Antiviral effects of natural small molecules on aquatic rhabdovirus by interfering with early viral replication

Yan Zhou; Tian-Xiu Qiu; Yang Hu; Lei Liu; Jiong Chen

doi:10.24272/j.issn.2095-8137.2022.234

Volume 43 Issue 6

Nov. 2022

Turn off MathJax

Article Contents

Article Navigation > Zoological Research > 2022 > 43(6): 966-976

Yan Zhou, Tian-Xiu Qiu, Yang Hu, Lei Liu, Jiong Chen. Antiviral effects of natural small molecules on aquatic rhabdovirus by interfering with early viral replication. Zoological Research, 2022, 43(6): 966-976. doi: 10.24272/j.issn.2095-8137.2022.234

Citation:

Yan Zhou, Tian-Xiu Qiu, Yang Hu, Lei Liu, Jiong Chen. Antiviral effects of natural small molecules on aquatic rhabdovirus by interfering with early viral replication. Zoological Research, 2022, 43(6): 966-976. doi: 10.24272/j.issn.2095-8137.2022.234

Citation:

PDF( 14465 KB)

Antiviral effects of natural small molecules on aquatic rhabdovirus by interfering with early viral replication

doi: 10.24272/j.issn.2095-8137.2022.234

Yan Zhou^{1, 2, 3},
Tian-Xiu Qiu^{1, 2, 3},
Yang Hu^{1, 2, 3},
Lei Liu^{1, 2, 3
,
,},
Jiong Chen^{1, 2, 3
,
,}

1.
State Key Laboratory for Managing Biotic and Chemical Threats to the Quality and Safety of Agro-Products, Ningbo University, Ningbo, Zhejiang 315211, China
2.
Laboratory of Biochemistry and Molecular Biology, School of Marine Sciences, Meishan Campus, Ningbo University, Ningbo, Zhejiang 315832, China
3.
Key Laboratory of Applied Marine Biotechnology of Ministry of Education, Meishan Campus, Ningbo University, Ningbo, Zhejiang 315832, China

Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
J.C. and L.L. designed the study. Y.Z., T.X.Q., and Y.H. performed the experiments. Y.Z. drafted the manuscript with assistance from L.L. All authors read and approved the final version of the manuscript.

Funds: This work was supported by the National Natural Science Foundation of China (31902410), Natural Science Foundation of Zhejiang Province (LQ22C190002), Natural Science Foundation of Ningbo City (2021J117), Program of Science and Technology Department of Ningbo City (2021S058), One Health Interdisciplinary Research Project of Ningbo University (HZ202201), and Zhejiang Xinmiao Talents Programs (2022R405B066)

More Information

Corresponding author: E-mail: liulei2@nbu.edu.cn; jchen1975@163.com
Received Date: 2022-09-11
Accepted Date: 2022-10-10

Published Online: 2022-10-14

Publish Date: 2022-11-18

Abstract

Abstract

Spring viremia of carp virus (SVCV) is globally widespread and poses a serious threat to aquatic ecology and aquaculture due to its broad host range. To develop effective agents to control SVCV infection, we selected 16 naturally active small molecules to assess their anti-SVCV activity. Notably, dihydroartemisinin (DHA) (100 µmol/L) and (S, S)-(+)-tetrandrine (TET) (16 µmol/L) exhibited high antiviral effects in epithelioma papulosum cyprinid (EPC) cells, with inhibitory rates of 70.11% and 73.54%, respectively. The possible antiviral mechanisms were determined as follows: 1. Pre-incubation with DHA and TET decreased viral particle infectivity in fish cells, suggesting that horizontal transmission of SVCV in the aquatic environment was disrupted; 2. Although neither had an effect on viral adhesion, TET (but not DHA) interfered with SVCV entry into host cells (>80%), suggesting that TET may have an antiviral function in early viral replication. For in vivo study, both agents enhanced the survival rate of SVCV-infected zebrafish by 53.3%, significantly decreased viral load, and modulated the expression of antiviral-related genes, indicating that DHA and TET may stimulate the host innate immune response to prevent viral infection. Overall, our findings indicated that DHA and TET had positive effects on suppressing SVCV infection by affecting early-stage viral replication, thus holding great potential as immunostimulants to reduce the risk of aquatic rhabdovirus disease outbreaks.
- Spring viremia of carp virus,
- Natural small molecules,
- Antiviral effects,
- Virus internalization,
- Danio rerio

FullText(HTML)

References(46)

References

[1]	Adamek M, Matras M, Dawson A, Piackova V, Gela D, Kocour M, et al. 2019. Type I interferon responses of common carp strains with different levels of resistance to koi herpesvirus disease during infection with CyHV-3 or SVCV. Fish & Shellfish Immunology, 87: 809−819.
[2]	Ahne W, Bjorklund HV, Essbauer S, Fijan N, Kurath G, Winton JR. 2002. Spring viremia of carp (SVC). Diseases of Aquatic Organisms, 52(3): 261−272.
[3]	Ashraf U, Lu YA, Lin L, Yuan JF, Wang M, Liu XQ. 2016. Spring viraemia of carp virus: recent advances. Journal of General Virology, 97(5): 1037−1051. doi: 10.1099/jgv.0.000436
[4]	Balmer BF, Getchell RG, Powers RL, Lee J, Zhang TH, Jung ME, et al. 2018. Broad-spectrum antiviral JL122 blocks infection and inhibits transmission of aquatic rhabdoviruses. Virology, 525: 143−149. doi: 10.1016/j.virol.2018.09.009
[5]	Balmer BF, Powers RL, Zhang TH, Lee J, Vigant F, Lee B, et al. 2017. Inhibition of an aquatic rhabdovirus demonstrates promise of a broad-spectrum antiviral for use in aquaculture. Journal of Virology, 91(4): e02181−16.
[6]	Bearzotti M, Delmas B, Lamoureux A, Loustau AM, Chilmonczyk S, Bremont M. 1999. Fish rhabdovirus cell entry is mediated by fibronectin. Journal of Virology, 73(9): 7703−7709. doi: 10.1128/JVI.73.9.7703-7709.1999
[7]	Beutler B. 2004. Innate immunity: an overview. Molecular Immunology, 40(12): 845−859. doi: 10.1016/j.molimm.2003.10.005
[8]	Chang MX, Zou J, Nie P, Huang B, Yu ZL, Collet B, et al. 2013. Intracellular interferons in fish: a unique means to combat viral infection. PLoS Pathogens, 9(11): e1003736. doi: 10.1371/journal.ppat.1003736
[9]	Chen C, Shen YF, Hu Y, Liu L, Chen WC, Wang GX, et al. 2018. Highly efficient inhibition of spring viraemia of carp virus replication in vitro mediated by bavachin, a major constituent of psoralea corlifonia Lynn. Virus Research, 255: 24−35. doi: 10.1016/j.virusres.2018.06.002
[10]	Elumalai P, Kurian A, Lakshmi S, Faggio C, Esteban MA, Ringø E. 2021. Herbal immunomodulators in aquaculture. Reviews in Fisheries Science & Aquaculture, 29(1): 33−57.
[11]	Fouad AM, Elkamel AA, Ibrahim S, El-Matbouli M, Soliman H, Abdallah ESH. 2022. Control of spring viremia of carp in common carp using RNA interference. Aquaculture, 559: 738417. doi: 10.1016/j.aquaculture.2022.738417
[12]	Ghasemi M, Zamani H, Hosseini SM, Haghighi Karsidani S, Bergmann SM. 2014. Caspian white fish (Rutilus frisii kutum) as a host for spring viraemia of carp virus. Veterinary Microbiology, 170(3–4): 408–413.
[13]	Gotesman M, Soliman H, Besch R, El-Matbouli M. 2015. Inhibition of spring viraemia of carp virus replication in an Epithelioma papulosum cyprini cell line by RNAi. Journal of Fish Diseases, 38(2): 197−207. doi: 10.1111/jfd.12227
[14]	Huang AG, Tan XP, Cui HB, Qi XZ, Zhu B, Wang GX. 2020. Antiviral activity of geniposidic acid against white spot syndrome virus replication in red swamp crayfish Procambarus clarkii. Aquaculture, 528: 735533.
[15]	Huang AG, Tan XP, Qu SY, Wang GX, Zhu B. 2019. Evaluation on the antiviral activity of genipin against white spot syndrome virus in crayfish. Fish & Shellfish Immunology, 93: 380−386.
[16]	Hung PY, Ho BC, Lee SY, Chang SY, Kao CL, Lee SS, et al. 2015. Houttuynia cordata targets the beginning stage of herpes simplex virus infection. PLoS One, 10(2): e0115475. doi: 10.1371/journal.pone.0115475
[17]	Kachur K, Suntres Z. 2020. The antibacterial properties of phenolic isomers, carvacrol and thymol. Critical Reviews in Food Science and Nutrition, 60(18): 3042−3053. doi: 10.1080/10408398.2019.1675585
[18]	Lalani S, Poh CL. 2020. Flavonoids as antiviral agents for Enterovirus A71 (EV-A71). Viruses, 12(2): 184. doi: 10.3390/v12020184
[19]	Li S, Lu LF, Liu SB, Zhang C, Li ZC, Zhou XY, et al. 2019. Spring viraemia of carp virus modulates p53 expression using two distinct mechanisms. PLoS Pathogens, 15(3): e1007695. doi: 10.1371/journal.ppat.1007695
[20]	Licata JM, Harty RN. 2003. Rhabdoviruses and apoptosis. International Reviews of Immunology, 22(5–6): 451–476.
[21]	Liu L, Hu Y, Lu JF, Wang GX. 2019. An imidazole coumarin derivative enhances the antiviral response to spring viremia of carp virus infection in zebrafish. Virus Research, 263: 112−118. doi: 10.1016/j.virusres.2019.01.009
[22]	Liu L, Qiu TX, Song DW, Shan LP, Chen J. 2020a. Inhibition of a novel coumarin on an aquatic rhabdovirus by targeting the early stage of viral infection demonstrates potential application in aquaculture. Antiviral Research, 174: 104672. doi: 10.1016/j.antiviral.2019.104672
[23]	Liu L, Shan LP, Xue MY, Lu JF, Hu Y, Liu GL, et al. 2021. Potential application of antiviral coumarin in aquaculture against IHNV infection by reducing viral adhesion to the epithelial cell surface. Antiviral Research, 195: 105192. doi: 10.1016/j.antiviral.2021.105192
[24]	Liu MZ, Yu Q, Xiao HH, Li MM, Huang YM, Zhang Q, et al. 2020b. The inhibitory activities and antiviral mechanism of medicinal plant ingredient quercetin against grouper iridovirus infection. Frontiers in Microbiology, 11: 586331. doi: 10.3389/fmicb.2020.586331
[25]	Medina-Gali RM, Ortega-Villaizan MDM, Mercado L, Novoa B, Coll J, Perez L. 2018. Beta-glucan enhances the response to SVCV infection in zebrafish. Developmental & Comparative Immunology, 84: 307−314.
[26]	Musarra-Pizzo M, Pennisi R, Ben-Amor I, Mandalari G, Sciortino MT. 2021. Antiviral activity exerted by natural products against human viruses. Viruses, 13(5): 828. doi: 10.3390/v13050828
[27]	Newman DJ, Cragg GM. 2020. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. Journal of Natural Products, 83(3): 770−803. doi: 10.1021/acs.jnatprod.9b01285
[28]	Pereiro P, Figueras A, Novoa B. 2021. Compilation of antiviral treatments and strategies to fight fish viruses. Reviews in Aquaculture, 13(3): 1223−1254. doi: 10.1111/raq.12521
[29]	Qian XY, Zhu F. 2019. Hesperetin protects crayfish Procambarus clarkii against white spot syndrome virus infection. Fish & Shellfish Immunology, 93: 116−123.
[30]	Qiu TX, Song DW, Shan LP, Liu GL, Liu L. 2020. Potential prospect of a therapeutic agent against spring viraemia of carp virus in aquaculture. Aquaculture, 515: 734558. doi: 10.1016/j.aquaculture.2019.734558
[31]	Shao L, Zhao JR. 2017. Isolation of a highly pathogenic spring viraemia of carp virus strain from grass carp (Ctenopharyngodon idella) in late summer, China, 2016. Virus Research, 238: 183−192. doi: 10.1016/j.virusres.2017.06.025
[32]	Shao L, Zhao JR, Zhang HQ. 2016. Spring viraemia of carp virus enters grass carp ovary cells via clathrin-mediated endocytosis and macropinocytosis. Journal of General Virology, 97(11): 2824−2836. doi: 10.1099/jgv.0.000595
[33]	Shen YF, Hu Y, Zhang Z, Liu L, Chen C, Tu X, et al. 2019. Saikosaponin D efficiently inhibits SVCV infection in vitro and in vivo. Aquaculture, 504: 281–290.
[34]	Shen YF, Liu L, Chen WC, Hu Y, Zhu B, Wang GX. 2018. Evaluation on the antiviral activity of arctigenin against spring viraemia of carp virus. Aquaculture, 483: 252−262. doi: 10.1016/j.aquaculture.2017.09.001
[35]	Song DW, Liu GL, Xue MY, Qiu TX, Wang H, Shan LP, et al. 2021. In vitro and in vivo evaluation of antiviral activity of a phenylpropanoid derivative against spring viraemia of carp virus. Virus Research, 291: 198221. doi: 10.1016/j.virusres.2020.198221
[36]	Song DW, Liu L, Shan LP, Qiu TX, Chen J, Chen JP. 2020a. Rhabdoviral clearance effect of a phenylpropanoid medicine against spring viremia of carp virus infection in vitro and in vivo. Aquaculture, 526: 735412.
[37]	Song DW, Liu L, Shan LP, Qiu TX, Chen J, Chen JP. 2020b. Therapeutic potential of phenylpropanoid-based small molecules as anti-SVCV agents in aquaculture. Aquaculture, 526: 735349. doi: 10.1016/j.aquaculture.2020.735349
[38]	Su H, Su JG. 2018. Cyprinid viral diseases and vaccine development. Fish & Shellfish Immunology, 83: 84−95.
[39]	Tadese DA, Song CY, Sun CX, Liu B, Liu B, Zhou QL, et al. 2022. The role of currently used medicinal plants in aquaculture and their action mechanisms: a review. Reviews in Aquaculture, 14(2): 816−847. doi: 10.1111/raq.12626
[40]	Van Hai N. 2015. The use of medicinal plants as immunostimulants in aquaculture: a review. Aquaculture, 446: 88−96. doi: 10.1016/j.aquaculture.2015.03.014
[41]	Vigant F, Lee J, Hollmann A, Tanner LB, Akyol Ataman Z, Yun T, et al. 2013. A mechanistic paradigm for broad-spectrum antivirals that target virus-cell fusion. PLoS Pathogens, 9(4): e1003297. doi: 10.1371/journal.ppat.1003297
[42]	Walker PJ, Bigarré L, Kurath G, Dacheux L, Pallandre L. 2022. Revised taxonomy of rhabdoviruses infecting fish and marine mammals. Animals (Basel), 12(11): 1363.
[43]	Wang H, Qiu TX, Lu JF, Liu HW, Hu L, Liu L, et al. 2021. Potential aquatic environmental risks of trifloxystrobin: enhancement of virus susceptibility in zebrafish through initiation of autophagy. Zoological Research, 42(3): 339−349. doi: 10.24272/j.issn.2095-8137.2021.056
[44]	Wu XY, Xiong JB, Fei CJ, Dai T, Zhu TF, Zhao ZY, et al. 2022. Prior exposure to ciprofloxacin disrupts intestinal homeostasis and predisposes ayu (Plecoglossus altivelis) to subsequent Pseudomonas plecoglossicida-induced infection. Zoological Research, 43(4): 648−665. doi: 10.24272/j.issn.2095-8137.2022.159
[45]	Zheng DT, Huang CX, Huang HH, Zhao Y, Khan MRU, Zhao H, et al. 2020. Antibacterial mechanism of curcumin: a review. Chemistry & Biodiversity, 17(8): e2000171.
[46]	Zhou S, Dong J, Liu YT, Yang QH, Xu N, Yang YB, et al. 2020. Anthelmintic efficacy of 35 herbal medicines against a monogenean parasite, Gyrodactylus kobayashii, infecting goldfish (Carassius auratus). Aquaculture, 521: 734992. doi: 10.1016/j.aquaculture.2020.734992