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Research Article

Inhibition of NS2B-NS3 protease from all four serotypes of dengue virus by punicalagin, punicalin and ellagic acid identified from Punica granatum

, , , , , , , , & ORCID Icon show all
Received 04 Nov 2023, Accepted 29 Jan 2024, Published online: 19 Feb 2024

References

  • Abduraman, M. A., Hariono, M., Yusof, R., Rahman, N. A., Wahab, H. A., & Tan, M. L. (2018). Development of a NS2B/NS3 protease inhibition assay using AlphaScreen((R)) beads for screening of anti-dengue activities. Heliyon, 4(12), e01023. https://doi.org/10.1016/j.heliyon.2018.e01023
  • Acquadro, S., Civra, A., Cagliero, C., Marengo, A., Rittà, M., Francese, R., Sanna, C., Bertea, C., Sgorbini, B., Lembo, D., Donalisio, M., & Rubiolo, P. (2020). Punica granatum leaf ethanolic extract and ellagic acid as inhibitors of Zika virus infection. Planta Medica, 86(18), 1363–1374. https://doi.org/10.1055/a-1232-5705
  • Alagarasu, K., Patil, P., Kaushik, M., Chowdhury, D., Joshi, R. K., Hegde, H. V., Kakade, M. B., Hoti, S. L., Cherian, S., & Parashar, D. (2022). In vitro antiviral activity of potential medicinal plant extracts against Dengue and Chikungunya viruses. Frontiers in Cellular and Infection Microbiology, 12, 866452. https://doi.org/10.3389/fcimb.2022.866452
  • Alexova, R., Alexandrova, S., Dragomanova, S., Kalfin, R., Solak, A., Mehan, S., Petralia, M. C., Fagone, P., Mangano, K., Nicoletti, F., & Tancheva, L. (2023). Anti-COVID-19 potential of ellagic acid and polyphenols of Punica granatum L. Molecules (Basel, Switzerland), 28(9), 3772. https://doi.org/10.3390/molecules28093772
  • Balasubramanian, A., Manzano, M., Teramoto, T., Pilankatta, R., & Padmanabhan, R. (2016). High-throughput screening for the identification of small-molecule inhibitors of the flaviviral protease. Antiviral Research, 134, 6–16. https://doi.org/10.1016/j.antiviral.2016.08.014
  • Berendsen, H. J., 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
  • Chandramouli, S., Joseph, J. S., Daudenarde, S., Gatchalian, J., Cornillez-Ty, C., & Kuhn, P. (2010). Serotype-specific structural differences in the protease-cofactor complexes of the dengue virus family. Journal of Virology, 84(6), 3059–3067. https://doi.org/10.1128/JVI.02044-09
  • Colic, M., Mihajlovic, D., & Bekic, M. (2022). Immunomodulatory activity of punicalagin, punicalin, and ellagic acid differs from the effect of pomegranate peel extract. Molecules, 27(22), 7871. https://doi.org/10.3390/molecules27227871
  • Daina, A., & Zoete, V. (2019). Application of the SwissDrugDesign Online Resources in Virtual Screening. International Journal of Molecular Sciences, 20(18), 4612. https://doi.org/10.3390/ijms20184612
  • Dwivedi, V. D., Bharadwaj, S., Afroz, S., Khan, N., Ansari, M. A., Yadava, U., Tripathi, R. C., Tripathi, I. P., Mishra, S. K., & Kang, S. G. (2021). Anti-dengue infectivity evaluation of bioflavonoid from Azadirachta indica by dengue virus serine protease inhibition. Journal of Biomolecular Structure & Dynamics, 39(4), 1417–1430. https://doi.org/10.1080/07391102.2020.1734485
  • El-Aguel, A., Pennisi, R., Smeriglio, A., Kallel, I., Tamburello, M. P., D'Arrigo, M., Barreca, D., Gargouri, A., Trombetta, D., Mandalari, G., & Sciortino, M. T. (2022). Punica granatum peel and leaf extracts as promising strategies for HSV-1 treatment. Viruses, 14(12), 2639. https://doi.org/10.3390/v14122639
  • Erbel, P., Schiering, N., D'Arcy, A., Renatus, M., Kroemer, M., Lim, S. P., Yin, Z., Keller, T. H., Vasudevan, S. G., & Hommel, U. (2006). Structural basis for the activation of flaviviral NS3 proteases from dengue and West Nile virus. Nature Structural & Molecular Biology, 13(4), 372–373. https://doi.org/10.1038/nsmb1073
  • Fujimoto, Y., Ijiri, M., Matsuo, T., & Kawaguchi, H. (2023). In vitro antiviral activity of persimmon-derived tannin against avian influenza viruses. Letters in Applied Microbiology, 76(2), ovac053. https://doi.org/10.1093/lambio/ovac053
  • Furukawa, R., Kitabatake, M., Ouji-Sageshima, N., Suzuki, Y., Nakano, A., Matsumura, Y., Nakano, R., Kasahara, K., Kubo, K., Kayano, S-I., Yano, H., & Ito, T. (2021). Persimmon-derived tannin has antiviral effects and reduces the severity of infection and transmission of SARS-CoV-2 in a Syrian hamster model. Scientific Reports, 11(1), 23695. https://doi.org/10.1038/s41598-021-03149-3
  • González, M. E., Martínez-Abarca, F., & Carrasco, L. (1990). Flavonoids: Potent inhibitors of poliovirus RNA synthesis. Antiviral Chemistry and Chemotherapy, 1(3), 203–209. https://doi.org/10.1177/095632029000100
  • Haidari, M., Ali, M., Ward Casscells, S., 3rd,., & Madjid, M. (2009). Pomegranate (Punica granatum) purified polyphenol extract inhibits influenza virus and has a synergistic effect with oseltamivir. Phytomedicine: International Journal of Phytotherapy and Phytopharmacology, 16(12), 1127–1136. https://doi.org/10.1016/j.phymed.2009.06.002
  • Hanwell, M. D., Curtis, D. E., Lonie, D. C., Vandermeersch, T., Zurek, E., & Hutchison, G. R. (2012). Avogadro: An advanced semantic chemical editor, visualization, and analysis platform. Journal of Cheminformatics, 4(1), 17. https://doi.org/10.1186/1758-2946-4-17
  • Huber, R. G., Lim, X. N., Ng, W. C., Sim, A. Y. L., Poh, H. X., Shen, Y., Lim, S. Y., Sundstrom, K. B., Sun, X., Aw, J. G., Too, H. K., Boey, P. H., Wilm, A., Chawla, T., Choy, M. M., Jiang, L., de Sessions, P. F., Loh, X. J., Alonso, S., … Wan, Y. (2019). Structure mapping of dengue and Zika viruses reveals functional long-range interactions. Nature Communications, 10(1), 1408. https://doi.org/10.1038/s41467-019-09391-8
  • Khalifa, I., Zhu, W., Mohammed, H. H. H., Dutta, K., & Li, C. (2020). Tannins inhibit SARS-CoV-2 through binding with catalytic dyad residues of 3CL(pro): An in silico approach with 19 structural different hydrolysable tannins. Journal of Food Biochemistry, 44(10), e13432. https://doi.org/10.1111/jfbc.13432
  • Khan, M., Rauf, W., Habib, FAZAL-e., Rahman, M., Iqbal, S., Shehzad, A., & Iqbal, M. (2022). Hesperidin identified from Citrus extracts potently inhibits HCV genotype 3a NS3 protease. BMC Complementary Medicine and Therapies, 22(1), 98. https://doi.org/10.1186/s12906-022-03578-1
  • 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. (2023). PubChem 2023 update. Nucleic Acids Research, 51(D1), D1373–D1380. https://doi.org/10.1093/nar/gkac956
  • Konishi, E., & Hotta, S. (1979). Effects of tannic acid and its related compounds upon Chikungunya virus. Microbiology and Immunology, 23(7), 659–667. https://doi.org/10.1111/j.1348-0421.1979.tb00507.x
  • Kullappan, M., Benedict, B. A., Rajajagadeesan, A., Baskaran, P., Periadurai, N. D., Ambrose, J. M., Gandhamaneni, S. H., Nakkella, A. K., Agarwal, A., Veeraraghavan, V. P., & Surapaneni, K. M. (2022). Ellagic acid as a potential inhibitor against the nonstructural protein NS3 helicase of Zika virus: A molecular modelling study. BioMed Research International, 2022, 2044577–2044515. https://doi.org/10.1155/2022/2044577
  • Kusmiyati, K., Rahmawati, E., Waangsir, F. W. F., & Selasa, P. (2022). Alkaloids, flavonoids, tannins and saponins contents in Moringa oleifera leaves. Indonesian Journal of Global Health Research, 4(1), 139–144. https://doi.org/10.37287/ijghr.v4i1.832
  • Lankatillake, C., Luo, S., Flavel, M., Lenon, G. B., Gill, H., Huynh, T., & Dias, D. A. (2021). Screening natural product extracts for potential enzyme inhibitors: Protocols, and the standardisation of the usage of blanks in alpha-amylase, alpha-glucosidase and lipase assays. Plant Methods. 17(1), 3. https://doi.org/10.1186/s13007-020-00702-5
  • Leung, D., Schroder, K., White, H., Fang, N. X., Stoermer, M. J., Abbenante, G., Martin, J. L., Young, P. R., & Fairlie, D. P. (2001). Activity of recombinant dengue 2 virus NS3 protease in the presence of a truncated NS2B co-factor, small peptide substrates, and inhibitors. The Journal of Biological Chemistry, 276(49), 45762–45771. https://doi.org/10.1074/jbc.M107360200
  • Li, J., Lim, S. P., Beer, D., Patel, V., Wen, D., Tumanut, C., Tully, D. C., Williams, J. A., Jiricek, J., Priestle, J. P., Harris, J. L., & Vasudevan, S. G. (2005). Functional profiling of recombinant NS3 proteases from all four serotypes of dengue virus using tetrapeptide and octapeptide substrate libraries. The Journal of Biological Chemistry, 280(31), 28766–28774. https://doi.org/10.1074/jbc.M500588200
  • Lim, S. K., Othman, R., Yusof, R., & Heh, C. H. (2021). Rational drug discovery: Ellagic acid as a potent dual-target inhibitor against hepatitis C virus genotype 3 (HCV G3) NS3 enzymes. Chemical Biology & Drug Design, 97(1), 28–40. https://doi.org/10.1111/cbdd.13756
  • Lin, K. H., Ali, A., Rusere, L., Soumana, D. I., Kurt Yilmaz, N., & Schiffer, C. A. (2017). Dengue virus NS2B/NS3 protease inhibitors exploiting the prime side. Journal of Virology, 91(10), e00045-17. https://doi.org/10.1128/JVI.00045-17
  • Lin, L.-T., Chen, T.-Y., Lin, S.-C., Chung, C.-Y., Lin, T.-C., Wang, G.-H., Anderson, R., Lin, C.-C., & Richardson, C. D. (2013). Broad-spectrum antiviral activity of chebulagic acid and punicalagin against viruses that use glycosaminoglycans for entry. BMC Microbiology, 13(1), 187. https://doi.org/10.1186/1471-2180-13-187
  • Liu, C., Cai, D., Zhang, L., Tang, W., Yan, R., Guo, H., & Chen, X. (2016). Identification of hydrolyzable tannins (punicalagin, punicalin and geraniin) as novel inhibitors of hepatitis B virus covalently closed circular DNA. Antiviral Research, 134, 97–107. https://doi.org/10.1016/j.antiviral.2016.08.026
  • Low, J. S., Wu, K. X., Chen, K. C., Ng, M. M., & Chu, J. J. (2011). Narasin, a novel antiviral compound that blocks dengue virus protein expression. Antiviral Therapy, 16(8), 1203–1218. https://doi.org/10.3851/IMP1884
  • Lu, L., Peng, Y., Yao, H., Wang, Y., Li, J., Yang, Y., & Lin, Z. (2022). Punicalagin as an allosteric NSP13 helicase inhibitor potently suppresses SARS-CoV-2 replication in vitro. Antiviral Research, 206, 105389. https://doi.org/10.1016/j.antiviral.2022.105389
  • Luo, D., Xu, T., Hunke, C., Grüber, G., Vasudevan, S. G., & Lescar, J. (2008). Crystal structure of the NS3 protease-helicase from dengue virus. Journal of Virology, 82(1), 173–183. https://doi.org/10.1128/JVI.01788-07
  • Man, G., Xu, L., Wang, Y., Liao, X., & Xu, Z. (2021). Profiling Phenolic Composition in Pomegranate Peel From Nine Selected Cultivars Using UHPLC-QTOF-MS and UPLC-QQQ-MS. Frontiers in Nutrition, 8, 807447. https://doi.org/10.3389/fnut.2021.807447
  • Miller, B. R., 3rd, McGee, T. D., Jr., Swails, J. M., Homeyer, N., Gohlke, H., & Roitberg, A. E. (2012). MMPBSA.py: An Efficient Program for End-State Free Energy Calculations. Journal of Chemical Theory and Computation, 8(9), 3314–3321. https://doi.org/10.1021/ct300418h
  • Noble, C. G., Seh, C. C., Chao, A. T., & Shi, P. Y. (2012). Ligand-bound structures of the dengue virus protease reveal the active conformation. Journal of Virology, 86(1), 438–446. https://doi.org/10.1128/JVI.06225-11
  • Norshidah, H., Leow, C. H., Ezleen, K. E., Wahab, H. A., Vignesh, R., Rasul, A., & Lai, N. S. (2023). Assessing the potential of NS2B/NS3 protease inhibitors biomarker in curbing dengue virus infections: In silico vs. In vitro approach. Frontiers in Cellular and Infection Microbiology, 13, 1061937. https://doi.org/10.3389/fcimb.2023.1061937
  • Packová, D., Maruniaková, N., Halenár, M., Carbonell-Barrachina, Á. A., & Kolesárová, A. (2014). Effective compounds of pomegranate and their effect on animal cells. J Microbiol Biotechnol Food Sci, 2021, 142–144. https://office2.jmbfs.org/index.php/JMBFS/article/view/7639
  • Park, S. W., Kwon, M. J., Yoo, J. Y., Choi, H. J., & Ahn, Y. J. (2014). Antiviral activity and possible mode of action of ellagic acid identified in Lagerstroemia speciosa leaves toward human rhinoviruses. BMC Complementary and Alternative Medicine, 14(1), 171. https://doi.org/10.1186/1472-6882-14-171
  • Pong, L. Y., Yew, P. N., Lee, W. L., Lim, Y. Y., & Sharifah, S. H. (2020). Anti-dengue virus serotype 2 activity of tannins from porcupine dates. Chinese Medicine, 15(1), 49. https://doi.org/10.1186/s13020-020-00329-7
  • Reddy, B. U., Mullick, R., Kumar, A., Sudha, G., Srinivasan, N., & Das, S. (2014). Small molecule inhibitors of HCV replication from pomegranate. Scientific Reports, 4(1), 5411. https://doi.org/10.1038/srep05411
  • Saleem, H. N., Batool, F., Mansoor, H. J., Shahzad-Ul-Hussan, S., & Saeed, M. (2019). Inhibition of dengue virus protease by eugeniin, isobiflorin, and biflorin isolated from the flower buds of Syzygium aromaticum (Cloves). ACS Omega. 4(1), 1525–1533. https://doi.org/10.1021/acsomega.8b02861
  • Salles, T. S., Meneses, M. D. F., Caldas, L. A., Sá-Guimarães, T. E., de Oliveira, D. M., Ventura, J. A., Azevedo, R. C., Kuster, R. M., Soares, M. R., & Ferreira, D. F. (2021). Virucidal and antiviral activities of pomegranate (Punica granatum) extract against the mosquito-borne Mayaro virus. Parasites & Vectors, 14(1), 443. https://doi.org/10.1186/s13071-021-04955-4
  • Saparbekova, A. A., Kantureyeva, G. O., Kudasova, D. E., Konarbayeva, Z. K., & Latif, A. S. (2023). Potential of phenolic compounds from pomegranate (Punica granatum L.) by-product with significant antioxidant and therapeutic effects: A narrative review. Saudi Journal of Biological Sciences, 30(2), 103553. https://doi.org/10.1016/j.sjbs.2022.103553
  • Silva, A., Morais, S., & Marques, M. (2011). Antiviral activities of extracts and phenolic components of two Spondias species against dengue virus. Journal of Venomous Animals and Toxins including Tropical Diseases, 17, 406–413. https://doi.org/10.1590/S1678-91992011000400007
  • Studio D. Discovery studio. Accelrys [21] (2008).
  • Tabassum, S., Naeem, A., Nazir, A., Naeem, F., Gill, S., & Tabassum, S. (2023). Year-round dengue fever in Pakistan, highlighting the surge amidst ongoing flood havoc and the COVID-19 pandemic: A comprehensive review. Annals of Medicine and Surgery (2012), 85(4), 908–912. https://doi.org/10.1097/MS9.0000000000000418
  • Teixeira, R. R., Pereira, W. L., Oliveira, A. F. C. D S., da Silva, A. M., de Oliveira, A. S., da Silva, M. L., da Silva, C. C., & de Paula, S. O. (2014). Natural products as source of potential dengue antivirals. Molecules (Basel, Switzerland), 19(6), 8151–8176. https://doi.org/10.3390/molecules19068151
  • Tomlinson, S. M., Malmstrom, R. D., Russo, A., Mueller, N., Pang, Y. P., & Watowich, S. J. (2009). Structure-based discovery of dengue virus protease inhibitors. Antiviral Research, 82(3), 110–114. https://doi.org/10.1016/j.antiviral.2009.02.190
  • Tran, T. T., Tran, Q. H., Nguyen, Q. T., Le, M. T., Trinh, D. T., & Thai, K. M. (2022). Identification of potential interleukin-8 inhibitors acting on the interactive site between chemokine and CXCR2 receptor: A computational approach. PloS One, 17(2), e0264385. https://doi.org/10.1371/journal.pone.0264385
  • Triratapiban, C., Lueangaramkul, V., Phecharat, N., Pantanam, A., Lekcharoensuk, P., & Theerawatanasirikul, S. (2023). First study on in vitro antiviral and virucidal effects of flavonoids against feline infectious peritonitis virus at the early stage of infection. Veterinary World, 16(3), 618–630. https://doi.org/10.14202/vetworld.2023.618-630
  • 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
  • WHO. (2013). The global distribution and burden of dengue. 0028–0836.
  • WHO. (2018). Dengue Vaccine: WHO position paper–September 2018. Wkly Epidemiol Rec, 93, 457–476.
  • WHO. (2023). Dengue and severe dengue Fact Sheet. https://www.who.int/news-room/fact-sheets/detail/dengue-and-severe-dengue.
  • Wu, D-W., Mao, F., Ye, Y., Li, J., Xu, C-L., Luo, X-M., Chen, J., & Shen, X. (2015). Policresulen, a novel NS2B/NS3 protease inhibitor, effectively inhibits the replication of DENV2 virus in BHK-21 cells. Acta Pharmacologica Sinica, 36(9), 1126–1136. https://doi.org/10.1038/aps.2015.56
  • ww PDBc. (2019). Protein Data Bank: The single global archive for 3D macromolecular structure data. Nucleic Acids Research. 47(D1), D520–D528. https://doi.org/10.1093/nar/gky949
  • Yousaf, Numan, Alharthy, Rima D, Kamal, Iqra, Saleem, Muhammad, Muddassar, Muhammad, Maryam,. Identification of human phosphoglycerate mutase 1 (PGAM1) inhibitors using hybrid virtual screening approaches. PeerJ. 2023;11: E 14936. https://doi.org/10.7717/peerj.14936
  • Zaremba, A. A., Zaremba, P. Y., & Zahorodnia, S. D. (2023). In silico study of HASDI (high-affinity selective DNA intercalator) as a new agent capable of highly selective recognition of the DNA sequence. Scientific Reports, 13(1), 5395. https://doi.org/10.1038/s41598-023-32595-4

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