Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response
Mammalian TGF-β1 plays a crucial role in maintaining immune tolerance and inhibiting autoimmunity. Although several TGF-β1 homologues have been identified in teleosts, their immunosuppressive functions remain unclear. Herein, we identified and characterized LcTGF-β1, a TGF-β1 homologue from the larg...
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KeAi Communications Co. Ltd.
2022-02-01
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2772735122000026 |
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| author | Xiaofeng Li Pengfei Mu Yan Teng Xiaomeng Li Yinanzi Wu Xinhua Chen |
| author_facet | Xiaofeng Li Pengfei Mu Yan Teng Xiaomeng Li Yinanzi Wu Xinhua Chen |
| author_sort | Xiaofeng Li |
| collection | DOAJ |
| description | Mammalian TGF-β1 plays a crucial role in maintaining immune tolerance and inhibiting autoimmunity. Although several TGF-β1 homologues have been identified in teleosts, their immunosuppressive functions remain unclear. Herein, we identified and characterized LcTGF-β1, a TGF-β1 homologue from the large yellow croaker (Larimichthys crocea). LcTGF-β1 possesses several features characteristic of the TGF-β superfamily, including an RGD integrin binding site, an RSKR tetrabasic cut site, and nine conserved cysteines in the mature peptide. The LcTGF-β1 gene was constitutively expressed in all examined tissues, with the highest expression in the spleen, which is rich in immune cells. LcTGF-β1 was significantly upregulated in the head kidney and spleen after Vibrio alginolyticus stimulation. LcTGF-β1 was also expressed in primary head kidney lymphocytes (PKLs), monocytes/macrophages (MO/Mφs), and granulocytes (PKGs), and was significantly upregulated in the MO/Mφs after lipopolysaccharide (LPS) stimulation. Recombinant LcTGF-β1 protein (rLcTGF-β1) significantly suppressed reactive oxygen species (ROS) and nitrogen oxide (NO) production in LPS-activated head kidney MO/Mφs. Furthermore, in these MO/Mφs, rLcTGF-β1 strongly inhibited the expression of pro-inflammatory cytokine (TNF-α) and inducible NO synthase (iNOS), while it induced anti-inflammatory cytokines (TGF-β1 and IL-10), arginase-1, and CD206. The phagocytic activity of LPS-activated MO/Mφs was also increased by rLcTGF-β1. Finally, rLcTGF-β1 significantly inhibited the proliferation of T cells (ZAP70+ cells) and downregulated T-cell activation genes (CD3ζ, TCRα, and ZAP70), T-cell marker genes (CD4 and CD8), and IL-2 in PKLs. These results thus provide strong evidence that LcTGF-β1 promotes the alternative activation of head kidney MO/Mφs and inhibits T-cell proliferation in PKLs, highlighting its role in the regulation of immune response in large yellow croaker. |
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| institution | Directory Open Access Journal |
| issn | 2772-7351 |
| language | English |
| last_indexed | 2024-04-10T06:18:44Z |
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| spelling | doaj.art-ae78fbcce31d4556a8628c135cddd0cd2023-03-02T05:03:27ZengKeAi Communications Co. Ltd.Water Biology and Security2772-73512022-02-0111100006Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune responseXiaofeng Li0Pengfei Mu1Yan Teng2Xiaomeng Li3Yinanzi Wu4Xinhua Chen5Key Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, ChinaKey Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China; Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China; Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, 519000, China; Corresponding author. Key Laboratory of Marine Biotechnology of Fujian Province, Institute of Oceanology, Fujian Agriculture and Forestry University, Fuzhou, 350002, China.Mammalian TGF-β1 plays a crucial role in maintaining immune tolerance and inhibiting autoimmunity. Although several TGF-β1 homologues have been identified in teleosts, their immunosuppressive functions remain unclear. Herein, we identified and characterized LcTGF-β1, a TGF-β1 homologue from the large yellow croaker (Larimichthys crocea). LcTGF-β1 possesses several features characteristic of the TGF-β superfamily, including an RGD integrin binding site, an RSKR tetrabasic cut site, and nine conserved cysteines in the mature peptide. The LcTGF-β1 gene was constitutively expressed in all examined tissues, with the highest expression in the spleen, which is rich in immune cells. LcTGF-β1 was significantly upregulated in the head kidney and spleen after Vibrio alginolyticus stimulation. LcTGF-β1 was also expressed in primary head kidney lymphocytes (PKLs), monocytes/macrophages (MO/Mφs), and granulocytes (PKGs), and was significantly upregulated in the MO/Mφs after lipopolysaccharide (LPS) stimulation. Recombinant LcTGF-β1 protein (rLcTGF-β1) significantly suppressed reactive oxygen species (ROS) and nitrogen oxide (NO) production in LPS-activated head kidney MO/Mφs. Furthermore, in these MO/Mφs, rLcTGF-β1 strongly inhibited the expression of pro-inflammatory cytokine (TNF-α) and inducible NO synthase (iNOS), while it induced anti-inflammatory cytokines (TGF-β1 and IL-10), arginase-1, and CD206. The phagocytic activity of LPS-activated MO/Mφs was also increased by rLcTGF-β1. Finally, rLcTGF-β1 significantly inhibited the proliferation of T cells (ZAP70+ cells) and downregulated T-cell activation genes (CD3ζ, TCRα, and ZAP70), T-cell marker genes (CD4 and CD8), and IL-2 in PKLs. These results thus provide strong evidence that LcTGF-β1 promotes the alternative activation of head kidney MO/Mφs and inhibits T-cell proliferation in PKLs, highlighting its role in the regulation of immune response in large yellow croaker.http://www.sciencedirect.com/science/article/pii/S2772735122000026Large yellow croakerTGF-β1Monocytes/macrophageT cellsImmunoregulation |
| spellingShingle | Xiaofeng Li Pengfei Mu Yan Teng Xiaomeng Li Yinanzi Wu Xinhua Chen Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response Water Biology and Security Large yellow croaker TGF-β1 Monocytes/macrophage T cells Immunoregulation |
| title | Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response |
| title_full | Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response |
| title_fullStr | Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response |
| title_full_unstemmed | Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response |
| title_short | Identification of a TGF-β1 homologue in the large yellow croaker (Larimichthys crocea) revealed its role in regulation of immune response |
| title_sort | identification of a tgf β1 homologue in the large yellow croaker larimichthys crocea revealed its role in regulation of immune response |
| topic | Large yellow croaker TGF-β1 Monocytes/macrophage T cells Immunoregulation |
| url | http://www.sciencedirect.com/science/article/pii/S2772735122000026 |
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