The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis
SOCS8, also known as CISHb, is a fish-specific type II SOCS. Because CISH binds to cytokine receptors and may inhibit STAT5 activation (a substrate of the insulin receptor), SOCS8 may be involved in the control of metaflammation. The socs8−/− zebrafish were created, and both longer trunks and intest...
Main Authors: | , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
KeAi Communications Co. Ltd.
2023-04-01
|
Series: | Water Biology and Security |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2772735122001718 |
_version_ | 1797847682334588928 |
---|---|
author | Junwei Shan Guangxin Wang Heng Li Xuyang Zhao Weidong Ye Lian Su Qingsong Zhu Yuhang Liu Yingyin Cheng Wanting Zhang Nan Wu Xiao-Qin Xia |
author_facet | Junwei Shan Guangxin Wang Heng Li Xuyang Zhao Weidong Ye Lian Su Qingsong Zhu Yuhang Liu Yingyin Cheng Wanting Zhang Nan Wu Xiao-Qin Xia |
author_sort | Junwei Shan |
collection | DOAJ |
description | SOCS8, also known as CISHb, is a fish-specific type II SOCS. Because CISH binds to cytokine receptors and may inhibit STAT5 activation (a substrate of the insulin receptor), SOCS8 may be involved in the control of metaflammation. The socs8−/− zebrafish were created, and both longer trunks and intestinal villi were observed in 1-month-old (mo) fish. Altered mucosal immunity and gut-liver metabolism were also found in socs8−/− fish. Increased intestinal neutrophils and macrophages, together with overexpression of cytokines and T cell markers in this mutant fish, suggested SOCS8's immunoregulating role. During modeling of soybean-induced enteritis using the 3 mo zebrafish, lower expression levels of inflammatory genes but more mucosa barrier disruption were discovered in socs8−/− zebrafish, compared with wide type counterparts. Furthermore, the shrunk villi at 6 mo in socs8−/− fish suggested that the mucosa might have been protected by SOCS8. This is also consistent with the assertion that metaflammation eventually leads to tissue degeneration and premature death. The fact that socs8−/− fish had more hepatic oil droplets compared to their wild-type counterparts suggested SOCS8's role in inhibiting hepatic metaflammation. Transcriptomic analysis as well as 16S rRNA gene sequencing were done on 3 mo socs8−/− fish to methodically reveal the altered immunity and metabolic reprogramming in the gut and liver caused by socs8−/−. The enriched GO terms for the intestinal tract, such as ''cytokine-mediated signaling pathway'' and ''response to external biotic stimulus'', as well as KEGG pathways in both gut and liver like ''carbon metabolism'' and ''glycolysis/gluconeogenesis'', were consistent with previously revealed pathological clues and improved growth performance at early age, respectively. In addition, the microbiota in the socs8−/− strain had adapted to the host's increased carbohydrate metabolism, as evidenced by higher levels of Bacteroidota. Furthermore, Verrucomicrobiota associated with immunoregulation were found in lower abundance in socs8−/− fish. As a result, current findings indicate that SOCS8 plays immunoregulatory and mucosa-protective roles in the fish gut and liver by inhibiting carbohydrate metabolism. |
first_indexed | 2024-04-09T18:15:23Z |
format | Article |
id | doaj.art-269d1888bd6845e3ba8774e06c7533fe |
institution | Directory Open Access Journal |
issn | 2772-7351 |
language | English |
last_indexed | 2024-04-09T18:15:23Z |
publishDate | 2023-04-01 |
publisher | KeAi Communications Co. Ltd. |
record_format | Article |
series | Water Biology and Security |
spelling | doaj.art-269d1888bd6845e3ba8774e06c7533fe2023-04-13T04:27:37ZengKeAi Communications Co. Ltd.Water Biology and Security2772-73512023-04-0122100131The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axisJunwei Shan0Guangxin Wang1Heng Li2Xuyang Zhao3Weidong Ye4Lian Su5Qingsong Zhu6Yuhang Liu7Yingyin Cheng8Wanting Zhang9Nan Wu10Xiao-Qin Xia11College of Fisheries and Life Science, Dalian Ocean University, Dalian, China; Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, China; Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, China; Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaCollege of Fisheries and Life Science, Dalian Ocean University, Dalian, China; Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, ChinaInstitute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, China; Corresponding author. Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China; College of Advanced Agricultural Sciences, University of Chinese Academy of Sciences, Beijing, China; Corresponding author. Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, China.SOCS8, also known as CISHb, is a fish-specific type II SOCS. Because CISH binds to cytokine receptors and may inhibit STAT5 activation (a substrate of the insulin receptor), SOCS8 may be involved in the control of metaflammation. The socs8−/− zebrafish were created, and both longer trunks and intestinal villi were observed in 1-month-old (mo) fish. Altered mucosal immunity and gut-liver metabolism were also found in socs8−/− fish. Increased intestinal neutrophils and macrophages, together with overexpression of cytokines and T cell markers in this mutant fish, suggested SOCS8's immunoregulating role. During modeling of soybean-induced enteritis using the 3 mo zebrafish, lower expression levels of inflammatory genes but more mucosa barrier disruption were discovered in socs8−/− zebrafish, compared with wide type counterparts. Furthermore, the shrunk villi at 6 mo in socs8−/− fish suggested that the mucosa might have been protected by SOCS8. This is also consistent with the assertion that metaflammation eventually leads to tissue degeneration and premature death. The fact that socs8−/− fish had more hepatic oil droplets compared to their wild-type counterparts suggested SOCS8's role in inhibiting hepatic metaflammation. Transcriptomic analysis as well as 16S rRNA gene sequencing were done on 3 mo socs8−/− fish to methodically reveal the altered immunity and metabolic reprogramming in the gut and liver caused by socs8−/−. The enriched GO terms for the intestinal tract, such as ''cytokine-mediated signaling pathway'' and ''response to external biotic stimulus'', as well as KEGG pathways in both gut and liver like ''carbon metabolism'' and ''glycolysis/gluconeogenesis'', were consistent with previously revealed pathological clues and improved growth performance at early age, respectively. In addition, the microbiota in the socs8−/− strain had adapted to the host's increased carbohydrate metabolism, as evidenced by higher levels of Bacteroidota. Furthermore, Verrucomicrobiota associated with immunoregulation were found in lower abundance in socs8−/− fish. As a result, current findings indicate that SOCS8 plays immunoregulatory and mucosa-protective roles in the fish gut and liver by inhibiting carbohydrate metabolism.http://www.sciencedirect.com/science/article/pii/S2772735122001718Gut-liver axisImmunoregulationInsulin signalingSOCS8Zebrafish |
spellingShingle | Junwei Shan Guangxin Wang Heng Li Xuyang Zhao Weidong Ye Lian Su Qingsong Zhu Yuhang Liu Yingyin Cheng Wanting Zhang Nan Wu Xiao-Qin Xia The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis Water Biology and Security Gut-liver axis Immunoregulation Insulin signaling SOCS8 Zebrafish |
title | The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis |
title_full | The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis |
title_fullStr | The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis |
title_full_unstemmed | The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis |
title_short | The immunoregulatory role of fish specific type II SOCS via inhibiting metaflammation in the gut-liver axis |
title_sort | immunoregulatory role of fish specific type ii socs via inhibiting metaflammation in the gut liver axis |
topic | Gut-liver axis Immunoregulation Insulin signaling SOCS8 Zebrafish |
url | http://www.sciencedirect.com/science/article/pii/S2772735122001718 |
work_keys_str_mv | AT junweishan theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT guangxinwang theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT hengli theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT xuyangzhao theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT weidongye theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT liansu theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT qingsongzhu theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT yuhangliu theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT yingyincheng theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT wantingzhang theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT nanwu theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT xiaoqinxia theimmunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT junweishan immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT guangxinwang immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT hengli immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT xuyangzhao immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT weidongye immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT liansu immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT qingsongzhu immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT yuhangliu immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT yingyincheng immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT wantingzhang immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT nanwu immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis AT xiaoqinxia immunoregulatoryroleoffishspecifictypeiisocsviainhibitingmetaflammationinthegutliveraxis |