Molecular mechanism of ATP and RNA binding to Zika virus NS3 helicase and identification of repurposed drugs using molecular dynamics simulations

References

• Abola, E. E., Bernstein, F. C., & Koetzle, T. F. (1984). The protein data bank. In B. P. Schoenborn (Ed.), Neutrons in biology. Basic Life Sciences (Vol. 27, pp. 441–441). Boston, MA: Springer. https://doi.org/10.1007/978-1-4899-0375-4_26
   Google Scholar
• Ahmad, N., Badshah, S. L., Junaid, M., Ur Rehman, A., Muhammad, A., & Khan, K. (2021). Structural insights into the Zika virus NS1 protein inhibition using a computational approach. Journal of Biomolecular Structure & Dynamics, 39(8), 3004–3011. https://doi.org/10.1080/07391102.2020.1759453
   PubMed Web of Science ®Google Scholar
• Al-Bari, M. A. A. (2015). Chloroquine analogues in drug discovery: New directions of uses, mechanisms of actions and toxic manifestations from malaria to multifarious diseases. The Journal of Antimicrobial Chemotherapy, 70(6), 1608–1621. https://doi.org/10.1093/jac/dkv018
   PubMed Web of Science ®Google Scholar
• Alexandrov, V., Lehnert, U., Echols, N., Milburn, D., Engelman, D., & Gerstein, M. (2005). Normal modes for predicting protein motions: A comprehensive database assessment and associated Web tool. Protein Science, 14(3), 633–643. https://doi.org/10.1110/ps.04882105
   PubMed Web of Science ®Google Scholar
• Ashburn, T. T., & Thor, K. B. (2004). Drug repositioning: Identifying and developing new uses for existing drugs. Nature Reviews. Drug Discovery, 3(8), 673–683. https://doi.org/10.1038/nrd1468
   PubMed Web of Science ®Google Scholar
• Atilgan, A. R., Durell, S. R., Jernigan, R. L., Demirel, M. C., Keskin, O., & Bahar, I. (2001). Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophysical Journal, 80(1), 505–515. https://doi.org/10.1016/S0006-3495(01)76033-X
   PubMed Web of Science ®Google Scholar
• Badshah, S. L., Ahmad, N., Ur Rehman, A., Khan, K., Ullah, A., Alsayari, A., Muhsinah, A. B., & N Mabkhot, Y. (2019). Molecular docking and simulation of Zika virus NS3 helicase. BMC Chemistry, 13(1), 67–68. https://doi.org/10.1186/s13065-019-0582-y
   PubMed Web of Science ®Google Scholar
• Basavannacharya, C., & Vasudevan, S. G. (2014). Suramin inhibits helicase activity of NS3 protein of dengue virus in a fluorescence-based high throughput assay format. Biochemical and Biophysical Research Communications, 453(3), 539–544. https://doi.org/10.1016/j.bbrc.2014.09.113
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J., Postma, J. V., van Gunsteren, W. F., DiNola, A. R. H. J., & Haak, J. R. (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
• Berendsen, H. J. C., Postma, J. P. M., van Gunsteren, W. F., & Hermans, J. (1981). Interaction models for water in relation to protein hydration. In B. Pullman (Ed.), Intermolecular Forces. The Jerusalem Symposia on Quantum Chemistry and Biochemistry, (vol. 14, p. 331–342). Dordrecht: Springer. https://doi.org/10.1007/978-94-015-7658-1_21
   Google Scholar
• Beveridge, D. L., & Ravishanker, G. (1994). Molecular dynamics studies of DNA. Current Opinion in Structural Biology, 4(2), 246–255. https://doi.org/10.1016/S0959-440X(94)90316-6
   Web of Science ®Google Scholar
• Brasil, P., Pereira, J. P., Moreira, M. E., Ribeiro Nogueira, R. M., Damasceno, L., Wakimoto, M., Rabello, R. S., Valderramos, S. G., Halai, U.-A., Salles, T. S., Zin, A. A., Horovitz, D., Daltro, P., Boechat, M., Raja Gabaglia, C., Carvalho de Sequeira, P., Pilotto, J. H., Medialdea-Carrera, R., Cotrim da Cunha, D., … Nielsen-Saines, K. (2016). Zika virus infection in pregnant women in Rio de Janeiro. New England Journal of Medicine, 375(24), 2321–2334. https://doi.org/10.1056/NEJMoal1602412
   PubMed Web of Science ®Google Scholar
• Bussi, G., Donadio, D., & Parrinello, M. (2007). Canonical sampling through velocity rescaling. The Journal of Chemical Physics, 126(1), 014101. https://doi.org/10.1063/1.2408420
   PubMed Web of Science ®Google Scholar
• Cheatham, T. E. I., Miller, J. L., Fox, T., Darden, T. A., & Kollman, P. A. (1995). Molecular Dynamics simulations on solvated biomolecular systems: The particle mesh Ewald method leads to stable trajectories of DNA, RNA, and proteins. Journal of the American Chemical Society, 117(14), 4193–4194. https://doi.org/10.1021/ja00119a045
   Web of Science ®Google Scholar
• Cheatham, T. E., Miller, J. L., Spector, T. I., Cieplak, P., & Kollman, P. A. (1997). Molecular dynamics simulations on nucleic acid systems using the Cornell. Force field and particle mesh Ewald electrostatics. In Molecular modeling of nucleic acids, ACS Symposium Series (Vol. 682, p. 285–303). https://doi.org/10.1021/bk-1998-0682.ch017.
   Google Scholar
• Chen, J., Liu, D., Liu, L., Liu, P., Xu, Q., Xia, L., Ling, Y., Huang, D., Song, S., Zhang, D., Qian, Z., Li, T., Shen, Y., & Lu, H. (2020). A pilot study of hydroxychloroquine in treatment of patients with moderate COVID-19. Zhejiang da Xue Xue Bao. Yi Xue Ban = Journal of Zhejiang University. Medical Sciences, 49(2), 215–219. https://doi.org/10.3785/j.issn.1008-9292.2020.03.03
   PubMedGoogle Scholar
• Chen, F., Sun, H., Wang, J., Zhu, F., Liu, H., Wang, Z., Lei, T., Li, Y., & Hou, T. (2018). Assessing the performance of MM/PBSA and MM/GBSA methods. 8. Predicting binding free energies and poses of protein-RNA complexes. RNA (New York, NY), 24(9), 1183–1194. https://doi.org/10.1261/rna.065896.118
   PubMed Web of Science ®Google Scholar
• Daura, X., Gademann, K., Jaun, B., Seebach, D., Van Gunsteren, W. F., & Mark, A. E. (1999). Peptide folding: When simulation meets experiment. Angewandte Chemie International Edition, 38(1–2), 236–240. https://doi.org/10.1002/(SICI)1521-3773(19990115)38:1/2<236::AID-ANIE236>3.0.CO;2-M
   PubMed Web of Science ®Google Scholar
• Davidson, R. B., Hendrix, J., Geiss, B. J., & McCullagh, M. (2018). Allostery in the dengue virus NS3 helicase: Insights into the NTPase cycle from molecular simulations. PLoS Computational Biology, 14(4), e1006103. https://doi.org/10.1371/journal.pcbi.1006103
   PubMed Web of Science ®Google Scholar
• De Groot, N. S., Armaos, A., Graña-Montes, R., Alriquet, M., Calloni, G., Vabulas, R. M., & Tartaglia, G. G. (2019). RNA structure drives interaction with proteins. Nature Communications, 10(1), 3246. https://doi.org/10.1038/s41467-019-10923-5
   PubMedGoogle Scholar
• Draper, D. E. (1995). Protein-RNA recognition. Annual Review of Biochemistry, 64(1), 593–620. https://doi.org/10.1146/annurev.bi.64.070195.003113
   PubMedGoogle Scholar
• Eyal, E., & Bahar, I. (2008). Toward a molecular understanding of the anisotropic response of proteins to external forces: Insights from elastic network models. Biophysical Journal, 94(9), 3424–3435. https://doi.org/10.1529/biophysj.107.120733
   PubMed Web of Science ®Google Scholar
• Eyal, E., Lum, G., & Bahar, I. (2015). The anisotropic network model web server at 2015 (ANM 2.0). Bioinformatics (Oxford, England), 31(9), 1487–1489. https://doi.org/10.1093/bioinformatics/btu847
   PubMed Web of Science ®Google Scholar
• Flores, J. K., & Ataide, S. F. (2018). Structural changes of RNA in complex with proteins in the SRP. Frontiers in Molecular Biosciences, 5(7), 7. https://doi.org/10.3389/fmolb.2019.00117
   PubMedGoogle Scholar
• Gagnon, J. K., Law, S. M., & Brooks III, C. L. (2016). Flexible CDOCKER: Development and application of a pseudo-explicit structure-based docking method within CHARMM. Journal of Computational Chemistry, 37(8), 753–762. https://doi.org/10.1002/jcc.24259
   PubMed Web of Science ®Google Scholar
• Gehlhaar, D. K., Verkhivker, G. M., Rejto, P. A., Sherman, C. J., Fogel, D. R., Fogel, L. J., & Freer, S. T. (1995). Molecular recognition of the inhibitor AG-1343 by HIV-1 protease: Conformationally flexible docking by evolutionary programming. Chemistry & Biology, 2(5), 317–324. https://doi.org/10.1016/1074-5521(95)90050-0
   PubMedGoogle Scholar
• Gilson, M. K., Liu, T., Baitaluk, M., Nicola, G., Hwang, L., & Chong, J. (2016). BindingDB in 2015: A public database for medicinal chemistry, computational chemistry and systems pharmacology. Nucleic Acids Research, 44(D1), D1045–D1053. https://doi.org/10.1093/nar/gkv1072
   PubMed Web of Science ®Google Scholar
• Gosline, J., Lillie, M., Carrington, E., Guerette, P., Ortlepp, C., & Savage, K. (2002). Elastic proteins: Biological roles and mechanical properties. Philosophical Transactions of the Royal Society of London, Series B, 357(1418), 121–132. https://doi.org/10.1098/rstb.2001.1022
   PubMed Web of Science ®Google Scholar
• Han, Y., Mesplède, T., Xu, H., Quan, Y., & Wainberg, M. A. (2018). The antimalarial drug amodiaquine possesses anti-ZIKA virus activities. Journal of Medical Virology, 90(5), 796–802. https://doi.org/10.1002/jmv.25031
   PubMed Web of Science ®Google Scholar
• He, D., Gao, D., Lou, Y., Zhao, S., & Ruan, S. (2017). A comparison study of Zika virus outbreaks in French Polynesia, Colombia and the State of Bahia in Brazil. Scientific Reports, 7(1), 273–276. https://doi.org/10.1038/s41598-017-00253-1
   PubMedGoogle Scholar
• Hermann, T., & Westhof, E. (1998). Aminoglycoside binding to the hammerhead ribozyme: A general model for the interaction of cationic antibiotics with RNA. Journal of Molecular Biology, 276(5), 903–912. https://doi.org/10.1006/jmbi.1997.1590
   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
• Hess, B., Kutzner, C., Van Der Spoel, D., & Lindahl, E. (2008). GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. Journal of Chemical Theory and Computation, 4(3), 435–447. https://doi.org/10.1021/ct700301q
   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. https://doi.org/10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Ioos, S., Mallet, H. P., Goffart, I. L., Gauthier, V., Cardoso, T., & Herida, M. (2014). Current Zika virus epidemiology and recent epidemics. Medecine et Maladies Infectieuses, 44(7), 302–307. https://doi.org/10.1016/j.medmal.2014.04.008
   PubMed Web of Science ®Google Scholar
• Koplin, J., Mu, Y., Richter, C., Schwalbe, H., & Stock, G. (2005). Structure and dynamics of an RNA tetraloop: A joint molecular dynamics and NMR study. Structure (London, England: 1993), 13(9), 1255–1267. https://doi.org/10.1016/j.str.2005.
   PubMed Web of Science ®Google Scholar
• Kumar, D., Aarthy, M., Kumar, P., Singh, S. K., Uversky, V. N., & Giri, R. (2020). Targeting the NTPase site of Zika virus NS3 helicase for inhibitor discovery. Journal of Biomolecular Structure & Dynamics, 38(16), 4827–4837. https://doi.org/10.1080/07391102.2019.1689851
   PubMed Web of Science ®Google Scholar
• Kumari, R., Kumar, R., Lynn, A., & Open Source Drug Discovery Consortium. (2014). g_mmpbsa-a GROMACS tool for high-throughput MM-PBSA calculations. Journal of Chemical Information and Modeling, 54(7), 1951–1962. https://doi.org/10.1021/ci500020m
   PubMed Web of Science ®Google Scholar
• Lu, X. J., Bussemaker, H. J., & Olson, W. K. (2015). DSSR: An integrated software tool for dissecting the spatial structure of RNA. Nucleic Acids Research, 43(21), e142. https://doi.org/10.1093/nar/gkv716
   PubMed Web of Science ®Google Scholar
• Mastrangelo, E., Pezzullo, M., De Burghgraeve, T., Kaptein, S., Pastorino, B., Dallmeier, K., de Lamballerie, X., Neyts, J., Hanson, A. M., Frick, D. N., Bolognesi, M., & Milani, M. (2012). Ivermectin is a potent inhibitor of flavivirus replication specifically targeting NS3 helicase activity: New prospects for an old drug. The Journal of Antimicrobial Chemotherapy, 67(8), 1884–1894. https://doi.org/10.1093/jac/dks147
   PubMed Web of Science ®Google Scholar
• Meng, X. Y., Zhang, H. X., Mezei, M., & Cui, M. (2011). Molecular docking: A powerful approach for structure-based drug discovery. Current Computer-Aided Drug Design, 7(2), 146–157. https://doi.org/10.2174/157340911795677602
   PubMed Web of Science ®Google Scholar
• Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., Vizjak, A., Pižem, J., Petrovec, M., & Avšič Županc, T. (2016). Zika virus associated with microcephaly. The New England Journal of Medicine, 374(10), 951–958. https://doi.org/10.1056/NEJMoa1600651
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Huey, R., Lindstrom, W., Sanner, M. F., Belew, R. K., Goodsell, D. S., & Olson, A. J. (2009). AutoDock4 and AutoDockTools4: Automated docking with selective receptor flexibility. Journal of Computational Chemistry, 30(16), 2785–2791. https://doi.org/10.1002/jcc.21256
   PubMed Web of Science ®Google Scholar
• Muegge, I. (2006). PMF scoring revisited. Journal of Medicinal Chemistry, 49(20), 5895–5902. https://doi.org/10.1021/jm050038s
   PubMed Web of Science ®Google Scholar
• Muegge, I., & Martin, Y. C. (1999). A general and fast scoring function for protein-ligand interactions: A simplified potential approach. Journal of Medicinal Chemistry, 42(5), 791–804. https://doi.org/10.1021/jm980536j
   PubMed Web of Science ®Google Scholar
• Nifosì, R., Reyes, C. M., & Kollman, P. A. (2000). Molecular dynamics studies of the HIV-1 TAR and its complex with argininamide. Nucleic Acids Research, 28(24), 4944–4955. https://doi.org/10.1093/nar/28.24.4944
   PubMed Web of Science ®Google Scholar
• Parrill, A. L., & Reddy, M. R. (Eds.). (1999). Rational drug design: Novel methodology and practical applications. American Chemical Society. https://pubs.acs.org/doi/abs/10.1021/bk-1999-0719
   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
• Pattnaik, A., Sahoo, B. R., & Pattnaik, A. K. (2020). Current status of Zika virus vaccines: Successes and challenges. Vaccines, 8(2), 266. https://doi.org/10.3390/vaccines8020266
   Web of Science ®Google Scholar
• Pérez-Villa, A., Darvas, M., & Bussi, G. (2015). ATP dependent NS3 helicase interaction with RNA: Insights from molecular simulations. Nucleic Acids Research, 43(18), 8725–8734. https://doi.org/10.1093/nar/gkv872
   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
• Pierson, T. C., & Diamond, M. (2013). Flaviviruses. In Fields virology (6th ed.). Wolters Kluwer Health Adis (ESP).
   Google Scholar
• Pushpakom, S., Iorio, F., Eyers, P. A., Escott, K. J., Hopper, S., Wells, A., Doig, A., Guilliams, T., Latimer, J., McNamee, C., Norris, A., Sanseau, P., Cavalla, D., & Pirmohamed, M. (2019). Drug repurposing: Progress, challenges and recommendations. Nature Reviews Drug Discovery, 18(1), 41–58. https://doi.org/10.1038/nrd.2018.168
   PubMed Web of Science ®Google Scholar
• Reyes, C. M., & Kollman, P. A. (1999). Molecular dynamics studies of U1A-RNA complexes. RNA (New York, NY), 5(2), 235–244. https://doi.org/10.1017/s1355838299981657
   PubMed Web of Science ®Google Scholar
• Ross, C., Nizami, B., Glenister, M., Sheik Amamuddy, O., Atilgan, A. R., Atilgan, C., & Tastan Bishop, Ö. (2018). MODE-TASK: Large-scale protein motion tools. Bioinformatics (Oxford, England), 34(21), 3759–3763. https://doi.org/10.1093/bioinformatics/bty427
   PubMed Web of Science ®Google Scholar
• Ruchusatsawat, K., Wongjaroen, P., Posanacharoen, A., Rodriguez-Barraquer, I., Sangkitporn, S., Cummings, D. A. T., & Salje, H. (2019). Long-term circulation of Zika virus in Thailand: An observational study. The Lancet Infectious Diseases, 19(4), 439–446. https://doi.org/10.1016/S1473-3099(18)30718-7
   PubMed Web of Science ®Google Scholar
• Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234(3), 779–815. https://doi.org/10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Sanseau, P., & Koehler, J. (2011). Editorial: Computational methods for drug repurposing. Briefings in Bioinformatics, 12(4), 301–302. https://doi.org/10.1093/bib/bbr047
   PubMed Web of Science ®Google Scholar
• Saxena, S. K., Kumar, S., Sharma, R., Maurya, V. K., Dandu, H. R., & Bhatt, M. L. (2019). Zika virus disease in India - Update October 2018. Travel Medicine and Infectious Disease, 27, 121–122. doi:10.1016/j.tamid.2018.10.022.
   PubMed Web of Science ®Google Scholar
• Shadrick, W. R., Mukherjee, S., Hanson, A. M., Sweeney, N. L., & Frick, D. N. (2013). Aurintricarboxylic acid modulates the affinity of hepatitis C virus NS3 helicase for both nucleic acid and ATP. Biochemistry, 52(36), 6151–6159. https://doi.org/10.1021/bi4006495
   PubMed Web of Science ®Google Scholar
• da Silva, A. W., & Vranken, W. F. (2012). ACPYPE - AnteChamber PYthon Parser interfacE. BMC Research Notes, 5(1), 1–8. https://doi.org/10.1186/1756-0500-5-367
   PubMedGoogle Scholar
• Sun, H., Li, Y., Shen, M., Tian, S., Xu, L., Pan, P., Guan, Y., & Hou, T. (2014). Assessing the performance of MM/PBSA and MM/GBSA methods. 5. Improved docking performance using high solute dielectric constant MM/GBSA and MM/PBSA rescoring. Physical Chemistry Chemical Physics: PCCP, 16(40), 22035–22045. https://doi.org/10.1039/c4cp03179b
   PubMed Web of Science ®Google Scholar
• Tang, Y., & Nilsson, L. (1999). Molecular dynamics simulations of the complex between human U1A protein and hairpin II of U1 small nuclear RNA and of free RNA in solution. Biophysical Journal, 77(3), 1284–1305. https://doi.org/10.1016/S0006-3495(99)76979-1
   PubMed Web of Science ®Google Scholar
• Tian, H., Ji, X., Yang, X., Zhang, Z., Lu, Z., Yang, K., Chen, C., Zhao, Q., Chi, H., Mu, Z., Xie, W., Wang, Z., Lou, H., Yang, H., & Rao, Z. (2016). Structural basis of Zika virus helicase in recognizing its substrates. Protein & Cell, 7(8), 562–570. https://doi.org/10.1007/s13238-016-0293-2
   PubMed Web of Science ®Google Scholar
• Uyar, A., Kurkcuoglu, O., Nilsson, L., & Doruker, P. (2011). The elastic network model reveals a consistent picture on intrinsic functional dynamics of type II restriction endonucleases. Physical Biology, 8(5), 056001. https://doi.org/10.1088/1478-3975/8/5/056001
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (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
• Viveiros-Rosa, S. G., Regis, E. G., & Santos, W. C. (2020). Vector competence of Culex mosquitoes (Diptera: Culicidae) in Zika virus transmission: An integrative review. Revista Panamericana de Salud Publica = Pan American Journal of Public Health, 44, e7. https://doi.org/10.26633/RPSP.2020.7
   PubMed Web of Science ®Google Scholar
• Watts, A. G., Carmen Huber, M. S. A., Bogoch, I. I., Brady, O. J., Kraemer, M. U. G., & Khan, K. (2019). Potential Zika virus spread within and beyond India. Journal of Travel Medicine, 26(1), tay132. https://doi.org/10.1093/jtm/tay132
   Google Scholar
• Weng, G., Wang, E., Chen, F., Sun, H., Wang, Z., & Hou, T. (2019). Assessing the performance of MM/PBSA and MM/GBSA methods. 9. Prediction reliability of binding affinities and binding poses for protein-peptide complexes. Physical Chemistry Chemical Physics: PCCP, 21(19), 10135–10145. https://doi.org/10.1039/c9cp01674k
   PubMed Web of Science ®Google Scholar
• Wikan, N., & Smith, D. R. (2016). Zika virus: History of a newly emerging arbovirus. The Lancet. Infectious Diseases, 16 (7), e119–e126. https://doi.org/10.1016/S1473-3099(16)30010-X
   PubMed Web of Science ®Google Scholar
• Wiley, E. A., MacDonald, M., Lambropoulos, A., Harriman, D. J., & Deslongchamps, G. (2006). LGA-Dock/EM-Dock—Exploring Lamarckian genetic algorithms and energy-based local search for ligand–receptor docking. Canadian Journal of Chemistry, 84(3), 384–391. https://doi.org/10.1139/v06-012
   Web of Science ®Google Scholar
• Williams, D. J., & Hall, K. B. (2000). Experimental and computational studies of the G[UUCG]C RNA tetraloop. Journal of Molecular Biology, 297(5), 1045–1061. https://doi.org/10.1006/jmbi.2000.3623
   PubMed Web of Science ®Google Scholar
• Xu, S., Ci, Y., Wang, L., Yang, Y., Zhang, L., Xu, C., Qin, C., & Shi, L. (2019). Zika virus NS3 is a canonical RNA helicase stimulated by NS5 RNA polymerase. Nucleic Acids Research, 47(16), 8693–8707. https://doi.org/10.1093/nar/gkz650
   PubMed Web of Science ®Google Scholar
• Yadav, P. D., Malhotra, B., Sapkal, G., Nyayanit, D. A., Deshpande, G., Gupta, N., Padinjaremattathil, U. T., Sharma, H., Sahay, R. R., Sharma, P., & Mourya, D. T. (2019). Zika virus outbreak in Rajasthan, India in 2018 was caused by a virus endemic to Asia. Infection, Genetics and Evolution, 69, 199–202. https://doi.org/10.1016/j.meegid.2019.01.026
   PubMed Web of Science ®Google Scholar
• Yadav, R., Selvaraj, C., Aarthy, M., Kumar, P., Kumar, A., Singh, S. K., & Giri, R. (2021). Investigating into the molecular interactions of flavonoids targeting NS2B-NS3 protease from ZIKA virus through in-silico approaches. Journal of Biomolecular Structure & Dynamics, 39(1), 272–284. https://doi.org/10.1080/07391102.2019.1709546
   PubMed Web of Science ®Google Scholar
• Young, M. A., & Beveridge, D. L. (1998). Molecular dynamics simulations of an oligonucleotide duplex with adenine tracts phased by a full helix turn. Journal of Molecular Biology, 281(4), 675–687. https://doi.org/10.1006/jmbi.1998.1962
   PubMed Web of Science ®Google Scholar
• Zacharias, M. (2000). Simulation of the structure and dynamics of nonhelical RNA motifs. Current Opinion in Structural Biology, 10(3), 311–317. https://doi.org/10.1016/S0959-440X(00)00089-0
   PubMed Web of Science ®Google Scholar
• Zacharias, M., & Sklenar, H. (1999). Conformational analysis of single-base b + 69-ulges in A-form DNA and RNA using a hierarchical approach and energetic evaluation with a continuum solvent model. Journal of Molecular Biology, 289(2), 261–275. https://doi.org/10.1006/jmbi.1999.2760
   PubMed Web of Science ®Google Scholar