MiR-181a Negatively Regulates Claudin-3 to Facilitate Iridovirus Replication in Astroglia Cells

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2024 Oct 26

PMID 39459923

Authors

Yanping Ma

Jingjing Xu

Le Hao

Gang Wang

Wen Huang

Zhenxing Liu

Affiliations

Soon will be listed here.

Abstract

iridovirus (LMIV) is a variant strain of red sea bream iridovirus (RSIV), causing serious economic losses in aquaculture. Claudins (CLDNs) are major components of tight junctions (TJs) forming an important line of defense against pathogens. Our pilot miRNA-mRNA joint analysis indicated the degradation of CLDN3, as well as its interaction with miR-181a during LMIV infection. To elucidate the miR-181a/CLDN3/LMIV interactions, in vitro assays were carried out on LMB-L cells. We first confirmed that LMIV infection could decrease the expression of CLDN3, accompanied by the enhancement of permeability, suggesting the dysfunction of TJs. Contrary to the inhibition of CLDN3, the activation of miR-181a was proved, presenting a negative correlation between miR-181a and CLDN3 (Pearson = -0.773 and < 0.01). In addition, the influence of CLDN3 on LMIV replication was analyzed by knockdown and over-expression of CLDN3. When CLDN3 was silenced in LMB-L cells with siCLDN3-623 at 9 days post transfection (dpt), LMIV copies and titers were significantly up-regulated by 1.59-fold and 13.87-fold, respectively. By contrast, LMIV replication in LMB-L cells was reduced by 60% and 71%, post transfection with pcDNA3.1-CLDN3 over-expressed plasmid at 6 dpt and 9 dpt, respectively. Ultimately, the regulatory relationship between miR-181a and CLDN3 was further validated by dual luciferase reporter assays. Taking into account the above-described results, we proposed a "miR-181a/CLDN3/LMIV" regulatory relationship. This study provides a new insight for understanding the mechanism of LMIV replication.

References

Wang X, Song T, Zheng H, Li Y, Zheng Y . Jejunal epithelial barrier disruption triggered by reactive oxygen species in early SIV infected rhesus macaques. Free Radic Biol Med. 2021; 177:143-155. DOI: 10.1016/j.freeradbiomed.2021.10.026. View

Guo Y, Steitz J . Virus meets host microRNA: the destroyer, the booster, the hijacker. Mol Cell Biol. 2014; 34(20):3780-7. PMC: 4187717. DOI: 10.1128/MCB.00871-14. View

Baier F, Sanchez-Taltavull D, Yarahmadov T, Castella C, Jebbawi F, Keogh A . Loss of Claudin-3 Impairs Hepatic Metabolism, Biliary Barrier Function, and Cell Proliferation in the Murine Liver. Cell Mol Gastroenterol Hepatol. 2021; 12(2):745-767. PMC: 8273426. DOI: 10.1016/j.jcmgh.2021.04.003. View

Zhang C, Wang Q, Liu A, Zhang C, Liu L, Lu L . MicroRNA miR-155 inhibits cyprinid herpesvirus 3 replication via regulating AMPK-MAVS-IFN axis. Dev Comp Immunol. 2021; 129:104335. DOI: 10.1016/j.dci.2021.104335. View

Wei J, Huang Y, Zhu W, Li C, Huang X, Qin Q . Isolation and identification of Singapore grouper iridovirus Hainan strain (SGIV-HN) in China. Arch Virol. 2019; 164(7):1869-1872. DOI: 10.1007/s00705-019-04268-z. View

Harris H, Farquhar M, Mee C, Davis C, Reynolds G, Jennings A . CD81 and claudin 1 coreceptor association: role in hepatitis C virus entry. J Virol. 2008; 82(10):5007-20. PMC: 2346731. DOI: 10.1128/JVI.02286-07. View

Li H, Liu X, Chen F, Zuo K, Wu C, Yan Y . Avian Influenza Virus Subtype H9N2 Affects Intestinal Microbiota, Barrier Structure Injury, and Inflammatory Intestinal Disease in the Chicken Ileum. Viruses. 2018; 10(5). PMC: 5977263. DOI: 10.3390/v10050270. View

Yao Y, Chen Z, Norris E, Strickland S . Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat Commun. 2014; 5:3413. PMC: 3992931. DOI: 10.1038/ncomms4413. View

Hubatsch I, Ragnarsson E, Artursson P . Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers. Nat Protoc. 2007; 2(9):2111-9. DOI: 10.1038/nprot.2007.303. View

10.

Wang W, Sun J, Wang N, Sun Z, Ma Q, Li J . Enterovirus A71 capsid protein VP1 increases blood-brain barrier permeability and virus receptor vimentin on the brain endothelial cells. J Neurovirol. 2019; 26(1):84-94. PMC: 7040057. DOI: 10.1007/s13365-019-00800-8. View

11.

Jia K, Liu Z, Guo C, Xia Q, Mi S, Li X . The potential role of microfilaments in host cells for infection with infectious spleen and kidney necrosis virus infection. Virol J. 2013; 10:77. PMC: 3599308. DOI: 10.1186/1743-422X-10-77. View

12.

Yan L, Wang P, Zhao C, Zhang B, Guo J, Qiu L . Development of a spotted sea bass (Lateolabrax maculatus) bulbus arteriosus cell line and its application to fish virology and immunology. Fish Shellfish Immunol. 2023; 144:109298. DOI: 10.1016/j.fsi.2023.109298. View

13.

Nakamura S, Irie K, Tanaka H, Nishikawa K, Suzuki H, Saitoh Y . Morphologic determinant of tight junctions revealed by claudin-3 structures. Nat Commun. 2019; 10(1):816. PMC: 6379431. DOI: 10.1038/s41467-019-08760-7. View

14.

Colpitts C, Baumert T . Claudins in viral infection: from entry to spread. Pflugers Arch. 2016; 469(1):27-34. PMC: 5299967. DOI: 10.1007/s00424-016-1908-4. View

15.

Wu L, Song W, Xie Y, Hu L, Hou X, Wang R . miR-181a-5p suppresses invasion and migration of HTR-8/SVneo cells by directly targeting IGF2BP2. Cell Death Dis. 2018; 9(2):16. PMC: 5833820. DOI: 10.1038/s41419-017-0045-0. View

16.

Kerddee P, Dinh-Hung N, Dong H, Hirono I, Soontara C, Areechon N . Molecular evidence for homologous strains of infectious spleen and kidney necrosis virus (ISKNV) genotype I infecting inland freshwater cultured Asian sea bass (Lates calcarifer) in Thailand. Arch Virol. 2021; 166(11):3061-3074. DOI: 10.1007/s00705-021-05207-7. View

17.

Helm E, Curry S, De Mille C, Schweer W, Burrough E, Gabler N . Impact of viral disease hypophagia on pig jejunal function and integrity. PLoS One. 2020; 15(1):e0227265. PMC: 6946155. DOI: 10.1371/journal.pone.0227265. View

18.

Sun H, Su Y, Li P, He J, Chen H, Wang G . The Roles of Epinephelus coioides miR-122 in SGIV Infection and Replication. Mar Biotechnol (NY). 2021; 23(2):294-307. PMC: 8032594. DOI: 10.1007/s10126-021-10023-w. View

19.

Liu Z, Ma Y, Hao L . Characterization of three novel cell lines derived from the brain of spotted sea bass: Focusing on cell markers and susceptibility toward iridoviruses. Fish Shellfish Immunol. 2022; 130:175-185. DOI: 10.1016/j.fsi.2022.08.031. View

20.

Jurisch-Yaksi N, Yaksi E, Kizil C . Radial glia in the zebrafish brain: Functional, structural, and physiological comparison with the mammalian glia. Glia. 2020; 68(12):2451-2470. DOI: 10.1002/glia.23849. View