The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii)
IntroductionAs a unique type of immunological process, pregnancy and subsequent parturition are associated with a series of inflammatory events. As an anti-inflammatory cytokine, IL-22 has been proven to participate in the parturition process in mammals. However, less is known about ovoviviparous te...
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Frontiers Media S.A.
2022-12-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2022.1041681/full |
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| author | Shaojing Yan Likang Lyu Xiaojie Wang Haishen Wen Yun Li Jianshuang Li Yijia Yao Chenpeng Zuo Songyang Xie Zhijun Wang Xin Qi |
| author_facet | Shaojing Yan Likang Lyu Xiaojie Wang Haishen Wen Yun Li Jianshuang Li Yijia Yao Chenpeng Zuo Songyang Xie Zhijun Wang Xin Qi |
| author_sort | Shaojing Yan |
| collection | DOAJ |
| description | IntroductionAs a unique type of immunological process, pregnancy and subsequent parturition are associated with a series of inflammatory events. As an anti-inflammatory cytokine, IL-22 has been proven to participate in the parturition process in mammals. However, less is known about ovoviviparous teleosts. To investigate the role of IL-22 in fish parturition, black rockfish, an ovoviviparous teleost, was used. This fish is unique in that it provides over 60% nutrition supply for over 50 thousand embryos at the same time though a placenta-like structure during pregnancy while delivering all fries in two hours.MethodsSequence alignment, phylogenetic tree analysis and homology modeling were performed on IL-22 and its receptor. In situ hybridization demonstrated ovarian localization of il22 and il22r1. The protein of rIL-22 was obtained through the prokaryotic expression. RNA-seq analysis was performed on black rockfish ovarian cells treated with rIL-22.ResultsIn situ hybridization results showed that both il22 and il22ra1 were localized in the perinatal follicle layer and embryonic envelope. The il22 expression level was significantly increased during parturition compared to before and after parturition (P<0.05). To further understand the mechanism of IL-22 in parturition, rIL-22 was obtained. The downstream variation genes in primary cultured ovarian cells in the perinatal period were analyzed according to the transcriptomic results. A total of 168 differentially expressed genes (DEGs) were identified in the rIL-22 group compared with the PBS control group (padj < 0.05 and |log2FoldChange| 1). Of those, 134 DEGs were identified in the LPS and rIL-22 treatment groups, including chemokine, cytokine, and PG synthesis. 34 DEGs were mainly identified in immune-related pathways and reorganization of the cytoskeleton responded only to rIL-22 stimulation but not LPS. KEGG pathways mainly included immune response, PG synthesis, cell death and angiogenesis (p value < 0.05).DiscussionTaken together, our results indicated that IL-22 plays an important role in the parturition of black rockfish by upregulating PG synthesis and increasing chemokine, proinflammatory factor, as well as PG synthetase levels. |
| first_indexed | 2024-04-13T05:22:45Z |
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| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-04-13T05:22:45Z |
| publishDate | 2022-12-01 |
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| series | Frontiers in Marine Science |
| spelling | doaj.art-3c2bfcc543cf46cd81a831f2e1c1a33d2022-12-22T03:00:41ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-12-01910.3389/fmars.2022.10416811041681The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii)Shaojing Yan0Likang Lyu1Xiaojie Wang2Haishen Wen3Yun Li4Jianshuang Li5Yijia Yao6Chenpeng Zuo7Songyang Xie8Zhijun Wang9Xin Qi10Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaAdministration Department, Weihai Taifeng Seawater Seedling Co., LTD, Weihai, ChinaKey Laboratory of Mariculture, Ministry of Education, Ocean University of China, Qingdao, ChinaIntroductionAs a unique type of immunological process, pregnancy and subsequent parturition are associated with a series of inflammatory events. As an anti-inflammatory cytokine, IL-22 has been proven to participate in the parturition process in mammals. However, less is known about ovoviviparous teleosts. To investigate the role of IL-22 in fish parturition, black rockfish, an ovoviviparous teleost, was used. This fish is unique in that it provides over 60% nutrition supply for over 50 thousand embryos at the same time though a placenta-like structure during pregnancy while delivering all fries in two hours.MethodsSequence alignment, phylogenetic tree analysis and homology modeling were performed on IL-22 and its receptor. In situ hybridization demonstrated ovarian localization of il22 and il22r1. The protein of rIL-22 was obtained through the prokaryotic expression. RNA-seq analysis was performed on black rockfish ovarian cells treated with rIL-22.ResultsIn situ hybridization results showed that both il22 and il22ra1 were localized in the perinatal follicle layer and embryonic envelope. The il22 expression level was significantly increased during parturition compared to before and after parturition (P<0.05). To further understand the mechanism of IL-22 in parturition, rIL-22 was obtained. The downstream variation genes in primary cultured ovarian cells in the perinatal period were analyzed according to the transcriptomic results. A total of 168 differentially expressed genes (DEGs) were identified in the rIL-22 group compared with the PBS control group (padj < 0.05 and |log2FoldChange| 1). Of those, 134 DEGs were identified in the LPS and rIL-22 treatment groups, including chemokine, cytokine, and PG synthesis. 34 DEGs were mainly identified in immune-related pathways and reorganization of the cytoskeleton responded only to rIL-22 stimulation but not LPS. KEGG pathways mainly included immune response, PG synthesis, cell death and angiogenesis (p value < 0.05).DiscussionTaken together, our results indicated that IL-22 plays an important role in the parturition of black rockfish by upregulating PG synthesis and increasing chemokine, proinflammatory factor, as well as PG synthetase levels.https://www.frontiersin.org/articles/10.3389/fmars.2022.1041681/fullinterleukin-22parturitionblack rockfishRNA-seqcytokine |
| spellingShingle | Shaojing Yan Likang Lyu Xiaojie Wang Haishen Wen Yun Li Jianshuang Li Yijia Yao Chenpeng Zuo Songyang Xie Zhijun Wang Xin Qi The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) Frontiers in Marine Science interleukin-22 parturition black rockfish RNA-seq cytokine |
| title | The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) |
| title_full | The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) |
| title_fullStr | The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) |
| title_full_unstemmed | The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) |
| title_short | The anti-inflammatory cytokine IL-22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish (Sebastes schlegelii) |
| title_sort | anti inflammatory cytokine il 22 exhibited a proinflammatory effect in the ovary aiding with the parturition of ovoviviparous black rockfish sebastes schlegelii |
| topic | interleukin-22 parturition black rockfish RNA-seq cytokine |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2022.1041681/full |
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