Recent progress in plant-derived antiviral compounds against African swine fever virus https://doi.org/10.12982/VIS.2024.066

Main Article Content

Fredmoore L. orosco

Abstract

African Swine Fever Virus (ASFV) poses a significant threat to the global swine industry, necessitating the development of effective therapeutic strategies. Through a detailed exploration of ASFV biology, pathogenesis, and replication cycle, critical targets for intervention were identified. The aim of this review was to evaluate the antiviral activity of different plant-derived compounds against ASFV, discuss research gaps, and highlight future perspectives. Key findings from the literature highlight the diverse mechanisms by which plant-derived compounds exert their antiviral effects on ASFV. Notably, flavonoids, alkaloids, and terpenoids exhibit promising antiviral potential via distinct modes of action. However, research gaps persist in the understanding of the precise mechanisms of action, strain-specific effects, and potential toxicity. With a growing understanding of ASFV biology and its intricate replication cycle, these compounds offer a promising avenue for intervention. Addressing research gaps and optimizing formulations are vital for translating these findings into effective therapeutic solutions. Interdisciplinary collaborations in virology, pharmacology, and plant science present an opportunity to combat ASFV, ensuring the security of the food supply and animal health on a global scale.

Article Details

How to Cite
orosco, F. L. (2024). Recent progress in plant-derived antiviral compounds against African swine fever virus: https://doi.org/10.12982/VIS.2024.066. Veterinary Integrative Sciences, 22(3), 969–991. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/266053
Section
Review Article

References

Adhikari, B., Marasini, B.P., Rayamajhee, B., Bhattarai, B.R., Lamichhane, G., Khadayat, K., Adhikari, A., Khanal, S., Parajuli, N., 2021. Potential roles of medicinal plants for the treatment of viral diseases focusing on COVID-19: A review. Phytother. Res. 35, 1298–1312.

Afe, A.E., Shen, Z.-J., Guo, X., Zhou, R., Li, K., 2023. African Swine Fever Virus Interaction with Host Innate Immune Factors. Viruses 15, 1220.

Alejo, A., Matamoros, T., Guerra, M., Andrés, G., 2018. A Proteomic Atlas of the African Swine Fever Virus Particle. J. Virol. 92, e01293-18.

Arabyan, E., Hakobyan, A., Hakobyan, T., Grigoryan, R., Izmailyan, R., Avetisyan, A., Karalyan, Z., Jackman, J.A., Ferreira, F., Elrod, C.C., Zakaryan, H., 2021. Flavonoid Library Screening Reveals Kaempferol as a Potential Antiviral Agent Against African Swine Fever Virus. Front. Microbiol. 12.

Arabyan, E., Hakobyan, A., Kotsinyan, A., Karalyan, Z., Arakelov, V., Arakelov, G., Nazaryan, K., Simonyan, A., Aroutiounian, R., Ferreira, F., Zakaryan, H., 2018. Genistein inhibits African swine fever virus replication in vitro by disrupting viral DNA synthesis. Antiviral Res. 156, 128–137.

Arabyan, E., Kotsynyan, A., Hakobyan, A., Zakaryan, H., 2019. Antiviral agents against African swine fever virus. Virus Res. 270, 197669.

Arias, M., Jurado, C., Gallardo, C., Fernández-Pinero, J., Sánchez-Vizcaíno, J.M., 2018. Gaps in African swine fever: Analysis and priorities. Transbound. Emerg. Dis. 65 Suppl 1, 235–247.

Babikian, H.Y., Jha, R.K., Truong, Q.L., Nguyen, L.T., Babikyan, Y., Nguyen, H.T., To, T.L., Agus, A., 2021. Novel formulation with essential oils as a potential agent to minimize African swine fever virus transmission in an in vivo trial in swine. Vet. World 14, 1853–1866.

Breese, S.S., DeBoer, C.J., 1966. Electron microscope observations of African swine fever virus in tissue culture cells. Virology 28, 420–428.

Byun, E.-B., Kim, H.-M., Sung, N.-Y., Yang, M.-S., Kim, W.S., Choi, D., Mushtaq, S., Lee, S.S., Byun, E.-H., 2018. Gamma irradiation of aloe-emodin induced structural modification and apoptosis through a ROS- and caspase-dependent mitochondrial pathway in stomach tumor cells. Int. J. Radiat. Biol. 94, 403–416.

Cheek, M., 2000. A Synoptic Revision of Ancistrocladus (Ancistrocladaceae) in Africa, with a New Species from Western Cameroon. Kew Bull. 55, 871–882.

Chen, T.-X., Cheng, X.-Y., Wang, Y., Yin, W., 2018. Toosendanin inhibits adipogenesis by activating Wnt/β-catenin signaling. Sci. Rep. 8, 4626.

Chen, Y., Guo, Y., Song, Z., Chang, H., Kuang, Q., Zheng, Z., Wang, H., Zhang, G., 2022. Luteolin restricts ASFV replication by regulating the NF-κB/STAT3/ATF6 signaling pathway. Vet. Microbiol. 273, 109527.

Chen, Y., Song, Z., Chang, H., Guo, Y., Wei, Z., Sun, Y., Gong, L., Zheng, Z., Zhang, G., 2023a. Dihydromyricetin inhibits African swine fever virus replication by downregulating toll-like receptor 4-dependent pyroptosis in vitro. Vet. Res. 54, 58.

Chen, Y., Wei, Z., Song, Z., Chang, H., Guo, Y., Sun, Y., Wang, H., Zheng, Z., Zhang, G., 2023b. Theaflavin inhibits African swine fever virus replication by disrupting lipid metabolism through activation of the AMPK signaling pathway in virto. Virus Res. 334, 199159.

Chen, Z., He, Y., Hu, F., Li, M., Yao, Y., 2022. Genkwanin Alleviates Mitochondrial Dysfunction and Oxidative Stress in a Murine Model of Experimental Colitis: The Participation of Sirt1. Ann. Clin. Lab. Sci. 52, 301–313.

Chiang, L.C., Chiang, W., Liu, M.C., Lin, C.C., 2003. In vitro antiviral activities of Caesalpinia pulcherrima and its related flavonoids. J. Antimicrob. Chemother. 52, 194–198.

Choi, H.-J., 2018. Chemical Constituents of Essential Oils Possessing Anti-Influenza A/WS/33 Virus Activity. Osong Public Health Res. Perspect. 9, 348–353.

Chowdhury, P., Sahuc, M.-E., Rouillé, Y., Rivière, C., Bonneau, N., Vandeputte, A., Brodin, P., Goswami, M., Bandyopadhyay, T., Dubuisson, J., Séron, K., 2018. Theaflavins, polyphenols of black tea, inhibit entry of hepatitis C virus in cell culture. PLOS ONE 13, e0198226.

Coelho, J., Leitão, A., 2020. The African Swine Fever Virus (ASFV) Topoisomerase II as a Target for Viral Prevention and Control. Vaccines 8, 312.

Colgrove, G.S., Haelterman, E.O., Coggins, L., 1969. Pathogenesis of African swine fever in young pigs. Am. J. Vet. Res. 30, 1343–1359.

D, D., T, S., M, S., B, T., A, K., 2018. An evaluation of the impact of aloe vera and licorice extracts on the course of experimental pigeon paramyxovirus type 1 infection in pigeons. Poult. Sci. 97.

de Villiers, E.P., Gallardo, C., Arias, M., da Silva, M., Upton, C., Martin, R., Bishop, R.P., 2010. Phylogenomic analysis of 11 complete African swine fever virus genome sequences. Virology 400, 128–136.

Dixon, L.K., Chapman, D.A.G., Netherton, C.L., Upton, C., 2013. African swine fever virus replication and genomics. Virus Res., African swine fever virus 173, 3–14.

Dixon, L.K., Islam, M., Nash, R., Reis, A.L., 2019. African swine fever virus evasion of host defences. Virus Res. 266, 25–33.

Dixon, L.K., Sánchez-Cordón, P.J., Galindo, I., Alonso, C., 2017. Investigations of Pro- and Anti-Apoptotic Factors Affecting African Swine Fever Virus Replication and Pathogenesis. Viruses 9, 241.

Dong, X., Zeng, Y., Liu, Y., You, L., Yin, X., Fu, J., Ni, J., 2020. Aloe-emodin: A review of its pharmacology, toxicity, and pharmacokinetics. Phytother. Res. PTR 34, 270–281.

Duthie, G., Morrice, P., 2012. Antioxidant capacity of flavonoids in hepatic microsomes is not reflected by antioxidant effects in vivo. Oxid. Med. Cell. Longev. 2012, 165127.

El-Wassimy, T.M., Hegazy, M.-E., Mohamed, T.A., Youns, S.H., Al-Badry, H.A., 2019. Antiproliferative Activity of two compounds isolated from Artemisia sieberi. J. Environ. Stud. 19, 14–21.

Evers, D.L., Chao, C.-F., Wang, X., Zhang, Z., Huong, S.-M., Huang, E.-S., 2005. Human cytomegalovirus-inhibitory flavonoids: Studies on antiviral activity and mechanism of action. Antiviral Res. 68, 124–134.

Fasina, F.O., Olaokun, O.O., Oladipo, O.O., Fasina, M.M., Makinde, A.A., Heath, L., Bastos, A.D., 2013. Phytochemical analysis and in-vitro anti-African swine fever virus activity of extracts and fractions of Ancistrocladus uncinatus, Hutch and Dalziel (Ancistrocladaceae). BMC Vet. Res. 9, 120.

Galindo, I., Alonso, C., 2017. African Swine Fever Virus: A Review. Viruses 9, 103.

Galindo, I., Cuesta-Geijo, M.A., Hlavova, K., Muñoz-Moreno, R., Barrado-Gil, L., Dominguez, J., Alonso, C., 2015. African swine fever virus infects macrophages, the natural host cells, via clathrin- and cholesterol-dependent endocytosis. Virus Res. 200, 45–55.

Gansukh, E., Gopal, J., Paul, D., Muthu, M., Kim, D.-H., Oh, J.-W., Chun, S., 2018. Ultrasound mediated accelerated Anti-influenza activity of Aloe vera. Sci. Rep. 8, 17782.

Gao, Y., Liu, F., Fang, L., Cai, R., Zong, C., Qi, Y., 2014. Genkwanin Inhibits Proinflammatory Mediators Mainly through the Regulation of miR-101/MKP-1/MAPK Pathway in LPS-Activated Macrophages. PLOS ONE 9, e96741.

Golnar, A.J., Martin, E., Wormington, J.D., Kading, R.C., Teel, P.D., Hamer, S.A., Hamer, G.L., 2019. Reviewing the Potential Vectors and Hosts of African Swine Fever Virus Transmission in the United States. Vector Borne Zoonotic Dis. Larchmt. N 19, 512–524.

Gómez-Villamandos, J.C., Bautista, M.J., Sánchez-Cordón, P.J., Carrasco, L., 2013. Pathology of African swine fever: the role of monocyte-macrophage. Virus Res. 173, 140–149.

Goulding, L.V., Kiss, E., Goatley, L., Vrancken, R., Goris, N.E.J., Dixon, L., 2022. In vitro and in vivo antiviral activity of nucleoside analogue cHPMPC against African swine fever virus replication. Antiviral Res. 208, 105433.

Guinat, C., Gogin, A., Blome, S., Keil, G., Pollin, R., Pfeiffer, D.U., Dixon, L., 2016. Transmission routes of African swine fever virus to domestic pigs: current knowledge and future research directions. Vet. Rec. 178, 262–267.

Guo, Y., Chen, Y., Wang, Q., Wang, Z., Gong, L., Sun, Y., Song, Z., Chang, H., Zhang, G., Wang, H., 2023. Emodin and rhapontigenin inhibit the replication of African swine fever virus by interfering with virus entry. Vet. Microbiol. 284, 109794.

Gupta, S., Afaq, F., Mukhtar, H., 2001. Selective Growth-Inhibitory, Cell-Cycle Deregulatory and Apoptotic Response of Apigenin in Normal versus Human Prostate Carcinoma Cells. Biochem. Biophys. Res. Commun. 287, 914–920.

Hakobyan, A., Arabyan, E., Avetisyan, A., Abroyan, L., Hakobyan, L., Zakaryan, H., 2016. Apigenin inhibits African swine fever virus infection in vitro. Arch. Virol. 161, 3445–3453.

Hakobyan, A., Arabyan, E., Kotsinyan, A., Karalyan, Z., Sahakyan, H., Arakelov, V., Nazaryan, K., Ferreira, F., Zakaryan, H., 2019. Inhibition of African swine fever virus infection by genkwanin. Antiviral Res. 167, 78–82.

Hallock, Y.F., Cardellina, J.H., Schäffer, M., Bringmann, G., François, G., Boyd, M.R., 1998. Korundamine A, a novel HIV-inhibitory and antimalarial “hybrid” naphthylisoquinoline alkaloid heterodimer from Ancistrocladus korupensis. Bioorg. Med. Chem. Lett. 8, 1729–1734.

Hernáez, B., Guerra, M., Salas, M.L., Andrés, G., 2016. African Swine Fever Virus Undergoes Outer Envelope Disruption, Capsid Disassembly and Inner Envelope Fusion before Core Release from Multivesicular Endosomes. PLOS Pathog. 12, e1005595.

Heuschele, W.P., 1967. Studies on the pathogenesis of african swine fever I. Quantitative studies on the sequential development of virus in pig tissues. Arch. Für Gesamte Virusforsch. 21, 349–356.

Ho, T.-Y., Wu, S.-L., Chen, J.-C., Li, C.-C., Hsiang, C.-Y., 2007. Emodin blocks the SARS coronavirus spike protein and angiotensin-converting enzyme 2 interaction. Antiviral Res. 74, 92–101.

Huang, L., Kim, M.-Y., Cho, J.Y., 2023. Immunopharmacological Activities of Luteolin in Chronic Diseases. Int. J. Mol. Sci. 24, 2136.

Huang, L., Li, H., Ye, Z., Xu, Q., Fu, Q., Sun, W., Qi, W., Yue, J., 2021. Berbamine inhibits Japanese encephalitis virus (JEV) infection by compromising TPRMLs-mediated endolysosomal trafficking of low-density lipoprotein receptor (LDLR). Emerg. Microbes Infect. 10, 1257–1271.

Hübner, A., Petersen, B., Keil, G.M., Niemann, H., Mettenleiter, T.C., Fuchs, W., 2018. Efficient inhibition of African swine fever virus replication by CRISPR/Cas9 targeting of the viral p30 gene (CP204L). Sci. Rep. 8, 1449.

Imran, M., Salehi, B., Sharifi-Rad, J., Aslam Gondal, T., Saeed, F., Imran, A., Shahbaz, M., Tsouh Fokou, P.V., Umair Arshad, M., Khan, H., Guerreiro, S.G., Martins, N., Estevinho, L.M., 2019. Kaempferol: A Key Emphasis to Its Anticancer Potential. Molecules 24, 2277.

Jin, Y.-H., Choi, J.-G., Cho, W.-K., Ma, J.Y., 2017. Ethanolic Extract of Melia Fructus Has Anti-influenza A Virus Activity by Affecting Viral Entry and Viral RNA Polymerase. Front. Microbiol. 8, 476.

Jin, Y.-H., Kwon, S., Choi, J.-G., Cho, W.-K., Lee, B., Ma, J.Y., 2019. Toosendanin From Melia Fructus Suppresses Influenza A Virus Infection by Altering Nuclear Localization of Viral Polymerase PA Protein. Front. Pharmacol. 10, 1025.

Jo, S., Kim, S., Shin, D.H., Kim, M.-S., 2020. Inhibition of African swine fever virus protease by myricetin and myricitrin. J. Enzyme Inhib. Med. Chem. 35, 1045–1049.

Jori, F., Bastos, A.D.S., 2009. Role of Wild Suids in the Epidemiology of African Swine Fever. EcoHealth 6, 296–310.

Juergens, U.R., 2014. Anti-inflammatory properties of the monoterpene 1.8-cineole: current evidence for co-medication in inflammatory airway diseases. Drug Res. 64, 638–646.

Juszkiewicz, M., Walczak, M., Woźniakowski, G., Szczotka-Bochniarz, A., 2021. Virucidal Activity of Plant Extracts against African Swine Fever Virus. Pathogens 10, 1357.

Kan, X., Liu, B., Guo, W., Wei, L., Lin, Y., Guo, Y., Gong, Q., Li, Y., Xu, D., Cao, Y., Huang, B., Dong, A., Ma, H., Fu, S., Liu, J., 2019. Myricetin relieves LPS-induced mastitis by inhibiting inflammatory response and repairing the blood-milk barrier. J. Cell. Physiol. 234, 16252–16262.

Kaur, P., Shukla, S., Gupta, S., 2008. Plant flavonoid apigenin inactivates Akt to trigger apoptosis in human prostate cancer: an in vitro and in vivo study. Carcinogenesis 29, 2210–2217.

Kausar, S., Said Khan, F., Ishaq Mujeeb Ur Rehman, M., Akram, M., Riaz, M., Rasool, G., Hamid Khan, A., Saleem, I., Shamim, S., Malik, A., 2021. A review: Mechanism of action of antiviral drugs. Int. J. Immunopathol. Pharmacol. 35, 20587384211002621.

Keita, D., Heath, L., Albina, E., 2010. Control of African swine fever virus replication by small interfering RNA targeting the A151R and VP72 genes. Antivir. Ther. 15, 727–736.

Lei, X., Guo, J., Wang, Y., Cui, J., Feng, B., Su, Y., Zhao, H., Yang, W., Hu, Y., 2019. Inhibition of endometrial carcinoma by Kaempferol is interceded through apoptosis induction, G2/M phase cell cycle arrest, suppression of cell invasion and upregulation of m-TOR/PI3K signalling pathway. J. BUON Off. J. Balk. Union Oncol. 24, 1555–1561.

Lelešius, R., Karpovaitė, A., Mickienė, R., Drevinskas, T., Tiso, N., Ragažinskienė, O., Kubilienė, L., Maruška, A., Šalomskas, A., 2019. In vitro antiviral activity of fifteen plant extracts against avian infectious bronchitis virus. BMC Vet. Res. 15, 178.

Li, L., Wang, R., Hu, H., Chen, X., Yin, Z., Liang, X., He, C., Yin, L., Ye, G., Zou, Y., Yue, G., Tang, H., Jia, R., Song, X., 2021. The antiviral activity of kaempferol against pseudorabies virus in mice. BMC Vet. Res. 17, 247.

Li, Q., Zhang, P., Cai, Y., 2021. Genkwanin suppresses MPP+-induced cytotoxicity by inhibiting TLR4/MyD88/NLRP3 inflammasome pathway in a cellular model of Parkinson’s disease. NeuroToxicology 87, 62–69.

Li, S., Ye, M., Chen, Y., Zhang, Y., Li, J., Liu, W., Li, H., Peng, K., 2021. Screening of a Small Molecule Compound Library Identifies Toosendanin as an Inhibitor Against Bunyavirus and SARS-CoV-2. Front. Pharmacol. 12, 735223.

Li, W., Xu, C., Hao, C., Zhang, Y., Wang, Z., Wang, S., Wang, W., 2020. Inhibition of herpes simplex virus by myricetin through targeting viral gD protein and cellular EGFR/PI3K/Akt pathway. Antiviral Res. 177, 104714.

Li, Y., Liu, Y., Ma, A., Bao, Y., Wang, M., Sun, Z., 2017. In vitro antiviral, anti-inflammatory, and antioxidant activities of the ethanol extract of Mentha piperita L. Food Sci. Biotechnol. 26, 1675–1683.

Liu, Y., Zhang, X., Liu, Z., Huang, L., Jia, W., Lian, X., Weng, C., Zhang, G., Qi, W., Chen, J., 2022. Toosendanin suppresses African swine fever virus replication through upregulating interferon regulatory factor 1 in porcine alveolar macrophage cultures. Front. Microbiol. 13.

Lucarini, R., Tozatti, M.G., Silva, M.L.A., Gimenez, V.M.M., Pauletti, P.M., Groppo, M., Turatti, I.C.C., Cunha, W.R., Martins, C.H.G., 2015. Antibacterial and anti-inflammatory activities of an extract, fractions, and compounds isolated from Gochnatia pulchra aerial parts. Braz. J. Med. Biol. Res. 48, 822–830.

Luo, Y., Yang, Y., Wang, W., Gao, Q., Gong, T., Feng, Y., Wu, D., Zheng, X., Zhang, G., Wang, H., 2023. Aloe-emodin inhibits African swine fever virus replication by promoting apoptosis via regulating NF-κB signaling pathway. Virol. J. 20, 158.

Ma, P.-Y., Li, X.-Y., Wang, Y.-L., Lang, D.-Q., Liu, L., Yi, Y.-K., Liu, Q., Shen, C.-Y., 2022. Natural bioactive constituents from herbs and nutraceuticals promote browning of white adipose tissue. Pharmacol. Res. 178, 106175.

Ma, Z., Gulia-Nuss, M., Zhang, X., Brown, M.R., 2013. Effects of the botanical insecticide, toosendanin, on blood digestion and egg production by female Aedes aegypti (Diptera: Culicidae): topical application and ingestion. J. Med. Entomol. 50, 112–121.

Machuka, E.M., Juma, J., Muigai, A.W.T., Amimo, J.O., Pelle, R., Abworo, E.O., 2022. Transcriptome profile of spleen tissues from locally-adapted Kenyan pigs (Sus scrofa) experimentally infected with three varying doses of a highly virulent African swine fever virus genotype IX isolate: Ken12/busia.1 (ken-1033). BMC Genomics 23, 522.

Mahedi, M.R.A., Rawat, A., Rabbi, F., Babu, K.S., Tasayco, E.S., Areche, F.O., Pacovilca-Alejo, O.V., Flores, D.D.C., Aguilar, S.V., Orosco, F.L., Syrmos, N., Mudhafar, M., Afrin, S., Rahman, M.M., 2023. Understanding the Global Transmission and Demographic Distribution of Nipah Virus (NiV). Res. J. Pharm. Technol. 16, 3588–3594.

McMahon, J.B., Currens, M.J., Gulakowski, R.J., Buckheit, R.W., Lackman-Smith, C., Hallock, Y.F., Boyd, M.R., 1995. Michellamine B, a novel plant alkaloid, inhibits human immunodeficiency virus-induced cell killing by at least two distinct mechanisms. Antimicrob. Agents Chemother. 39, 484–488.

Mohamed, I.M.A., Ogawa, H., Takeda, Y., 2022. In vitro virucidal activity of the theaflavin-concentrated tea extract TY-1 against influenza A virus. J. Nat. Med. 76, 152–160.

Mohammad, A., Alshawaf, E., Marafie, S.K., Abu-Farha, M., Al-Mulla, F., Abubaker, J., 2021. Molecular Simulation-Based Investigation of Highly Potent Natural Products to Abrogate Formation of the nsp10–nsp16 Complex of SARS-CoV-2. Biomolecules 11, 573.

Mohammed, A., Gbonjubola, V.A., Koorbanally, N.A., Islam, Md.S., 2017. Inhibition of key enzymes linked to type 2 diabetes by compounds isolated from Aframomum melegueta fruit. Pharm. Biol. 55, 1010–1016.

Mottola, C., Freitas, F.B., Simões, M., Martins, C., Leitão, A., Ferreira, F., 2013. In vitro antiviral activity of fluoroquinolones against African swine fever virus. Vet. Microbiol., Special Issue: One World, One Health, One Virology 165, 86–94.

Muñoz-Moreno, R., Cuesta-Geijo, M.Á., Martínez-Romero, C., Barrado-Gil, L., Galindo, I., García-Sastre, A., Alonso, C., 2016. Antiviral Role of IFITM Proteins in African Swine Fever Virus Infection. PLOS ONE 11, e0154366.

Naz, S., Siddiqi, R., Ahmad, S., Rasool, S.A., Sayeed, S.A., 2007. Antibacterial activity directed isolation of compounds from Punica granatum. J. Food Sci. 72, M341-345.

Netherton, C.L., Connell, S., Benfield, C.T.O., Dixon, L.K., 2019. The Genetics of Life and Death: Virus-Host Interactions Underpinning Resistance to African Swine Fever, a Viral Hemorrhagic Disease. Front. Genet. 10.

O’Neill, E.J., Termini, D., Albano, A., Tsiani, E., 2021. Anti-Cancer Properties of Theaflavins. Molecules 26, 987.

Orosco, F., 2023. Advancing the frontiers: Revolutionary control and prevention paradigms against Nipah virus. Open Vet. J. 13, 1056–1056.

Orosco, F.L., 2024. Immune evasion mechanisms of porcine epidemic diarrhea virus: A comprehensive review: Vet. Integr. Sci. 22, 171–192.

Orosco, F.L., 2023. Current progress in diagnostics, therapeutics, and vaccines for African swine fever virus: Vet. Integr. Sci. 21, 751–781.

Park, E.-K., Choo, M.-K., Yoon, H.-K., Kim, D.-H., 2002. Antithrombotic and antiallergic activities of rhaponticin from Rhei Rhizoma are activated by human intestinal bacteria. Arch. Pharm. Res. 25, 528–533.

Patil, S.S., Suresh, K.P., Vashist, V., Prajapati, A., Pattnaik, B., Roy, P., 2020. African swine fever: A permanent threat to Indian pigs. Vet. World 13, 2275–2285.

Pikalo, J., Zani, L., Hühr, J., Beer, M., Blome, S., 2019. Pathogenesis of African swine fever in domestic pigs and European wild boar - Lessons learned from recent animal trials. Virus Res. 271, 197614.

Probst, C., Gethmann, J., Amler, S., Globig, A., Knoll, B., Conraths, F.J., 2019. The potential role of scavengers in spreading African swine fever among wild boar. Sci. Rep. 9, 11450.

Punia Bangar, S., Kajla, P., Chaudhary, V., Sharma, N., Ozogul, F., 2023. Luteolin: A flavone with myriads of bioactivities and food applications. Food Biosci. 52, 102366.

Qian, K., Gao, A., Zhu, M., Shao, H., Jin, W., Ye, J., Qin, A., 2014. Genistein inhibits the replication of avian leucosis virus subgroup J in DF-1 cells. Virus Res. 192, 114–120.

Qian, S., Fan, W., Qian, P., Zhang, D., Wei, Y., Chen, H., Li, X., 2015. Apigenin Restricts FMDV Infection and Inhibits Viral IRES Driven Translational Activity. Viruses 7, 1613–1626.

Reis, A.L., Netherton, C., Dixon, L.K., 2017. Unraveling the Armor of a Killer: Evasion of Host Defenses by African Swine Fever Virus. J. Virol. 91, e02338-16.

Ren, R., Yin, S., Lai, B., Ma, L., Wen, J., Zhang, X., Lai, F., Liu, S., Li, L., 2018. Myricetin antagonizes semen-derived enhancer of viral infection (SEVI) formation and influences its infection-enhancing activity. Retrovirology 15, 49.

Rock, D.L., 2017. Challenges for African swine fever vaccine development—“… perhaps the end of the beginning.” Vet. Microbiol., Recent Advances in Vaccine Research Against Economically Important Viral Diseases of Food Animals 206, 52–58.

Rodríguez, J.M., Salas, M.L., 2013. African swine fever virus transcription. Virus Res., African swine fever virus 173, 15–28.

Salguero, F.J., 2020. Comparative Pathology and Pathogenesis of African Swine Fever Infection in Swine. Front. Vet. Sci. 7.

Sánchez, E.G., Quintas, A., Pérez-Núñez, D., Nogal, M., Barroso, S., Carrascosa, Á.L., Revilla, Y., 2012. African Swine Fever Virus Uses Macropinocytosis to Enter Host Cells. PLOS Pathog. 8, e1002754.

Sánchez-Cordón, P.J., Floyd, T., Hicks, D., Crooke, H.R., McCleary, S., McCarthy, R.R., Strong, R., Dixon, L.K., Neimanis, A., Wikström-Lassa, E., Gavier-Widén, D., Núñez, A., 2021. Evaluation of Lesions and Viral Antigen Distribution in Domestic Pigs Inoculated Intranasally with African Swine Fever Virus Ken05/Tk1 (Genotype X). Pathogens 10, 768.

Sánchez-Cordón, P.J., Montoya, M., Reis, A.L., Dixon, L.K., 2018. African swine fever: A re-emerging viral disease threatening the global pig industry. Vet. J. Lond. Engl. 1997 233, 41–48.

Sauter, D., Schwarz, S., Wang, K., Zhang, R., Sun, B., Schwarz, W., 2014. Genistein as Antiviral Drug against HIV Ion Channel. Planta Med. 80, 682–687.

Schäfer, A., Franzoni, G., Netherton, C.L., Hartmann, L., Blome, S., Blohm, U., 2022. Adaptive Cellular Immunity against African Swine Fever Virus Infections. Pathogens 11.

Schwikkard, S., van Heerden, F.R., 2002. Antimalarial activity of plant metabolites. Nat. Prod. Rep. 19, 675–692.

Singh, P., Mishra, S.K., Noel, S., Sharma, S., Rath, S.K., 2012. Acute Exposure of Apigenin Induces Hepatotoxicity in Swiss Mice. PLOS ONE 7, e31964.

Sroka, Z., Żbikowska, B., Hładyszowski, J., 2015. The antiradical activity of some selected flavones and flavonols. Experimental and quantum mechanical study. J. Mol. Model. 21, 307.

Stompor-Gorący, M., 2021. The Health Benefits of Emodin, a Natural Anthraquinone Derived from Rhubarb-A Summary Update. Int. J. Mol. Sci. 22, 9522.

Sun, Y., Bao, Y., Yu, H., Chen, Q., Lu, F., Zhai, S., Zhang, C., Li, F., Wang, C., Yuan, C., 2020. Anti-rheumatoid arthritis effects of flavonoids from Daphne genkwa. Int. Immunopharmacol. 83, 106384.

Taheri, Y., Sharifi-Rad, J., Antika, G., Yılmaz, Y.B., Tumer, T.B., Abuhamdah, S., Chandra, S., Saklani, S., Kılıç, C.S., Sestito, S., Daştan, S.D., Kumar, M., Alshehri, M.M., Rapposelli, S., Cruz-Martins, N., Cho, W.C., 2021. Paving Luteolin Therapeutic Potentialities and Agro-Food-Pharma Applications: Emphasis on In Vivo Pharmacological Effects and Bioavailability Traits. Oxid. Med. Cell. Longev. 2021, 1987588.

Taheri, Y., Suleria, H.A.R., Martins, N., Sytar, O., Beyatli, A., Yeskaliyeva, B., Seitimova, G., Salehi, B., Semwal, P., Painuli, S., Kumar, A., Azzini, E., Martorell, M., Setzer, W.N., Maroyi, A., Sharifi-Rad, J., 2020. Myricetin bioactive effects: moving from preclinical evidence to potential clinical applications. BMC Complement. Med. Ther. 20, 241.

Thomas, D.W., Gereau, R.E., 1993. Ancistrocladus korupensis (Ancistrocladaceae): A New Species of Liana from Cameroon. Novon 3, 494–498.

Truong, Q.L., Nguyen, L.T., Babikian, H.Y., Jha, R.K., Nguyen, H.T., To, T.L., 2021. Natural oil blend formulation as an anti-African swine fever virus agent in in vitro primary porcine alveolar macrophage culture. Vet. World 14, 794–802.

Vela, E.M., Bowick, G.C., Herzog, N.K., Aronson, J.F., 2008. Genistein treatment of cells inhibits arenavirus infection. Antiviral Res. 77, 153–156.

Wang, G., Feng, C.-C., Chu, S.-J., Zhang, R., Lu, Y.-M., Zhu, J.-S., Zhang, J., 2015. Toosendanin inhibits growth and induces apoptosis in colorectal cancer cells through suppression of AKT/GSK-3β/β-catenin pathway. Int. J. Oncol. 47, 1767–1774.

Wang, Jun, Yang, G., Zhang, L., Zhang, J., Wang, Jing, Zou, Y., Wang, Jiufeng, 2022. Berbamine hydrochloride inhibits bovine viral diarrhea virus replication via interfering in late-stage autophagy. Virus Res. 321, 198905.

Wang, L., Madera, R., Li, Y., McVey, D.S., Drolet, B.S., Shi, J., 2020. Recent Advances in the Diagnosis of Classical Swine Fever and Future Perspectives. Pathog. Basel Switz. 9, 658.

Wang, N., Zhao, D., Wang, Jialing, Zhang, Y., Wang, M., Gao, Y., Li, F., Wang, Jingfei, Bu, Z., Rao, Z., Wang, X., 2019. Architecture of African swine fever virus and implications for viral assembly. Science 366, 640–644.

Wang, S., Ling, Y., Yao, Y., Zheng, G., Chen, W., 2020. Luteolin inhibits respiratory syncytial virus replication by regulating the MiR-155/SOCS1/STAT1 signaling pathway. Virol. J. 17, 187.

Wang, Y., Kang, W., Yang, W., Zhang, J., Li, D., Zheng, H., 2021. Structure of African Swine Fever Virus and Associated Molecular Mechanisms Underlying Infection and Immunosuppression: A Review. Front. Immunol. 12, 715582.

Watanabe, T., Sakamoto, N., Nakagawa, M., Kakinuma, S., Itsui, Y., Nishimura-Sakurai, Y., Ueyama, M., Funaoka, Y., Kitazume, A., Nitta, S., Kiyohashi, K., Murakawa, M., Azuma, S., Tsuchiya, K., Oooka, S., Watanabe, M., 2011. Inhibitory effect of a triterpenoid compound, with or without alpha interferon, on hepatitis C virus infection. Antimicrob. Agents Chemother. 55, 2537–2545.

Xian, M., Cai, J., Zheng, K., Liu, Q., Liu, Y., Lin, H., Liang, S., Wang, S., 2021. Aloe-emodin prevents nerve injury and neuroinflammation caused by ischemic stroke via the PI3K/AKT/mTOR and NF-κB pathway. Food Funct. 12, 8056–8067.

Xie, Y., Wang, Y., Xiang, W., Wang, Q., Cao, Y., 2020. Molecular Mechanisms of the Action of Myricetin in Cancer. Mini Rev. Med. Chem. 20, 123–133.

Xu, Z., Huang, M., Xia, Y., Peng, P., Zhang, Y., Zheng, S., Wang, X., Xue, C., Cao, Y., 2021. Emodin from Aloe Inhibits Porcine Reproductive and Respiratory Syndrome Virus via Toll-Like Receptor 3 Activation. Viruses 13, 1243.

Yu, M.-S., Lee, J., Lee, J.M., Kim, Y., Chin, Y.-W., Jee, J.-G., Keum, Y.-S., Jeong, Y.-J., 2012. Identification of myricetin and scutellarein as novel chemical inhibitors of the SARS coronavirus helicase, nsP13. Bioorg. Med. Chem. Lett. 22, 4049–4054.

Yu, R., Chen, L., Lan, R., Shen, R., Li, P., 2020. Computational screening of antagonists against the SARS-CoV-2 (COVID-19) coronavirus by molecular docking. Int. J. Antimicrob. Agents 56, 106012.

Zhan, Y., Chen, Q., Song, Y., Wei, X., Zhao, T., Chen, B., Li, C., Zhang, W., Jiang, Y., Tan, Y., Du, B., Xiao, J., Wang, K., 2022. Berbamine Hydrochloride inhibits lysosomal acidification by activating Nox2 to potentiate chemotherapy-induced apoptosis via the ROS-MAPK pathway in human lung carcinoma cells. Cell Biol. Toxicol.

Zhang, D., Xie, L., Jia, G., Cai, S., Ji, B., Liu, Y., Wu, W., Zhou, F., Wang, A., Chu, L., Wei, Y., Liu, J., Gao, F., 2011. Comparative study on antioxidant capacity of flavonoids and their inhibitory effects on oleic acid-induced hepatic steatosis in vitro. Eur. J. Med. Chem. 46, 4548–4558.

Zhang, Z.-R., Zhang, Y.-N., Zhang, H.-Q., Zhang, Q.-Y., Li, N., Li, Q., Deng, C.-L., Zhang, B., Li, X.-D., Ye, H.-Q., 2022. Berbamine hydrochloride potently inhibits SARS-CoV-2 infection by blocking S protein-mediated membrane fusion. PLoS Negl. Trop. Dis. 16, e0010363.

Zhao, C., Wang, F., Tang, B., Han, J., Li, Xiang, Lian, G., Li, Xiaolong, Hao, S., 2021. Anti-inflammatory effects of kaempferol-3-O-rhamnoside on HSV-1 encephalitis in vivo and in vitro. Neurosci. Lett. 765, 136172.

Zhao, D., Liu, R., Zhang, X., Li, F., Wang, J., Zhang, Jiwen, Liu, X., Wang, L., Zhang, Jiaoer, Wu, X., Guan, Y., Chen, W., Wang, X., He, X., Bu, Z., 2019. Replication and virulence in pigs of the first African swine fever virus isolated in China. Emerg. Microbes Infect. 8, 438–447.

Zhou, Q., Wu, X., Wen, C., Wang, Huihui, Wang, Huashe, Liu, H., Peng, J., 2018. Toosendanin induces caspase-dependent apoptosis through the p38 MAPK pathway in human gastric cancer cells. Biochem. Biophys. Res. Commun. 505, 261–266.

Zhu, J., Huang, L., Gao, F., Jian, W., Chen, H., Liao, M., Qi, W., 2023. Berbamine Hydrochloride Inhibits African Swine Fever Virus Infection In Vitro. Molecules 28, 170.