Abstract
Although the modulation of immune-related genes after viral infection has been widely described in vertebrates, the potential implications of non-coding RNAs (ncRNAs), especially long non-coding RNAs (lncRNAs), in immunity are still a nascent research field. The model species zebrafish could serve as a useful organism for studying the functionality of lncRNAs due to the numerous advantages of this teleost, including the existence of numerous mutant lines. In this work, we conducted a whole-transcriptome analysis of wild-type (WT) and heterozygous rag1 mutant (rag1+/−) zebrafish after infection with the pathogen spring viraemia of carp virus (SVCV). WT and rag1+/− zebrafish were infected with SVCV for 24 h. Kidney samples were sampled from infected and uninfected fish for transcriptome sequencing. From a total of 198,540 contigs, 12,165 putative lncRNAs were identified in zebrafish. Most of the putative lncRNAs were shared by the two zebrafish lines. However, by comparing the lncRNA profiles induced after SVCV infection in WT and rag1+/− fish, most of the lncRNAs that were significantly induced after viral challenge were exclusive to each line, reflecting a highly differential response to the virus. Analysis of the neighboring genes of lncRNAs that were exclusively modulated in WT revealed high representation of metabolism-related terms, whereas those from rag1+/− fish showed enrichment in terms related to the adaptive immune response, among others. On the other hand, genes involved in numerous antiviral processes surrounded commonly modulated lncRNAs, as expected. These results clearly indicate that after SVCV infection in zebrafish, the expression of an array of lncRNAs with functions in different aspects of immunity is induced.
Highlights
For understanding the role of long non-coding RNAs (lncRNAs), one of most useful species is zebrafish (Danio rerio)
In contrast to what is observed in homozygous rag[1] mutant zebrafish, which are more resistant to infection with spring viraemia of carp virus (SVCV) compared to WT fish[31,32], no significant differences in survival were found between the WT and rag1-heterozygous fish after SVCV challenge (Supplementary Fig. S1)
Modulation of lncRNAs was described after rhabdovirus infection in mice infected with the rabies virus (RABV)[42]
Summary
For understanding the role of lncRNAs, one of most useful species is zebrafish (Danio rerio). In the case of the fish immunity, lncRNAs are key players that in turn can display complex mechanism to modulate the expression of Toll-like receptors, NF-kB activity, differentiation of the Th1/Th2 response, and other immune-relevant functions[2]. Knockdown analysis demonstrated the role of the PU.[1] gene in adaptive immunity and the negative regulation of this gene by its antisense long non-coding RNA (AS lncRNA)[7]. An excellent model for understanding the role of lncRNAs in the immune response and their modulation after infections is the zebrafish mutant line rag[1]. Comparison of the lncRNA expression pattern after SVCV challenge in wild-type (WT) and rag1-heterozygous mutant fish (rag1+/−) would allow us to elucidate the potential implications of the diversity of lncRNAs in different aspects of innate and adaptive immunity. This study gives new genomic knowledge of how lncRNAs are key molecular components of the immune system in teleost
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