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...

Full description

Bibliographic Details
Main Authors: 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
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