285
Views
0
CrossRef citations to date
0
Altmetric
Research Articles

Antimalarial phytochemicals as potential inhibitors of SARS-CoV-2 guanine N7-methyltransferase (nsp 14): an integrated computational approach

ORCID Icon, , , , , , ORCID Icon, , , , , & show all
Pages 5022-5044 | Received 07 Dec 2021, Accepted 11 May 2022, Published online: 28 May 2022

References

  • Benkert, P., Biasini, M., & Schwede, T. (2011). Toward the estimation of the absolute quality of individual protein structure models. Bioinformatics (Oxford, England), 27(3), 343–350. https://doi.org/10.1093/bioinformatics/btq662
  • Bhattacharya, D., Nowotny, J., Cao, R., & Cheng, J. (2016). 3Drefine: An interactive web server for efficient protein structure refinement. Nucleic Acids Research, 44(W1), W406–W409. https://doi.org/10.1093/nar/gkw336
  • Biasini, M., Bienert, S., Waterhouse, A., Arnold, K., Studer, G., Schmidt, T., Kiefer, F., Gallo Cassarino, T., Bertoni, M., Bordoli, L., & Schwede, T. (2014). SWISS-MODEL: Modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Research, 42(Web Server issue), W252–W258. https://doi.org/10.1093/nar/gku340
  • Borquaye, L. S., Gasu, E. N., Ampomah, G. B., Kyei, L. K., Amarh, M. A., Mensah, C. N., Nartey, D., Commodore, M., Adomako, A. K., Acheampong, P., Mensah, J. O., Mormor, D. B., & Aboagye, C. I. (2020). Alkaloids from Cryptolepis sanguinolenta as potential inhibitors of SARS-CoV-2 viral proteins: An in silico study. BioMed Research International, 2020, 5324560. https://doi.org/10.1155/2020/5324560
  • Borquaye, L. S., Gasu, E. N., Ampomah, G. B., Kyei, L. K., Amarh, M. A., Mensah, C. N., Nartey, D., Commodore, M., Adomako, A. K., Acheampong, P., Mensah, J. O., Mormor, D. B., & Aboagye, C. I. (2020). Alkaloids from Cryptolepis sanguinolenta as potential inhibitors of SARS-CoV-2 viral proteins: An in silico study. BioMed Research International, 2020, 1–14. https://doi.org/10.1155/2020/5324560
  • Bouvet, M., Debarnot, C., Imbert, I., Selisko, B., Snijder, E. J., Canard, B., & Decroly, E. (2010). In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathogens, 6(4), e1000863. https://doi.org/10.1371/journal.ppat.1000863
  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., & Madden, T. L. (2009). BLAST+: Architecture and applications. BMC Bioinformatics, 10(1), 421. https://doi.org/10.1186/1471-2105-10-421
  • Chen, Y., Cai, H., Pan, J., Xiang, N., Tien, P., Ahola, T., & Guo, D. (2009). Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proceedings of the National Academy of Sciences of the United States of America, 106(9), 3484–3489. https://doi.org/10.1073/pnas.0808790106
  • Cheng, X., & Ivanov, I. (2012). Molecular dynamics. In Computational toxicology, 929, 243–285. https://doi.org/10.1007/978-1-62703-050-2_11
  • Cheng, V. C., Lau, S. K., Woo, P. C., & Yuen, K. Y. (2007). Severe acute respiratory syndrome coronavirus as an agent of emerging and reemerging infection. Clinical Microbiology Reviews, 20(4), 660–694. https://doi.org/10.1128/CMR.00023-07
  • Cheng, F., Li, W., Zhou, Y., Shen, J., Wu, Z., Liu, G., Lee, P. W., & Tang, Y. (2012). admetSAR: A comprehensive source and free tool for assessment of chemical ADMET properties. Journal of Chemical Information and Modeling, 52(11), 3099–3105. https://doi.org/10.1021/ci300367a
  • Cilia, E., Pancsa, R., Tompa, P., Lenaerts, T., & Vranken, W. F. (2014). The DynaMine webserver: Predicting protein dynamics from sequence. Nucleic Acids Research, 42(Web Server issue), W264–W270. https://doi.org/10.1093/nar/gku270
  • Cimanga, K., De Bruyne, T., Lasure, A., Van Poel, B., Pieters, L., Claeys, M., Berghe, D. V., Kambu, K., Tona, L., & Vlietinck, A. J. (1996). In vitro biological activities of alkaloids from Cryptolepis sanguinolenta. Planta Medica, 62(01), 22–27. https://doi.org/10.1055/s-2006-957789
  • Cimanga, K., De Bruyne, T., Pieters, L., Totte, J., Tona, L., Kambu, K., Berghe, D. V., & Vlietinck, A. (1998). Antibacterial and antifungal activities of neocryptolepine, biscryptolepine and cryptoquindoline, alkaloids isolated from Cryptolepis sanguinolenta. Phytomedicine, 5(3), 209–214. https://doi.org/10.1016/S0944-7113(98)80030-5
  • Colovos, C., & Yeates, T. O. (1993). Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Science : A Publication of the Protein Society, 2(9), 1511–1519. https://doi.org/10.1002/pro.5560020916
  • Daina, A., Michielin, O., & Zoete, V. (2017). SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Scientific Reports, 7, 42717. https://doi.org/10.1038/srep42717
  • Dallakyan, S., & Olson, A. J. (2015). Small-molecule library screening by docking with PyRx. Chemical biology, 1263, 243–250. https://doi.org/10.1007/978-1-4939-2269-7_19
  • Decroly, E., Debarnot, C., Ferron, F., Bouvet, M., Coutard, B., Imbert, I., Gluais, L., Papageorgiou, N., Sharff, A., Bricogne, G., Ortiz-Lombardia, M., Lescar, J., & Canard, B. (2011). Crystal structure and functional analysis of the SARS-coronavirus RNA cap 2′-O-methyltransferase nsp10/nsp16 complex. PLoS Pathogens, 7(5), e1002059. https://doi.org/10.1371/journal.ppat.1002059
  • Eckerle, L. D., Becker, M. M., Halpin, R. A., Li, K., Venter, E., Lu, X., Scherbakova, S., Graham, R. L., Baric, R. S., Stockwell, T. B., Spiro, D. J., & Denison, M. R. (2010). Infidelity of SARS-CoV Nsp14-exonuclease mutant virus replication is revealed by complete genome sequencing. PLoS Pathogens, 6(5), e1000896. https://doi.org/10.1371/journal.ppat.1000896
  • Fabrega, C., Hausmann, S., Shen, V., Shuman, S., & Lima, C. D. (2004). Structure and mechanism of mRNA cap (guanine-N7) methyltransferase. Molecular Cell, 13(1), 77–89. https://doi.org/10.1016/S1097-2765(03)00522-7
  • Fukai, T., Hano, Y., HIRAKURA, K., NOMURA, T., Uzawa, J., & FUKUSHIMA, K. (1985). Structures of two natural hypotensive diels-alder type adducts, mulberrofurans f and g, from the cultivated mulberry tree (morus lhou koidz.). Chemical & Pharmaceutical Bulletin, 33(8), 3195–3204. https://doi.org/10.1248/cpb.33.3195
  • Gendrot, M., Andreani, J., Boxberger, M., Jardot, P., Fonta, I., Le Bideau, M., Duflot, I., Mosnier, J., Rolland, C., Bogreau, H., Hutter, S., La Scola, B., & Pradines, B. (2020). Antimalarial drugs inhibit the replication of SARS-CoV-2: An in vitro evaluation. Travel Medicine and Infectious Disease, 37, 101873. https://doi.org/10.1016/j.tmaid.2020.101873
  • Gyebi, G. A., Adegunloye, A. P., Ibrahim, I. M., Ogunyemi, O. M., Afolabi, S. O., & Ogunro, O. B. (2022). Prevention of SARS-CoV-2 cell entry: Insight from in silico interaction of drug-like alkaloids with spike glycoprotein, human ACE2, and TMPRSS2. Journal of Biomolecular Structure and Dynamics, 40(5), 2121-2145. https://doi.org/10.1080/07391102.2020.1764868
  • Gyebi, G. A., Ogunro, O. B., Adegunloye, A. P., Ogunyemi, O. M., & Afolabi, S. O. (2020). Potential inhibitors of coronavirus 3-chymotrypsin-like protease (3CLpro): An in silico screening of alkaloids and terpenoids from African medicinal plants. Journal of Biomolecular Structure and Dynamics, 39(9), 3396-3408.https://doi.org/10.1080/07391102.2020.1764868
  • Haagmans, B. L., Al Dhahiry, S. H. S., Reusken, C. B. E. M., Raj, V. S., Galiano, M., Myers, R., Godeke, G.-J., Jonges, M., Farag, E., Diab, A., Ghobashy, H., Alhajri, F., Al-Thani, M., Al-Marri, S. A., Al Romaihi, H. E., Al Khal, A., Bermingham, A., Osterhaus, A. D. M. E., AlHajri, M. M., & Koopmans, M. P. G. (2014). Middle East respiratory syndrome coronavirus in dromedary camels: An outbreak investigation. The Lancet. Infectious Diseases, 14(2), 140–145. https://doi.org/10.1016/S1473-3099(13)70690-X
  • Heo, L., Park, H., & Seok, C. (2013). GalaxyRefine: Protein structure refinement driven by side-chain repacking. Nucleic Acids Research, 41(Web Server issue), W384–W388. https://doi.org/10.1093/nar/gkt458
  • Hoffmann, M., Kleine-Weber, H., Schroeder, S., Krüger, N., Herrler, T., Erichsen, S., Schiergens, T. S., Herrler, G., Wu, N.-H., Nitsche, A., Müller, M. A., Drosten, C., & Pöhlmann, S. (2020). SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell, 181(2), 271–280.e8. https://doi.org/10.1016/j.cell.2020.02.052
  • Hosseini, F. S., & Amanlou, M. (2020). Anti-HCV and anti-malaria agent, potential candidates to repurpose for coronavirus infection: Virtual screening, molecular docking, and molecular dynamics simulation study. Life Sciences, 258, 118205. https://doi.org/10.1016/j.lfs.2020.118205
  • Hussein, M. I. H., Albashir, A. A. D., Elawad, O. A. M. A., & Homeida, A. (2020). Malaria and COVID-19: Unmasking their ties. Malaria Journal, 19(1), 1–10. https://doi.org/10.1186/s12936-020-03541-w
  • Ivanov, K. A., Thiel, V., Dobbe, J. C., Van Der Meer, Y., Snijder, E. J., & Ziebuhr, J. (2004). Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. Journal of Virology, 78(11), 5619–5632. https://doi.org/10.1128/JVI.78.11.5619-5632.2004
  • Jin, X., Chen, Y., Sun, Y., Zeng, C., Wang, Y., Tao, J., Wu, A., Yu, X., Zhang, Z., Tian, J., & Guo, D. (2013). Characterization of the guanine-N7 methyltransferase activity of coronavirus nsp14 on nucleotide GTP. Virus Research, 176(1–2), 45–52. https://doi.org/10.1016/j.virusres.2013.05.001
  • Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W., & Klein, M. L. (1983). Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics79(2), 926–935. https://doi.org/10.1063/1.445869
  • Kratz, J. M., Grienke, U., Scheel, O., Mann, S. A., & Rollinger, J. M. (2017). Natural products modulating the hERG channel: Heartaches and hope. Natural Product Reports, 34(8), 957–980. https://doi.org/10.1039/c7np00014f
  • Laskowski, R., MacArthur, M., Moss, D., & Thornton, J. (1993). SFCHECK: A unified set of procedures for evaluating the quality of macromolecular structure-factor data and their agreement with the atomic model. Journal of Applied Crystallography, 26(2), 283–291. https://doi.org/10.1107/S0021889892009944
  • Li, W., Moore, M. J., Vasilieva, N., Sui, J., Wong, S. K., Berne, M. A., Somasundaran, M., Sullivan, J. L., Luzuriaga, K., Greenough, T. C., Choe, H., & Farzan, M. (2003). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature, 426(6965), 450–454. https://doi.org/10.1038/nature02145
  • Lim, Y. X., Ng, Y. L., Tam, J. P., & Liu, D. X. (2016). Human coronaviruses: A review of virus–host interactions. Diseases, 4(4), 26. https://doi.org/10.3390/diseases4030026
  • Lin, J. H., & Yamazaki, M. (2003). Role of P-glycoprotein in pharmacokinetics: Clinical implications. Clinical Pharmacokinetics, 42(1), 59–98. https://doi.org/10.2165/00003088-200342010-00003
  • Lipinski, C. A. (2000). Drug-like properties and the causes of poor solubility and poor permeability. Journal of Pharmacological and Toxicological Methods, 44(1), 235–249. https://doi.org/10.1016/S1056-8719(00)00107-6
  • Liu, J., Cao, R., Xu, M., Wang, X., Zhang, H., Hu, H., Li, Y., Hu, Z., Zhong, W., & Wang, M. (2020). Hydroxychloroquine, a less toxic derivative of chloroquine, is effective in inhibiting SARS-CoV-2 infection in vitro. Cell Discovery, 6, 16. 2020. https://doi.org/10.1038/s41421-020-0156-0
  • Luo, H., Chen, Q., Chen, J., Chen, K., Shen, X., & Jiang, H. (2005). The nucleocapsid protein of SARS coronavirus has a high binding affinity to the human cellular heterogeneous nuclear ribonucleoprotein A1. FEBS Letters, 579(12), 2623–2628. https://doi.org/10.1016/j.febslet.2005.03.080
  • Ma, Y., Wu, L., Shaw, N., Gao, Y., Wang, J., Sun, Y., Lou, Z., Yan, L., Zhang, R., & Rao, Z. (2015). Structural basis and functional analysis of the SARS coronavirus nsp14-nsp10 complex. Proceedings of the National Academy of Sciences of the United States of America, 112(30), 9436–9441. https://doi.org/10.1073/pnas.1508686112
  • Martyna, G. J., Klein, M. L., & Tuckerman, M. (1992). Nosé–Hoover chains: The canonical ensemble via continuous dynamics. The Journal of Chemical Physics, 97(4), 2635–2643. https://doi.org/10.1063/1.463940
  • Masters, P. S. (2006). The molecular biology of coronaviruses. Advances in Virus Research, 66, 193–292.
  • Maurya, A. K., & Mishra, N. (2021). In silico validation of coumarin derivatives as potential inhibitors against Main Protease, NSP10/NSP16-Methyltransferase, Phosphatase and Endoribonuclease of SARS CoV-2. Journal of Biomolecular Structure & Dynamics, 39(18), 7306–7321. https://doi.org/10.1080/07391102.2020.1808075
  • Napoli, P. E., & Nioi, M. (2020). Global spread of coronavirus disease 2019 and malaria: An epidemiological paradox in the early stage of a pandemic. Multidisciplinary Digital Publishing Institute.
  • O'Boyle, N. M., Banck, M., James, C. A., Morley, C., Vandermeersch, T., & Hutchison, G. R. (2011). Open Babel: An Open chemical toolbox. Journal of Cheminformatics, 3(1), 33–33. https://doi.org/10.1186/1758-2946-3-33
  • O'Brien, D., Tobin, S., Brown, G. V., & Torresi, J. (2001). Fever in returned travelers: Review of hospital admissions for a 3-year period. Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 33(5), 603–609. https://doi.org/10.1086/322602
  • Onguéné, P. A., Ntie-Kang, F., Lifongo, L. L., Ndom, J. C., Sippl, W., & Mbaze, L. M. a. (2013). The potential of anti-malarial compounds derived from African medicinal plants, part I: A pharmacological evaluation of alkaloids and terpenoids. Malaria Journal, 12(1), 449. https://doi.org/10.1186/1475-2875-12-449
  • Osafo, N., Mensah, K. B., & Yeboah, O. K. (2017). Phytochemical and pharmacological review of Cryptolepis sanguinolenta (Lindl.) Schlechter. Advances in Pharmacological Sciences, 2017, 3026370. https://doi.org/10.1155/2017/3026370
  • Peiris, J. S. M., Chu, C. M., Cheng, V. C. C., Chan, K. S., Hung, I. F. N., Poon, L. L. M., Law, K. I., Tang, B. S. F., Hon, T. Y. W., Chan, C. S., Chan, K. H., Ng, J. S. C., Zheng, B. J., Ng, W. L., Lai, R. W. M., Guan, Y., & Yuen, K. Y. (2003). Clinical progression and viral load in a community outbreak of coronavirus-associated SARS pneumonia: A prospective study. The Lancet, 361(9371), 1767–1772. https://doi.org/10.1016/S0140-6736(03)13412-5
  • Peiris, J. S. M., Lai, S. T., Poon, L. L. M., Guan, Y., Yam, L. Y. C., Lim, W., Nicholls, J., Yee, W. K. S., Yan, W. W., Cheung, M. T., Cheng, V. C. C., Chan, K. H., Tsang, D. N. C., Yung, R. W. H., Ng, T. K., & Yuen, K. Y. (2003). Coronavirus as a possible cause of severe acute respiratory syndrome. The Lancet, 361(9366), 1319–1325. https://doi.org/10.1016/S0140-6736(03)13077-2
  • Peiris, J. S., Yuen, K. Y., Osterhaus, A. D., & Stöhr, K. (2003). The severe acute respiratory syndrome. The New England Journal of Medicine, 349(25), 2431–2441. https://doi.org/10.1056/NEJMra032498
  • Raies, A. B., & Bajic, V. B. (2016). In silico toxicology: Computational methods for the prediction of chemical toxicity. Wiley Interdisciplinary Reviews. Computational Molecular Science, 6(2), 147–172. https://doi.org/10.1002/wcms.1240
  • Raj, V. S., Mou, H., Smits, S. L., Dekkers, D. H. W., Müller, M. A., Dijkman, R., Muth, D., Demmers, J. A. A., Zaki, A., Fouchier, R. A. M., Thiel, V., Drosten, C., Rottier, P. J. M., Osterhaus, A. D. M. E., Bosch, B. J., & Haagmans, B. L. (2013). Dipeptidyl peptidase 4 is a functional receptor for the emerging human coronavirus-EMC. Nature, 495(7440), 251–254. https://doi.org/10.1038/nature12005
  • Raschi, E., Vasina, V., Poluzzi, E., & De Ponti, F. (2008). The hERG K + channel: Target and antitarget strategies in drug development. Pharmacological Research, 57(3), 181–195. https://doi.org/10.1016/j.phrs.2008.01.009
  • Remmert, M., Biegert, A., Hauser, A., & Söding, J. (2011). HHblits: Lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nature Methods, 9(2), 173–175. https://doi.org/10.1038/nmeth.1818
  • Rodrigues-Diez, R. R., Tejera-Muñoz, A., Marquez-Exposito, L., Rayego-Mateos, S., Santos Sanchez, L., Marchant, V., Tejedor Santamaria, L., Ramos, A. M., Ortiz, A., Egido, J., & Ruiz-Ortega, M. (2020). Statins: Could an old friend help in the fight against COVID-19? British Journal of Pharmacology, 177(21), 4873–4886. https://doi.org/10.1111/bph.15166
  • Saldívar-González, F. I., Gómez-García, A., Chavez-Ponce de Leon, D. E., Sánchez-Cruz, N., Ruiz-Rios, J., Pilón-Jiménez, B. A., & Medina-Franco, J. L. (2018). Inhibitors of DNA methyltransferases from natural sources: A computational perspective. Frontiers in Pharmacology, 9, 1144. https://doi.org/10.3389/fphar.2018.01144
  • Saramago, M., Bárria, C., Costa, V., Souza, C. S., Viegas, S. C., Domingues, S., Lousa, D., Soares, C. M., Arraiano, C. M., & Matos, R. G. (2021). New targets for drug design: Importance of nsp14/nsp10 complex formation for the 3'-5'exoribonucleolytic activity on SARS-CoV-2. bioRxiv,
  • Savarino, A., Boelaert, J. R., Cassone, A., Majori, G., & Cauda, R. (2003). Effects of chloroquine on viral infections: An old drug against today's diseases. The Lancet. Infectious Diseases, 3(11), 722–727. https://doi.org/10.1016/S1473-3099(03)00806-5
  • Schlagenhauf, P., Grobusch, M. P., Maier, J. D., & Gautret, P. (2020). Repurposing antimalarials and other drugs for COVID-19. Travel Medicine and Infectious Disease, 34, 101658. https://doi.org/10.1016/j.tmaid.2020.101658
  • Selvaraj, C., Dinesh, D. C., Panwar, U., Abhirami, R., Boura, E., & Singh, S. K. (2021). Structure-based virtual screening and molecular dynamics simulation of SARS-CoV-2 Guanine-N7 methyltransferase (nsp14) for identifying antiviral inhibitors against COVID-19. Journal of Biomolecular Structure & Dynamics, 39(13), 4582–4593. https://doi.org/10.1080/07391102.2020.1778535
  • Sinha, S., & Wang, S. M. (2020). Classification of VUS and unclassified variants in BRCA1 BRCT repeats by molecular dynamics simulation. Computational and Structural Biotechnology Journal, 18, 723–736. https://doi.org/10.1016/j.csbj.2020.03.013
  • Sola, I., Moreno, J. L., Zúniga, S., Alonso, S., & Enjuanes, L. (2005). Role of nucleotides immediately flanking the transcription-regulating sequence core in coronavirus subgenomic mRNA synthesis. Journal of Virology, 79(4), 2506–2516. https://doi.org/10.1128/JVI.79.4.2506-2516.2005
  • Tahir, M. (2021). Coronavirus genomic nsp14-ExoN, structure, role, mechanism, and potential application as a drug target. Journal of Medical Virology, 93(7), 4258–4264. https://doi.org/10.1002/jmv.27009
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. https://doi.org/10.1002/jcc.21334
  • Van Miert, S., Hostyn, S., Maes, B. U. W., Cimanga, K., Brun, R., Kaiser, M., Mátyus, P., Dommisse, R., Lemière, G., Vlietinck, A., & Pieters, L. (2005). Isoneocryptolepine, a synthetic indoloquinoline alkaloid, as an antiplasmodial lead compound. Journal of Natural Products, 68(5), 674–677. https://doi.org/10.1021/np0496284
  • Veber, D. F., Johnson, S. R., Cheng, H.-Y., Smith, B. R., Ward, K. W., & Kopple, K. D. (2002). Molecular properties that influence the oral bioavailability of drug candidates. Journal of Medicinal Chemistry, 45(12), 2615–2623. https://doi.org/10.1021/jm020017n
  • Voss, A., Coombs, G., Unal, S., Saginur, R., & Hsueh, P.-R. (2020). Publishing in face of the COVID-19 pandemic. International Journal of Antimicrobial Agents, 56(1), 106081. Arthttps://doi.org/10.1016/j.ijantimicag.2020.106081
  • Wang, M., Cao, R., Zhang, L., Yang, X., Liu, J., Xu, M., Shi, Z., Hu, Z., Zhong, W., & Xiao, G. (2020). Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Research, 30(3), 269–271. https://doi.org/10.1038/s41422-020-0282-0
  • Waterhouse, A., Bertoni, M., Bienert, S., Studer, G., Tauriello, G., Gumienny, R., Heer, F. T., de Beer, T. A. P., Rempfer, C., Bordoli, L., Lepore, R., & Schwede, T. (2018). SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Research, 46(W1), W296–W303. https://doi.org/10.1093/nar/gky427
  • Webster, R. G. (2004). Wet markets—a continuing source of severe acute respiratory syndrome and influenza? The Lancet, 363(9404), 234–236. https://doi.org/10.1016/S0140-6736(03)15329-9
  • Wiederstein, M., & Sippl, M. J. (2007). ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research, 35(Web Server issue), W407–W410. https://doi.org/10.1093/nar/gkm290
  • Woo, P. C., Lau, S. K., & Yuen, K-y. (2006). Infectious diseases emerging from Chinese wet-markets: Zoonotic origins of severe respiratory viral infections. Current Opinion in Infectious Diseases, 19(5), 401–407. https://doi.org/10.1097/01.qco.0000244043.08264.fc
  • World Health Organization. (2019). World malaria report 2019. World Health Organization.
  • Xiang, Z. (2006). Advances in homology protein structure modeling. Current Protein & Peptide Science, 7(3), 217–227. https://doi.org/10.2174/138920306777452312
  • Yang, D., & Leibowitz, J. L. (2015). The structure and functions of coronavirus genomic 3' and 5' ends. Virus Research, 206, 120–133. https://doi.org/10.1016/j.virusres.2015.02.025
  • Yao, X., Ye, F., Zhang, M., Cui, C., Huang, B., Niu, P., Liu, X., Zhao, L., Dong, E., Song, C., Zhan, S., Lu, R., Li, H., Tan, W., & Liu, D. (2020). In vitro antiviral activity and projection of optimized dosing design of hydroxychloroquine for the treatment of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Clinical Infectious Diseases : An Official Publication of the Infectious Diseases Society of America, 71(15), 732–739. https://doi.org/10.1093/cid/ciaa237
  • Zanin, L., Saraceno, G., Panciani, P. P., Renisi, G., Signorini, L., Migliorati, K., & Fontanella, M. M. (2020). SARS-CoV-2 can induce brain and spine demyelinating lesions. Acta Neurochirurgica, 162(7), 1491–1494. https://doi.org/10.1007/s00701-020-04374-x
  • Zhou, D., Dai, S.-M., & Tong, Q. (2020). COVID-19: A recommendation to examine the effect of hydroxychloroquine in preventing infection and progression. The Journal of Antimicrobial Chemotherapy, 75(7), 1667–1670. https://doi.org/10.1093/jac/dkaa114
  • Zhu, N., Zhang, D., Wang, W., Li, X., Yang, B., Song, J., Zhao, X., Huang, B., Shi, W., Lu, R., Niu, P., Zhan, F., Ma, X., Wang, D., Xu, W., Wu, G., Gao, G. F., & Tan, W. (2020). A novel coronavirus from patients with pneumonia in China, 2019. The New England Journal of Medicine, 382(8), 727–733. https://doi.org/10.1056/NEJMoa2001017

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.