RNA-Seq-Based Whole Transcriptome Analysis of IPEC-J2 Cells During Swine Acute Diarrhea Syndrome Coronavirus Infection

Overview

Journal Front Vet Sci

Specialty Veterinary Medicine

Date 2020 Sep 9

PMID 32903570

Citations 8

Authors

Fanfan Zhang

Weifeng Yuan

Zhiquan Li

Yuhan Zhang

Yu Ye

Kai Li

Zhen Ding

Yunyan Chen

Ting Cheng

Qiong Wu

Yuxin Tang

Deping Song

Affiliations

Soon will be listed here.

Abstract

The new emergence of swine acute diarrhea syndrome coronavirus (SADS-CoV) has resulted in high mortality in suckling pigs in China. To date, the transcriptional expression of host cells during SADS-CoV infection has not been documented. In this study, by means of RNA-Seq technology, we investigated the whole genomic expression profiles of intestinal porcine epithelial cells (IPEC-J2) infected with a SADS-CoV strain SADS-CoV-CH-FJWT-2018. A total of 24,676 genes were identified: 23,677 were known genes, and 999 were novel genes. A total of 1,897 differentially expressed genes (DEGs) were identified between SADS-CoV-infected and uninfected cells at 6, 24, and 48 h post infection (hpi). Of these, 1,260 genes were upregulated and 637 downregulated. A Gene Ontology enrichment analysis revealed that DEGs in samples from 6, 24, and 48 hpi were enriched in 79, 383, and 233 GO terms, respectively, which were mainly involved in immune system process, response to stimulus, signal transduction, and cytokine-cytokine receptor interactions. The 1,897 DEGs were mapped to 109 KEGG Ontology (KO) pathways classified into four main categories. Most of the DEGs annotated in the KEGG pathways were related to the immune system, infectious viral disease, and signal transduction. The mRNA of porcine serum amyloid A-3 protein (SAA3), an acute phase response protein, was significantly upregulated during the infection. Over-expressed SAA3 in IPEC-J2 cells drastically inhibited the replication of SADS-CoV, while under-expressed SAA3 promoted virus replication. To our knowledge, this is the first report on the profiles of gene expression of IPEC-J2 cells infected by SADS-CoV by means of RNA- technology. Our results indicate that SADS-CoV infection significantly modified the host cell gene expression patterns, and the host cells responded in highly specific manners, including immune response, signal and cytokine transduction, and antiviral response. The findings provide important insights into the transcriptome of IPEC-J2 in SADS-CoV infection.

Citing Articles

Remdesivir inhibits Porcine epidemic diarrhea virus infection in vitro.

Huang Z, Zhou S, Wang J, Yang Z, Wang Z Heliyon. 2023; 9(11):e21468.

PMID: 38027806 PMC: 10663732. DOI: 10.1016/j.heliyon.2023.e21468.

Combined Analysis of the Whole Transcriptome of Piglets Infected with SADS-CoV Virulent and Avirulent Strains.

Li Q, Tang X, Zhou L, Lv X, Gao L, Lan T Microorganisms. 2023; 11(2).

PMID: 36838374 PMC: 9964493. DOI: 10.3390/microorganisms11020409.

LACpG10-HL Functions Effectively in Antibiotic-Free and Healthy Husbandry by Improving the Innate Immunity.

Pan W, Zhao Z, Wu J, Fan Q, Huang H, He R Int J Mol Sci. 2022; 23(19).

PMID: 36232768 PMC: 9569488. DOI: 10.3390/ijms231911466.

The Effects of Swine Coronaviruses on ER Stress, Autophagy, Apoptosis, and Alterations in Cell Morphology.

Chen Y, Burrough E Pathogens. 2022; 11(8).

PMID: 36015060 PMC: 9416022. DOI: 10.3390/pathogens11080940.

Foot-and-mouth disease virus VP1 promotes viral replication by regulating the expression of chemokines and GBP1.

Yang L, Chen H, Liu L, Song J, Feng T, Li Y Front Vet Sci. 2022; 9:937409.

PMID: 35937300 PMC: 9353127. DOI: 10.3389/fvets.2022.937409.

References

Westermann A, Vogel J . Host-Pathogen Transcriptomics by Dual RNA-Seq. Methods Mol Biol. 2018; 1737:59-75. DOI: 10.1007/978-1-4939-7634-8_4. View

Cao L, Ge X, Gao Y, Ren Y, Ren X, Li G . Porcine epidemic diarrhea virus infection induces NF-κB activation through the TLR2, TLR3 and TLR9 pathways in porcine intestinal epithelial cells. J Gen Virol. 2015; 96(Pt 7):1757-67. DOI: 10.1099/vir.0.000133. View

Pan Y, Tian X, Qin P, Wang B, Zhao P, Yang Y . Discovery of a novel swine enteric alphacoronavirus (SeACoV) in southern China. Vet Microbiol. 2017; 211:15-21. PMC: 7117260. DOI: 10.1016/j.vetmic.2017.09.020. View

Zhou J, Sheng J, Fan Y, Zhu X, Tao Q, He Y . Association between serum amyloid A levels and cancers: a systematic review and meta-analysis. Postgrad Med J. 2018; 94(1115):499-507. DOI: 10.1136/postgradmedj-2018-136004. View

Salguero F, Frossard J, Rebel J, Stadejek T, Morgan S, Graham S . Host-pathogen interactions during porcine reproductive and respiratory syndrome virus 1 infection of piglets. Virus Res. 2015; 202:135-43. PMC: 7172408. DOI: 10.1016/j.virusres.2014.12.026. View

Wang X, Jia Y, Ren J, Huo N, Liu H, Xiao S . Newcastle Disease Virus Nonstructural V Protein Upregulates SOCS3 Expression to Facilitate Viral Replication Depending on the MEK/ERK Pathway. Front Cell Infect Microbiol. 2019; 9:317. PMC: 6748215. DOI: 10.3389/fcimb.2019.00317. View

Yang Y, Liang Q, Xu S, Mazing E, Xu G, Peng L . Characterization of a novel bat-HKU2-like swine enteric alphacoronavirus (SeACoV) infection in cultured cells and development of a SeACoV infectious clone. Virology. 2019; 536:110-118. PMC: 7112019. DOI: 10.1016/j.virol.2019.08.006. View

Zhang Y, Zhang J, Sheng H, Li H, Wang R . Acute phase reactant serum amyloid A in inflammation and other diseases. Adv Clin Chem. 2019; 90:25-80. DOI: 10.1016/bs.acc.2019.01.002. View

Sun D, Zhang X, Zhang Q, Ji X, Jia Y, Wang H . Comparative transcriptome profiling uncovers a Lilium regale NAC transcription factor, LrNAC35, contributing to defence response against cucumber mosaic virus and tobacco mosaic virus. Mol Plant Pathol. 2019; 20(12):1662-1681. PMC: 6859495. DOI: 10.1111/mpp.12868. View

10.

Zhang Q, Yoo D . Immune evasion of porcine enteric coronaviruses and viral modulation of antiviral innate signaling. Virus Res. 2016; 226:128-141. PMC: 7111337. DOI: 10.1016/j.virusres.2016.05.015. View

11.

Gao S, Wang Z, Jiang H, Sun J, Diao Y, Tang Y . Transcriptional analysis of host responses related to immunity in chicken spleen tissues infected with reticuloendotheliosis virus strain SNV. Infect Genet Evol. 2019; 74:103932. DOI: 10.1016/j.meegid.2019.103932. View

12.

Yoshinaga N, Shindo K, Matsui Y, Takiuchi Y, Fukuda H, Nagata K . A screening for DNA damage response molecules that affect HIV-1 infection. Biochem Biophys Res Commun. 2019; 513(1):93-98. DOI: 10.1016/j.bbrc.2019.03.168. View

13.

Sun P, Wu H, Huang J, Xu Y, Yang F, Zhang Q . Porcine epidemic diarrhea virus through p53-dependent pathway causes cell cycle arrest in the G0/G1 phase. Virus Res. 2018; 253:1-11. PMC: 7114671. DOI: 10.1016/j.virusres.2018.05.019. View

14.

Tarazona S, Garcia-Alcalde F, Dopazo J, Ferrer A, Conesa A . Differential expression in RNA-seq: a matter of depth. Genome Res. 2011; 21(12):2213-23. PMC: 3227109. DOI: 10.1101/gr.124321.111. View

15.

Diez-Fuertes F, De La Torre-Tarazona H, Calonge E, Pernas M, Alonso-Socas M, Capa L . Transcriptome Sequencing of Peripheral Blood Mononuclear Cells from Elite Controller-Long Term Non Progressors. Sci Rep. 2019; 9(1):14265. PMC: 6776652. DOI: 10.1038/s41598-019-50642-x. View

16.

Lin H, Chen L, Gao L, Yuan X, Ma Z, Fan H . Epidemic strain YC2014 of porcine epidemic diarrhea virus could provide piglets against homologous challenge. Virol J. 2016; 13:68. PMC: 4840883. DOI: 10.1186/s12985-016-0529-z. View

17.

Moon C, Stappenbeck T . Viral interactions with the host and microbiota in the intestine. Curr Opin Immunol. 2012; 24(4):405-10. PMC: 3423491. DOI: 10.1016/j.coi.2012.05.002. View

18.

Li F, Tam J, Liu D . Cell cycle arrest and apoptosis induced by the coronavirus infectious bronchitis virus in the absence of p53. Virology. 2007; 365(2):435-45. PMC: 7103336. DOI: 10.1016/j.virol.2007.04.015. View

19.

Xu Z, Zhang Y, Gong L, Huang L, Lin Y, Qin J . Isolation and characterization of a highly pathogenic strain of Porcine enteric alphacoronavirus causing watery diarrhoea and high mortality in newborn piglets. Transbound Emerg Dis. 2018; 66(1):119-130. PMC: 7168553. DOI: 10.1111/tbed.12992. View

20.

Cai Z, Cai L, Jiang J, Chang K, van der Westhuyzen D, Luo G . Human serum amyloid A protein inhibits hepatitis C virus entry into cells. J Virol. 2007; 81(11):6128-33. PMC: 1900255. DOI: 10.1128/JVI.02627-06. View