Food Plant Secondary Metabolites Antiviral Activity and Their Possible Roles in SARS-CoV-2 Treatment: An Overview
Abstract
:1. Introduction
2. Antiviral Potential of Selected Natural Phytochemicals
3. Coronaviruses and Phytochemicals
4. Natural Phytocompounds with Potential to Inhibit the Coronavirus SARS-CoV-2 According to In Silico Approaches
5. In Vitro Evaluation of SARS-CoV-2 Antiviral Activity of Natural Phytocompounds
6. In Vivo Studies and Clinical Trials
7. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Garagounis, C.; Delkis, N.; Papadopoulou, K.K. Unraveling the roles of plant specialized metabolites: Using synthetic biology to design molecular biosensors. New Phytol. 2021, 231, 1338–1352. [Google Scholar] [CrossRef] [PubMed]
- Weremczuk-Jeżyna, I.; Hnatuszko-Konka, K.; Lebelt, L.; Grzegorczyk-Karolak, I. The Protective Function and Modification of Secondary Metabolite Accumulation in Response to Light Stress in Dracocephalum forrestii Shoots. Int. J. Mol. Sci. 2021, 22, 7965. [Google Scholar] [CrossRef] [PubMed]
- Liu, R.H. Health bene fits of phytochemicals in whole foods. In Nutritional Health: Strategies for Disease Prevention, 3rd ed.; Temple, N.J., Wilson, T., Jacobs, D.R., Jr., Eds.; Humana Press: Totowa, NJ, USA, 2012; pp. 293–310. [Google Scholar] [CrossRef]
- Abou Baker, D.H. An ethnopharmacological review on the therapeutical properties of fla-vonoids and their mechanisms of actions: A comprehensive review based on up to date knowledge. Toxicol. Rep. 2022, 9, 445–469. [Google Scholar] [CrossRef] [PubMed]
- Panche, A.N.; Diwan, A.D.; Chandra, S.R. Flavonoids: An overview. J. Nutr. Sci. 2016, 5, e47. [Google Scholar] [CrossRef] [Green Version]
- Periwal, V.; Bassler, S.; Andrejev, S.; Gabrielli, N.; Patil, K.R.; Typas, A.; Patil, K.R. Bioactivity assessment of natural compounds using machine learning models trained on target similarity between drugs. PLoS Comput. Biol. 2022, 18, e1010029. [Google Scholar] [CrossRef]
- Behl, T.; Rocchetti, G.; Chadha, S.; Zengin, G.; Bungau, S.; Kumar, A.; Mehta, V.; Uddin, M.S.; Khullar, G.; Setia, D.; et al. Phytochemicals from Plant Foods as Potential Source of Antiviral Agents: An Overview. Pharmaceuticals 2021, 14, 381. [Google Scholar] [CrossRef]
- Tirado-Kulieva, V.; Atoche-Dioses, S.; Hernandez-Martínez, E. Phenolic compounds of mango (Mangifera indica) by-products: Antioxidant and antimicrobial potential, use in disease prevention and food industry, methods of extraction and microencapsulation. Sci. Agropecu. 2021, 12, 283–293. [Google Scholar] [CrossRef]
- Tirado-Kulieva, V.A.; Gutierrez-Valverde, K.S.; Villegas-Yarleque, M.; Camacho-Orbegoso, E.W.; Villegas-Aguilar, G.F. Research trends on mango by-products: A literature review with bibliometric analysis. J. Food Meas. Charact. 2022, 16, 2760–2771. [Google Scholar] [CrossRef]
- Pérez de la Lastra, J.M.; Andrés-Juan, C.; Plou, F.J.; Pérez-Lebeña, E. Impact of Zinc, Glutathione, and Polyphenols as Antioxidants in the Immune Response against SARS-CoV-2. Processes 2021, 9, 506. [Google Scholar] [CrossRef]
- Mehany, T.; Khalifa, I.; Barakat, H.; Althwab, S.A.; Alharbi, Y.M.; El-Sohaimy, S. Polyphenols as promising biologically active substances for preventing SARS-CoV-2: A review with research evidence and underlying mechanisms. Food Biosci. 2021, 40, 100891. [Google Scholar] [CrossRef]
- Davis, C.; Bryan, J.; Hodgson, J.; Murphy, K. Definition of the Mediterranean Diet; A Literature Review. Nutrients 2015, 7, 9139–9153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Khalifa, S.A.M.; Yosri, N.; El-Mallah, M.F.; Ghonaim, R.; Guo, Z.; Musharraf, S.G.; Du, M.; Khatib, A.; Xiao, J.; Saeed, A.; et al. Screening for natural and derived bio-active compounds in preclinical and clinical studies: One of the frontlines of fighting the coronaviruses pandemic. Phytomedicine 2021, 85, 153311. [Google Scholar] [CrossRef] [PubMed]
- Yosri, N.; Abd El-Wahed, A.A.; Ghonaim, R.; Khattab, O.M.; Sabry, A.; Ibrahim, M.A.A.; Moustafa, M.F.; Guo, Z.; Zou, X.; Algethami, A.F.M.; et al. Anti-Viral and Immunomodulatory Properties of Propolis: Chemical Diversity, Pharmacological Properties, Preclinical and Clinical Applications, and In Silico Potential against SARS-CoV-2. Foods 2021, 10, 1776. [Google Scholar] [CrossRef]
- World Health Organization. Weekly Epidemiological Update on COVID-19–22 February 2023, Edition 131, 22 February 2023. Available online: https://www.who.int/publications/m/item/weekly-epidemiological-update-on-covid (accessed on 22 February 2023).
- da Silva, S.J.R.; do Nascimento, J.C.F.; Germano Mendes, R.P.; Guarines, K.M.; Targino Alves da Silva, C.; da Silva, P.G.; de Magalhães, J.J.F.; Vigar, J.R.J.; Silva-Júnior, A.; Kohl, A.; et al. Two Years into the COVID-19 Pandemic: Lessons Learned. ACS Infect. Dis. 2022, 8, 1758–1814. [Google Scholar] [CrossRef]
- Ikeda, K.; Tsujimoto, K.; Uozaki, M.; Nishide, M.; Suzuki, Y.; Koyama, A.H.; Yamasaki, H. Inhibition of multiplication of herpes simplex virus by caffeic acid. Int. J. Mol. Med. 2011, 28, 595–598. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chiang, L.C.; Chiang, W.; Chang, M.Y.; Ng, L.T.; Lin, C.C. Antiviral activity of Plantago major extracts and related compounds in vitro. Antivir. Res. 2002, 55, 53–62. [Google Scholar] [CrossRef]
- Shen, J.; Wang, G.; Zuo, J. Caffeic acid inhibits HCV replication via induction of IFNα antiviral response through p62-mediated Keap1/Nrf2 signaling pathway. Antivir. Res. 2018, 154, 166–173. [Google Scholar] [CrossRef]
- Utsunomiya, H.; Ichinose, M.; Ikeda, K.; Uozaki, M.; Morishita, J.; Kuwahara, T.; Koyama, A.H.; Yamasaki, H. Inhibition by caffeic acid of the influenza A virus multiplication in vitro. Int. J. Mol. Med. 2014, 34, 1020–1024. [Google Scholar] [CrossRef] [Green Version]
- Weng, J.R.; Lin, C.S.; Lai, H.C.; Lin, Y.P.; Wang, C.Y.; Tsai, Y.C.; Wu, K.C.; Huang, S.H.; Lin, C.W. Antiviral activity of Sambucus FormosanaNakai ethanol extract and related phenolic acid constituents against human coronavirus NL63. Virus Res. 2019, 273, 197767. [Google Scholar] [CrossRef]
- Bhowmik, D.; Nandi, R.; Jagadeesan, R.; Kumar, N.; Prakash, A.; Kumar, D. Identification of potential inhibitors against SARS-CoV-2 by targeting proteins responsible for envelope formation and virion assembly using docking based virtual screening, and pharmacokinetics approaches. Infect. Genet. Evol. 2020, 84, 104451. [Google Scholar] [CrossRef]
- Patil, R.S.; Khatib, N.A.; Patil, V.S.; Suryawanshi, S.S. Chlorogenic acid may be a potent inhibitor of dimeric SARS-CoV-2 main protease 3CLpro: An in silico study. Tradit. Med. Res. 2021, 6, 20. [Google Scholar] [CrossRef]
- El Gizawy, H.A.; Boshra, S.A.; Mostafa, A.; Mahmoud, S.H.; Ismail, M.I.; Alsfouk, A.A.; Taher, A.T.; Al-Karmalawy, A.A. Pimenta dioica (L.) Merr. Bioactive Constituents Exert Anti-SARS-CoV-2 and Anti-Inflammatory Activities: Molecular Docking and Dynamics, In vitro, and In Vivo Studies. Molecules 2021, 26, 5844. [Google Scholar] [CrossRef] [PubMed]
- Hsu, W.-C.; Chang, S.-P.; Lin, L.-C.; Li, C.-L.; Richardson, C.D.; Lin, C.-C.; Lin, L.-T. Limonium Sinense and gallic acid suppress hepatitis C virus infection by blocking early viral entry. Antivir. Res. 2015, 118, 139–147. [Google Scholar] [CrossRef] [PubMed]
- Nutan, M.M.; Goel, T.; Das, T.; Malik, S.; Suri, S.; Rawat, A.K.; Srivastava, S.K.; Tuli, R.; Malhotra, S.; Gupta, S.K. Ellagic acid & gallic acid from Lagerstroemia speciosa L. inhibit HIV-1 infection through inhibition of HIV-1 protease & reverse transcriptase activity. Ind. J. Med. Res. 2013, 137, 540–548. [Google Scholar]
- Choi, H.J.; Song, J.H.; Park, K.S.; Baek, S.H. In vitro anti-enterovirus 71 activity of gallic acid from Woodfordia fruticosa flowers. Lett. Appl. Microb. 2010, 50, 438–440. [Google Scholar] [CrossRef]
- Lee, J.H.; Oh, M.; Seok, J.H.; Kim, S.; Lee, D.B.; Bae, G.; Bae, H.I.; Bae, S.Y.; Hong, Y.M.; Kwon, S.O.; et al. Antiviral Effects of Black Raspberry (Rubus coreanus) Seed and Its Gallic Acid against Influenza Virus Infection. Viruses 2016, 8, 157. [Google Scholar] [CrossRef] [Green Version]
- Treml, J.; Gazdová, M.; Šmejkal, K.; Šudomová, M.; Kubatka, P.; Hassan, S.T.S. Natural products-derived chemicals: Breaking barriers to novel anti-HSV drug development. Viruses 2020, 12, 154. [Google Scholar] [CrossRef] [Green Version]
- Alrasheid, A.A.; Babiker, M.Y.; Awad, T.A. Evaluation of certain medicinal plants compounds as new potential inhibitors of novel corona virus (COVID-19) using molecular docking analysis. In silico. Pharmacology 2021, 9, 10. [Google Scholar] [CrossRef]
- Kwon, M.J.; Shin, H.M.; Perumalsamy, H.; Wang, X.; Ahn, Y.-J. Antiviral effects and possible mechanisms of action of constituents from Brazilian propolis and related compounds. J. Apic. Res. 2019, 59, 413–425. [Google Scholar] [CrossRef]
- Shaldam, M.A.; Yahya, G.; Mohamed, N.H.; Abdel-Daim, M.M.; Al Naggar, Y. In silico Screening of Potent Bioactive Compounds from Honey Bee Products Against COVID-19 Target Enzymes. Environ. Sci. Pollut. Res. 2021, 28, 40507–40514. [Google Scholar] [CrossRef]
- Orfali, R.; Rateb, M.E.; Hassan, H.M.; Alonazi, M.; Gomaa, M.R.; Mahrous, N.; GabAllah, M.; Kandeil, A.; Perveen, S.; Abdelmohsen, U.R.; et al. Sinapic Acid Suppresses SARS-CoV-2 Replication by Targeting Its Envelope Protein. Antibiotics 2021, 10, 420. [Google Scholar] [CrossRef] [PubMed]
- Bertelli, M.; Kiani, A.K.; Paolacci, S.; Manara, E.; Kurti, D.; Dhuli, K.; Bushati, V.; Miertus, J.; Pangallo, D.; Baglivo, M.; et al. Hydroxytyrosol: A natural compound with promising pharmacological activities. J. Biotechnol. 2020, 309, 29–33. [Google Scholar] [CrossRef] [PubMed]
- Yamada, K.; Ogawa, H.; Hara, A.; Yoshida, Y.; Yonezawa, Y.; Karibe, K.; Nghia, V.B.; Yoshimura, H.; Yamamoto, Y.; Yamada, M.; et al. Mechanism of the antiviral effect of hydroxytyrosol on influenza virus appears to involve morphological change of the virus. Antivir. Res. 2009, 83, 35–44. [Google Scholar] [CrossRef] [PubMed]
- Paolacci, S.; Kiani, A.K.; Shree, P.; Tripathi, D.; Tripathi, Y.B.; Tripathi, P.; Tartaglia, G.M.; Farronato, M.; Farronato, G.; Connelly, S.T.; et al. Scoping review on the role and interactions of hydroxytyrosol and alpha-cyclodextrin in lipid-raft-mediated endocytosis of SARS-CoV-2 and bioinformatic molecular docking studies. Eur. Rev. Med. Pharmacol. Sci. 2021, 25 (Suppl. 1), 90–100. [Google Scholar] [CrossRef]
- Crudele, A.; Smeriglio, A.; Ingegneri, M.; Panera, N.; Bianchi, M.; Braghini, M.R.; Pastore, A.; Tocco, V.; Carsetti, R.; Zaffina, S.; et al. Hydroxytyrosol Recovers SARS-CoV-2-PLpro-Dependent Impairment of Interferon Related Genes in Polarized Human Airway, Intestinal and Liver Epithelial Cells. Antioxidants 2022, 11, 1466. [Google Scholar] [CrossRef]
- Wang, L.; Song, J.; Liu, A.; Xiao, B.; Li, S.; Wen, Z.; Lu, Y.; Du, G. Research Progress of the Antiviral Bioactivities of Natural Flavonoids. Nat. Prod. Bioprospect. 2020, 10, 271–283. [Google Scholar] [CrossRef]
- Pandey, P.; Rane, J.S.; Chatterjee, A.; Kumar, A.; Khan, R.; Prakash, A.; Ray, S. Targeting SARS-CoV-2 spike protein of COVID-19 with naturally occurring phytochemicals: An in silico study for drug development. J. Biomol. Struct. Dyn. 2020, 22, 1–11. [Google Scholar] [CrossRef] [PubMed]
- Muhammad, S.; Hira, S.; Al-sehemi, A.G.; Abdullah, H.; Khan, M.; Irfan, M.; Iqbal, J. Exploring the new potential antiviral constituents of Moringa oliefera for SARS-CoV-2 pathogenesis: An in silico molecular docking and dynamic studies. Chem. Phys. Lett. 2021, 767, 138379. [Google Scholar] [CrossRef]
- Omotuyi, I.O.; Nash, O.; Ajiboye, B.O.; Olumekun, V.O.; Oyinloye, B.E.; Olonisakin, A.; Ajayi, A.O.; Olusanya, O.; Akomolafe, F.S.; Adelakun, N. Aframomum melegueta secondary metabolites exhibit polypharmacology against SARS-CoV-2 drug targets: In vitro validation of furin inhibition. Phyther. Res. 2020, 35, 908–919. [Google Scholar] [CrossRef]
- Hariono, M.; Hariyono, P.; Dwiastuti, R.; Setyani, W.; Yusuf, M.; Salin, N.; Wahab, H. Potential SARS-CoV-2 Mpro inhibitors from chromene, flavonoid and hydroxamic acid compound based on fret assay, docking and pharmacophore studies. Res. Chem. 2021, 3, 100195. [Google Scholar] [CrossRef]
- Ojha, D.; Das, R.; Sobia, P.; Dwivedi, V.; Ghosh, S.; Samanta, A.; Chattopadhyay, D. Pedilanthus tithymaloides Inhibits HSV infection by modulating NF-κB signaling. PLoS ONE 2015, 10, e0139338. [Google Scholar] [CrossRef] [PubMed]
- Mishra, R.C.; Kumari, R.; Yadav, S.; Yadav, J.P. Antiviral potential of phytoligands against chymotrypsin-like protease of COVID-19 virus using molecular docking studies: An optimistic approach. Res. Square, 2020; ahead of print. [Google Scholar] [CrossRef] [Green Version]
- Rakshit, G.; Dagur, P.; Satpathy, S.; Patra, A.; Jain, A.; Ghosh, M. Flavonoids as potential therapeutics against novel coronavirus disease-2019 (nCOVID-19). J. Biomol. Struct. Dyn. 2022, 40, 6989–7001. [Google Scholar] [CrossRef] [PubMed]
- Munafò, F.; Donati, E.; Brindani, N.; Ottonello, G.; Armirotti, A.; De Vivo, M. Quercetin and luteolin are single-digit micromolar inhibitors of the SARS-CoV-2 RNA-dependent RNA polymerase. Sci. Rep. 2022, 12, 10571. [Google Scholar] [CrossRef] [PubMed]
- Jo, S.; Kim, S.; Shin, D.H.; Kim, M.S. Inhibition of SARSCoV 3CL protease by flavonoids. J. Enzyme. Inhib. Med. Chem. 2020, 35, 145–151. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tallei, T.E.; Tumilaar, S.G.; Niode, N.J.; Fatimawali, F.; Kepel, B.J.; Idroes, R.; Effendi, Y.; Sakib, S.A.; Emran, T.B. Potential of Plant Bioactive Compounds as SARS-CoV-2 Main Protease (Mpro) and Spike (S) Glycoprotein Inhibitors: A Molecular Docking Study. Scientifica 2020, 2020, 6307457. [Google Scholar] [CrossRef]
- Jo, S.; Kim, S.; Kim, D.Y.; Kim, M.S.; Shin, D.H. Flavonoids with inhibitory activity against SARS-CoV-2 3CLpro. J. Enzyme Inhib. Med. Chem. 2020, 35, 1539–1544. [Google Scholar] [CrossRef]
- Yan, H.; Wang, H.; Ma, L.; Ma, X.; Yin, J.; Wu, S.; Huang, H.; Li, Y. Cirsimaritin inhibits influenza A virus replication by downregulating the NF-κB signal transduction pathway. Virol. J. 2018, 15, 88. [Google Scholar] [CrossRef]
- Sekiou, O.; Bouziane, I.; Frissou, N.; Bouslama, Z.; Honcharova, O.; Djemel, A.; Benselhoub, A. In-Silico Identification of Potent Inhibitors of COVID-19 Main Protease (Mpro) from Natural Products. Int. J. Biochem. Physiol. 2020, 5, 16000189. [Google Scholar] [CrossRef]
- Pitsillou, E.; Liang, J.; Ververis, K.; Lim, K.W.; Hung, A.; Karagiannis, T.C. Identification of Small Molecule Inhibitors of the Deubiquitinating Activity of the SARS-CoV-2 Papain-Like Protease: In silico Molecular Docking Studies and in vitro Enzymatic Activity Assay. Front. Chem. 2020, 8, 623971. [Google Scholar] [CrossRef]
- Dayem, A.A.; Choi, H.Y.; Kim, Y.B.; Cho, S.-G. Antiviral Effect of Methylated Flavonol Isorhamnetin against Influenza. PLoS ONE 2015, 10, e0121610. [Google Scholar] [CrossRef] [Green Version]
- Vicidomini, C.; Roviello, V.; Roviello, G.N. In silico Investigation on the Interaction of Chiral Phytochemicals from Opuntia ficus-indica with SARS-CoV-2 Mpro. Symmetry 2021, 13, 1041. [Google Scholar] [CrossRef]
- Zhan, Y.; Ta, W.; Tang, W.; Hua, R.; Wang, J.; Wang, C.; Lu, W. Potential antiviral activity of isorhamnetin against SARS-CoV-2 spike pseudotyped virus in vitro. Drug Dev. Res. 2021, 82, 1124–1130. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.; Heng, W.; Wang, Y.; Qiu, J.; Wei, X.; Peng, S.; Saleem, S.; Khan, M.; Ali, S.S.; Wei, D.Q. In silico and in vitro evaluation of kaempferol as a potential inhibitor of the SARS-CoV-2 main protease (3CLpro). Phytother. Res. 2021, 35, 2841–2845. [Google Scholar] [CrossRef] [PubMed]
- Khaerunnisa, S.; Kurniawan, H.; Awaluddin, R.; Suhartati, S.; Soetjipto, S. Potential Inhibitor of COVID-19 Main Protease (Mpro) From Several Medicinal Plant Compounds by Molecular Docking Study. Preprints 2020, 2020030226. [Google Scholar] [CrossRef] [Green Version]
- Bilginer, S.; Gözcü, S.; Güvenalp, Z. Molecular Docking Study of Several Seconder Metabolites from Medicinal Plants as Potential Inhibitors of COVID-19 Main Protease. Turk. J. Pharm. Sci. 2022, 19, 431–441. [Google Scholar] [CrossRef]
- Mukherjee, S.; Sharma, D.; Sharma, A.K.; Jaiswal, S.; Sharma, N.; Borah, S.; Kaur, G. Flavan-based phytoconstituents inhibit Mpro, a SARS-COV-2 molecular target, in silico. J. Biomol. Struct. Dyn. 2022, 40, 11545–11559. [Google Scholar] [CrossRef]
- Yarmolinsky, L.; Huleihel, M.; Zaccai, M.; Ben-Shabat, S. Potent antiviral flavone glycosides from Ficus benjamina leaves. Fitoterapia 2012, 83, 362–367. [Google Scholar] [CrossRef] [PubMed]
- Owis, A.I.; El-Hawary, M.S.; El Amir, D.; Aly, O.M.; Abdelmohsen, U.R.; Kamel, M.S. Molecular docking reveals the potential of Salvadora persica flavonoids to inhibit COVID-19 virus main protease. RSC Adv. 2020, 10, 19570–19575. [Google Scholar] [CrossRef]
- Daino, G.L.; Frau, A.; Sanna, C.; Rigano, D.; Distinto, S.; Madau, V.; Esposito, F.; Fanunza, E.; Bianco, G.; Taglialatela-Scafati, O.; et al. Identification of Myricetin as an Ebola virus VP35-double-stranded RNA interaction inhibitor through a novel fluorescence-based assay. Biochemistry 2018, 57, 6367–6378. [Google Scholar] [CrossRef] [Green Version]
- Sang, H.; Huang, Y.; Tian, Y.; Liu, M.; Chen, L.; Li, L.; Liu, S.; Yang, J. Multiple modes of action of myricetin in influenza A virus infection. Phytother. Res. 2021, 35, 2797–2806. [Google Scholar] [CrossRef]
- Yu, M.S.; Lee, J.; Lee, J.M.; Kim, Y.; Chin, Y.W.; Jee, J.G.; Keum, Y.S.; Jeong, Y.J. Identification of myricetin and scutellarein as novel chemical inhibitors of the SARS coronavirus helicase, nsP13. Bioorg. Med. Chem. Lett. 2012, 22, 4049–4054. [Google Scholar] [CrossRef]
- Cherrak, S.A.; Merzouk, H.; Mokhtari-Soulimane, N. Potential bioactive glycosylated flavonoids as SARS-CoV-2 main protease inhibitors: A molecular docking and simulation studies. PLoS ONE 2020, 15, e0240653. [Google Scholar] [CrossRef] [PubMed]
- Xiao, T.; Cui, M.; Zheng, C.; Wang, M.; Sun, R.; Gao, D.; Bao, J.; Ren, S.; Yang, B.; Lin, J.; et al. Myricetin Inhibits SARS-CoV-2 Viral Replication by Targeting Mpro and Ameliorates Pulmonary Inflammation. Front Pharmacol. 2021, 12, 669642. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Ye, F.; Sun, Q.; Liang, H.; Li, C.; Li, S.; Lu, R.; Huang, B.; Tan, W.; Lai, L. Scutellaria baicalensis extract and baicalein inhibit replication of SARS-CoV-2 and its 3C-like protease in vitro. J. Enzyme Inhib. Med. Chem. 2021, 36, 497–503. [Google Scholar] [CrossRef] [PubMed]
- Ortega, J.T.; Suárez, A.I.; Serrano, M.L.; Baptista, J.; Pujol, F.H.; Rangel, H.R. The role of the glycosyl moiety of myricetin derivatives in anti-HIV-1 activity in vitro. AIDS Res. Ther. 2017, 14, 57. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Joshi, R.S.; Jagdale, S.S.; Bansode, S.B.; Shiva Shankar, S.; Tellis, M.B.; Pandya, V.K.; Chugh, A.; Giri, A.P.; Kulkarni, M.J. Discovery of potential multi-target-directed ligands by targeting host-specific SARS-CoV-2 structurally conserved main protease. J. Biomol. Struct. Dyn. 2020, 39, 3099–3114. [Google Scholar] [CrossRef] [Green Version]
- Lulu, S.S.; Thabitha, A.; Vino, S.; Priya, A.M.; Rout, M. Naringenin and quercetin—Potential anti-HCV agents for NS2 protease targets. Nat. Prod. Res. 2016, 30, 464–468. [Google Scholar] [CrossRef]
- Lee, S.; Lee, H.H.; Shin, Y.S.; Kang, H.; Cho, H. The anti-HSV-1 effect of quercetin is dependent on the suppression of TLR-3 in Raw 264.7 cells. Arch. Pharmacal. Res. 2017, 40, 623–630. [Google Scholar] [CrossRef]
- Kalita, R.; Bhattacharya, K.; Ali, A.; Sandilya, S. Quercitin as an antiviral weapon-A review. J. Appl. Pharm. Res. 2021, 9, 1–7. [Google Scholar] [CrossRef]
- Wu, W.; Li, R.; Li, X.; He, J.; Jiang, S.; Liu, S.; Yang, J. Quercetin as an antiviral agent inhibits influenza A virus (IAV) entry. Viruses 2015, 8, 6. [Google Scholar] [CrossRef]
- Abian, O.; Ortega-Alarcon, D.; Jimenez-Alesanco, A.; Ceballos-Laita, L.; Vega, S.; Reyburn, H.T.; Rizzuti, B.; Velazquez-Campoy, A. Structural stability of SARS-CoV-2 3CLpro and identification of quercetin as an inhibitor by experimental screening. Int. J. Biol. Macromol. 2020, 164, 1693–1703. [Google Scholar] [CrossRef]
- Liu, X.; Raghuvanshi, R.; Ceylan, F.D.; Bolling, B.W. Quercetin and Its Metabolites Inhibit Recombinant Human AngiotensinConverting Enzyme 2 (ACE2) Activity. J. Agric. Food Chem. 2020, 68, 13982–13989. [Google Scholar] [CrossRef]
- Chen, L.; Li, J.; Luo, C.; Liu, H.; Xu, W.; Chen, G.; Liew, O.W.; Zhu, W.; Puah, C.M.; Shen, X.; et al. Binding interaction of quercetin-3-β-galactoside and its synthetic derivatives with SARS-CoV 3CLpro: Structure-activity relationship studies reveal salient pharmacophore features. Bioorg. Med. Chem. 2006, 14, 8295–8306. [Google Scholar] [CrossRef] [PubMed]
- Bose, M.; Kamra, M.; Mullick, R.; Bhattacharya, S.; Das, S.; Karande, A.A. Identification of a flavonoid isolated from plum (Prunus domestica) as a potent inhibitor of Hepatitis C virus entry. Sci. Rep. 2017, 7, 3965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, H.J.; Song, J.H.; Park, K.S.; Kwon, D.H. Inhibitory effects of quercetin 3-rhamnoside on influenza A virus replication. Eur. J. Pharm. Sci. 2009, 37, 329–333. [Google Scholar] [CrossRef] [PubMed]
- Frengki, F.; Putra, D.P.; Wahyuni, F.S.; Khambri, D.; Vanda, H.; Sofia, V. Potential antiviral of catechins and their derivatives to inhibit sars-cov-2 receptors of Mpro protein and spike glycoprotein in COVID-19 through the in silico approach. J. Kedokt. Hewan 2020, 14, 59–65. [Google Scholar] [CrossRef]
- Ghosh, R.; Chakraborty, A.; Biswas, A.; Chowdhuri, S. Evaluation of green tea polyphenols as novel corona virus (SARS-CoV-2) main protease (Mpro) inhibitors—An in silico docking and molecular dynamics simulation study. J. Biomol. Struct. Dyn. 2021, 39, 4362–4374. [Google Scholar] [CrossRef]
- Halder, P.; Pal, U.; Paladhi, P.; Dutta, S.; Paul, P.; Pal, S.; Das, D.; Ganguly, A.; Dutta, I.; Mandal, S.; et al. Evaluation of potency of the selected bioactive molecules from Indian medicinal plants with MPro of SARS-CoV-2 through in silico analysis. J. Ayurveda Integr. Med. 2022, 13, 100449. [Google Scholar] [CrossRef]
- Pandey, A.K.; Verma, S. An in-silico evaluation of dietary components for structural inhibition of SARS-Cov-2 main protease. J. Biomol. Struct. Dyn. 2022, 40, 136–142. [Google Scholar] [CrossRef]
- Xu, J.; Xu, Z.; Zheng, W. A Review of the Antiviral Role of Green Tea Catechins. Molecules 2017, 22, 1337. [Google Scholar] [CrossRef] [Green Version]
- Mhatre, S.; Naik, S.; Patravale, V. A molecular docking study of EGCG and theaflavin digallate with the druggable targets of SARS-CoV-2. Comput. Biol. Med. 2021, 129, 104137. [Google Scholar] [CrossRef] [PubMed]
- Jang, M.; Park, Y.-I.; Cha, Y.-E.; Park, R.; Namkoong, S.; Lee, J.I.; Park, J. Tea polyphenols EGCG and theaflavin inhibit the activity of SARS-CoV-2 3CL protease in vitro. Evid. Based Complem. Altern. Med. 2020, 2020, 5630838. [Google Scholar] [CrossRef] [PubMed]
- Henss, L.; Auste, A.; Schürmann, C.; Schmidt, C.; von Rhein, C.; Mühlebach, M.D.; Schnierle, B.S. The green tea catechin epigallocatechin gallate inhibits SARS-CoV-2 infection. J. Gen. Virol. 2021, 102, 001574. [Google Scholar] [CrossRef] [PubMed]
- Sahoo, M.; Jena, L.; Rath, S.N.; Kumar, S. Identification of Suitable Natural Inhibitor against Influenza A (H1N1) Neuraminidase Protein by Molecular Docking. Genom. Inf. 2016, 14, 96–103. [Google Scholar] [CrossRef] [Green Version]
- Mostafa, N.M.; Ismail, M.I.; El-Araby, A.M.; Bahgat, D.M.; Elissawy, A.M.; Mostafa, A.M.; Eldahshan, O.A.; Singab, A.N.B. Investigation of SARS-CoV-2 Main Protease Potential Inhibitory Activities of Some Natural Antiviral Compounds Via Molecular Docking and Dynamics Approaches. Phyton Int. J. Exp. Bot. 2022, 91, 1089–1104. [Google Scholar] [CrossRef]
- Ahmadi, A.; Hassandarvish, P.; Lani, R.; Yadollahi, P.; Jokar, A.; Bakar, S.A.; Zandi, K. Inhibition of chikungunya virus replication by hesperetin and naringenin. RSC Adv. 2016, 6, 69421–69430. [Google Scholar] [CrossRef]
- Castrillo, M.; Córdova, T.; Cabrera, G.; Rodríguez-Ortega, M. Effect of naringenin, hesperetin and their glycosides forms on the replication of the 17D strain of yellow fever virus. Avan. Biomed. 2015, 4, 69–78. [Google Scholar]
- Piva, H.M.R.; Sá, J.M.; Miranda, A.S.; Tasic, L.; Fossey, M.A.; Souza, F.P.; Caruso, I. Insights into Interactions of Flavanones with Target Human Respiratory Syncytial Virus M2-1 Protein from STD-NMR, Fluorescence Spectroscopy, and Computational Simulations. Int. J. Mol. Sci. 2020, 21, 2241. [Google Scholar] [CrossRef] [Green Version]
- Lin, C.W.; Tsai, F.J.; Tsai, C.H.; Lai, C.C.; Wan, L.; Ho, T.Y.; Hsieh, C.C.; Chao, P.D. Anti-SARS coronavirus 3C-like protease effects of Isatis indigotica root and plant-derived phenolic compounds. Antivir. Res. 2005, 68, 36–42. [Google Scholar] [CrossRef]
- Cheng, F.-J.; Huynh, T.-K.; Yang, C.-S.; Hu, D.-W.; Shen, Y.-C.; Tu, C.-Y.; Wu, Y.-C.; Tang, C.-H.; Huang, W.-C.; Chen, Y.; et al. Hesperidin Is a Potential Inhibitor against SARS-CoV-2 Infection. Nutrients 2021, 13, 2800. [Google Scholar] [CrossRef]
- Depieri Cataneo, A.H.; Kuczera, D.; Koishi, A.C.; Zanluca, C.; Ferreira Silveira, G.; Bonato de Arruda, T.; Akemi Suzukawa, A.; Oliveira Bortot, L.; Dias-Baruffi, M.; Aparecido Verri, W., Jr.; et al. The citrus flavonoid naringenin impairs the in vitro infection of human cells by Zika virus. Sci. Rep. 2019, 9, 16348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Frabasile, S.; Koishi, A.C.; Kuczera, D.; Silveira, G.F.; Verri, W.A., Jr.; Duarte Dos Santos, C.N.; Bordignon, J. The citrus flavanone naringenin impairs dengue virus replication in human cells. Sci. Rep. 2017, 7, 41864. [Google Scholar] [CrossRef] [Green Version]
- Abdallah, H.M.; El-Halawany, A.M.; Sirwi, A.; El-Araby, A.M.; Mohamed, G.A.; Ibrahim, S.R.M.; Koshak, A.E.; Asfour, H.Z.; Awan, Z.A.; Elfaky, M.A. Repurposing of Some Natural Product Isolates as SARS-COV-2 Main Protease Inhibitors via In vitro Cell Free and Cell-Based Antiviral Assessments and Molecular Modeling Approaches. Pharmaceuticals 2021, 14, 213. [Google Scholar] [CrossRef] [PubMed]
- Clementi, N.; Scagnolari, C.; D’Amore, A.; Palombi, F.; Criscuolo, E.; Frasca, F.; Pierangeli, A.; Mancini, N.; Antonelli, G.; Clementi, M.; et al. Naringenin is a powerful inhibitor of SARS-CoV-2 infection in vitro. Pharmacol. Res. 2021, 163, 105255. [Google Scholar] [CrossRef] [PubMed]
- Hayati, R.F.; Better, C.D.; Denis, D.; Komarudin, A.G.; Bowolaksono, A.; Yohan, B.; Sasmono, R.T. [6]-Gingerol inhibits chikungunya virus infection by suppressing viral replication. BioMed. Res. Int. 2021, 2021, 6623400. [Google Scholar] [CrossRef]
- Rathinavel, T.; Palanisamy, M.; Palanisamy, S.; Subramanian, A.; Thangaswamy, S. Phytochemical 6-Gingerol—A promising Drug of choice for COVID-19. Int. J. Adv. Sci. Eng. 2020, 6, 1482–1489. [Google Scholar] [CrossRef]
- Abdallah, H.M.; El-Halawany, A.M.; Darwish, K.M.; Algandaby, M.M.; Mohamed, G.A.; Ibrahim, S.R.M.; Koshak, A.E.; Elhady, S.S.; Fadil, S.A.; Alqarni, A.A.; et al. Bio-Guided Isolation of SARS-CoV-2 Main Protease Inhibitors from Medicinal Plants: In vitro Assay and Molecular Dynamics. Plants 2022, 11, 1914. [Google Scholar] [CrossRef]
- Praditya, D.; Kirchhoff, L.; Bruning, J.; Rachmawati, H.; Steinmann, J.; Steinmann, E. Anti-infective properties of the golden spice curcumin. Front. Microbiol. 2019, 10, 912. [Google Scholar] [CrossRef] [Green Version]
- Baikerikar, S. Curcumin and natural derivatives inhibit Ebola viral proteins: An in silico approach. Pharmacogn. Res. 2017, 9, 15–22. [Google Scholar] [CrossRef]
- Goc, A.; Sumera, W.; Rath, M.; and Niedzwiecki, A. Phenolic compounds disrupt spike-mediated receptor-binding and entry of SARS-CoV-2 pseudo-virions. PLoS ONE 2021, 16, e0253489. [Google Scholar] [CrossRef]
- Goc, A.; Rath, M.; Niedzwiecki, A. Composition of naturally occurring compounds decreases activity of Omicron and SARS-CoV-2 RdRp complex. Eur. J. Microbiol. Immunol. 2022, 12, 39–45. [Google Scholar] [CrossRef]
- Annunziata, G.; Maisto, M.; Schisano, C.; Ciampaglia, R.; Narciso, V.; Tenore, G.C.; Novellino, E. Resveratrol as a novel antiherpes simplex virus nutraceutical agent: An overview. Viruses 2018, 10, 473. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, L.; Li, Y.; Gu, Z.; Wang, Y.; Shi, M.; Ji, Y.; Sun, J.; Xu, X.; Zhang, L.; Jiang, J.; et al. Resveratrol Inhibits Enterovirus 71 Replication and Pro-Inflammatory Cytokine Secretion in Rhabdosarcoma Cells through Blocking IKKs/NFκB Signaling Pathway. PLoS ONE 2015, 10, e0116879. [Google Scholar] [CrossRef] [Green Version]
- Wahedi, H.M.; Ahmad, S.; Abbasi, S.W. Stilbene-based natural compounds as promising drug candidates against COVID-19. J. Biomol. Struct. Dyn. 2020, 12, 1–10. [Google Scholar] [CrossRef]
- ter Ellen, B.M.; Dinesh Kumar, N.; Bouma, E.M.; Troost, B.; van de Pol, D.P.I.; van der Ende-Metselaar, H.H.; Apperloo, L.; van Gosliga, D.; van den Berge, M.; Nawijn, M.C.; et al. Resveratrol and Pterostilbene Inhibit SARS-CoV-2 Replication in Air–Liquid Interface Cultured Human Primary Bronchial Epithelial Cells. Viruses 2021, 13, 1335. [Google Scholar] [CrossRef] [PubMed]
- Pasquereau, S.; Nehme, Z.; Haidar Ahmad, S.; Daouad, F.; Van Assche, J.; Wallet, C.; Schwartz, C.; Rohr, O.; Morot-Bizot, S.; Herbein, G. Resveratrol inhibits HCoV-229E and SARS-CoV-2 coronavirus replication in vitro. Viruses 2021, 13, 354. [Google Scholar] [CrossRef]
- Yang, M.; Wei, J.; Huang, T.; Lei, L.; Shen, C.; Lai, J.; Yang, M.; Liu, L.; Yang, Y.; Liu, G.; et al. Resveratrol inhibits the replication of severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in cultured Vero cells. Phytother. Res. 2021, 35, 1127–1129. [Google Scholar] [CrossRef]
- David, A.B.; Diamant, E.; Dor, E.; Barnea, A.; Natan, N.; Levin, L.; Chapman, S.; Mimran, L.C.; Epstein, E.; Zichel, R.; et al. Identification of SARS-CoV-2 Receptor Binding Inhibitors by In vitro Screening of Drug Libraries. Molecules 2021, 26, 3213. [Google Scholar] [CrossRef]
- Yang, Y.; Xiu, J.; Liu, J.; Zhang, L.; Li, X.; Xu, Y.; Qin, C.; Zhang, L. Chebulagic Acid, a Hydrolyzable Tannin, Exhibited Antiviral Activity in vitro and in Vivo against Human Enterovirus 71. Int. J. Mol. Sci. 2013, 14, 9618–9627. [Google Scholar] [CrossRef] [Green Version]
- Kesharwani, A.; Polachira, S.K.; Nair, R.; Agarwal, A.; Mishra, N.N.; Gupta, S.K. Anti-HSV-2 activity of Terminalia chebula Retz extract and its constituents, chebulagic and chebulinic acids. BMC Complem. Altern. Med. 2017, 17, 110. [Google Scholar] [CrossRef] [Green Version]
- Du, R.; Cooper, L.; Chen, Z.; Lee, H.; Rong, L.; Cui, Q. Discovery of chebulagic acid and punicalagin as novel allosteric inhibitors of SARS-CoV-2 3CLpro. Antivir. Res. 2021, 190, 105075. [Google Scholar] [CrossRef] [PubMed]
- Yang, Y.; Xiu, J.; Zhang, L.; Qin, C.; Liu, J. Antiviral activity of punicalagin toward human enterovirus 71 in vitro and in vivo. Phytomedicine 2012, 20, 67–70. [Google Scholar] [CrossRef] [PubMed]
- Arunkumar, J.; Rajarajan, S. Study on antiviral activities, druglikeness and molecular docking of bioactive compounds of Punica granatum L. to herpes simplex virus - 2 (HSV-2). Microb Pathog 2018, 118, 301–309. [Google Scholar] [CrossRef] [PubMed]
- Suručić, R.; Tubić, B.; Stojiljković, M.P.; Djuric, D.M.; Travar, M.; Grabež, M.M.; Šavikin, K.; Škrbić, R. Computational study of pomegranate peel extract polyphenols as potential inhibitors of SARS-CoV-2 virus internalization. Mol. Cell. Biochem. 2021, 476, 1179–1193. [Google Scholar] [CrossRef] [PubMed]
- Ma, J.; Gu, Y.; Xu, P. A Roadmap to Engineering Antiviral Natural Products Synthesis in Microbes. Curr. Opin. Biotechnol. 2020, 66, 140–149. [Google Scholar] [CrossRef] [PubMed]
- Hussain, T.; Habib, A.H.; Rafeeq, M.M.; Alafnan, A.; Khafagy, E.-S.; Iqbal, D.; Jamal, Q.M.S.; Unissa, R.; Sharma, D.C.; Moin, A.; et al. Oleuropein as a Potent Compound against Neurological Complications Linked with COVID-19: A Computational Biology Approach. Entropy 2022, 24, 881. [Google Scholar] [CrossRef] [PubMed]
- Mishra, S.; Pandey, A.; Manvati, S. Coumarin: An emerging antiviral agent. Heliyon 2020, 6, e03217. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abdizadeh, R.; Hadizadeh, F.; Abdizadeh, T. In silico analysis and identification of antiviral coumarin derivatives against 3-chymotrypsin-like main protease of the novel coronavirus SARS-CoV-2. Mol. Divers 2022, 26, 1053–1076. [Google Scholar] [CrossRef]
- Özdemir, M.; Köksoy, B.; Ceyhan, D.; Sayın, K.; Erçağ, E.; Bulut, M.; Yalçın, B. Design and in silico study of the novel coumarin derivatives against SARS-CoV-2 main enzymes. J. Biomol. Struct. Dyn. 2020, 27, 1–16. [Google Scholar] [CrossRef]
- Tang, K.; Zhang, X.; Guo, Y. Identification of the dietary supplement capsaicin as an inhibitor of Lassa virus entry. Acta Pharm. Sin. B 2020, 10, 789–798. [Google Scholar] [CrossRef]
- Mahn, A.; Castillo, A. Potential of sulforaphane as a natural immune system enhancer: A review. Molecules 2021, 26, 752. [Google Scholar] [CrossRef] [PubMed]
- Ordonez, A.A.; Bullen, C.K.; Villabona-Rueda, A.F.; Thompson, E.A.; Turner, M.L.; Merino, V.F.; Yan, Y.; Kim, J.; Davis, S.L.; Komm, O.; et al. Sulforaphane exhibits antiviral activity against pandemic SARS-CoV-2 and seasonal HCoV-OC43 coronaviruses in vitro and in mice. Commun. Biol. 2022, 5, 242. [Google Scholar] [CrossRef] [PubMed]
- Rouf, R.; Uddin, S.J.; Sarker, D.K.; Islam, M.T.; Ali, E.S.; Shilpi, J.A.; Nahar, L.; Tiralongo, E.; Sarker, S.D. Antiviral potential of garlic (Allium sativum) and its organosulfur compounds: A systematic update of pre-clinical and clinical data. Trends Food Sci. Technol. 2020, 104, 219–234. [Google Scholar] [CrossRef]
- Shekh, S.; Reddy, K.K.A.; Gowd, K.H. In silico allicin induced S-thioallylation of SARS-CoV-2 main protease. J. Sulf. Chem. 2021, 42, 109–120. [Google Scholar] [CrossRef]
- Asif, M.; Saleem, M.; Saadullah, M.; Yaseen, H.S.; Al Zarzour, R. COVID-19 and therapy with essential oils having antiviral, anti-inflammatory, and immunomodulatory properties. Inflammopharmacology 2020, 28, 1153–1161. [Google Scholar] [CrossRef] [PubMed]
- Lane, T.; Anantpadma, M.; Freundlich, J.S.; Davey, R.A.; Madrid, P.B.; Ekins, S. The Natural Product Eugenol Is an Inhibitor of the Ebola Virus In vitro. Pharm. Res. 2019, 36, 104. [Google Scholar] [CrossRef]
- Rizzuti, B.; Ceballos-Laita, L.; Ortega-Alarcon, D.; Jimenez-Alesanco, A.; Vega, S.; Grande, F.; Conforti, F.; Abian, O.; Velazquez-Campoy, A. Sub-Micromolar Inhibition of SARS-CoV-2 3CLpro by Natural Compounds. Pharmaceuticals 2021, 14, 892. [Google Scholar] [CrossRef]
- Paidi, R.K.; Jana, M.; Raha, S.; McKay, M.; Sheinin, M.; Mishra, R.K.; Pahan, K. Eugenol, a Component of Holy Basil (Tulsi) and Common Spice Clove, Inhibits the Interaction Between SARS-CoV-2 Spike S1 and ACE2 to Induce Therapeutic Responses. J. Neuroimmune Pharmacol. 2021, 16, 743–755. [Google Scholar] [CrossRef]
- Musarra-Pizzo, M.; Pennisi, R.; Ben-Amor, I.; Mandalari, G.; Sciortino, M.T. Antiviral Activity Exerted by Natural Products against Human Viruses. Viruses 2021, 13, 828. [Google Scholar] [CrossRef]
- Lynch, J.P., 3rd; Kajon, A.E. Adenovirus: Epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin. Respir. Crit. Care Med. 2016, 37, 586–602. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Wang, L.; Si, H.; Yu, Z.; Tian, S.; Xiang, R.; Deng, X.; Liang, R.; Jiang, S.; Yu, F. Influenza virus glycoprotein-reactive human monoclonal antibodies. Microbes Infect. 2020, 22, 263–271. [Google Scholar] [CrossRef] [PubMed]
- Bacelar Júnior, A.J.; Vieira Andrade, A.L.; Gomes Ferreira, A.A.; Andrade Oliveira, S.M.; Silva Pinheiro, T. Human Immunodeficiency Virus—HIV: A Review. Braz. J. Surg. Clin. Res. 2015, 9, 43–48. [Google Scholar]
- International Committee on Taxonomy of Viruses (ICTV). Virus Taxonomy: The Classification and Nomenclature of Viruses. The 9th Report of the ICTV. ICTV. 2011. Available online: https://ictv.global/report_9th (accessed on 5 February 2023).
- Yin, Y.; Wunderink, R.G. MERS, SARS and other coronaviruses as causes of pneumonia. Respirology 2018, 23, 130–137. [Google Scholar] [CrossRef] [Green Version]
- World Health Organization (WHO). WHO Statement Regarding Cluster of Pneumonia Cases in Wuhan, China; WHO: Geneva, Switzerland, 2020; Available online: https://www.who.int/china/news/detail/09-01-2020-who-statement-regarding-cluster-of-pneumonia-cases-in-wuhan-china (accessed on 5 February 2023).
- World Health Organization (WHO). Disease Outbreak News Update. Novel Coronavirus—China 2020; WHO: Geneva, Switzerland, 2020; Available online: https://www.who.int/emergencies/disease-outbreak-news/item/2020-DON233 (accessed on 5 February 2023).
- Kanjanasirirat, P.; Suksatu, A.; Manopwisedjaroen, S.; Munyoo, B.; Tuchinda, P.; Jearawuttanakul, K.; Seemakhan, S.; Charoensutthivarakul, S.; Wongtrakoongate, P.; Rangkasenee, N.; et al. High-content screening of Thai medicinal plants reveals Boesenbergia rotunda extract and its component Panduratin A as anti-SARS-CoV-2 agents. Sci. Rep. 2020, 10, 19963. [Google Scholar] [CrossRef]
- Guo, Y.R.; Cao, Q.D.; Hong, Z.S.; Tan, Y.-Y.; Chen, S.-D.; Jin, H.-J.; Tan, K.-S.; Wang, D.-Y.; Yan, Y. The origin, transmission and clinical therapies on coronavirus disease 2019 (COVID-19) outbreak—An update on the status. Mil. Med. Res. 2020, 7, 11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walls, A.C.; Park, Y.J.; Tortorici, M.A.; Wall, A.; McGuire, A.T.; Veesler, D. Structure, Function, and Antigenicity of the SARS-CoV-2 Spike Glycoprotein. Cell 2020, 181, 281–292.e6. [Google Scholar] [CrossRef]
- Bestle, D.; Heindl, M.R.; Limburg, H.; Van Lam van, T.; Pilgram, O.; Moulton, H.; Stein, D.A.; Hardes, K.; Eickmann, M.; Dolnik, O.; et al. TMPRSS2 and furin are both essential for proteolytic activation of SARS-CoV-2 in human airway cells. Life Sci. Allianc. 2020, 3, e202000786. [Google Scholar] [CrossRef]
- Yuan, M.; Wu, N.C.; Zhu, X.; Lee, C.D.; So, R.T.Y.; Lv, H.; Mok, C.K.P.; Wilson, I.A. A highly conserved cryptic epitope in the receptor-binding domains of SARS-CoV-2 and SARS-CoV. Science 2020, 368, 630–633. [Google Scholar] [CrossRef] [Green Version]
- Hillen, H.S.; Kokic, G.; Farnung, L.; Dienemann, C.; Tegunov, D.; Cramer, P. Structure of replicating SARS-CoV-2 polymerase. Nature 2020, 584, 154–156. [Google Scholar] [CrossRef]
- Chapman, R.L.; Andurkar, S.V. A review of natural products, their effects on SARS-CoV-2 and their utility as lead compounds in the discovery of drugs for the treatment of COVID-19. Med. Chem. Res. 2022, 31, 40–51. [Google Scholar] [CrossRef]
- Keflie, T.S.; Biesalski, H.K. Micronutrients and bioactive substances: Their potential roles in combating COVID-19. Nutrition 2021, 84, 111103. [Google Scholar] [CrossRef] [PubMed]
- Luo, E.; Zhang, D.; Luo, H.; Liu, B.; Zhao, K.; Zhao, Y.; Bian, Y.; Wang, Y. Treatment efficacy analysis of traditional Chinese medicine for novel coronavirus pneumonia (COVID-19): An empirical study from Wuhan, Hubei Province. China Chin. Med. 2020, 15, 34. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahmad, R.; Srivastava, S.; Ghosh, S.; Khare, S.K. Phytochemical delivery through nanocarriers: A review. Colloids Surf. B Biointerfaces 2021, 197, 111389. [Google Scholar] [CrossRef] [PubMed]
- Di Pierro, F.; Derosa, G.; Maffioli, P.; Bertuccioli, A.; Togni, S.; Riva, A.; Allegrini, P.; Khan, A.; Khan, S.; Khan, B.A.; et al. Possible Therapeutic Effects of Adjuvant Quercetin Supplementation Against Early-Stage COVID-19 Infection: A Prospective, Randomized, Controlled, and Open-Label Study. Int. J. Gen. Med. 2021, 14, 2359–2366. [Google Scholar] [CrossRef] [PubMed]
- Di Pierro, F.; Iqtadar, S.; Khan, A.; Ullah Mumtaz, S.; Masud Chaudhry, M.; Bertuccioli, A.; Derosa, G.; Maffioli, P.; Togni, S.; Riva, A.; et al. Potential Clinical Benefits of Quercetin in the Early Stage of COVID-19: Results of a Second, Pilot, Randomized, Controlled and Open-Label Clinical Trial. Int. J. Gen. Med. 2021, 14, 2807–2816. [Google Scholar] [CrossRef]
- Rondanelli, M.; Perna, S.; Gasparri, C.; Petrangolini, G.; Allegrini, P.; Cavioni, A.; Faliva, M.A.; Mansueto, F.; Patelli, Z.; Peroni, G.; et al. Promising Effects of 3-Month Period of Quercetin Phytosome® Supplementation in the Prevention of Symptomatic COVID-19 Disease in Healthcare Workers: A Pilot Study. Life 2022, 12, 66. [Google Scholar] [CrossRef]
- McCreary, M.R.; Schnell, P.M.; Rhoda, D.A. Randomized double-blind placebo-controlled proof-of-concept trial of resveratrol for outpatient treatment of mild coronavirus disease (COVID-19). Sci. Rep. 2022, 12, 10978. [Google Scholar] [CrossRef]
- Valizadeh, H.; Abdolmohammadi-Vahid, S.; Danshina, S.; Ziya Gencer, M.; Ammari, A.; Sadeghi, A.; Roshangar, L.; Aslani, S.; Esmaeilzadeh, A.; Ghaebi, M.; et al. Nano-curcumin therapy, a promising method in modulating inflammatory cytokines in COVID-19 patients. Int. Immunopharmacol. 2020, 89, 107088. [Google Scholar] [CrossRef]
- Saber-Moghaddam, N.; Salari, S.; Hejazi, S.; Amini, M.; Taherzadeh, Z.; Eslami, S.; Rezayat, S.M.; Jaafari, M.R.; Elyasi, S. Oral nano-curcumin formulation efficacy in management of mild to moderate hospitalized coronavirus disease-19 patients: An open label nonrandomized clinical trial. Phytother. Res. 2021, 35, 2616–2623. [Google Scholar] [CrossRef]
- Ahmadi, R.; Salari, S.; Sharifi, M.D.; Reihani, H.; Rostamiani, M.B.; Behmadi, M.; Taherzadeh, Z.; Eslami, S.; Rezayat, S.M.; Jaafari, M.R.; et al. Oral nano-curcumin formulation efficacy in the management of mild to moderate outpatient COVID-19: A randomized triple-blind placebo controlled clinical trial. Food Sci. Nutr. 2021, 9, 4068–4075. [Google Scholar] [CrossRef]
Compounds | Principal Food Sources | Class | Virus | SARS-CoV-2 Activity |
---|---|---|---|---|
Caffeic acid | Carrots, cabbage, tomatoes, several berries, coffee, basil, thyme, oregano, apples | Phenolic acids | HSV-1, HSV-2, ADV-3 [17,18] HCV [19] IAV [20] HCoV-NL63 [21] | Potential inhibition of SARS-CoV-2 membrane protein M (in silico approach) [22] |
Chlorogenic acid | Apples, artichokes, carrots, coffee beans, eggplants, grapes, kiwi fruit, pears, plums, potatoes, tea, tomatoes | Phenolic acids | ADV-3, ADV-8, ADV-11 [18] HCoV-NL63 [21] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [23] Inhibition of SARS-CoV-2 replication (in vitro approach) [24] |
Ferulic acid | Rice, wheat, oats, pineapple, artichoke, peanuts, and nuts | Phenolic acids | Potential inhibition of SARS-CoV-2 membrane protein M (in silico approach) [22] Anti-inflammatory effects (in vitro approach) [24] | |
Gallic acid | Blueberry, blackberry, strawberry, plums, grapes, mango, cashew nut, hazelnut, walnut, tea, wine | Phenolic acids | HCV [25] HIV [26] EV71 [27] IAV, IBV [28] HCoV-NL63 [21] HSV [29] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [30] Inhibition of SARS-CoV-2 replication (in vitro approach) [24] |
p-Coumaric acid | Eggplant, broccoli, asparagus, sweet cherries, plums, blueberries, cranberries, citrus, orange juice | Phenolic acids | HRV-3 [31] | Inhibition of (Mpro) and RdRp enzymes (in silico approach) [32] |
Sinapic acid | Oranges, grapefruits, cranberries | Phenolic acid | Inhibition of SARS-CoV-2 envelope protein E (in silico approach) and inhibition of SARS-CoV-2 replication (in vitro approach) [33] | |
Hydroxytyrosol | Olives, virgin olive oil, wine | Phenolic alcohols | HIV-1 [34] H1N1, H3N2, H5N1, H9N2, NDV [35] | Interaction with SARS-CoV-2 spike protein and human ACE-2 receptor (in silico approach) [36] Reduction of PLpro-dependent adverse effects in long-COVID (in vitro approach) [37] |
Apigenin | Parsley, celery, onions, oranges, tea, chamomile, spinach, basil | Flavones | ASFV, HCV, PEDV, FMD virus, HIV, IV, EBV, SARS-CoV (experimental and in silico approach) [38] HBV [39] | Interaction with SARS-CoV-2 NSP10 (in silico approach) [40] Inhibition of SARS-CoV-2 Mpro (in silico approach) [41] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [42] |
Luteolin | Capsicum, carrots, apple, cabbage, onion leaves, parsley, basil, spinach | Flavones | HSV-2 [43] HIV-1, EBV [39] IAV, JEV, DENV, HBV, SARS-CoV [38] | Inhibition of COVID-19 Mpro protease (in silico approach) [44,45] Interaction with SARS-CoV-2 RdRp (in vitro approach) [46] |
Pectolinarin | Cirsium setidens Nakai | Flavones | SARS-CoV (experimental and in silico approach) [47] | Inhibition of SARS-CoV-2 Mpro and spike (S) glycoprotein (in silico approach) [48] Inhibition of SARS-CoV-2 Mpro (in silico and in vitro approach) [49] |
Rhoifolin | Quinoas, triticales, German camomiles, rice, and oriental wheats | Flavone Glycosides | SARS-CoV (experimental and in silico approach) [47] | Inhibition of SARS-CoV-2 Mpro and spike (S) glycoprotein (in silico approach) [48] Inhibition of SARS-CoV-2 Mpro (in silico and in vitro approach) [49] |
Cirsimaritin | Oregano, lemon verbena, winter savory, rosemary | Dimethoxyflavone | H1N1 [50] | Potential inhibitor against SARS-CoV-2 Mpro and ACE2 (in silico approach) [51] |
Cyanidin-3-O-glucoside | Leafy vegetables, berries, red cabbages, teas, colored grains, plums, black grape | Anthocyanins | Potential inhibitor of SARS-CoV-2 PLpro deubiquitinase activity (in silico and in vitro approach) [52] | |
Isorhamnetin | Parsley, green bell peppers, dill, romaine lettuces, pears, lemons, chickpeas, apples | Flavonols | A/PR/8/34 (H1N1) [53] EV71, HHV-1, HHV-2, ZIKV * (* in silico approach) [38] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [54] Binds to ACE2 receptor (in vitro approach) [55] |
Herbacetin | Ephedra sinica Stapf | Flavonols | SARS-CoV (experimental and in silico approach) [47] | Inhibition of SARS-CoV-2 Mpro (in silico and in vitro approach) [49] |
Kaempferol | Apples, tomatoes, green tea, potatoes, onions, brussels sprouts, lettuce, green and black beans, peaches, blackberries, raspberries, spinach, grapes, broccoli, capers, chives | Flavonols | HCMV, HSV-1, HSV-2, IAV [39] | Potential inhibition of COVID-19 Mpro and RdRp enzymes (in silico approach) [32] Inhibition of SARS-CoV-2 Mpro (in vitro and in silico approach) [56] Inhibition of SARS-CoV-2 Mpro (in silico approach) [57,58,59] |
Kaempferol-3-O-robinobioside | Opuntia | Flavonols | HSV-1, HSV-2 [60] | Potential inhibition of COVID-19 main protease (in silico approach) [61] |
Kaempferol-3-O-rutinoside | Red wine, tea, apples, black tea | Flavonols | HSV-1, HSV-2 [60] | Potential inhibition of COVID-19 main protease (in silico approach) [61] |
Myricetin | Walnuts, carobs, fennels, welsh onions, yellow bell peppers | Flavonols | HIV [62] IAV [63] HSV [29] SARS-CoV [64] | Inhibition of SARS-CoV-2 Mpro (in silico and in vitro approach) [65,66] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [67] |
Myricetin-3-rhamnoside (Myricitrin) | Summer grapes, blackberry, raspberry, hazelnuts, sapodillas | Flavonols | HIV [68] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [65,69] |
Quercetin | Apples, berries, grapes, citrus fruits, tea, many seeds, nuts, honey, propolis, radish, fennel | Flavonols | HCV (in silico approach) [70] HSV-1 [71] HIV [72] IAV [73] | Inhibition of SARS-CoV-2 Mpro and RdRp enzymes (in silico approach) [30,32,65] Perturbation of the binding of hACE2-S complex (in silico approach) [39,51] Interaction with SARS-CoV-2 NSP16 (in silico approach) [41] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [42,74] Inhibition of SARS-CoV-2 Mpro (in silico approach) [57,58,59] Interaction with SARS-CoV-2 RdRp (in vitro approach) [46] Inhibition of rhACE2 activity (in vitro approach) [75] |
Quercetin 3-O-glucuronide | Wine, green beans | Flavonols | Inhibition of SARS-CoV-2 Mpro (in silico approach) [65] Inhibition of rhACE2 activity (in vitro approach) [75] | |
Quercetin-3-beta-galactoside | Walnuts, black chokeberries, red raspberries, summer grapes, almonds | Flavonols | SARS-CoV (in silico approach) [76] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [65] Inhibition of rhACE2 activity (in vitro approach) [75] |
Quercetin-3-O-rutinoside (Rutin) | Parsley, common buckwheats, grape wines, Italian sweet red peppers, nectarines, summer grapes, broccoli, rosemaries, orange, lemon | Flavonols | HCV [77] HSV-1, HSV-2 [60] | Inhibition of SARS-CoV-2 envelope protein E (in silico approach) [22] Inhibition of SARS-CoV-2 Mpro (in silico approach) [65] Inhibitor of SARS-CoV-2 PLpro deubiquitinase activity (in silico and in vitro approach) [52] Inhibition of rhACE2 activity (in vitro approach) [75] Inhibition of SARS-CoV-2 replication and anti-inflammatory effects (in vitro approach) [24] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [49] |
Quercetin-3-O-rhamnoside (Quercitrin) | Lingonberries, American cranberries, olives, beans, tea, Welsh onions, bilberries, common pea, apricots, spearmints | Flavonols | A/WS/33 (H1N1) [78] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [65] |
Catechin | Blackcurrants, blackberries, European plums, redcurrants, cocoa powder. rice, pineapples, cloves, lingonberries, Italian sweet red peppers, argan oil | Flavanols | Inhibition of Mpro protein and Spike glycoprotein (in silico approach) [57,79,80,81] | |
Epicatechin | Pears, star fruits, red tea, common buckwheats, apples, Asian pears | Flavanols | HSV-1, HSV-2 [29] HIV1, HIV2, IAV, IBV [38] | Inhibition of Mpro protein and Spike glycoprotein (in silico approach) [79,82] |
(-)-Epicatechin-3-O-gallate (ECG) | Red tea, herbal tea, green tea, peppermints, common grapes, medlars, kiwifruits, blackberry, raspberry, sweet oranges, common wheats, pistachios | Flavanols | HSV-1, HSV-2 [29] HIV1, HIV2, IAV, IBV [38] | Inhibition of COVID-19 Mpro (in silico approach) [57,59] Inhibition of SARS-CoV-2 Mpro (in silico approach) [80] |
(-)-Epigallocatechin (EGC) | Cocoa beans, green tea, black tea, herbal tea, peanuts, pomegranates, beets, pine nuts, common mushrooms, red bell peppers, allia | Flavanols | HSV [29] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [80] |
Epigallocatechin-3-gallate (EGCG) | Black and green tea, apples, plums | Flavanols | HBV, HSV, EBV, ADV, HIV, HCV, IV, DENV, JEV, TBEV, ZIKV, CHIKV, HTLV-1, EV71, EBOV, PRRSV, VHSV, IHNV, SVCV [83] | Inhibition of S protein of SARS-CoV-2 (in silico approach) [48] Inhibition of SARS-CoV-2 Mpro (in silico approach) [80] Interaction with SARS-CoV-2 Mpro, RdRp, PLpro, S RBD, and ACE2 with S RBD (in silico approach) [84] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [85] Inhibition of SARS-CoV-2 RBD/ACE2 binding (in vitro approach) [86] |
Theaflavin | Black tea, green tea, herbal tea, red tea | Flavanols | H1N1 (in silico approach) [87] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [88] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [85] |
Hesperetin | Citrus fruits, peppermint | Flavanones | CHIKV [89] YFV (experimental and in silico approach) [90] RSV (experimental and in silico approach) [91] SARS-CoV [92] | Inhibition of SARS-CoV-2 spike protein/ACE2 binding and interaction with TMPRSS2 (in silico and in vitro approach) [93] |
Naringenin | Sweet oranges, oregano, sorghums, grape wines, clementine, tangerine, saffrons, white lupines, dates, elderberries | Flavanones | HCV (in silico approach) [70] YFV (experimental and in silico approach) [90] ZIKV (experimental and in silico approach) [94] DENV [95] HSV [29] CHIKV [89] | Inhibition of COVID-19 Mpro (in silico approach) [57] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [96] Inhibition of TPC2 (in vitro approach) [97] |
6-Gingerol | Gingers, cloves, star anises, Ceylon cinnamons, pepper, nutmegs | Gingerols | CHIKV [98] | Interaction with COVID-19 main proteins (in silico approach) [99] Inhibition of SARS-CoV-2 Mpro and moderate activity against the SARSCoV-2 virus (in vitro approach) [100] |
Curcumin | Turmerics, curry powder, saskatoon berries, peanuts, lettuces, green bell peppers | Curcuminoids | HIV, HSV, HCV, HPV, DENV, ZIKV, CHIKV, HBV, IAV, JEV, MNV, RSV, RVFV [101] EBOV (in silico approach) [102] | Inhibition of COVID-19 Mpro (in silico approach) [57,81] Inhibition of SARS-CoV-2 RBD/ACE2 binding; Decrease activity of TMPRSS2 (in vitro approach) [103] Inhibition of RdRP viral complex of both SARS-CoV-2 and the Omicron variant (in vitro approach) [104] |
Resveratrol (3,5,4′-trihydroxy-trans-stilbene) | Broccoli, yellow wax bean, turnip, grapes, blueberries, raspberries, mulberries | Stilbenes | HSV-1, HSV-2 [105] HIV-1, PVR, MERS-CoV [39] EV71 [106] | Interaction with SARS-CoV-2 spike protein and human ACE-2 receptor (in silico approach) [107] Inhibition of SARS-CoV-2 replication (in vitro approach) [108,109,110] |
Ellagic acid | Raspberries, strawberries, cranberries, walnuts, pecans, pomegranates | Hydrolyzable tannins | HIV-1 [26] | Interaction with SARS-CoV-2 Mpro and RdRp enzymes (in silico approach) [32,82] Interaction with SARS-CoV-2 NSP9 (in silico approach) [40] Inhibition of SARS-CoV-2 RBD/ACE2 binding (in vitro approach) [111] |
Chebulagic acid | Indian gooseberry | Hydrolyzable tannins | EV71 [112] HSV-2 [113] | Inhibition of SARS-CoV-2 Mpro (in vitro and in silico approach) [114] |
Punicalagin | Pomegranate | Hydrolyzable tannins | EV71 [115] HSV-2 [116] (experimental and in silico approach) | Inhibition of SARS-CoV-2 Mpro (in vitro and in silico approach) [114] Interaction with SARS-CoV-2 S glycoprotein and TMPRSS2 (in silico approach) [117] |
Oleuropein | Olives, extra-virgin olive oil, some species of the Oleaceae family | Secoiridoids | RSV, HPIV-3 [118] | Inhibition of COVID-19 Mpro (in silico approach) [57,58] Interaction with 3CLpro, TLR4, and POP (in silico approach) [119] |
Coumarin derivatives | Citrus fruits | Cumarins | HIV-1 *, HCV, IV *, EV71, CHIKV, DENV * (* in silico approach) [120] | Inhibition of SARS-CoV-2 3CLpro (in silico approach) [121] Interaction with NSP12 receptor (in silico approach) [122] |
Capsaicin | Green and red peppers, hot chili peppers | Alcaloids | LASV [123] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [30,82] |
Sulforaphane | Brussels sprout, white cabbage, broccoli, cabbage | Isothiocyanates | IV, HCV, HIV [124] | Inhibition of the in vitro and in vivo replication of SARS-CoV-2 [125] |
Allicin | Garlic, onions, shallots, Chinese chives, leeks, saskatoon berry, arrowroot, summer savory | Organosulfur compound | REV, HSV- 1, HSV-2, HPIV-3, VV, VSV, HRV-2 [126] | Inhibition of SARS-CoV-2 Mpro (in silico approach) [127] |
Eugenol | Cloves, allspices, carrots, walnuts, Ceylon cinnamons, shea tree, passion fruits, winged beans, fireweeds, gingers | Allylbenzenes | HSV-1, HSV-2 [128] IAV, EBOV [129] | Binding affinities towards SARS-CoV-2 spike protein, main protease (Mpro), RdRp, and human ACE-2 proteins (in silico approach) [128] Inhibition of SARS-CoV-2 Mpro (in vitro approach) [130] Interaction with SARS-CoV-2 spike protein and human ACE-2 receptor (in vitro approach) [131] |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Giordano, D.; Facchiano, A.; Carbone, V. Food Plant Secondary Metabolites Antiviral Activity and Their Possible Roles in SARS-CoV-2 Treatment: An Overview. Molecules 2023, 28, 2470. https://doi.org/10.3390/molecules28062470
Giordano D, Facchiano A, Carbone V. Food Plant Secondary Metabolites Antiviral Activity and Their Possible Roles in SARS-CoV-2 Treatment: An Overview. Molecules. 2023; 28(6):2470. https://doi.org/10.3390/molecules28062470
Chicago/Turabian StyleGiordano, Deborah, Angelo Facchiano, and Virginia Carbone. 2023. "Food Plant Secondary Metabolites Antiviral Activity and Their Possible Roles in SARS-CoV-2 Treatment: An Overview" Molecules 28, no. 6: 2470. https://doi.org/10.3390/molecules28062470