Effect of Local Stress on Accurate Modeling of Bacterial Outer Membranes Using All-Atom Molecular Dynamics

Pirhadi, Emad; Vanegas, Juan M.; Farin, Mithila; Schertzer, Jeffrey W.; Yong, Xin

doi:10.1021/acs.jctc.2c01026

Effect of Local Stress on Accurate Modeling of Bacterial Outer Membranes Using All-Atom Molecular Dynamics

Journal Article · 29 December 2022 · Journal of Chemical Theory and Computation

DOI:https://doi.org/10.1021/acs.jctc.2c01026· OSTI ID:2425413

Pirhadi, Emad ^[1]; Vanegas, Juan M. ^[2]; Farin, Mithila ^[1]; Schertzer, Jeffrey W. ^[3]; ^[1]

Department of Mechanical Engineering, Binghamton University, Binghamton, New York 13902-6000, United States
Department of Biochemistry and Biophysics, Oregon State University, Corvallis, Oregon 97331-4003, United States
Department of Biological Sciences, Binghamton University, Binghamton, New York 13902-6000, United States

Not provided.

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States). Center for Functional Nanomaterials (CFN)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0012704

OSTI ID:: 2425413

Journal Information:: Journal of Chemical Theory and Computation, Journal Name: Journal of Chemical Theory and Computation Journal Issue: 1 Vol. 19; ISSN 1549-9618

Publisher:: American Chemical Society

Country of Publication:: United States

Language:: English

References (88)

Curvature and Hydrophobic Forces Drive Oligomerization and Modulate Activity of Rhodopsin in Membranes Botelho, Ana Vitória; Huber, Thomas; Sakmar, Thomas P. Biophysical Journal, Vol. 91, Issue 12 https://doi.org/10.1529/biophysj.106.082776	journal	December 2006
Spontaneous Curvature, Differential Stress, and Bending Modulus of Asymmetric Lipid Membranes Hossein, Amirali; Deserno, Markus Biophysical Journal, Vol. 118, Issue 3 https://doi.org/10.1016/j.bpj.2019.11.3398	journal	February 2020
Ca2+-dependent mechanism of membrane insertion and destabilization by the SARS-CoV-2 fusion peptide Khelashvili, George; Plante, Ambrose; Doktorova, Milka Biophysical Journal, Vol. 120, Issue 6 https://doi.org/10.1016/j.bpj.2021.02.023	journal	March 2021
Nonphysical sampling distributions in Monte Carlo free-energy estimation: Umbrella sampling Torrie, G. M.; Valleau, J. P. Journal of Computational Physics, Vol. 23, Issue 2 https://doi.org/10.1016/0021-9991(77)90121-8	journal	February 1977
The bacterial outer membrane as a drug barrier Hancock, R. Trends in Microbiology, Vol. 5, Issue 1 https://doi.org/10.1016/S0966-842X(97)81773-8	journal	January 1997
Federal Funding for the Study of Antimicrobial Resistance in Nosocomial Pathogens: No ESKAPE Rice, Louis B. The Journal of Infectious Diseases, Vol. 197, Issue 8 https://doi.org/10.1086/533452	journal	April 2008
A Bilayer-Couple Model of Bacterial Outer Membrane Vesicle Biogenesis Schertzer, Jeffrey W.; Whiteley, Marvin mBio, Vol. 3, Issue 2 https://doi.org/10.1128/mBio.00297-11	journal	May 2012
Crystalline, Ordered and Disordered Lipid Membranes: Convergence of Stress Profiles due to Ergosterol Vanegas, Juan M.; Longo, Marjorie L.; Faller, Roland Journal of the American Chemical Society, Vol. 133, Issue 11 https://doi.org/10.1021/ja110327r	journal	March 2011
Sampling errors in free energy simulations of small molecules in lipid bilayers Neale, Chris; Pomès, Régis Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1858, Issue 10 https://doi.org/10.1016/j.bbamem.2016.03.006	journal	October 2016
Methodological problems in pressure profile calculations for lipid bilayers Sonne, Jacob; Hansen, Flemming Y.; Peters, Günther H. The Journal of Chemical Physics, Vol. 122, Issue 12 https://doi.org/10.1063/1.1862624	journal	March 2005
How Tolerant are Membrane Simulations with Mismatch in Area per Lipid between Leaflets? Park, Soohyung; Beaven, Andrew H.; Klauda, Jeffery B. Journal of Chemical Theory and Computation, Vol. 11, Issue 7 https://doi.org/10.1021/acs.jctc.5b00232	journal	June 2015
Interaction of quorum signals with outer membrane lipids: insights into prokaryotic membrane vesicle formation Mashburn‐Warren, Lauren; Howe, Jörg; Garidel, Patrick Molecular Microbiology, Vol. 69, Issue 2 https://doi.org/10.1111/j.1365-2958.2008.06302.x	journal	June 2008
Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes Nickels, Jonathan D.; Smith, Jeremy C.; Cheng, Xiaolin Chemistry and Physics of Lipids, Vol. 192 https://doi.org/10.1016/j.chemphyslip.2015.07.012	journal	November 2015
Dynamics of folded proteins McCammon, J. Andrew; Gelin, Bruce R.; Karplus, Martin Nature, Vol. 267, Issue 5612 https://doi.org/10.1038/267585a0	journal	June 1977
g_wham—A Free Weighted Histogram Analysis Implementation Including Robust Error and Autocorrelation Estimates Hub, Jochen S.; de Groot, Bert L.; van der Spoel, David Journal of Chemical Theory and Computation, Vol. 6, Issue 12 https://doi.org/10.1021/ct100494z	journal	November 2010
Outer-membrane vesicles from Gram-negative bacteria: biogenesis and functions Schwechheimer, Carmen; Kuehn, Meta J. Nature Reviews Microbiology, Vol. 13, Issue 10 https://doi.org/10.1038/nrmicro3525	journal	September 2015
3D Pressure Field in Lipid Membranes and Membrane-Protein Complexes Ollila, O. H. Samuli; Risselada, H. Jelger; Louhivuori, Martti Physical Review Letters, Vol. 102, Issue 7 https://doi.org/10.1103/PhysRevLett.102.078101	journal	February 2009
Spontaneous curvature of bilayer membranes from molecular simulations: Asymmetric lipid densities and asymmetric adsorption Różycki, Bartosz; Lipowsky, Reinhard The Journal of Chemical Physics, Vol. 142, Issue 5 https://doi.org/10.1063/1.4906149	journal	February 2015
Separation and Characterization of Toxic and Nontoxic Forms of Lipid A Takayama, K.; Qureshi, N.; Ribi, E. Clinical Infectious Diseases, Vol. 6, Issue 4 https://doi.org/10.1093/clinids/6.4.439	journal	July 1984
Lateral pressure profiles in lipid monolayers Baoukina, Svetlana; Marrink, Siewert J.; Tieleman, D. Peter Faraday Discuss., Vol. 144 https://doi.org/10.1039/B905647E	journal	January 2010
From Dynamics to Membrane Organization: Experimental Breakthroughs Occasion a “Modeling Manifesto” Lyman, Edward; Hsieh, Chia-Lung; Eggeling, Christian Biophysical Journal, Vol. 115, Issue 4 https://doi.org/10.1016/j.bpj.2018.07.012	journal	August 2018
The hierarchy quorum sensing network in Pseudomonas aeruginosa Lee, Jasmine; Zhang, Lianhui Protein & Cell, Vol. 6, Issue 1 https://doi.org/10.1007/s13238-014-0100-x	journal	September 2014
Accurate In Silico Modeling of Asymmetric Bilayers Based on Biophysical Principles Doktorova, Milka; Weinstein, Harel Biophysical Journal, Vol. 115, Issue 9 https://doi.org/10.1016/j.bpj.2018.09.008	journal	November 2018
Polymorphic transitions in single crystals: A new molecular dynamics method Parrinello, M.; Rahman, A. Journal of Applied Physics, Vol. 52, Issue 12 https://doi.org/10.1063/1.328693	journal	December 1981
Structure and function of bacterial outer membrane proteins: barrels in a nutshell Koebnik, Ralf; Locher, Kaspar P.; Van Gelder, Patrick Molecular Microbiology, Vol. 37, Issue 2 https://doi.org/10.1046/j.1365-2958.2000.01983.x	journal	July 2000
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
General and Specific Porins from Bacterial Outer Membranes Schirmer, Tilman Journal of Structural Biology, Vol. 121, Issue 2 https://doi.org/10.1006/jsbi.1997.3946	journal	January 1998
Fabrication and electromechanical characterization of freestanding asymmetric membranes Liu, Paige; Zabala-Ferrera, Oscar; Beltramo, Peter J. Biophysical Journal, Vol. 120, Issue 9 https://doi.org/10.1016/j.bpj.2021.02.036	journal	May 2021
Fixed-Charge Atomistic Force Fields for Molecular Dynamics Simulations in the Condensed Phase: An Overview Riniker, Sereina Journal of Chemical Information and Modeling, Vol. 58, Issue 3 https://doi.org/10.1021/acs.jcim.8b00042	journal	February 2018
Lipopolysaccharide Simulations Are Sensitive to Phosphate Charge and Ion Parameterization Rice, Amy; Rooney, Mary T.; Greenwood, Alexander I. Journal of Chemical Theory and Computation, Vol. 16, Issue 3 https://doi.org/10.1021/acs.jctc.9b00868	journal	February 2020
A Glycam-Based Force Field for Simulations of Lipopolysaccharide Membranes: Parametrization and Validation Kirschner, Karl N.; Lins, Roberto D.; Maass, Astrid Journal of Chemical Theory and Computation, Vol. 8, Issue 11 https://doi.org/10.1021/ct300534j	journal	September 2012
Computational ‘microscopy’ of cellular membranes Ingólfsson, Helgi I.; Arnarez, Clément; Periole, Xavier Journal of Cell Science, Vol. 129, Issue 2 https://doi.org/10.1242/jcs.176040	journal	January 2016
Membrane Distribution of the Pseudomonas Quinolone Signal Modulates Outer Membrane Vesicle Production in Pseudomonas aeruginosa Florez, Catalina; Raab, Julie E.; Cooke, Adam C. mBio, Vol. 8, Issue 4 https://doi.org/10.1128/mBio.01034-17	journal	September 2017
Computational Modeling of Realistic Cell Membranes Marrink, Siewert J.; Corradi, Valentina; Souza, Paulo C. T. Chemical Reviews, Vol. 119, Issue 9 https://doi.org/10.1021/acs.chemrev.8b00460	journal	January 2019
Molecular Model of a Cell Plasma Membrane With an Asymmetric Multicomponent Composition: Water Permeation and Ion Effects Vácha, Robert; Berkowitz, Max L.; Jungwirth, Pavel Biophysical Journal, Vol. 96, Issue 11 https://doi.org/10.1016/j.bpj.2009.03.010	journal	June 2009
CHARMM-GUI 10 years for biomolecular modeling and simulation: Biomolecular Modeling and Simulation Jo, Sunhwan; Cheng, Xi; Lee, Jumin Journal of Computational Chemistry, Vol. 38, Issue 15 https://doi.org/10.1002/jcc.24660	journal	November 2016
Membrane lipids: where they are and how they behave van Meer, Gerrit; Voelker, Dennis R.; Feigenson, Gerald W. Nature Reviews Molecular Cell Biology, Vol. 9, Issue 2 https://doi.org/10.1038/nrm2330	journal	February 2008
Biogenesis of the Gram-Negative Bacterial Outer Membrane Bos, Martine P.; Robert, Viviane; Tommassen, Jan Annual Review of Microbiology, Vol. 61, Issue 1 https://doi.org/10.1146/annurev.micro.61.080706.093245	journal	October 2007
Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa Pesci, E. C.; Milbank, J. B. J.; Pearson, J. P. Proceedings of the National Academy of Sciences, Vol. 96, Issue 20 https://doi.org/10.1073/pnas.96.20.11229	journal	September 1999
GROMACS: A message-passing parallel molecular dynamics implementation Berendsen, H. J. C.; van der Spoel, D.; van Drunen, R. Computer Physics Communications, Vol. 91, Issue 1-3 https://doi.org/10.1016/0010-4655(95)00042-E	journal	September 1995
Empirical force fields for biological macromolecules: Overview and issues Mackerell, Alexander D. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20082	journal	January 2004
Mechanisms of Antimicrobial Resistance in Bacteria Tenover, Fred C. The American Journal of Medicine, Vol. 119, Issue 6 https://doi.org/10.1016/j.amjmed.2006.03.011	journal	June 2006
The Bacterial Cell Envelope Silhavy, T. J.; Kahne, D.; Walker, S. Cold Spring Harbor Perspectives in Biology, Vol. 2, Issue 5 https://doi.org/10.1101/cshperspect.a000414	journal	April 2010
Thermodynamics of Hydrogen Bonding in Hydrophilic and Hydrophobic Media van der Spoel, David; van Maaren, Paul J.; Larsson, Per The Journal of Physical Chemistry B, Vol. 110, Issue 9 https://doi.org/10.1021/jp0572535	journal	March 2006
Accelerating potential of mean force calculations for lipid membrane permeation: System size, reaction coordinate, solute-solute distance, and cutoffs Nitschke, Naomi; Atkovska, Kalina; Hub, Jochen S. The Journal of Chemical Physics, Vol. 145, Issue 12 https://doi.org/10.1063/1.4963192	journal	September 2016
Antimicrobial-resistant pathogens associated with adult healthcare-associated infections: Summary of data reported to the National Healthcare Safety Network, 2015–2017 Weiner-Lastinger, Lindsey M.; Abner, Sheila; Edwards, Jonathan R. Infection Control & Hospital Epidemiology, Vol. 41, Issue 1 https://doi.org/10.1017/ice.2019.296	journal	November 2019
The outer membrane is an essential load-bearing element in Gram-negative bacteria Rojas, Enrique R.; Billings, Gabriel; Odermatt, Pascal D. Nature, Vol. 559, Issue 7715 https://doi.org/10.1038/s41586-018-0344-3	journal	July 2018
The Nose–Hoover thermostat Evans, D. J.; Holian, B. L. The Journal of Chemical Physics, Vol. 83, Issue 8 https://doi.org/10.1063/1.449071	journal	October 1985
Characterization of Pseudomonas aeruginosa fatty acid profiles in biofilms and batch planktonic cultures Chao, Jerry; Wolfaardt, Gideon M.; Arts, Michael T. Canadian Journal of Microbiology, Vol. 56, Issue 12 https://doi.org/10.1139/W10-093	journal	December 2010
Flip-Flop-Induced Relaxation of Bending Energy: Implications for Membrane Remodeling Bruckner, R. J.; Mansy, S. S.; Ricardo, A. Biophysical Journal, Vol. 97, Issue 12 https://doi.org/10.1016/j.bpj.2009.09.025	journal	December 2009
Bacterial Outer Membrane Vesicles in Trafficking, Communication and the Host-Pathogen Interaction Schertzer, Jeffrey W.; Whiteley, Marvin Microbial Physiology, Vol. 23, Issue 1-2 https://doi.org/10.1159/000346770	journal	January 2013
P-LINCS: A Parallel Linear Constraint Solver for Molecular Simulation Hess, Berk Journal of Chemical Theory and Computation, Vol. 4, Issue 1 https://doi.org/10.1021/ct700200b	journal	December 2007
On simulating lipid bilayers with an applied surface tension: periodic boundary conditions and undulations Feller, S. E.; Pastor, R. W. Biophysical Journal, Vol. 71, Issue 3 https://doi.org/10.1016/S0006-3495(96)79337-2	journal	September 1996
CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields Vanommeslaeghe, K.; Hatcher, E.; Acharya, C. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21367	journal	January 2009
Pressure control using stochastic cell rescaling Bernetti, Mattia; Bussi, Giovanni The Journal of Chemical Physics, Vol. 153, Issue 11 https://doi.org/10.1063/5.0020514	journal	September 2020
Bilayer Properties of Lipid A from Various Gram-Negative Bacteria Kim, Seonghoon; Patel, Dhilon S.; Park, Soohyung Biophysical Journal, Vol. 111, Issue 8 https://doi.org/10.1016/j.bpj.2016.09.001	journal	October 2016
Membrane vesicles traffic signals and facilitate group activities in a prokaryote Mashburn, Lauren M.; Whiteley, Marvin Nature, Vol. 437, Issue 7057 https://doi.org/10.1038/nature03925	journal	September 2005
Importance of Force Decomposition for Local Stress Calculations in Biomembrane Molecular Simulations Vanegas, Juan M.; Torres-Sánchez, Alejandro; Arroyo, Marino Journal of Chemical Theory and Computation, Vol. 10, Issue 2 https://doi.org/10.1021/ct4008926	journal	January 2014
Quantitative Proteomics Reveals That the Protein Components of Outer Membrane Vesicles (OMVs) in Aeromonas hydrophila Play Protective Roles in Antibiotic Resistance Lin, Ling; Wang, Yuqian; Srinivasan, Ramanathan Journal of Proteome Research, Vol. 21, Issue 7 https://doi.org/10.1021/acs.jproteome.2c00114	journal	June 2022
Characterization of Membrane Lipidome Changes in Pseudomonas aeruginosa during Biofilm Growth on Glass Wool Benamara, Hayette; Rihouey, Christophe; Abbes, Imen PLoS ONE, Vol. 9, Issue 9 https://doi.org/10.1371/journal.pone.0108478	journal	September 2014
Constant surface tension simulations of lipid bilayers: The sensitivity of surface areas and compressibilities Feller, Scott E.; Pastor, Richard W. The Journal of Chemical Physics, Vol. 111, Issue 3 https://doi.org/10.1063/1.479313	journal	July 1999
Molecular dynamics with coupling to an external bath Berendsen, H. J. C.; Postma, J. P. M.; van Gunsteren, W. F. The Journal of Chemical Physics, Vol. 81, Issue 8 https://doi.org/10.1063/1.448118	journal	October 1984
GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers Abraham, Mark James; Murtola, Teemu; Schulz, Roland SoftwareX, Vol. 1-2 https://doi.org/10.1016/j.softx.2015.06.001	journal	September 2015
Characterization of Phospholipids in Membrane Vesicles Derived fromPseudomonas aeruginosa Tashiro, Yosuke; Inagaki, Aya; Shimizu, Motoyuki Bioscience, Biotechnology, and Biochemistry, Vol. 75, Issue 3 https://doi.org/10.1271/bbb.100754	journal	March 2011
Molecular dynamics at constant Cauchy stress Miller, Ronald E.; Tadmor, Ellad B.; Gibson, Joshua S. The Journal of Chemical Physics, Vol. 144, Issue 18 https://doi.org/10.1063/1.4948711	journal	May 2016
Developing initial conditions for simulations of asymmetric membranes: a practical recommendation Park, Soohyung; Im, Wonpil; Pastor, Richard W. Biophysical Journal, Vol. 120, Issue 22 https://doi.org/10.1016/j.bpj.2021.10.009	journal	November 2021
Phospholipid - Driven gene regulation Musille, Paul M.; Kohn, Jeffrey A.; Ortlund, Eric A. FEBS Letters, Vol. 587, Issue 8 https://doi.org/10.1016/j.febslet.2013.01.004	journal	January 2013
THE weighted histogram analysis method for free-energy calculations on biomolecules. I. The method Kumar, Shankar; Rosenberg, John M.; Bouzida, Djamal Journal of Computational Chemistry, Vol. 13, Issue 8 https://doi.org/10.1002/jcc.540130812	journal	October 1992
Improved Parametrization of Li ⁺ , Na ⁺ , K ⁺ , and Mg ²⁺ Ions for All-Atom Molecular Dynamics Simulations of Nucleic Acid Systems Yoo, Jejoong; Aksimentiev, Aleksei The Journal of Physical Chemistry Letters, Vol. 3, Issue 1 https://doi.org/10.1021/jz201501a	journal	December 2011
Molecular Dynamics Simulations of Lipid Bilayers: Major Artifacts Due to Truncating Electrostatic Interactions Patra, M.; Karttunen, M.; Hyvönen, M. T. Biophysical Journal, Vol. 84, Issue 6 https://doi.org/10.1016/S0006-3495(03)75094-2	journal	June 2003
Isothermal molecular dynamics calculations for liquid salts Woodcock, L. V. Chemical Physics Letters, Vol. 10, Issue 3 https://doi.org/10.1016/0009-2614(71)80281-6	journal	August 1971
Automation of the CHARMM General Force Field (CGenFF) II: Assignment of Bonded Parameters and Partial Atomic Charges Vanommeslaeghe, K.; Raman, E. Prabhu; MacKerell, A. D. Journal of Chemical Information and Modeling, Vol. 52, Issue 12 https://doi.org/10.1021/ci3003649	journal	November 2012
Reciprocal cross-species induction of outer membrane vesicle biogenesis via secreted factors Horspool, Alexander M.; Schertzer, Jeffrey W. Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-28042-4	journal	June 2018
Bacterial outer membrane vesicles and the host-pathogen interaction Kuehn, M. J. Genes & Development, Vol. 19, Issue 22 https://doi.org/10.1101/gad.1299905	journal	November 2005
Molecular conformation affects the interaction of the Pseudomonas quinolone signal with the bacterial outer membrane Li, Ao; Schertzer, Jeffrey W.; Yong, Xin Journal of Biological Chemistry, Vol. 294, Issue 4 https://doi.org/10.1074/jbc.AC118.006844	journal	January 2019
A Unified Interpretation of Stress in Molecular Systems Admal, Nikhil Chandra; Tadmor, E. B. Journal of Elasticity, Vol. 100, Issue 1-2 https://doi.org/10.1007/s10659-010-9249-6	journal	May 2010
Complementary biophysical tools to investigate lipid specificity in the interaction between bioactive molecules and the plasma membrane: A review Deleu, Magali; Crowet, Jean-Marc; Nasir, Mehmet N. Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1838, Issue 12 https://doi.org/10.1016/j.bbamem.2014.08.023	journal	December 2014
Automated Builder and Database of Protein/Membrane Complexes for Molecular Dynamics Simulations Jo, Sunhwan; Kim, Taehoon; Im, Wonpil PLoS ONE, Vol. 2, Issue 9 https://doi.org/10.1371/journal.pone.0000880	journal	September 2007
Bending Free Energy from Simulation: Correspondence of Planar and Inverse Hexagonal Lipid Phases Sodt, Alexander J.; Pastor, Richard W. Biophysical Journal, Vol. 104, Issue 10 https://doi.org/10.1016/j.bpj.2013.03.048	journal	May 2013
CHARMM additive and polarizable force fields for biophysics and computer-aided drug design Vanommeslaeghe, K.; MacKerell, A. D. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1850, Issue 5 https://doi.org/10.1016/j.bbagen.2014.08.004	journal	May 2015
Molecular dynamics modeling of Pseudomonas aeruginosa outer membranes Li, Ao; Schertzer, Jeffrey W.; Yong, Xin Physical Chemistry Chemical Physics, Vol. 20, Issue 36 https://doi.org/10.1039/C8CP04278K	journal	January 2018
Particle mesh Ewald: An N ⋅log( N ) method for Ewald sums in large systems Darden, Tom; York, Darrin; Pedersen, Lee The Journal of Chemical Physics, Vol. 98, Issue 12 https://doi.org/10.1063/1.464397	journal	June 1993
Bacterial Quorum Sensing: Its Role in Virulence and Possibilities for Its Control Rutherford, S. T.; Bassler, B. L. Cold Spring Harbor Perspectives in Medicine, Vol. 2, Issue 11 https://doi.org/10.1101/cshperspect.a012427	journal	November 2012
Molecular Basis of Bacterial Outer Membrane Permeability Revisited Nikaido, H. Microbiology and Molecular Biology Reviews, Vol. 67, Issue 4 https://doi.org/10.1128/MMBR.67.4.593-656.2003	journal	December 2003
CHARMM-GUI: A web-based graphical user interface for CHARMM Jo, Sunhwan; Kim, Taehoon; Iyer, Vidyashankara G. Journal of Computational Chemistry, Vol. 29, Issue 11 https://doi.org/10.1002/jcc.20945	journal	March 2008
Phospholipid subcellular localization and dynamics Yang, Yanbo; Lee, Minhyoung; Fairn, Gregory D. Journal of Biological Chemistry, Vol. 293, Issue 17 https://doi.org/10.1074/jbc.R117.000582	journal	April 2018
Graph–Theoretic Analysis of Monomethyl Phosphate Clustering in Ionic Solutions Han, Kyungreem; Venable, Richard M.; Bryant, Anne-Marie The Journal of Physical Chemistry B, Vol. 122, Issue 4 https://doi.org/10.1021/acs.jpcb.7b10730	journal	January 2018
Examining the Mechanical Equilibrium of Microscopic Stresses in Molecular Simulations Torres-Sánchez, Alejandro; Vanegas, Juan M.; Arroyo, Marino Physical Review Letters, Vol. 114, Issue 25 https://doi.org/10.1103/PhysRevLett.114.258102	journal	June 2015

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