Physiological models to study the effect of molecular crowding on multi-drug bound proteins: insights from SARS-CoV-2 main protease

References

• Abriata, L. A., Spiga, E., & Dal Peraro, M. (2016). Molecular effects of concentrated solutes on protein hydration, dynamics, and electrostatics. Biophysical Journal, 111(4), 743–755.
   PubMed Web of Science ®Google Scholar
• Ådén, J., & Wittung-Stafshede, P. (2014). Folding of an unfolded protein by macromolecular crowding in vitro. Biochemistry, 53(14), 2271–2277. https://doi.org/10.1021/bi500222g
   PubMed Web of Science ®Google Scholar
• Arakawa, T., & Timasheff, S. N. (1985). Mechanism of poly(ethylene glycol) interaction with proteins. Biochemistry, 24(24), 6756–6762.
   PubMed Web of Science ®Google Scholar
• Aumiller, W. M., Jr., Davis, B. W., Hatzakis, E., & Keating, C. D. (2014). Interactions of macromolecular crowding agents and cosolutes with small-molecule substrates: Effect on horseradish peroxidase activity with two different substrates. The Journal of Physical Chemistry B, 118(36), 10624–10632.
   PubMed Web of Science ®Google Scholar
• Bellissent-Funel, M.-C., Hassanali, A., Havenith, M., Henchman, R., Pohl, P., Sterpone, F., van der Spoel, D., Xu, Y., & Garcia, A. E. (2016). Water determines the structure and dynamics of proteins. Chemical Reviews, 116(13), 7673–7697. https://doi.org/10.1021/acs.chemrev.5b00664
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81(8), 3684–3690. https://doi.org/10.1063/1.448118
   Web of Science ®Google Scholar
• Bhat, Z. A., Chitara, D., Iqbal, J., Sanjeev, B. S., & Madhumalar, A. (2021). Targeting allosteric pockets of SARS-CoV-2 main protease Mpro. Journal of Biomolecular Structure and Dynamics., 1–16. https://doi.org/10.1080/07391102.2021.1891141
   Google Scholar
• Bhat, M. Y., Singh, L. R., & Dar, T. A. (2017). Trimethylamine N-oxide abolishes the chaperone activity of α-casein: An intrinsically disordered protein. Scientific Reports, 7(1), 6572. https://doi.org/10.1038/s41598-017-06836-2
   PubMedGoogle Scholar
• Bieschke, J., Herbst, M., Wiglenda, T., Friedrich, R. P., Boeddrich, A., Schiele, F., Kleckers, D., Lopez del Amo, J. M., Grüning, B. A., Wang, Q., Schmidt, M. R., Lurz, R., Anwyl, R., Schnoegl, S., Fändrich, M., Frank, R. F., Reif, B., Günther, S., Walsh, D. M., & Wanker, E. E. (2011). Small-molecule conversion of toxic oligomers to nontoxic β-sheet-rich amyloid fibrils. Nature Chemical Biology, 8(1), 93–101. https://doi.org/10.1038/nchembio.719
   PubMed Web of Science ®Google Scholar
• Case, D., Ben-Shalom, I., Brozell, S., Cerutti, D., Cheatham, T., III., & Cruzeiro, V. (2018). AMBER 2018. University of California.
   Google Scholar
• Chen, Y., Liu, Q., & Guo, D. (2020). Emerging coronaviruses: Genome structure, replication, and pathogenesis. Journal of Medical Virology, 92(4), 418–423. https://doi.org/10.1002/jmv.25681
   PubMed Web of Science ®Google Scholar
• De Vivo, M., Masetti, M., Bottegoni, G., & Cavalli, A. (2016). Role of molecular dynamics and related methods in drug discovery. Journal of Medicinal Chemistry, 59(9), 4035–4061.
   PubMed Web of Science ®Google Scholar
• Deshwal, A., & Maiti, S. (2021). Macromolecular crowding effect on the activity of liposome-bound alkaline phosphatase: A paradoxical inhibitory action. Langmuir, 37(23), 7273–7284. https://doi.org/10.1021/acs.langmuir.1c01177
   PubMed Web of Science ®Google Scholar
• Durai, P., Batool, M., Shah, M., & Choi, S. (2015, Aug). Middle East respiratory syndrome coronavirus: Transmission, virology and therapeutic targeting to aid in outbreak control. Experimental & Molecular Medicine, 47, e181. https://doi.org/10.1038/emm.2015.76
   PubMed Web of Science ®Google Scholar
• Ellson, J., Gansner, E. R., Koutsofios, E., North, S. C., & Woodhull, G. (2003). Graphviz and dynagraph – static and dynamic graph drawing tools. In Graph drawing software (pp. 127–148). Springer-Verlag.
   Google Scholar
• Essman, U., Perera, L., Berkowitz, M., Darden, T., Lee, H., & Pedersen, L. (1995). A smooth particle mesh ewald potential. Journal of Chemical Physics., 103(19), 8577–8592. https://doi.org/10.1063/1.470117
   Web of Science ®Google Scholar
• Estrada, E. (2020). Topological analysis of Sars-CoV-2 main protease. Chaos (Woodbury, NY), 30(6), 061102. https://doi.org/10.1063/5.0013029
   PubMed Web of Science ®Google Scholar
• Feig, M., & Sugita, Y. (2012). Variable interactions between protein crowders and biomolecular solutes are important in understanding cellular crowding. The Journal of Physical Chemistry B, 116(1), 599–605.
   PubMed Web of Science ®Google Scholar
• Feig, M., Yu, I., Wang, P-h., Nawrocki, G., & Sugita, Y. (2017). Crowding in cellular environments at an atomistic level from computer simulations. The Journal of Physical Chemistry B, 121(34), 8009–8025. https://doi.org/10.1021/acs.jpcb.7b03570
   PubMed Web of Science ®Google Scholar
• Gallagher, T., Alexander, P., Bryan, P., & Gilliland, G. L. (1994). Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein g and comparison with NMR. Biochemistry, 33(15), 4721–4729.
   PubMed Web of Science ®Google Scholar
• Gao, M., Estel, K., Seeliger, J., Friedrich, R. P., Dogan, S., Wanker, E. E., Winter, R., & Ebbinghaus, S. (2015). Modulation of human iapp fibrillation: Cosolutes, crowders and chaperones. Physical Chemistry Chemical Physics: PCCP, 17(13), 8338–8348. https://doi.org/10.1039/c4cp04682j
   PubMed Web of Science ®Google Scholar
• Gao, M., & Winter, R. (2015). The effects of lipid membranes, crowding and osmolytes on the aggregation, and fibrillation propensity of human IAPP. Journal of Diabetes Research, 2015, 849017. https://doi.org/10.1155/2015/849017
   PubMed Web of Science ®Google Scholar
• Harada, R., Tochio, N., Kigawa, T., Sugita, Y., & Feig, M. (2013). Reduced native state stability in crowded cellular environment due to protein-protein interactions. Journal of the American Chemical Society, 135(9), 3696–3701.
   PubMed Web of Science ®Google Scholar
• Horn, A. H. (2014). A consistent force field parameter set for zwitterionic amino acid residues. Journal of Molecular Modeling, 20(11), 2478. https://doi.org/10.1007/s00894-014-2478-z
   PubMed Web of Science ®Google Scholar
• Horvath, I., Kumar, R., & Wittung-Stafshede, P. (2021). Macromolecular crowding modulates α-synuclein amyloid fiber growth. Biophysical Journal, 120(16), 3374–3381.
   PubMed Web of Science ®Google Scholar
• Hou, S., Trochimczyk, P., Sun, L., Wisniewska, A., Kalwarczyk, T., & Zhang, X. (2016). How can macromolecular crowding inhibit biological reactions? The enhanced formation of DNA nanoparticles. Scientific Reports, 6(1), 1–11.
   PubMedGoogle Scholar
• Huang, L., Jin, R., Li, J., Luo, K., Huang, T., Wu, D., Wang, W., Chen, R., & Xiao, G. (2010). Macromolecular crowding converts the human recombinant PRPC to the soluble neurotoxic beta-oligomers. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 24(9), 3536–3543. https://doi.org/10.1096/fj.09-150987
   PubMed Web of Science ®Google Scholar
• Hubbard, R. E., & Kamran Haider, M. (2001). Hydrogen bonds in proteins: Role and strength. e LS.
   Google 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
• Jentsch, T. J. (2016). Vracs and other ion channels and transporters in the regulation of cell volume and beyond. Nature Reviews. Molecular Cell Biology, 17(5), 293–307. https://doi.org/10.1038/nrm.2016.29
   PubMed Web of Science ®Google Scholar
• Jin, Z., Du, X., Xu, Y., Deng, Y., Liu, M., & Zhao, Y. (2020). Structure of m pro from SARS-CoV-2 and discovery of its inhibitors. Nature, 582, 289–293.
   PubMed Web of Science ®Google Scholar
• Kanduc, M., Schlaich, A., Schneck, E., & Netz, R. R. (2016). Water-mediated interactions between hydrophilic and hydrophobic surfaces. Langmuir: The ACS Journal of Surfaces and Colloids, 32(35), 8767–8782.
   PubMed Web of Science ®Google Scholar
• Kasahara, K., Re, S., Nawrocki, G., Oshima, H., Mishima-Tsumagari, C., Miyata-Yabuki, Y., Kukimoto-Niino, M., Yu, I., Shirouzu, M., Feig, M., & Sugita, Y. (2021). Reduced efficacy of a Src kinase inhibitor in crowded protein solution. Nature Communications, 12(1), 1–8. https://doi.org/10.1038/s41467-021-24349-5
   PubMed Web of Science ®Google Scholar
• Kastritis, P. L., Rodrigues, J. P. G. L. M., & Bonvin, A. M. J. J. (2014). HADDOCK(2P2I): A biophysical model for predicting the binding affinity of protein-protein interaction inhibitors. Journal of Chemical Information and Modeling, 54(3), 826–836. https://doi.org/10.1021/ci4005332
   PubMed Web of Science ®Google Scholar
• Kuznetsova, I. M., Turoverov, K. K., & Uversky, V. N. (2014). What macromolecular crowding can do to a protein. International Journal of Molecular Sciences, 15(12), 23090–23140. https://doi.org/10.3390/ijms151223090
   PubMed Web of Science ®Google Scholar
• Liao, Y.-T., Manson, A. C., DeLyser, M. R., Noid, W. G., & Cremer, P. S. (2017). Trimethylamine n-oxide stabilizes proteins via a distinct mechanism compared with betaine and glycine. Proceedings of the National Academy of Sciences of the United States of America, 114(10), 2479–2484. https://www.pnas.org/content/114/10/2479 https://doi.org/10.1073/pnas.1614609114
   PubMed Web of Science ®Google Scholar
• Löwe, M., Kalacheva, M., Boersma, A. J., & Kedrov, A. (2020). The more the merrier: Effects of macromolecular crowding on the structure and dynamics of biological membranes. The FEBS Journal, 287(23), 5039–5067.
   PubMed Web of Science ®Google Scholar
• Mahdi, M., Mótyán, J. A., Szojka, Z. I., Golda, M., Miczi, M., & Tőzsér, J. (2020). Analysis of the efficacy of HIV protease inhibitors against SARS-CoV-2’s main protease. Virology Journal, 17(1), 1–8.
   PubMed Web of Science ®Google Scholar
• MATLAB. (2020). R2020b. The MathWorks Inc.
   Google Scholar
• Meagher, K. L., Redman, L. T., & Carlson, H. A. (2003). Development of polyphosphate parameters for use with the amber force field. Journal of Computational Chemistry, 24(9), 1016–1025.
   PubMed Web of Science ®Google Scholar
• Miklos, A. C., Sarkar, M., Wang, Y., & Pielak, G. J. (2011). Protein crowding tunes protein stability. Journal of the American Chemical Society, 133(18), 7116–7120.
   PubMed Web of Science ®Google Scholar
• Neidigh, J. W., Fesinmeyer, R. M., & Andersen, N. H. (2002). Designing a 20-residue protein. Nature Structural Biology, 9(6), 425–430.
   PubMedGoogle Scholar
• Oelmeier, S. A., Dismer, F., & Hubbuch, J. (2012). Molecular dynamics simulations on aqueous two-phase systems-single peg-molecules in solution. BMC Biophysics, 5(1), 14.
   PubMed Web of Science ®Google Scholar
• Okamoto, D. N., Oliveira, L. C. G., Kondo, M. Y., Cezari, M. H. S., Szeltner, Z., Juhász, T., Juliano, M. A., Polgár, L., Juliano, L., & Gouvea, I. E. (2010). Increase of SARS-CoV 3CL peptidase activity due to macromolecular crowding effects in the milieu composition. Biological Chemistry, 391(12), 1461–1468. https://doi.org/10.1515/BC.2010.145
   PubMed Web of Science ®Google Scholar
• Ostrowska, N., Feig, M., & Trylska, J. (2019). Modeling crowded environment in molecular simulations. Frontiers in Molecular Biosciences, 6, 86. https://www.frontiersin.org/article/103389/fmolb.2019.00086 https://doi.org/10.3389/fmolb.2019.00086
   PubMed Web of Science ®Google Scholar
• Palhano, F. L., Lee, J., Grimster, N. P., & Kelly, J. W. (2013). Toward the molecular mechanism (s) by which egcg treatment remodels mature amyloid fibrils. Journal of the American Chemical Society, 135(20), 7503–7510.
   PubMed Web of Science ®Google Scholar
• Park, J. O., Rubin, S. A., Xu, Y.-F., Amador-Noguez, D., Fan, J., Shlomi, T., & Rabinowitz, J. D. (2016). Metabolite concentrations, fluxes and free energies imply efficient enzyme usage. Nature Chemical Biology, 12(7), 482–489. https://doi.org/10.1038/nchembio.2077
   PubMed Web of Science ®Google Scholar
• Ribeiro, J., Ríos-Vera, C., Melo, F., & Schüller, A. (2019). Calculation of accurate interatomic contact surface areas for the quantitative analysis of non-bonded molecular interactions. Bioinformatics (Oxford, England), 35(18), 3499–3501.
   PubMed Web of Science ®Google Scholar
• Rincón, V., Bocanegra, R., Rodríguez-Huete, A., Rivas, G., & Mateu, M. G. (2011). Effects of macromolecular crowding on the inhibition of virus assembly and virus-cell receptor recognition. Biophysical Journal, 100(3), 738–746.
   PubMed Web of Science ®Google Scholar
• Roe, D. R., & Cheatham, T. E. III., (2013). Ptraj and cpptraj: Software for processing and analysis of molecular dynamics trajectory data. Journal of Chemical Theory and Computation, 9(7), 3084–3095.
   PubMed Web of Science ®Google Scholar
• Satyam, A., Kumar, P., Fan, X., Gorelov, A., Rochev, Y., Joshi, L., Peinado, H., Lyden, D., Thomas, B., Rodriguez, B., Raghunath, M., Pandit, A., & Zeugolis, D. (2014). Macromolecular crowding meets tissue engineering by self-assembly: A paradigm shift in regenerative medicine. Advanced Materials, 26(19), 3024–3034. https://doi.org/10.1002/adma.201304428
   PubMed Web of Science ®Google Scholar
• Schrödinger LLC. (2015, November). The PyMOL molecular graphics system. version 1.8.
   Google Scholar
• Seeliger, J., Werkmüller, A., & Winter, R. (2013). Macromolecular crowding as a suppressor of human iapp fibril formation and cytotoxicity. PloS One, 8(7), e69652.
   PubMed Web of Science ®Google Scholar
• Smith, S., Cianci, C., & Grima, R. (2017). Macromolecular crowding directs the motion of small molecules inside cells. Journal of the Royal Society Interface, 14(131), 20170047. https://royalsocietypublishing.org/doi/abs/10.1098/rsif.2017.0047 https://doi.org/10.1098/rsif.2017.0047
   PubMed Web of Science ®Google Scholar
• Stagg, L., Zhang, S.-Q., Cheung, M. S., & Wittung-Stafshede, P. (2007). Molecular crowding enhances native structure and stability of α/β protein flavodoxin. Proceedings of the National Academy of Sciences, 104(48), 18976–18981. https://www.pnas.org/content/104/48/18976
   PubMed Web of Science ®Google Scholar
• Tan, Y. S., Reeks, J., Brown, C. J., Thean, D., Ferrer Gago, F. J., Yuen, T. Y., Goh, E. T. L., Lee, X. E. C., Jennings, C. E., Joseph, T. L., Lakshminarayanan, R., Lane, D. P., Noble, M. E. M., & Verma, C. S. (2016). Benzene probes in molecular dynamics simulations reveal novel binding sites for ligand design. The Journal of Physical Chemistry Letters, 7(17), 3452–3457. https://doi.org/10.1021/acs.jpclett.6b01525
   PubMed Web of Science ®Google Scholar
• Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A., & Case, D. A. (2004). Development and testing of a general amber force field. Journal of Computational Chemistry, 25(9), 1157–1174.
   PubMed Web of Science ®Google Scholar
• Yadav, J. K. (2012). Macromolecular crowding enhances catalytic efficiency and stability of α-amylase. ISRN Biotechnology, 2013, 737805. https://doi.org/10.5402/2013/737805
   PubMedGoogle Scholar
• Yu, I., Mori, T., Ando, T., Harada, R., Jung, J., Sugita, Y., & Feig, M. (2016). Biomolecular interactions modulate macromolecular structure and dynamics in atomistic model of a bacterial cytoplasm. eLife, 5, e19274. https://doi.org/10.7554/eLife.19274
   PubMed Web of Science ®Google Scholar
• Zhang, L., Lin, D., Sun, X., Curth, U., Drosten, C., Sauerhering, L., Becker, S., Rox, K., & Hilgenfeld, R. (2020). Crystal structure of SARS-CoV-2 main protease provides a basis for design of improved α-ketoamide inhibitors. Science (New York, NY), 368(6489), 409–412.
   Google Scholar
• Zhou, P., Yang, X.-L., Wang, X.-G., Hu, B., Zhang, L., Zhang, W., Si, H.-R., Zhu, Y., Li, B., Huang, C.-L., Chen, H.-D., Chen, J., Luo, Y., Guo, H., Jiang, R.-D., Liu, M.-Q., Chen, Y., Shen, X.-R., Wang, X., … Shi, Z.-L. (2020). A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature, 579(7798), 270–273.
   PubMed Web of Science ®Google Scholar
• Zimmerman, S. B., & Minton, A. P. (1993). Macromolecular crowding: Biochemical, biophysical, and physiological consequences. Annual Review of Biophysics and Biomolecular Structure, 22, 27–65.
   PubMedGoogle Scholar