Computational and experimental validation of phthalocyanine and hypericin as effective SARS-CoV-2 fusion inhibitors

References

• Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindah, 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
• Amadei, A., Linssen, A. B. M., & Berendsen, H. J. C. (1993). Essential dynamics of proteins. Proteins, 17(4), 412–425. https://doi.org/10.1002/prot.340170408
   PubMed Web of Science ®Google Scholar
• Bajrai, L. H., Ali, S., Kafrawy, E., Hassan, A. M., Tolah, A. M., Alnahas, R. S., Sohrab, S. S., Rehan, M., & Azhar, E. I. (2022). In vitro screening of anti ‑ viral and virucidal effects against SARS ‑ CoV ‑ 2 by Hypericum perforatum and Echinacea. Scientific Reports, 12(1), 17. https://doi.org/10.1038/s41598-022-26157-3
   PubMed Web of Science ®Google Scholar
• Battles, M. B., Langedijk, J. P., Furmanova-Hollenstein, P., Chaiwatpongsakorn, S., Costello, H. M., Kwanten, L., Vranckx, L., Vink, P., Jaensch, S., Jonckers, T. H. M., Koul, A., Arnoult, E., Peeples, M. E., Roymans, D., & McLellan, J. S. (2016). Molecular mechanism of respiratory syncytial virus fusion inhibitors. Nature Chemical Biology, 12(2), 87–93. https://doi.org/10.1038/nchembio.1982
   PubMed Web of Science ®Google Scholar
• Battles, M. B., & McLellan, J. S. (2019). Respiratory syncytial virus entry and how to block it. Nature Reviews. Microbiology, 17(4), 233–245. https://doi.org/10.1038/s41579-019-0149-x
   PubMed Web of Science ®Google Scholar
• Biocca, S., Arcangeli, T., Tagliaferri, E., Testa, B., Vindigni, G., Oteri, F., Giorgi, A., Iacovelli, F., Novelli, G., Desideri, A., & Falconi, M. (2013). Simulative and experimental investigation on the cleavage site that generates the soluble human LOX-1. Archives of Biochemistry and Biophysics, 540(1-2), 9–18. https://doi.org/10.1016/j.abb.2013.10.001
   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
• Casalino, L., Gaieb, Z., Goldsmith, J. A., Hjorth, C. K., Dommer, A. C., Harbison, A. M., Fogarty, C. A., Barros, E. P., Taylor, B. C., Mclellan, J. S., Fadda, E., & Amaro, R. E. (2020). Beyond shielding: The roles of glycans in the SARS-CoV-2 spike protein. ACS Central Science, 6(10), 1722–1734. https://doi.org/10.1021/acscentsci.0c01056
   PubMed Web of Science ®Google Scholar
• Chen, H., Feng, R., Muhammad, I., Abbas, G., Zhang, Y., Ren, Y., Huang, X., Zhang, R., Diao, L., Wang, X., & Li, G. (2019). Protective effects of hypericin against infectious bronchitis virus induced apoptosis and reactive oxygen species in chicken embryo kidney cells. Poultry Science, 98(12), 6367–6377. https://doi.org/10.3382/ps/pez465
   PubMed Web of Science ®Google Scholar
• Chen, H., Muhammad, I., Zhang, Y., Ren, Y., Zhang, R., Huang, X., Diao, L., Liu, H., Li, X., Sun, X., Abbas, G., & Li, G. (2019). Antiviral activity against infectious bronchitis virus and bioactive components of Hypericum perforatum L. Frontiers in Pharmacology, 10, 1272. https://doi.org/10.3389/fphar.2019.01272
   PubMed Web of Science ®Google Scholar
• Choi, Y. K., Cao, Y., Frank, M., Woo, H., Park, S. J., Yeom, M. S., Croll, T. I., Seok, C., & Im, W. (2021). Structure, dynamics, receptor binding, and antibody binding of the fully glycosylated full-length SARS-CoV-2 spike protein in a viral membrane. Journal of Chemical Theory and Computation, 17(4), 2479–2487. https://doi.org/10.1021/acs.jctc.0c01144
   PubMed Web of Science ®Google Scholar
• da Silva Santos, P. S., da Fonseca Orcina, B., Machado, R. R. G., Vilhena, F. V., da Costa Alves, L. M., Zangrando, M. S. R., de Oliveira, R. C., Soares, M. Q. S., Simão, A. N. C., Pietro, E. C. I. N., Kuroda, J. P. G., de Almeida Benjamim, I. A., Araujo, D. B., Toma, S. H., Flor, L., Araki, K., & Durigon, E. L. (2021). Beneficial effects of a mouthwash containing an antiviral phthalocyanine derivative on the length of hospital stay for COVID-19: Randomised trial. Scientific Reports, 11(1), 19937. https://doi.org/10.1038/s41598-021-99013-5
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N ⋅log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98(12), 10089–10092. https://doi.org/10.1063/1.464397
   Web of Science ®Google Scholar
• Degar, S., Prince, A. M., Pascual, D., Lavie, G., Levin, B., Mazur, Y., Lavie, D., Ehrlich, L. S., Carter, C., & Meruelo, D. (1992). Inactivation of the human immunodeficiency virus by hypericin: evidence for photochemical alterations of p24 and a Block in Uncoating. AIDS Research and Human Retroviruses, 8(11), 1929–1936. https://doi.org/10.1089/aid.1992.8.1929
   PubMed Web of Science ®Google Scholar
• Delcanale, P., Uriati, E., Mariangeli, M., Mussini, A., Moreno, A., Lelli, D., Cavanna, L., Bianchini, P., Diaspro, A., Abbruzzetti, S., & Viappiani, C. (2022). The Interaction of Hypericin with SARS-CoV-2 Reveals a Multimodal Antiviral Activity. ACS Applied Materials & Interfaces, 14(12), 14025–14032. https://doi.org/10.1021/acsami.1c22439
   PubMed Web of Science ®Google Scholar
• Feller, S. E., Zhang, Y., Pastor, R. W., & Brooks, B. R. (1995). Constant pressure molecular dynamics simulation: The Langevin piston method. The Journal of Chemical Physics, 103(11), 4613–4621. https://doi.org/10.1063/1.470648
   Web of Science ®Google Scholar
• François, K. O., Pannecouque, C., Auwerx, J., Lozano, V., Pérez-Pérez, M. J., Schols, D., & Balzarini, J. (2009). The phthalocyanine prototype derivative Alcian blue is the first synthetic agent with selective anti-human immunodeficiency virus activity due to its gp120 glycan-binding potential. Antimicrobial Agents and Chemotherapy, 53(11), 4852–4859. https://doi.org/10.1128/AAC.00811-09
   PubMed Web of Science ®Google Scholar
• Gattuso, H., Marazzi, M., Dehez, F., & Monari, A. (2017). Deciphering the photosensitization mechanisms of hypericin towards biological membranes. Physical Chemistry Chemical Physics : PCCP, 19(34), 23187–23193. https://doi.org/10.1039/c7cp03723f
   PubMed Web of Science ®Google Scholar
• Goga, N., Rzepiela, A. J., De Vries, A. H., Marrink, S. J., & Berendsen, H. J. C. (2012). Efficient algorithms for langevin and DPD dynamics. Journal of Chemical Theory and Computation, 8(10), 3637–3649. https://doi.org/10.1021/ct3000876
   PubMed Web of Science ®Google Scholar
• Greco, E., Quintiliani, G., Santucci, M. B., Serafino, A., Ciccaglione, A. R., Marcantonio, C., Papi, M., Maulucci, G., Delogu, G., Martino, A., Goletti, D., Sarmati, L., Andreoni, M., Altieri, A., Alma, M., Caccamo, N., Di Liberto, D., De Spirito, M., Savage, N. D., … Fraziano, M. (2012). Janus-faced liposomes enhance antimicrobial innate immune response in Mycobacterium tuberculosis infection. Proceedings of the National Academy of Sciences, 109(21), E1360-1368. https://doi.org/10.1073/pnas.1200484109
   PubMed Web of Science ®Google Scholar
• Grünewald, F., Kroon, P. C., Souza, P. C. T., & Marrink, S. J. (2021). Protocol for simulations of PEGylated proteins with Martini 3. Methods in Molecular Biology, 2199, 315–335. https://doi.org/10.1007/978-1-0716-0892-0_18
   PubMedGoogle Scholar
• Guixà-González, R., Rodriguez-Espigares, I., Ramírez-Anguita, J. M., Carrió-Gaspar, P., Martinez-Seara, H., Giorgino, T., & Selent, J. (2014). MEMBPLUGIN: Studying membrane complexity in VMD. Bioinformatics (Oxford, England), 30(10), 1478–1480. https://doi.org/10.1093/bioinformatics/btu037
   PubMed Web of Science ®Google Scholar
• Guvench, O., Mallajosyula, S. S., Raman, E. P., Hatcher, E., Vanommeslaeghe, K., Foster, T. J., Jamison, F. W., & MacKerell, A. D. (2011). CHARMM additive all-atom force field for carbohydrate derivatives and its utility in polysaccharide and carbohydrate–protein modeling. Journal of Chemical Theory and Computation, 7(10), 3162–3180. https://doi.org/10.1021/ct200328p
   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
• Huang, J., Rauscher, S., Nawrocki, G., Ran, T., Feig, M., De Groot, B. L., Grubmüller, H., & MacKerell, A. D. (2017). CHARMM36m: An improved force field for folded and intrinsically disordered proteins. Nature Methods, 14(1), 71–73. https://doi.org/10.1038/nmeth.4067
   PubMed Web of Science ®Google Scholar
• Hudson, J. B., Harris, L., & Towers, G. H. N. (1993). The importance of light in the anti-HIV effect of hypericin. Antiviral Research, 20(2), 173–178. https://doi.org/10.1016/0166-3542(93)90006-5
   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
• Iannone, F., Ambrosino, F., Bracco, G., De Rosa, M., Funel, A., Guarnieri, G., Migliori, S., Palombi, F., Ponti, G., Santomauro, G., & Procacci, P. (2019). CRESCO ENEA HPC clusters: A working example of a multifabric GPFS Spectrum Scale layout. 2019 International Conference on High Performance Computing and Simulation, HPCS, 2019, 1051–1052. https://doi.org/10.1109/HPCS48598.2019.9188135
   Google Scholar
• Jang, W. D., Jeon, S., Kim, S., & Lee, S. Y. (2021). Drugs repurposed for COVID-19 by virtual screening of 6,218 drugs and cell-based assay. Proceedings of the National Academy of Sciences, 118(30), e2024302118. https://doi.org/10.1073/pnas.2024302118
   PubMed Web of Science ®Google 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. https://doi.org/10.1002/jcc.20945
   PubMed Web of Science ®Google Scholar
• 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 Physics, 79(2), 926–935. https://doi.org/10.1063/1.445869
   Web of Science ®Google Scholar
• Karioti, A., & Bilia, A. R. (2010). Hypericins as potential leads for new therapeutics. International Journal of Molecular Sciences, 11(2), 562–594. https://doi.org/10.3390/ijms11020562
   PubMed Web of Science ®Google Scholar
• Ke, Z., Oton, J., Qu, K., Cortese, M., Zila, V., McKeane, L., Nakane, T., Zivanov, J., Neufeldt, C. J., Cerikan, B., Lu, J. M., Peukes, J., Xiong, X., Kräusslich, H. G., Scheres, S. H. W., Bartenschlager, R., & Briggs, J. A. G. (2020). Structures and distributions of SARS-CoV-2 spike proteins on intact virions. Nature, 588(7838), 498–502. https://doi.org/10.1038/s41586-020-2665-2
   PubMed Web of Science ®Google Scholar
• Kim, S., Chen, J., Cheng, T., Gindulyte, A., He, J., He, S., Li, Q., Shoemaker, B. A., Thiessen, P. A., Yu, B., Zaslavsky, L., Zhang, J., & Bolton, E. E. (2021). PubChem in 2021: New data content and improved web interfaces. Nucleic Acids Research, 49(D1), D1388–D1395. https://doi.org/10.1093/nar/gkaa971
   PubMed Web of Science ®Google Scholar
• Klauda, J. B., Venable, R. M., Freites, J. A., O'Connor, J. W., Tobias, D. J., Mondragon-Ramirez, C., Vorobyov, I., MacKerell, A. D., & 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. https://doi.org/10.1021/jp101759q
   PubMed Web of Science ®Google Scholar
• Korneev, D., Kurskaya, O., Sharshov, K., Eastwood, J., & Strakhovskaya, M. (2019). Ultrastructural aspects of photodynamic inactivation of highly pathogenic avian H5N8 influenza virus. Viruses, 11(10), 955. https://doi.org/10.3390/v11100955
   PubMed Web of Science ®Google Scholar
• Kubin, A., Wierrani, F., Burner, U., Alth, G., & Grunberger, W. (2005). Hypericin - the facts about a controversial agent. Current Pharmaceutical Design, 11(2), 233–253. https://doi.org/10.2174/1381612053382287
   PubMed Web of Science ®Google Scholar
• Kumar, S., & Nussinov, R. (2002). Close-range electrostatic interactions in proteins. ChemBioChem. 3(7), 604. https://doi.org/10.1002/1439-7633(20020703)3:7<604::AID-CBIC604>3.0.CO;2-X
   PubMed Web of Science ®Google Scholar
• Lenard, J., Rabson, A., & Vanderoef, R. (1993). Photodynamic inactivation of infectivity of human immunodeficiency virus and other enveloped viruses using hypericin and rose bengal: Inhibition of fusion and syncytia formation. Proceedings of the National Academy of Sciences of the United States of America, 90(1), 158–162. https://doi.org/10.1073/pnas.90.1.158
   PubMed Web of Science ®Google Scholar
• Lopes, B. R. P., da Costa, M. F., Genova Ribeiro, A., da Silva, T. F., Lima, C. S., Caruso, I. P., de Araujo, G. C., Kubo, L. H., Iacovelli, F., Falconi, M., Desideri, A., de Oliveira, J., Regasini, L. O., de Souza, F. P., & Toledo, K. A. (2020). Quercetin pentaacetate inhibits in vitro human respiratory syncytial virus adhesion. Virus Research, 276(May 2019), 197805. https://doi.org/10.1016/j.virusres.2019.197805
   PubMed Web of Science ®Google Scholar
• Martínez, L., Andrade, R., Birgin, E. G., & Martínez, J. M. (2009). PACKMOL: A package for building initial configurations for molecular dynamics simulations. Journal of Computational Chemistry, 30(13), 2157–2164. https://doi.org/10.1002/jcc.21224
   PubMed Web of Science ®Google Scholar
• Martyna, G. J., Tobias, D. J., & Klein, M. L. (1994). Constant pressure molecular dynamics algorithms. The Journal of Chemical Physics, 101(5), 4177–4189. https://doi.org/10.1063/1.467468
   Web of Science ®Google Scholar
• Matos, A. d R., Caetano, B. C., de Almeida Filho, J. L., Martins, J. S. C. d C., de Oliveira, M. G. P., Sousa, T., das, C., Horta, M. A. P., Siqueira, M. M., & Fernandez, J. H. (2022). Identification of hypericin as a candidate repurposed therapeutic agent for COVID-19 and its potential anti-SARS-CoV-2 activity. Frontiers in Microbiology, 13(February), 828984. https://doi.org/10.3389/fmicb.2022.828984
   PubMedGoogle Scholar
• Miao, Y., Feher, V. A., & McCammon, J. A. (2015). Gaussian accelerated molecular dynamics: Unconstrained enhanced sampling and free energy calculation. Journal of Chemical Theory and Computation, 11(8), 3584–3595. https://doi.org/10.1021/acs.jctc.5b00436
   PubMed Web of Science ®Google Scholar
• Mohamed, F. F., Anhlan, D., Schöfbänker, M., Schreiber, A., Classen, N., Hensel, A., Hempel, G., Scholz, W., Kühn, J., Hrincius, E. R., & Ludwig, S. (2022). Hypericum perforatum and its ingredients hypericin and pseudohypericin demonstrate an antiviral activity against SARS-CoV-2. Pharmaceuticals, 15(5), 530. https://doi.org/10.3390/ph15050530
   Web of Science ®Google Scholar
• Nikolaeva-Glomb, L., Mukova, L., Nikolova, N., Kussovski, V., Doumanova, L., Mantareva, V., Angelov, I., Wöhrle, D., & Galabov, A. S. (2017). Photodynamic effect of some phthalocyanines on enveloped and naked viruses. Acta Virologica, 61(3), 341–346. https://doi.org/10.4149/av_2017_313
   PubMed Web of Science ®Google Scholar
• Pan, B. W., Xiao, J. W., Li, S. M., Yang, X., Zhou, X., Sun, Q. W., Chen, M., Xie, S. X., Sakharkar, M. K., Yang, J., Zhou, Y., & Wei, Y. (2022). Inhibitors of HIV-1 and Cathepsin L proteases identified from the insect gall of hypericum kouytchense. Pharmaceuticals, 15(12), 1499. https://doi.org/10.3390/ph15121499
   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
• Pezeshkian, W., Grünewald, F., Narykov, O., Lu, S., Wassenaar, T. A., Marrink, S. J., & Korkin, D. (2023). Molecular architecture of SARS-CoV-2 envelope by integrative modeling. BioRxiv, 2021.09.15.459697. https://www.biorxiv.org/content/10.1101/2021.09.15.459697
   Google Scholar
• Phillips, J. C., Braun, R., Wang, W., Gumbart, J., Tajkhorshid, E., Villa, E., Chipot, C., Skeel, R. D., Kalé, L., & Schulten, K. (2005). Scalable molecular dynamics with NAMD. Journal of Computational Chemistry, 26(16), 1781–1802. https://doi.org/10.1002/jcc.20289
   PubMed Web of Science ®Google Scholar
• Romeo, A., Iacovelli, F., & Falconi, M. (2020). Targeting the SARS-CoV-2 spike glycoprotein prefusion conformation: Virtual screening and molecular dynamics simulations applied to the identification of potential fusion inhibitors. Virus Research, 286(June), 198068. https://doi.org/10.1016/j.virusres.2020.198068
   PubMedGoogle Scholar
• Saadi, F., Pal, D., & Sarma, J. D. (2021). Spike glycoprotein is central to coronavirus pathogenesis-parallel between m-CoV and SARS-CoV-2. Annals of Neurosciences, 28(3-4), 201–218. https://doi.org/10.1177/09727531211023755
   PubMed Web of Science ®Google Scholar
• Santos, K. L. M., Barros, R. M., da Silva Lima, D. P., Nunes, A. M. A., Sato, M. R., Faccio, R., de Lima Damasceno, B. P. G., & Oshiro-Junior, J. A. (2020). Prospective application of phthalocyanines in the photodynamic therapy against microorganisms and tumor cells: A mini-review. Photodiagnosis and Photodynamic Therapy, 32(August), 102032. https://doi.org/10.1016/j.pdpdt.2020.102032
   PubMedGoogle Scholar
• Sen, C. K., & Packer, L. (1996). Antioxidant and redox regulation of gene transcription. FASEB Journal : Official Publication of the Federation of American Societies for Experimental Biology, 10(7), 709–720. https://doi.org/10.1096/fasebj.10.7.8635688
   PubMed Web of Science ®Google Scholar
• Smetana, Z., Mendelson, E., Manor, J., van Lier, J. E., Ben-Hur, E., Salzberg, S., & Malik, Z. (1994). Photodynamic inactivation of herpes viruses with phthalocyanine derivatives. Journal of Photochemistry and Photobiology. B, Biology, 22(1), 37–43. https://doi.org/10.1016/1011-1344(93)06949-4
   PubMed Web of Science ®Google Scholar
• Smith, M., & Smith, J. C. (2020). Repurposing therapeutics for COVID-19: Supercomputer-based docking to the SARS-CoV-2 viral spike protein and viral spike protein-human ACE2 interface, ChemRxiv, 2. https://doi.org/10.26434/chemrxiv.11871402.v4
   Google Scholar
• Sorokin, A. B. (2013). Phthalocyanine metal complexes in catalysis. Chemical Reviews, 113(10), 8152–8191. https://doi.org/10.1021/cr4000072
   PubMed Web of Science ®Google Scholar
• Souza, P. C. T., Alessandri, R., Barnoud, J., Thallmair, S., Faustino, I., Grünewald, F., Patmanidis, I., Abdizadeh, H., Bruininks, B. M. H., Wassenaar, T. A., Kroon, P. C., Melcr, J., Nieto, V., Corradi, V., Khan, H. M., Domański, J., Javanainen, M., Martinez-Seara, H., Reuter, N., … Marrink, S. J. (2021). Martini 3: A general purpose force field for coarse-grained molecular dynamics. Nature Methods, 18(4), 382–388. https://doi.org/10.1038/s41592-021-01098-3
   PubMed Web of Science ®Google Scholar
• Souza, P. C. T., Thallmair, S., Conflitti, P., Ramírez-Palacios, C., Alessandri, R., Raniolo, S., Limongelli, V., & Marrink, S. J. (2020). Protein–ligand binding with the coarse-grained Martini model. Nature Communications, 11(1), 1–11. https://doi.org/10.1038/s41467-020-17437-5
   PubMed Web of Science ®Google Scholar
• Stevenson, N. R., & Lenard, J. (1993). Antiretroviral activities of hypericin and rose bengal: Photodynamic effects on Friend leukemia virus infection of mice. Antiviral Research, 21(2), 119–127. https://doi.org/10.1016/0166-3542(93)90048-N
   PubMed Web of Science ®Google Scholar
• Tang, T., Bidon, M., Jaimes, J. A., Whittaker, G. R., & Daniel, S. (2020). Coronavirus membrane fusion mechanism offers a potential target for antiviral development. Antiviral Research, 178(January), 104792. https://doi.org/10.1016/j.antiviral.2020.104792
   PubMedGoogle Scholar
• Telenti, A., Arvin, A., Corey, L., Corti, D., Diamond, M. S., García-Sastre, A., Garry, R. F., Holmes, E. C., Pang, P. S., & Virgin, H. W. (2021). After the pandemic: Perspectives on the future trajectory of COVID-19. Nature, 596(7873), 495–504. https://doi.org/10.1038/s41586-021-03792-w
   PubMed Web of Science ®Google Scholar
• Vanommeslaeghe, K., Hatcher, E., Acharya, C., Kundu, S., Zhong, S., Shim, J., Darian, E., Guvench, O., Lopes, P., Vorobyov, I., & Mackerell, A. D. (2010). CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields. Journal of Computational Chemistry, 31(4), 671–690. https://doi.org/10.1002/jcc.21367
   PubMed Web of Science ®Google Scholar
• Vzorov, A. N., Marzilli, L. G., Compans, R. W., & Dixon, D. W. (2003). Prevention of HIV-1 infection by phthalocyanines. Antiviral Research, 59(2), 99–109. https://doi.org/10.1016/S0166-3542(03)00035-4
   PubMed Web of Science ®Google Scholar
• Wang, B., Zhong, C., & Tieleman, D. P. (2022). Supramolecular organization of SARS-CoV and SARS-CoV-2 virions revealed by coarse-grained models of intact virus envelopes. Journal of Chemical Information and Modeling, 62(1), 176–186. https://doi.org/10.1021/acs.jcim.1c01240
   PubMed Web of Science ®Google Scholar
• Wang, J., Arantes, P. R., Bhattarai, A., Hsu, R. V., Pawnikar, S., Huang, Y. M., Palermo, G., & Miao, Y. (2021). Gaussian accelerated molecular dynamics: Principles and applications. WIREs Computational Molecular Science, 11(5), 1–32. https://doi.org/10.1002/wcms.1521
   Google Scholar
• Wassenaar, T. A., Ingólfsson, H. I., Böckmann, R. A., Tieleman, D. P., & Marrink, S. J. (2015). Computational lipidomics with insane: A versatile tool for generating custom membranes for molecular simulations. Journal of Chemical Theory and Computation, 11(5), 2144–2155. https://doi.org/10.1021/acs.jctc.5b00209
   PubMed Web of Science ®Google Scholar
• Weber, N. D., Murray, B. K., North, J. A., & Wood, S. G. (1994). The antiviral agent hypericin has in vitro activity against HSV-1 through non-specific association with viral and cellular membranes. Antiviral Chemistry and Chemotherapy, 5(2), 83–90. https://doi.org/10.1177/095632029400500204
   Web of Science ®Google Scholar
• Woo, H., Park, S. J., Choi, Y. K., Park, T., Tanveer, M., Cao, Y., Kern, N. R., Lee, J., Yeom, M. S., Croll, T. I., Seok, C., & Im, W. (2020). Developing a fully glycosylated Full-length SARS-CoV-2 spike protein model in a viral membrane. The Journal of Physical Chemistry. B, 124(33), 7128–7137. https://doi.org/10.1021/acs.jpcb.0c04553
   PubMed Web of Science ®Google Scholar
• Wright, J. D. (2001). Phthalocyanines. In Encyclopedia of materials: science and technology (pp. 6987–6991). Elsevier. https://doi.org/10.1016/B0-08-043152-6/01238-9
   Google Scholar
• Wu, J.-J., Zhang, J., Xia, C.-Y., Ding, K., Li, X.-X., Pan, X.-G., Xu, J.-K., He, J., & Zhang, W.-K. (2023). Hypericin: A natural anthraquinone as promising therapeutic agent. Phytomedicine : international Journal of Phytotherapy and Phytopharmacology, 111(January), 154654. https://doi.org/10.1016/j.phymed.2023.154654
   PubMedGoogle Scholar
• Xiu, S., Dick, A., Ju, H., Mirzaie, S., Abdi, F., Cocklin, S., Zhan, P., & Liu, X. (2020). Inhibitors of SARS-CoV-2 entry: Current and future opportunities. Journal of Medicinal Chemistry, 63(21), 12256–12274. https://doi.org/10.1021/acs.jmedchem.0c00502
   PubMed Web of Science ®Google Scholar
• Yu, A., Pak, A. J., He, P., Monje-Galvan, V., Casalino, L., Gaieb, Z., Dommer, A. C., Amaro, R. E., & Voth, G. A. (2021). A multiscale coarse-grained model of the SARS-CoV-2 virion. Biophysical Journal, 120(6), 1097–1104. https://doi.org/10.1016/j.bpj.2020.10.048
   PubMed Web of Science ®Google Scholar