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Integrated analysis of mRNA and long non-coding RNA expression profiles reveals the potential roles of lncRNA-mRNA network in carp macrophage immune regulation

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Abstract

Long non-coding RNAs (lncRNAs) have emerged as a hot topic in research as mounting evidence has indicated their transcriptional or post-transcriptional regulatory potential in multiple biological processes. Previous studies have revealed the involvement of lncRNAs in the immunoregulation of mammalian macrophages by changing mRNA expression; however, studies on the lncRNAs in fish macrophages and their potential roles in the immune system remain unknown. Primary macrophages were isolated from the head kidney (HK) of red common carp (Cyprinus carpio) and high-throughput lncRNA-mRNA sequencing was performed using the Illumina HiSeq platform. The results revealed that the most highly expressed mRNAs in primary HK macrophages were mainly involved in immune-related signal pathways. Furthermore, the most enriched immune-related GO term and KEGG pathway of the mRNAs were “immune system development” and “chemokine signaling pathway,” respectively. A total of 20,333 lncRNAs, composed of 10,512 known and 9821 novel lncRNAs, were identified, and functional enrichment analysis of the lncRNA-mRNA network indicated that the expressed lncRNAs in primary HK macrophages could be associated with the regulation of multiple immune-related signaling pathways. In addition, the expressions of several selected lncRNAs and their related mRNAs were determined in carp macrophages following a 6-h exposure to lipopolysaccharide (LPS) and Poly(I: C), the results of which confirmed the co-expression regulation of lncRNAs and target mRNAs in the immune response of carp macrophages. These results suggest the correlative of the lncRNA-mRNA network in fish macrophage immune response, which may further affect the cross-talk of various signaling pathways by interaction with other network genes. Here, we provided fundamental data about the transcriptome profiles of primary HK macrophages from red common carp by analysis of the lncRNA-mRNA network, and ultimately suggest the potential roles of lncRNA-mRNA networks in immune regulation in teleost fish.

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Funding

This work was sponsored by the National Natural Science Foundation of China (Grant No.31971523), and the Natural Science Foundation of Fujian province, China (Grant No.2018J05066).

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  1. Shuai Liu and Ting Yu contributed equally to this work.

Authors and Affiliations

  1. School of Environmental and Chemical Engineering, Shanghai University, Shanghai, 200444, China

    Shuai Liu, Ting Yu, Yuanyuan Zhang, Chenyuan Pan & Ming Yang

  2. Research Institute of Poyang Lake, Jiangxi Academy of Sciences, Nanchang, 330012, China

    Shuai Liu

  3. Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, 361005, China

    Ling Cai

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  1. Shuai Liu
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  2. Ting Yu
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Correspondence to Ling Cai or Ming Yang.

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Liu, S., Yu, T., Zhang, Y. et al. Integrated analysis of mRNA and long non-coding RNA expression profiles reveals the potential roles of lncRNA-mRNA network in carp macrophage immune regulation. In Vitro Cell.Dev.Biol.-Animal 57, 835–847 (2021). https://doi.org/10.1007/s11626-021-00610-5

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