The Effect and Underlying Mechanism of Yeast β-glucan on Antiviral Resistance of Zebrafish Against Spring Viremia of Carp Virus Infection

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2022 Nov 21

PMID 36405758

Authors

Hui Liang

Yu Li

Ming Li

Wei Zhou

Jie Chen

Zhen Zhang

Yalin Yang

Chao Ran

Zhigang Zhou

Affiliations

Soon will be listed here.

Abstract

β-glucan has been used as immunostimulant for fish. However, the effect of yeast β-glucan on viral infections has been less studied in fish. In this study, we investigated the effects of β-glucan on the resistance of zebrafish against spring viraemia of carp virus (SVCV) and elucidated the underlying mechanisms. Zebrafish were fed with a control diet or diet supplemented with 0.01% and 0.025% β-glucan for 2 weeks, and were challenged by SVCV. Zebrafish embryonic fibroblast (ZF4) cells were treated with 5 μg/mL β-glucan and were infected by SVCV. We further investigated the effect of β-glucan on autophagy level post SVCV infection. The intestinal microbiota was evaluated by 16S RNA gene pyrosequencing. Results showed that dietary supplementation of 0.025% β-glucan significantly increased survival rate of zebrafish compared with control group after SVCV challenge ( < 0.05). Dietary β-glucan significantly increased the expression of genes related to type I IFN antiviral immune pathway in the spleen of zebrafish after viral infection, including type I IFN genes (, , ), IFN-stimulated genes (, ), as well as other genes involved in the IFN signaling pathway, including , , , and . Morpholino knockdown of type I IFN receptors dampened the antiviral effect of β-glucan in zebrafish larvae, indicating that β-glucan-mediated antiviral function was at least partially dependent on IFN immune response. Furthermore, β-glucan can inhibit the replication of SVCV in ZF4 cells. However, β-glucan did not stimulate type I IFN antiviral response in ZF4 cells, and the antiviral effect of β-glucan in ZF4 was independent of Myd88. Interestingly, β-glucan induced autophagy in ZF4 cells after SVCV infection. Inhibition of autophagy blocked the antiviral effect of β-glucan in ZF4 cells. Lastly, dietary β-glucan changed the composition of intestinal microbiota in zebrafish, with reduced abundance of Proteobacteria and an enrichment of Fusobacteria and Firmicutes. To sum up, our results indicate that the β-glucan enhanced resistance of zebrafish against SVCV and the mechanism involved stimulation of type I IFN antiviral immune response of fish after viral infection.

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References

Jackson W, Giddings Jr T, Taylor M, Mulinyawe S, Rabinovitch M, Kopito R . Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005; 3(5):e156. PMC: 1084330. DOI: 10.1371/journal.pbio.0030156. View

Keller M, Torres V, Cadwell K . Autophagy and microbial pathogenesis. Cell Death Differ. 2020; 27(3):872-886. PMC: 7205878. DOI: 10.1038/s41418-019-0481-8. View

Langevin C, Aleksejeva E, Passoni G, Palha N, Levraud J, Boudinot P . The antiviral innate immune response in fish: evolution and conservation of the IFN system. J Mol Biol. 2013; 425(24):4904-20. DOI: 10.1016/j.jmb.2013.09.033. View

Li X, Xue Y, Pang L, Len B, Lin Z, Huang J . Agaricus bisporus-derived β-glucan prevents obesity through PPAR γ downregulation and autophagy induction in zebrafish fed by chicken egg yolk. Int J Biol Macromol. 2018; 125:820-828. DOI: 10.1016/j.ijbiomac.2018.12.122. View

Ichinohe T, Pang I, Kumamoto Y, Peaper D, Ho J, Murray T . Microbiota regulates immune defense against respiratory tract influenza A virus infection. Proc Natl Acad Sci U S A. 2011; 108(13):5354-9. PMC: 3069176. DOI: 10.1073/pnas.1019378108. View

Rodriguez I, Chamorro R, Novoa B, Figueras A . beta-Glucan administration enhances disease resistance and some innate immune responses in zebrafish (Danio rerio). Fish Shellfish Immunol. 2009; 27(2):369-73. DOI: 10.1016/j.fsi.2009.02.007. View

Bacon J, FARMER V, Jones D, TAYLOR I . The glucan components of the cell wall of baker's yeast (Saccharomyces cerevisiae) considered in relation to its ultrastructure. Biochem J. 1969; 114(3):557-67. PMC: 1184928. DOI: 10.1042/bj1140557. View

Ran C, Xie M, Li J, Xie Y, Ding Q, Li Y . Dietary Nucleotides Alleviate Hepatic Lipid Deposition via Exogenous AMP-Mediated AMPK Activation in Zebrafish. J Nutr. 2021; 151(10):2986-2996. DOI: 10.1093/jn/nxab232. View

Korolenko T, Bgatova N, Vetvicka V . Glucan and Mannan-Two Peas in a Pod. Int J Mol Sci. 2019; 20(13). PMC: 6651133. DOI: 10.3390/ijms20133189. View

10.

Kim Y, Ke F, Zhang Q . Effect of beta-glucan on activity of antioxidant enzymes and Mx gene expression in virus infected grass carp. Fish Shellfish Immunol. 2009; 27(2):336-40. DOI: 10.1016/j.fsi.2009.06.006. View

11.

Falco A, Miest J, Pionnier N, Pietretti D, Forlenza M, Wiegertjes G . β-Glucan-supplemented diets increase poly(I:C)-induced gene expression of Mx, possibly via Tlr3-mediated recognition mechanism in common carp (Cyprinus carpio). Fish Shellfish Immunol. 2013; 36(2):494-502. DOI: 10.1016/j.fsi.2013.12.005. View

12.

Kiron V, Kulkarni A, Dahle D, Vasanth G, Lokesh J, Elvebo O . Recognition of purified beta 1,3/1,6 glucan and molecular signalling in the intestine of Atlantic salmon. Dev Comp Immunol. 2015; 56:57-66. DOI: 10.1016/j.dci.2015.11.007. View

13.

Heaton N, Randall G . Dengue virus and autophagy. Viruses. 2011; 3(8):1332-41. PMC: 3185800. DOI: 10.3390/v3081332. View

14.

Vetvicka V, Vannucci L, Sima P . The Effects of β - Glucan on Fish Immunity. N Am J Med Sci. 2013; 5(10):580-8. PMC: 3842698. DOI: 10.4103/1947-2714.120792. View

15.

Beaulaurier J, Bickford N, Gregg J, Grady C, Gannam A, Winton J . Susceptibility of Pacific herring to viral hemorrhagic septicemia is influenced by diet. J Aquat Anim Health. 2012; 24(1):43-8. DOI: 10.1080/08997659.2012.668511. View

16.

Shelly S, Lukinova N, Bambina S, Berman A, Cherry S . Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity. 2009; 30(4):588-98. PMC: 2754303. DOI: 10.1016/j.immuni.2009.02.009. View

17.

Liu L, Zhu B, Wu S, Lin L, Liu G, Zhou Y . Spring viraemia of carp virus induces autophagy for necessary viral replication. Cell Microbiol. 2014; 17(4):595-605. DOI: 10.1111/cmi.12387. View

18.

Mizushima N, Levine B, Cuervo A, Klionsky D . Autophagy fights disease through cellular self-digestion. Nature. 2008; 451(7182):1069-75. PMC: 2670399. DOI: 10.1038/nature06639. View

19.

Krishnan R, Jang Y, Oh M . Beta glucan induced immune priming protects against nervous necrosis virus infection in sevenband grouper. Fish Shellfish Immunol. 2022; 121:163-171. DOI: 10.1016/j.fsi.2022.01.005. View

20.

Garcia-Valtanen P, Ortega-Villaizan M, Martinez-Lopez A, Medina-Gali R, Perez L, Mackenzie S . Autophagy-inducing peptides from mammalian VSV and fish VHSV rhabdoviral G glycoproteins (G) as models for the development of new therapeutic molecules. Autophagy. 2014; 10(9):1666-80. PMC: 4206542. DOI: 10.4161/auto.29557. View