Molecular insights into substrate binding mechanism of undecaprenyl pyrophosphate with membrane integrated phosphatidyl glycerophosphate phosphatase B (PgpB) using molecular dynamics simulation approach

References

• Apfel, C. M., Takács, B., Fountoulakis, M., Stieger, M., & Keck, W. (1999). Use of genomics to identify bacterial undecaprenyl pyrophosphate synthetase: Cloning, expression, and characterization of the essential uppS gene. Journal of Bacteriology, 181(2), 483–492. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/9882662
   PubMed Web of Science ®Google Scholar
• Becke, A. D. (1993). Density-functional thermochemistry. III. The role of exact exchange. The Journal of Chemical Physics, 98(7), 5648. doi:10.1063/1.464913
   Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. R. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. doi:10.1063/1.448118
   Web of Science ®Google Scholar
• Botello-Smith, W. M., & Luo, R. (2015). Applications of MMPBSA to membrane proteins I: Efficient numerical solutions of periodic Poisson–Boltzmann equation. Journal of Chemical Information and Modeling, 55(10), 2187–2199. doi:10.1021/acs.jcim.5b00341
   PubMed Web of Science ®Google Scholar
• Cai, Q., Hsieh, M.-J., Wang, J., & Luo, R. (2010). Performance of nonlinear finite-difference Poisson–Boltzmann Solvers. Journal of Chemical Theory and Computation, 6(1), 203–211. doi:10.1021/ct900381r
   PubMed Web of Science ®Google Scholar
• Carman, G. M., & Han, G.-S. (2006). Roles of phosphatidate phosphatase enzymes in lipid metabolism. Trends in Biochemical Sciences, 31(12), 694–699. doi:10.1016/j.tibs.2006.10.003
   PubMed Web of Science ®Google Scholar
• Case, D. A., Betz, R. M., Botello-Smith, W., Cerutti, D. S., Cheatham I, T. E., Darden T. A., … Kollman, P. A. (2016). Amber 16; University of California, San Francisco: Amber 16. San Francisco, CA: University of California.
   Google Scholar
• Case, D. A., Cheatham, T. E., Darden, T., Gohlke, H., Luo, R., Merz, K. M., … Woods, R. J. (2005). The Amber biomolecular simulation programs. Journal of Computational Chemistry, 26(16), 1668–1688. doi:10.1002/jcc.20290
   PubMed Web of Science ®Google Scholar
• Chang, H.-Y., Chou, C.-C., Hsu, M.-F., & Wang, A. H. J. (2014). Proposed carrier lipid-binding site of undecaprenyl pyrophosphate phosphatase from Escherichia coli. Journal of Biological Chemistry, 289(27), 18719–18735. doi:10.1074/jbc.M114.575076.
   PubMed Web of Science ®Google Scholar
• Chung, B. C., Zhao, J., Gillespie, R. A., Kwon, D.-Y., Guan, Z., Hong, J., … Lee, S.-Y. (2013). Crystal structure of MraY, an essential membrane enzyme for bacterial cell wall synthesis. Science, 341(6149), 1012–1016. doi:10.1126/science.1236501
   PubMed Web of Science ®Google Scholar
• Cunningham, M. A. (2012). Dynamical probing of allosteric control in nuclear receptors. Journal of Molecular Modeling, 18(7), 3147–3152. doi:10.1007/s00894-011-1330-y
   PubMed Web of Science ®Google Scholar
• David, C. C., & Jacobs, D. J. (2014). Principal component analysis: A method for determining the essential dynamics of proteins In D. Livesay (Ed.), Protein dynamics (pp. 193–226). Totowa, NJ: Humana Press. doi:10.1007/978-1-62703-658-0_11
   Google Scholar
• Essmann, U., Perera, L., Berkowitz, M. L., Darden, T., Lee, H., & Pedersen, L. G. (1995). A smooth particle mesh Ewald method. The Journal of Chemical Physics, 103(19), 8577–8593. doi:10.1063/1.470117
   Web of Science ®Google Scholar
• Fan, J., Jiang, D., Zhao, Y., Liu, J., & Zhang, X. C. (2014). Crystal structure of lipid phosphatase Escherichia coli phosphatidylglycerophosphate phosphatase B. Proceedings of the National Academy of Sciences, 111(21), 7636–7640. doi:10.1073/pnas.1403097111
   PubMed Web of Science ®Google Scholar
• Ferreira, T. M., Coreta-Gomes, F., Ollila, O. H. S., Moreno, M. J., Vaz, W. L. C., & Topgaard, D. (2013). Cholesterol and POPC segmental order parameters in lipid membranes: Solid state 1 H– 13 C NMR and MD simulation studies. Physical Chemistry Chemical Physics: PCCP, 15(6), 1976–1989. doi:10.1039/C2CP42738A
   PubMed Web of Science ®Google Scholar
• Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., … Millam, J. M. (2003). GAUSSIAN03. In B.05 R. Pittsburgh, PA: Pople, Gaussian.
   Google Scholar
• Ghachi, M. E., Bouhss, A., Blanot, D., & Mengin-Lecreulx, D. (2004). The bacA Gene of Escherichia coli encodes an undecaprenyl pyrophosphate phosphatase activity. Journal of Biological Chemistry, 279(29), 30106–30113. doi:10.1074/jbc.M401701200
   PubMed Web of Science ®Google Scholar
• Girvan, M., & Newman, M. E. J. (2002). Community structure in social and biological networks. Proceedings of the National Academy of Sciences, 99(12), 7821–7826. doi:10.1073/pnas.122653799
   PubMed Web of Science ®Google Scholar
• Greene, D., Botello-Smith, W. M., Follmer, A., Xiao, L., Lambros, E., & Luo, R. (2016). Modeling membrane protein-ligand binding interactions: The human purinergic platelet receptor. The Journal of Physical Chemistry. B, 120(48), 12293–12304. doi:10.1021/acs.jpcb.6b09535
   PubMed Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. doi:10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jo, S., Kim, T., Iyer, V. G., & Im, W. (2008). CHARMM-GUI: A web-based graphical user interface for CHARMM. Journal of Computational Chemistry, 29(11), 1859–1865. doi:10.1002/jcc.20945
   PubMed Web of Science ®Google Scholar
• Jo, S., Lim, J. B., Klauda, J. B., & Im, W. (2009). CHARMM-GUI membrane builder for mixed bilayers and its application to yeast membranes. Biophysical Journal, 97(1), 50–58. doi:10.1016/j.bpj.2009.04.013
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., & Jenson, C. (1998). Temperature dependence of TIP3P, SPC, and TIP4P water from NPT Monte Carlo simulations: Seeking temperatures of maximum density. Journal of Computational Chemistry, 19(10), 1179–1186. doi:10.1002/(SICI)1096-987X(19980730)19:10<1179::AID-JCC6>3.0.CO;2-J
   Web of Science ®Google Scholar
• Klauda, J. B., Venable, R. M., Freites, J. A., O’Connor, J. W., Tobias, D. J., Mondragon-Ramirez, C., … Pastor, R. W. (2010). Update of the CHARMM All-atom additive force field for lipids: Validation on six lipid types. The Journal of Physical Chemistry. B, 114(23), 7830–7843. doi:10.1021/jp101759q
   PubMed Web of Science ®Google Scholar
• Lomize, M. A., Pogozheva, I. D., Joo, H., Mosberg, H. I., & Lomize, A. L. (2012). OPM database and PPM web server: Resources for positioning of proteins in membranes. Nucleic Acids Research, 40(D1), D370–D376. doi:10.1093/nar/gkr703
   PubMed Web of Science ®Google Scholar
• Manat, G., El Ghachi, M., Auger, R., Baouche, K., Olatunji, S., Kerff, F., … Bouhss, A. (2015). Membrane topology and biochemical characterization of the Escherichia coli BacA undecaprenyl-pyrophosphate phosphatase. PLoS ONE, 10(11), e0142870. doi:10.1371/journal.pone.0142870
   PubMed Web of Science ®Google Scholar
• Mezei, M. (2010). Simulaid: A simulation facilitator and analysis program. Journal of Computational Chemistry, 31(14), 2658–2668. doi:10.1002/jcc.21551
   PubMed Web of Science ®Google Scholar
• Mezei, M., & Filizola, M. (2006). TRAJELIX: A computational tool for the geometric characterization of protein helices during molecular dynamics simulations. Journal of Computer-Aided Molecular Design, 20(2), 97–107. doi:10.1007/s10822-006-9039-1
   PubMed Web of Science ®Google Scholar
• Mori, T., Ogushi, F., & Sugita, Y. (2012). Analysis of lipid surface area in protein-membrane systems combining voronoi tessellation and monte carlo integration methods. Journal of Computational Chemistry, 33(3), 286–293. doi:10.1002/jcc.21973
   PubMed Web of Science ®Google Scholar
• Pearlman, D. A., Case, D. A., Caldwell, J. W., Ross, W. S., Cheatham, T. E., DeBolt, S., … Kollman, P. (1995). AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Computer Physics Communications, 91(1-3), 1–41. doi:10.1016/0010-4655(95)00041-D
   Web of Science ®Google Scholar
• Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., & Ferrin, T. E. (2004). UCSF Chimera – A visualization system for exploratory research and analysis. Journal of Computational Chemistry, 25(13), 1605–1612. doi:10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. (2013). PTRAJ and CPPTRAJ: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095. doi:10.1021/ct400341p
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., Ciccotti, G., & Berendsen, H. J. (1977). Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. Journal of Computational Physics, 23(3), 327–341. doi:10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Schrödinger Release 2014-3: Macromodel, Schrödinger, LLC, New York, NY. (2014).
   Google Scholar
• Schrödinger Release 2014-3: Schrödinger Suite 2014-3 Protein Preparation Wizard; Epik version 2.9, Schrödinger, LLC, New York, NY, 2014; Impact version 6.4,Schrödinger, LLC, New York, NY, 2014; Prime version 3.7, Schrödinger, LLC, New York, NY, (2014).
   Google Scholar
• Seeley, J. R. (1949). The net of reciprocal influence: A problem in treating sociometric data. Canadian Journal of Psychology Revue Canadienne de Psychologie, 3(4), 234–240. doi:10.1037/h0084096
   Google Scholar
• Sethi, A., Eargle, J., Black, A. A., & Luthey-Schulten, Z. (2009). Dynamical networks in tRNA:Protein complexes. Proceedings of the National Academy of Sciences of the United States of America, 106(16), 6620–6625. doi:10.1073/pnas.0810961106
   PubMed Web of Science ®Google Scholar
• Small-Molecule Drug Discovery Suite 2014-3: Schrödinger Suite 2014-3 Induced Fit Docking protocol; Glide version 6.4, Schrödinger, LLC, New York, NY, 2014; Prime version 3.7, Schrödinger, LLC, New York, NY, (2014).
   Google Scholar
• Tong, S., Lin, Y., Lu, S., Wang, M., Bogdanov, M., & Zheng, L. (2016). structural insight into substrate selection and catalysis of lipid phosphate phosphatase PgpB in the cell membrane. Journal of Biological Chemistry, 291(35), 18342–18352. doi:10.1074/jbc.M116.737874
   PubMed Web of Science ®Google Scholar
• TouzÉ, T., & Mengin-Lecreulx, D. (2008). Undecaprenyl phosphate synthesis. EcoSal Plus, 3(1), doi:10.1128/ecosalplus.4.7.1.7
   PubMedGoogle Scholar
• Wang, J., Cai, Q., Li, Z.-L., Zhao, H.-K., & Luo, R. (2009). Achieving energy conservation in Poisson–Boltzmann molecular dynamics: Accuracy and precision with finite-difference algorithms. Chemical Physics Letters, 468(4-6), 112–118. doi:10.1016/j.cplett.2008.12.049
   PubMed Web of Science ®Google Scholar
• Wang, J., Cai, Q., Xiang, Y., & Luo, R. (2012). Reducing grid dependence in finite-difference Poisson–Boltzmann calculations. Journal of Chemical Theory and Computation, 8(8), 2741–2751. doi:10.1021/ct300341d
   PubMed Web of Science ®Google Scholar
• Xiao, L., Diao, J., Greene, D., Wang, J., & Luo, R. (2017). A continuum Poisson–Boltzmann model for membrane channel proteins. Journal of Chemical Theory and Computation, 13(7), 3398–3412. doi:10.1021/acs.jctc.7b00382
   PubMed Web of Science ®Google Scholar