RNA-Seq and miRNA-Seq data from Epstein-Barr virus-infected tree shrews reveal a ceRNA network contributing to immune microenvironment regulation

ABSTRACT

Epstein-Barr virus (EBV) infection in humans is ubiquitous and associated with various diseases. Remodeling of the immune microenvironment is the primary cause of EBV infection and pathogenesis; however, the underlying mechanism has not been fully elucidated. In this study, we used whole-transcriptome RNA-Seq to detect mRNAs, long non-coding RNAs (lncRNA), and microRNA (miRNA) profiles in the control group, 3 days, and 28 days after EBV infection, based on the tree shrew model that we reported previously. First, we estimated the proportion of 22 cell types in each sample using CIBERSORT software and identified 18 high-confidence DElncRNAs related to immune microenvironment regulation after EBV infection. Functional enrichment analysis of these differentially expressed lncRNAs primarily focused on the autophagy, endocytosis, and ferroptosis signalling pathways. Moreover, EBV infection affects miRNA expression patterns, and many miRNAs are silenced. Finally, three competing endogenous RNA regulatory networks were built using lncRNAs that significantly correlated with immune cell types, miRNAs that responded to EBV infection, and potentially targeted the mRNA of the miRNAs. Among them, MRPL42-AS-5 might act as an hsa-miR-296-5p “sponge” and compete with target mRNAs, thus increasing mRNA expression level, which could induce immune cell infiltration through the cellular senescence signalling pathway against EBV infection. Overall, we conducted a complete transcriptomic analysis of EBV infection in vivo for the first time and provided a novel perspective for further investigation of EBV-host interactions.

KEYWORDS:

• Epstein-Barr virus
• tree shrew
• long non-coding RNAs
• microRNA
• immune microenvironment

Acknowledgements

We thank the Experimental Animal Center of Guangxi Medical University for providing technical support for animal feeding. We thank the members of our research groups for providing technical assistance and participating in discussions.

Disclosure statement

No potential conflicts of interest were stated by the author(s).

Author contributions

W. X.: Conceptualization, Methodology, Investigation, Visualization, and Writing-Original Draft. N. S.: Resources and Investigation. A. Z. T. and C.Q.L.: Supervision, Project administration, and funding acquisition.

Data availability statement

Raw data have been deposited at the SRA databank (www.ncbi.nlm.nih.gov/sra) and are available under the accession number PRJNA981676.

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2024.2306795

Additional information

Funding

This study was supported by the National Natural Science Foundation of China (Grant Nos. 32060132, 82260519, and U21A20371), the Guangxi Clinic Medicine Research Center of Nasopharyngeal Carcinoma (Grant No. GuikeAD20297078).