Anticorrelated position fluctuation of lipids in forming membrane water pores: molecular dynamics simulations study with dengue virus capsid protein

References

• Abraham, M. J., Murtola, T., Schulz, R., Pall, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
   Google Scholar
• Acosta, E. G., Castilla, V., & Damonte, E. B. (2009). Alternative infectious entry pathways for dengue virus serotypes into mammalian cells. Cellular Microbiology, 11(10), 1533–1549. https://doi.org/10.1111/j.1462-5822.2009.01345.x
   PubMed Web of Science ®Google Scholar
• Acosta, E. G., Castilla, V., & EB, D. (2008). Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. The Journal of General Virology, 89(Pt 2), 474–484. https://doi.org/10.1099/vir.0.83357-0
   PubMedGoogle Scholar
• Agarraaberes, F. A., & Dice, J. F. (2001). Protein translocation across membrane. Biochimica et Biophysica Acta, 1513(1), 1–24. https://doi.org/10.1016/S0304-4157(01)00005-3
   PubMed Web of Science ®Google Scholar
• Alcaraz-Estrada, S. L., Yocupicio-Monroy, M., & Angel, R. M. d. (2010). Insights into dengue virus genome replication. Future Virology, 5(5), 575–592. https://doi.org/10.2217/fvl.10.49
   Web of Science ®Google Scholar
• Allen, W. J., Lemkul, J. A., & Bevan, D. R. (2009). GridMAT-MD: A grid-based membrane analysis tool for use with molecular dynamics. Journal of Computational Chemistry, 30(12), 1952–1958. https://doi.org/10.1002/jcc.21172
   PubMed Web of Science ®Google Scholar
• Ang, F., Wong, A. P. Y., Mah-Lee Ng, M., & Chu, J. J. H. (2010). Small interference RNA profiling reveals the essential role of human membrane trafficking genes in mediating the infectious entry of dengue virus. Virology Journal, 7, 24. https://doi.org/10.1186/1743-422X-7-24
   PubMed Web of Science ®Google Scholar
• Anusuya, S., Velmurugan, D., & Gromiha, M. M. (2016). Identification of dengue viral RNA-dependent RNA polymerase inhibitor using computational fragment-based approaches and molecular dynamics study. Journal of Biomolecular Structure & Dynamics, 34(7), 1512–1532. https://doi.org/10.1080/07391102.2015.1081620
   PubMed Web of Science ®Google Scholar
• Ben-Shaul, A., Ben-Tal, N., & Honig, B. (1996). Statistical thermodynamic analysis of peptide and protein insertion into lipid membranes. Biophysical Journal, 71(1), 130–137. https://doi.org/10.1016/S0006-3495(96)79208-1
   PubMed Web of Science ®Google Scholar
• Ben-Tal, N., Ben-Shaul, A., Nicholls, A., & Honig, B. (1996). Free-energy determinants of alpha-helix insertion into lipid bilayers. Biophysical Journal, 70(4), 1803–1812.
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., van der Spoel, D., & van Drunen, R. (1995). GROMACS: A message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1–3), 43–56. https://doi.org/10.1016/0010-4655(95)00042-E
   Web of Science ®Google Scholar
• Boyd, I. A., & Martin, A. R. (1956). The end-plate potential in mammalian muscle . The Journal of Physiology, 132(1), 74–91. https://doi.org/10.1113/jphysiol.1956.sp005503
   PubMed Web of Science ®Google Scholar
• Bruce, A. (1998). The cell as a collection of protein machines: Preparing the next generation of molecular biologists. Cell, 92, 291–294.
   PubMed Web of Science ®Google Scholar
• Byk, L. A., & Gamarnik, A. V. (2016). Properties and functions of the dengue virus capsid protein. Annual Review of Virology, 3(1), 263–281. https://doi.org/10.1146/annurev-virology-110615-042334
   PubMed Web of Science ®Google Scholar
• Chetwynd, A., Wee, C. L., Hall, B. A., & Sansom, M. S. P. (2010). The energetics of transmembrane helix insertion into a lipid bilayer. Biophysical Journal, 99(8), 2534–2540. https://doi.org/10.1016/j.bpj.2010.08.002
   PubMed Web of Science ®Google Scholar
• Collinson, I., Corey, R. A., & Allen, W. J. (2015). Channel crossing: How are proteins shipped across the bacterial plasma membrane? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 370(1679), 20150025. https://doi.org/10.1098/rstb.2015.0025
   Google Scholar
• Cruz-Oliveira, C., Freire, J. M., Conceição, T. M., Higa, L. M., Castanho, M. A. R. B., & Poian, A. T. D. (2015). Receptors and routes of dengue virus entry into the host cells. FEMS Microbiology Reviews, 39(2), 155–170. https://doi.org/10.1093/femsre/fuu004
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An Nlog(N) method for Ewald sums in large systems. Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• De La Guardia, C., & Lleonart, R. (2014). Progress in the identification of dengue virus entry/fusion inhibitors. BioMed Research International, 2014, 825039. https://doi.org/10.1155/2014/825039
   PubMed Web of Science ®Google Scholar
• Desikan, R., Maiti, P. K., & Ayappa, K. G. (2017). Assessing the structure and stability of transmembrane oligomeric intermediates of an α-helical toxin. Langmuir: The ACS Journal of Surfaces and Colloids, 33(42), 11496–11510. https://doi.org/10.1021/acs.langmuir.7b02277
   PubMed Web of Science ®Google Scholar
• Durzyńska, J., Przysiecka, Ł., Nawrot, R., Barylski, J., Nowicki, G., Warowicka, A., Musidlak, O., & Goździcka-Józefiak, A. (2015). Viral and other cell-penetrating peptides as vectors of therapeutic agents in medicine. The Journal of Pharmacology and Experimental Therapeutics, 354(1), 32–42. https://doi.org/10.1124/jpet.115.223305
   PubMed Web of Science ®Google Scholar
• Eaton, J. W., Bateman, D., Hauberg, S., & Wehbring, R. (2016). GNU Octave version 4.2.0 manual: a high-level interactive language for numerical computations. CreateSpace Independent Publishing Platform.
   Google Scholar
• Fajardo-Sánchez, E., Galiano, V., & Villalaín, J. (2017). Molecular dynamics study of the membrane interaction of a membranotropic dengue virus C protein-derived peptide. Journal of Biomolecular Structure & Dynamics, 35(6), 1283–1294. https://doi.org/10.1080/07391102.2016.1179595
   PubMed Web of Science ®Google Scholar
• Freire, J. M., Santos, N. C., Veiga, A. S., Da Poian, A. T., & Castanho, M. A. R. B. (2015). Rethinking the capsid proteins of enveloped viruses: Multifunctionality from genome packaging to genome transfection. The FEBS Journal, 282(12), 2267–2278. https://doi.org/10.1111/febs.13274
   PubMed Web of Science ®Google Scholar
• Freire, J. M., Veiga, A. S., Conceição, T. M., Kowalczyk, W., Mohana-Borges, R., Andreu, D., Santos, N. C., Da Poian, A. T., & Castanho, M. A. R. B. (2013). Intracellular nucleic acid delivery by the supercharged dengue virus capsid protein. PLOS One, 8(12), e81450. https://doi.org/10.1371/journal.pone.0081450
   PubMed Web of Science ®Google Scholar
• GNU, P. (2007). Free Software Foundation. Bash (3.2. 48) [Unix shell program].
   Google Scholar
• Grove, J., & Marsh, M. (2011). The cell biology of receptor-mediated virus entry. The Journal of Cell Biology, 195(7), 1071–1082. https://doi.org/10.1083/jcb.201108131
   PubMed Web of Science ®Google Scholar
• Guidotti, G., Brambilla, L., & Rossi, D. (2017). Cell-penetrating peptides: From basic research to clinics. Trends in Pharmacological Sciences, 38(4), 406–424. https://doi.org/10.1016/j.tips.2017.01.003
   PubMed Web of Science ®Google Scholar
• Guo, Z., Peng, H., Kang, J., & Sun, D. (2016). Cell-penetrating peptides: Possible transduction mechanisms and therapeutic applications. Biomedical Reports, 4(5), 528–534. https://doi.org/10.3892/br.2016.639
   PubMed Web of Science ®Google Scholar
• Gupta, B., Levchenko, T., & Torchilin, V. P. (2005). Intracellular delivery of large molecules and small particles by cell-penetrating proteins and peptides. Advanced Drug Delivery Reviews, 57(4), 637–651. https://doi.org/10.1016/j.addr.2004.10.007
   PubMed Web of Science ®Google Scholar
• Harayama, T., & Riezman, H. (2018). Understanding the diversity of membrane lipid composition. Nature Reviews. Molecular Cell Biology, 19(5), 281–296. https://doi.org/10.1038/nrm.2017.138
   PubMed Web of Science ®Google Scholar
• Herce, H. D., & Garcia, A. E. (2007). Molecular dynamics simulations suggest a mechanism for translocation of the HIV-1 TAT peptide across lipid membranes. Proceedings of the National Academy of Sciences of the United States of America, 104(52), 20805–20810. https://doi.org/10.1073/pnas.0706574105
   PubMed Web of Science ®Google Scholar
• Hess, B. (2008). P-LINCS: A parallel linear constraint solver for molecular simulation. Journal of Chemical Theory and Computation, 4(1), 116–122. https://doi.org/10.1021/ct700200b
   PubMed Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J. C., & Fraaije, J. G. E. M. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18(12), 1463–1472. https://doi.org/10.1002/(SICI)1096-987X(199709)18:12 < 1463::AID-JCC4 > 3.0.CO;2-H
   Web of Science ®Google Scholar
• Hoover, W. G. (1985). Canonical dynamics: Equilibrium phase-space distributions. Physical Review. A, General Physics, 31(3), 1695–1697. https://doi.org/10.1103/physreva.31.1695
   PubMedGoogle Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD – Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22(12), 2577–2637. https://doi.org/10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Krishnan, M. N., Sukumaran, B., Pal, U., Agaisse, H., Murray, J. L., Hodge, T. W., & Fikrig, E. (2007). Rab 5 is required for the cellular entry of dengue and West Nile viruses. Journal of Virology, 81(9), 4881–4885. https://doi.org/10.1128/JVI.02210-06
   PubMed Web of Science ®Google Scholar
• Kuhn, R. J., Zhang, W., Rossmann, M. G., Pletnev, S. V., Corver, J., Lenches, E., Jones, C. T., Mukhopadhyay, S., Chipman, P. R., Strauss, E. G., Baker, T. S., & Strauss, J. H. (2002). Structure of Dengue virus: Implications for flavivirus organization, maturation, and fusion. Cell, 108(5), 717–725. https://doi.org/10.1016/s0092-8674(02)00660-8
   PubMed Web of Science ®Google Scholar
• Leonenko, Z. V., Finot, E., Ma, H., Dahms, T. E., & Cramb, D. T. (2004). Investigation of temperature-induced phase transitions in DOPC and DPPC phospholipid bilayers using temperature-controlled scanning force microscopy. Biophysical Journal, 86(6), 3783–3793. https://doi.org/10.1529/biophysj.103.036681
   PubMed Web of Science ®Google Scholar
• Lombard, J. (2014). Once upon a time the cell membranes: 175 years of cell boundary research. Biology Direct, 9, 32. https://doi.org/10.1186/s13062-014-0032-7
   PubMed Web of Science ®Google Scholar
• Ma, L., Jones, C. T., Groesch, T. D., Kuhn, R. J., & Post, C. B. (2004). Solution structure of dengue virus capsid protein reveals another fold. Proceedings of the National Academy of Sciences of the United States of America, 101(10), 3414–3419. https://doi.org/10.1073/pnas.0305892101
   PubMed Web of Science ®Google Scholar
• Madani, F., Lindberg, S., Langel, U., Futaki, S., & Graslund, A. (2011). Mechanisms of cellular uptake of cell-penetrating peptides. Journal of Biophysics (Hindawi Publishing Corporation: Online), 2011, 414729. https://doi.org/10.1155/2011/414729
   PubMedGoogle Scholar
• Martins, I. C., Gomes-Neto, F., Faustino, A. F., Carvalho, F. A., Carneiro, F. A., Bozza, P. T., Mohana-Borges, R., Castanho, M. A., Almeida, F. C., Santos, N. C., & Da Poian, A. T. (2012). The disordered N-terminal region of dengue virus capsid protein contains a lipid-droplet-binding motif. The Biochemical Journal, 444(3), 405–415. https://doi.org/10.1042/BJ20112219
   PubMedGoogle Scholar
• McNaughton, B. R., Cronican, J. J., Thompson, D. B., & R, L. D. (2009). Mammalian cell penetration, siRNA transfection, and DNA transfection by supercharged proteins. Proceedings of the National Academy of Sciences of the United States of America, 106(15), 6111–6116. https://doi.org/10.1073/pnas.0807883106
   PubMed Web of Science ®Google Scholar
• Modis, Y., Ogata, S., Clements, D., & Harrison, S. C. (2003). A ligand-binding pocket in the dengue virus envelope glycoprotein. Proceedings of the National Academy of Sciences of the United States of America, 100(12), 6986–6991. https://doi.org/10.1073/pnas.0832193100
   PubMed Web of Science ®Google Scholar
• Modis, Y., Ogata, S., Clements, D., & Harrison, S. C. (2004). Structure of the dengue virus envelope protein after membrane fusion. Nature, 427(6972), 313–319. https://doi.org/10.1038/nature02165
   PubMed Web of Science ®Google Scholar
• Modis, Y., Ogata, S., Clements, D., & Harrison, S. C. (2005). Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. Journal of Virology, 79(2), 1223–1231. https://doi.org/10.1128/JVI.79.2.1223-1231.2005
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay, S., Kuhn, R. J., & Rossmann, M. G. (2005). A structural perspective of the flavivirus life cycle. Nature Reviews. Microbiology, 3(1), 13–22. https://doi.org/10.1038/nrmicro1067
   PubMed Web of Science ®Google Scholar
• Nośe, S. A. (1984). A unified formulation of the constant temperature molecular dynamics methods. Journal of Chemical Physics, 81, 511–519.
   Web of Science ®Google Scholar
• Parrinello, M., & Rahman, A. (1981). Polymorphic transitions in single crystals: A new molecular dynamics method. Journal of Applied Physics, 52(12), 7182–7190. https://doi.org/10.1063/1.328693
   Web of Science ®Google Scholar
• Perera, R., & Kuhn, R. J. (2008). Structural proteomics of dengue virus. Current Opinion in Microbiology, 11(4), 369–377. https://doi.org/10.1016/j.mib.2008.06.004
   PubMed 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. https://doi.org/10.1002/jcc.20084
   PubMed Web of Science ®Google Scholar
• Qi, R.-F., Zhang, L., & Chi, C-w. (2008). Biological characteristics of dengue virus and potential targets for drug design. Acta Biochimica et Biophysica Sinica, 40(2), 91–101. https://doi.org/10.1111/j.1745-7270.2008.00382.x
   PubMed Web of Science ®Google Scholar
• Rajapaksha, S. P., Pal, N., Zheng, D., & Lu, H. P. (2015). Protein-fluctuation-induced water-pore formation in ion channel voltage-sensor translocation across a lipid bilayer membrane. Physical Review E, 92(5), 052719. https://doi.org/10.1103/PhysRevE.92.052719
   Google Scholar
• Rapoport, T. A. (2007). Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature, 450(7170), 663–669. https://doi.org/10.1038/nature06384
   PubMed Web of Science ®Google Scholar
• Schmid, N., Eichenberger, A. P., Choutko, A., Riniker, S., Winger, M., Mark, A. E., & van Gunsteren, W. F. (2011). Definition and testing of the GROMOS force-field versions 54A7 and 54B7. European Biophysics Journal: EBJ, 40(7), 843–856. https://doi.org/10.1007/s00249-011-0700-9
   PubMed Web of Science ®Google Scholar
• Sengupta, D., Leontiadou, H., Mark, A. E., & Marrink, S. J. (2008). Toroidal pores formed by antimicrobial peptides show significant disorder. Biochimica et Biophysica Acta, 1778(10), 2308–2317. https://doi.org/10.1016/j.bbamem.2008.06.007
   PubMed Web of Science ®Google Scholar
• Stone, J. E. (1998). An efficient library for parallel ray tracing and animation. University of Missouri-Rolla.
   Google Scholar
• Tan, M., Waring, A. J., & Hong, M. (2007). Phosphate-mediated arginine insertion into lipid membranes and pore formation by a cationic membrane peptide from solid-state NMR. Journal of the American Chemical Society, 129(37), 11438–11446. https://doi.org/10.1021/ja072511s
   PubMed Web of Science ®Google Scholar
• Thompson, D. B., Cronican, J. J., & Liu, D. R. (2012). Engineering and identifying supercharged proteins for macromolecule delivery into mammalian cells. Methods in Enzymology, 503, 293–319. https://doi.org/10.1016/B978-0-12-396962-0.00012-4
   PubMed Web of Science ®Google Scholar
• Thompson, D. B., Villasenor, R., Dorr, B. M., Zerial, M., & Liu, D. R. (2012). Cellular uptake mechanisms and endosomal trafficking of supercharged proteins. Chemistry & Biology, 19(7), 831–843. https://doi.org/10.1016/j.chembiol.2012.06.014
   PubMedGoogle Scholar
• Tieleman, D. P. (2004). The molecular basis of electroporation. BMC Biochemistry, 5, 10–22. https://doi.org/10.1186/1471-2091-5-10
   PubMedGoogle Scholar
• Tieleman, D. P., & Berendsen, H. J. C. (1996). Molecular dynamics simulations of fully hydrated DPPC with different macroscopic boundary conditions and parameters. Journal of Chemical Physics, 105(11), 4871–4880. https://doi.org/10.1063/1.472323
   Web of Science ®Google Scholar
• Tieleman, P., Leontiadou, H., Mark, A. E., & Marrink, S.-J. (2003). Simulation of pore formation in lipid bilayers by mechanical stress and electric fields. Journal of the American Chemical Society, 125(21), 6382–6383. https://doi.org/10.1021/ja029504i
   PubMed Web of Science ®Google Scholar
• Trimble, W. S., & Grinstein, S. (2015). Barriers to the free diffusion of proteins and lipids in the plasma membrane. The Journal of Cell Biology, 208(3), 259–271. https://doi.org/10.1083/jcb.201410071
   PubMed Web of Science ®Google Scholar
• van der Schaar, H. M., Rust, M. J., Chen, C., van der Ende-Metselaar, H., Wilschut, J., Zhuang, X., & Smit, J. M. (2008). Dissecting the cell entry pathway of dengue virus by single-particle tracking in living cells. PLoS Pathogens, 4(12), e1000244. https://doi.org/10.1371/journal.ppat.1000244
   PubMed Web of Science ®Google Scholar
• van der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. C. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26(16), 1701–1718. https://doi.org/10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Wan, S. W., Lin, C. F., Wang, S., Chen, Y. H., Yeh, T. M., Liu, H. S., Anderson, R., & Lin, Y. S. (2013). Current progress in dengue vaccines. Journal of Biomedical Science, 20, 37–39. https://doi.org/10.1186/1423-0127-20-37
   PubMed Web of Science ®Google Scholar
• Watson, H. (2015). Biological membranes. Essays in Biochemistry, 59, 43–70. https://doi.org/10.1042/bse0590043
   PubMed Web of Science ®Google Scholar
• Whittam, R., & Wheeler, K. P. (1970). Transport across cell membranes. Annual Review of Physiology, 32, 21–60. https://doi.org/10.1146/annurev.ph.32.030170.000321
   PubMedGoogle Scholar
• Yesylevskyy, S., Marrink, S.-J., & Mark, A. E. (2009). Alternative mechanisms for the interaction of the cell-penetrating peptides penetratin and the TAT peptide with lipid bilayers. Biophysical Journal, 97(1), 40–49. https://doi.org/10.1016/j.bpj.2009.03.059
   PubMed Web of Science ®Google Scholar
• Zhang, W., Chipman, P. R., Corver, J., Johnson, P. R., Zhang, Y., Mukhopadhyay, S., Baker, T. S., Strauss, J. H., Rossmann, M. G., & Kuhn, R. J. (2003). Visualization of membrane protein domains by cryo-electron microscopy of dengue virus. Nature Structural Biology, 10(11), 907–912. https://doi.org/10.1038/nsb990
   PubMedGoogle Scholar