Abstract
Sebastes schlegelii, an important aquaculture species, has been widely cultured in East Asian countries. With the increase in the cultivation scale, various diseases have become major threats to the industry. Evidence has shown that non-coding RNAs (ncRNAs) have remarkable functions in the interactions between pathogens and their hosts. However, little is known about the mechanisms of circular RNAs (circRNAs) and coding RNAs in the process of preventing pathogen infection in the intestine in teleosts. In this study, we aimed to uncover the global landscape of mRNAs, circRNAs, and microRNAs (miRNAs) in response to Edwardsiella tarda infection at different time points (0, 2, 6, 12, and 24 h) and to construct regulatory networks for exploring the immune regulatory mechanism in the intestine of S. schlegelii. In total, 1,794 mRNAs, 87 circRNAs, and 79 miRNAs were differentially expressed. The differentially expressed RNAs were quantitatively validated using qRT-PCR. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that most of the differentially expressed mRNA genes and the target genes of ncRNAs were related to immune signaling pathways, such as the NF-κB signal pathway, pathogen recognition receptors related to signaling pathways (Toll-like receptors and Nod-like receptors), and the chemokine signaling pathway. Based on these differentially expressed genes, 624 circRNA-miRNA pairs and 2,694 miRNA-mRNA pairs were predicted using the miRanda software. Integrated analyses generated 25 circRNA-miRNA-mRNA interaction networks. In a novel_circ_0004195/novel-530/IκB interaction network, novel_530 was upregulated, while its two targets, novel_circ_0004195 and IκB, were downregulated after E. tarda infection. In addition, two circRNA-miRNA-mRNA networks related to apoptosis (novel_circ_0003210/novel_152/apoptosis-stimulating of p53 protein 1) and interleukin (novel_circ_0001907/novel_127/interleukin-1 receptor type 2) were also identified in our study. We thus speculated that the downstream NF-κB signaling pathway, p53 signaling pathway, and apoptosis pathway might play vital roles in the immune response in the intestine of S. schlegelii. This study revealed a landscape of RNAs in the intestine of S. schlegelii during E. tarda infection and provided clues for further study on the immune mechanisms and signaling networks based on the circRNA-miRNA-mRNA axis in S. schlegelii.
Highlights
The immune system of vertebrates is a complex network that consists of different types of molecules, cells, and organs and plays key roles in recognizing foreign “invaders,” such as bacteria and viruses, resisting pathogen invasion and maintaining homeostasis [1]
To understand the histopathological changes in intestinal tissues when exposed to pathogenic bacteria, E. tarda was used to infect S. schlegelii and the infected intestinal tissues were dissected for histopathological analysis
Our results indicated that the destruction of E. tarda to intestinal tissues of S. schlegelii is a time-dependent manner
Summary
The immune system of vertebrates is a complex network that consists of different types of molecules, cells, and organs and plays key roles in recognizing foreign “invaders,” such as bacteria and viruses, resisting pathogen invasion and maintaining homeostasis [1]. The mucosal surfaces, including the intestine, skin, and gills, serve as the first line of host defense, forming an immune barrier once the organism is invaded by pathogens [2]. As an important part of the mucosal immune system, the intestinal mucosa faces great challenges by being constantly exposed to a large microbial community [3]. More and more studies have proved that the intestinal mucosa plays an important role in protecting the host against pathogen infection. Characterized the role of the intestinal epithelial barrier in Ictalurus punctatus following Edwardsiella ictaluri challenge and identified 1,633 differentially expressed genes associated with immune activation and inflammatory responses [4]. The above studies proved that the intestinal mucosal immune system plays a vital role in the immune responses against infection in teleost fishes. The exploration of the key immune genes and signaling pathways is needed to further characterize its molecular regulatory mechanism
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