bacterial Outer Membrane Proteins: Barrels in a Nutshell Mol. Microbiol. 2000, 37, 239-253 10.1046/j.1365-2958.2000.01983.x
20. Voulhoux, R.; Bos, M. P.; Geurtsen, J.; Mols, M.; Tommassen, J. Role of a Highly Conserved Bacterial Protein in Outer Membrane Protein Assembly Science 2003, 299, 262-265 10.1126/science.1078973
21. Pages, J. M.; James, C. E.; Winterhalter, M. The Porin and the Permeating Antibiotic: A Selective Diffusion Barrier in Gram-Negative Bacteria Nat. Rev. Microbiol. 2008, 6, 893-903 10.1038/nrmicro1994
22. Caroff, M.; Karibian, D.; Cavaillon, J.-M.; Haeffner-Cavaillon, N. Structural and Functional Analyses of Bacterial Lipopolysaccharides Microbes Infect. 2002, 4, 915-926 10.1016/S1286-4579(02)01612-X
23. Erridge, C.; Bennett-Guerrero, E.; Poxton, I. R. Structure and Function of Lipopolysaccharides Microbes Infect. 2002, 4, 837-851 10.1016/S1286-4579(02)01604-0
24. Caroff, M.; Karibian, D. Structure of Bacterial Lipopolysaccharides Carbohydr. Res. 2003, 338, 2431-2447 10.1016/j.carres.2003.07.010
25. Zahringer, U.; Lindner, B.; Rietschel, E. T. Molecular-Structure of Lipid-a, the Endotoxic Center of Bacterial Lipopolysaccharides Adv. Carbohydr. Chem. Biochem. 1994, 50, 211-276 10.1016/S0065-2318(08)60152-3
26. Raetz, C. R. H.; Reynolds, C. M.; Trent, M. S.; Bishop, R. E. Lipid A Modification Systems in Gram-Negative Bacteria Annu. Rev. Biochem. 2007, 76, 295-329 10.1146/annurev.biochem.76.010307.145803
27. Kučerka, N.; Papp-Szabo, E.; Nieh, M.-P.; Harroun, T. A.; Schooling, S. R.; Pencer, J.; Nicholson, E. A.; Beveridge, T. J.; Katsaras, J. Effect of Cations on the Structure of Bilayers Formed by Lipopolysaccharides Isolated from Pseudomonas Aeruginosa PAO1 J. Phys. Chem. B 2008, 112, 8057-8062 10.1021/jp8027963
28. Knirel, Y. A.; Kochetkov, N. K. The Structure of Lipopolysaccharides of Gram-Negative Bacteria. III. The Structure of O-Antigens-A Review Biochemistry (Moscow) 1994, 59, 1325-1383
29. Feldman, M. F.; Wacker, M.; Hernandez, M.; Hitchen, P. G.; Marolda, C. L.; Kowarik, M.; Morris, H. R.; Dell, A.; Valvano, M. A.; Aebi, M. Engineering N-Linked Protein Glycosylation with Diverse O Antigen Lipopolysaccharide Structures in Escherichia Coli Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 3016-3021 10.1073/pnas.0500044102
30. Stenutz, R.; Weintraub, A.; Widmalm, G. The Structures of Escherichia Coli O-Polysaccharide Antigens FEMS Microbiol. Rev. 2006, 30, 382-403 10.1111/j.1574-6976.2006.00016.x
31. Kang, Y.; Barbirz, S.; Lipowsky, R.; Santer, M. Conformational Diversity of O-Antigen Polysaccharides of the Gram-Negative Bacterium Shigella Flexneri Serotype Y J. Phys. Chem. B 2014, 118, 2523-2534 10.1021/jp4111713
32. Parkin, J.; Khalid, S.; van den Berg, B. Identifying the Pathways to Permeation through Occd1 in the Outer Membranes of P. Aeruginosa Biophys. J. 2013, 104, 407A-407A 10.1016/j.bpj.2012.11.2271
33. Eren, E.; Vijayaraghavan, J.; Liu, J.; Cheneke, B. R.; Touw, D. S.; Lepore, B. W.; Indic, M.; Movileanu, L.; van den Berg, B. Substrate Specificity within a Family of Outer Membrane Carboxylate Channels PLoS Biol. 2012, 10, e1001242 10.1371/journal.pbio.1001242
34. Eren, E.; Parkin, J.; Adelanwa, A.; Cheneke, B.; Movileanu, L.; Khalid, S.; van den Berg, B. Toward Understanding the Outer Membrane Uptake of Small Molecules by Pseudomonas Aeruginosa J. Biol. Chem. 2013, 288, 12042-12053 10.1074/jbc.M113.463570
35. Abraham, T.; Schooling, S. R.; Nieh, M.-P.; Kucerka, N.; Beveridge, T. J.; Katsaras, J. Neutron Diffraction Study of Pseudomonas Aeruginosa Lipopolysaccharide Bilayers J. Phys. Chem. B 2007, 111, 2477-2483 10.1021/jp066012+
36. Labischinski, H.; Vorgel, E.; Uebach, W.; May, R. P.; Bradaczek, H. Architecture of Bacterial Lipid-a in Solution-a Neutron Small-Angle Scattering Study Eur. J. Biochem. 1990, 190, 359-363 10.1111/j.1432-1033.1990.tb15583.x
37. Brandenburg, K.; Seydel, U. Investigation into the Fluidity of Lipopolysaccharide and Free Lipid-a Membrane Systems by Fourier-Transform Infrared-Spectroscopy and Differential Scanning Calorimetry Eur. J. Biochem. 1990, 191, 229-236 10.1111/j.1432-1033.1990.tb19114.x
38. Bosch, A.; Minan, A.; Vescina, C.; Degrossi, J.; Gatti, B.; Montanaro, P.; Messina, M.; Franco, M.; Vay, C.; Schmitt, J. et al. Fourier Transform Infrared Spectroscopy for Rapid Identification of Nonfermenting Gram-Negative Bacteria Isolated from Sputum Samples from Cystic Fibrosis Patients J. Clin. Microbiol. 2008, 46, 2535-2546 10.1128/JCM.02267-07
39. Jo, H.; Jeong, E. Y.; Jeon, J.; Ban, C. Structural Insights into Escherichia Coli Polymyxin B Resistance Protein D with X-Ray Crystallography and Small-Angle X-Ray Scattering BMC Struct. Biol. 2014, 14, 24 10.1186/s12900-014-0024-y
40. Arora, A.; Abildgaard, F.; Bushweller, J. H.; Tamm, L. K. Structure of Outer Membrane Protein a Transmembrane Domain by NMR Spectroscopy Nat. Struct. Biol. 2001, 8, 334-338 10.1038/86214
41. Stukalov, O.; Korenevsky, A.; Beveridge, T. J.; Dutcher, J. R. Use of Atomic Force Microscopy and Transmission Electron Microscopy for Correlative Studies of Bacterial Capsules Appl. Environ. Microbiol. 2008, 74, 5457-5465 10.1128/AEM.02075-07
42. Ramos, J. L.; Gallegos, M. a.-T.; Marqués, S.; Ramos-González, M.-I.; Espinosa-Urgel, M.; Segura, A. Responses of Gram-Negative Bacteria to Certain Environmental Stressors Curr. Opin. Microbiol. 2001, 4, 166-171 10.1016/S1369-5274(00)00183-1
43. Soares, T. A.; Straatsma, T. P. Assessment of the Convergence of Molecular Dynamics Simulations of Lipopolysaccharide Membranes Mol. Simul. 2008, 34, 295-307 10.1080/08927020701829880
44. Straatsma, T. P.; Soares, T. A. Characterization of the Outer Membrane Protein Oprf of Pseudomonas Aeruginosa in a Lipopolysaccharide Membrane by Computer Simulation Proteins: Struct., Funct., Genet. 2009, 74, 475-488 10.1002/prot.22165
45. Kirschner, K. N.; Lins, R. D.; Maass, A.; Soares, T. A. A Glycam-Based Force Field for Simulations of Lipopolysaccharide Membranes: Parametrization and Validation J. Chem. Theory Comput. 2012, 8, 4719-4731 10.1021/ct300534j
46. Pontes, F. J. S.; Rusu, V. H.; Soares, T. A.; Lins, R. D. The Effect of Temperature, Cations, and Number of Acyl Chains on the Lamellar to Non-Lamellar Transition in Lipid-a Membranes: A Microscopic View J. Chem. Theory Comput. 2012, 8, 3830-3838 10.1021/ct300084v
47. Wu, E. L.; Engstrom, O.; Jo, S.; Stuhlsatz, D.; Yeom, M. S.; Klauda, J. B.; Widmalm, G.; Im, W. Molecular Dynamics and Nmr Spectroscopy Studies of E. Coli Lipopolysaccharide Structure and Dynamics Biophys. J. 2013, 105, 1444-1455 10.1016/j.bpj.2013.08.002
48. Dias, R. P.; da Hora, G. C. A.; Ramstedt, M.; Soares, T. A. Outer Membrane Remodeling: The Structural Dynamics and Electrostatics of Rough Lipopolysaccharide Chemotypes J. Chem. Theory Comput. 2014, 10, 2488-2497 10.1021/ct500075h
49. Dias, R. P.; Li, L.; Soares, T. A.; Alexov, E. Modeling the Electrostatic Potential of Asymmetric Lipopolysaccharide Membranes: The Mempot Algorithm Implemented in Delphi J. Comput. Chem. 2014, 35, 1418-1429 10.1002/jcc.23632
50. Nascimento, A., Jr.; Pontes, F. J. S.; Lins, R. D.; Soares, T. A. Hydration, Ionic Valence and Cross-Linking Propensities of Cations Determine the Stability of Lipopolysaccharide (LPS) Membranes Chem. Commun. 2014, 50, 231-233 10.1039/C3CC46918B
51. Brooks, B. R.; Brooks, C. L., 3rd; Mackerell, A. D., Jr.; Nilsson, L.; Petrella, R. J.; Roux, B.; Won, Y.; Archontis, G.; Bartels, C.; Boresch, S. et al. CHARMM: The Biomolecular Simulation Program J. Comput. Chem. 2009, 30, 1545-1614 10.1002/jcc.21287
52. Liu, P.; Izvekov, S.; Voth, G. A. Multiscale Coarse-Graining of Monosaccharides J. Phys. Chem. B 2007, 111, 11566-11575 10.1021/jp0721494
53. Marrink, S. J.; Risselada, H. J.; Yefimov, S.; Tieleman, D. P.; de Vries, A. H. The Martini Force Field: Coarse Grained Model for Biomolecular Simulations J. Phys. Chem. B 2007, 111, 7812-7824 10.1021/jp071097f
54. Monticelli, L.; Kandasamy, S. K.; Periole, X.; Larson, R. G.; Tieleman, D. P.; Marrink, S. J. The Martini Coarse-Grained Force Field: Extension to Proteins J. Chem. Theory Comput. 2008, 4, 819-834 10.1021/ct700324x
55. Apajalahti, T.; Niemela, P.; Govindan, P. N.; Miettinen, M. S.; Salonen, E.; Marrink, S.-J.; Vattulainen, I. Concerted Diffusion of Lipids in Raft-Like Membranes Faraday Discuss. 2010, 144, 411-430 10.1039/B901487J
56. Lopez, C. A.; Rzepiela, A. J.; de Vries, A. H.; Dijkhuizen, L.; Huenenberger, P. H.; Marrink, S. J. Martini Coarse-Grained Force Field: Extension to Carbohydrates J. Chem. Theory Comput. 2009, 5, 3195-3210 10.1021/ct900313w
57. Lopez, C. A.; Sovova, Z.; van Eerden, F. J.; de Vries, A. H.; Marrink, S. J. Martini Force Field Parameters for Glycolipids J. Chem. Theory Comput. 2013, 9, 1694-1708 10.1021/ct3009655
58. Nangia, S.; Sureshkumar, R. Effects of Nanoparticle Charge and Shape Anisotropy on Translocation through Cell Membranes Langmuir 2012, 28, 17666-17671 10.1021/la303449d
59. Gkeka, P.; Angelikopoulos, P. The Role of Patterned Hydrophilic Domains in Nanoparticle-Membrane Interactions Curr. Nanosci. 2011, 7, 690-698 10.2174/157341311797483754
60. Sangwai, A. V.; Sureshkumar, R. Coarse-Grained Molecular Dynamics Simulations of the Sphere to Rod Transition in Surfactant Micelles Langmuir 2011, 27, 6628-6638 10.1021/la2006315
61. Rossi, G.; Giannakopoulos, I.; Monticelli, L.; Rostedt, N. K. J.; Puisto, S. R.; Lowe, C.; Taylor, A. C.; Vattulainen, I.; Ala-Nissila, T. A Martini Coarse-Grained Model of a Thermoset Polyester Coating Macromolecules 2011, 44, 6198-6208 10.1021/ma200788a
62. Rossi, G.; Monticelli, L.; Puisto, S. R.; Vattulainen, I.; Ala-Nissila, T. Coarse-Graining Polymers with the Martini Force-Field: Polystyrene as a Benchmark Case Soft Matter 2011, 7, 698-708 10.1039/C0SM00481B
63. Jiang, W.; Luo, J.; Nangia, S. Multiscale Approach to Investigate Self-Assembly of Telodendrimer Based Nanocarriers for Anticancer Drug-Delivery Langmuir 2015, 31, 4270-4280 10.1021/la503949b
64. Jorgensen, W. L.; Chandrasekhar, J.; Madura, J. D.; Impey, R. W.; Klein, M. L. Comparison of Simple Potential Functions for Simulating Liquid Water J. Chem. Phys. 1983, 79, 926-935 10.1063/1.445869
65. Evans, D. A. History of the Harvard Chemdraw Project Angew. Chem., Int. Ed. 2014, 53, 11140-11145 10.1002/anie.201405820
66. Schuttelkopf, A. W.; van Aalten, D. M. Prodrg: A Tool for High-Throughput Crystallography of Protein-Ligand Complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 2004, 60, 1355-1363 10.1107/S0907444904011679
67. Hess, B.; Kutzner, C.; van der Spoel, D.; Lindahl, E. Gromacs 4: Algorithms for Highly Efficient, Load-Balanced, and Scalable Molecular Simulation J. Chem. Theory Comput. 2008, 4, 435-447 10.1021/ct700301q
68. Pronk, S.; Páll, S.; Schulz, R.; Larsson, P.; Bjelkmar, P.; Apostolov, R.; Shirts, M. R.; Smith, J. C.; Kasson, P. M.; van der Spoel, D. et al. Gromacs 4.5: A High-Throughput and Highly Parallel Open Source Molecular Simulation Toolkit Bioinformatics 2013, 29, 845-854 10.1093/bioinformatics/btt055
69. Wassenaar, T. A.; Ingólfsson, H. I.; Böckmann, R. A.; Tieleman, D. P.; Marrink, S. J. Computational Lipidomics with Insane: A Versatile Tool for Generating Custom Membranes for Molecular Simulations J. Chem. Theory Comput. 2015, 11, 2144-2155 10.1021/acs.jctc.5b00209
70. Yesylevskyy, S. O.; Schafer, L. V.; Sengupta, D.; Marrink, S. J. Polarizable Water Model for the Coarse-Grained Martini Force Field PLoS Comput. Biol. 2010, 6, e1000810 10.1371/journal.pcbi.1000810
71. Vermeer, L.; de Groot, B.; Réat, V.; Milon, A.; Czaplicki, J. Acyl Chain Order Parameter Profiles in Phospholipid Bilayers: Computation from Molecular Dynamics Simulations and Comparison with 2h Nmr Experiments Eur. Biophys. J. 2007, 36, 919-931 10.1007/s00249-007-0192-9
72. Marrink, S. J.; de Vries, A. H.; Mark, A. E. Coarse Grained Model for Semiquantitative Lipid Simulations J. Phys. Chem. B 2004, 108, 750-760 10.1021/jp036508g
73. Leekumjorn, S.; Sum, A. K. Molecular Studies of the Gel to Liquid-Crystalline Phase Transition for Fully Hydrated DPPC and DPPE Bilayers Biochim. Biophys. Acta, Biomembr. 2007, 1768, 354-365 10.1016/j.bbamem.2006.11.003
74. Lomize, A. L.; Pogozheva, I. D.; Mosberg, H. I. Anisotropic Solvent Model of the Lipid Bilayer. 2. Energetics of Insertion of Small Molecules, Peptides, and Proteins in Membranes J. Chem. Inf. Model. 2011, 51, 930-946 10.1021/ci200020k
75. Periole, X.; Cavalli, M.; Marrink, S.-J.; Ceruso, M. A. Combining an Elastic Network with a Coarse-Grained Molecular Force Field: Structure, Dynamics, and Intermolecular Recognition J. Chem. Theory Comput. 2009, 5, 2531-2543 10.1021/ct9002114
76. Parrinello, M.; Rahman, A. Polymorphic Transitions in Single Crystals: A New Molecular Dynamics Method J. Appl. Phys. 1981, 52, 7182-7190 10.1063/1.328693
77. Brandenburg, K.; Seydel, U. Orientation Measurements on Membrane Systems Made from Lipopolysaccharides and Free Lipid-A by FT-IR Spectroscopy Eur. Biophys. J. 1988, 16, 83-94 10.1007/BF00255517
78. Nakayama, H.; Mitsui, T.; Nishihara, M.; Kito, M. Relation between Growth Temperature of E. Coli and Phase Transition Temperatures of its Cytoplasmic and Outer Membranes Biochim. Biophys. Acta, Biomembr. 1980, 601, 1-10 10.1016/0005-2736(80)90508-8
79. Sinensky, M. Homeoviscous Adaptation - a Homeostatic Process That Regulates the Viscosity of Membrane Lipids in Escherichia Coli Proc. Natl. Acad. Sci. U. S. A. 1974, 71, 522-525 10.1073/pnas.71.2.522
80. Wassenaar, T. A.; Pluhackova, K.; Böckmann, R. A.; Marrink, S. J.; Tieleman, D. P. Going Backward: A Flexible Geometric Approach to Reverse Transformation from Coarse Grained to Atomistic Models J. Chem. Theory Comput. 2014, 10, 676-690 10.1021/ct400617g