Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus

The Mindin/Spondin family, as host extracellular matrix components, comprises key immune-related molecules in both mammals and Drosophila. While the detailed mechanisms of Mindin's function and its role in initiating an effective immune response have been elucidated in model animals, its immune...

Full description

Saved in:
Bibliographic Details
Main Authors: Kai-Min Zhou, Bao-Rui Zhao, Jie Gao, Yongzhen Zhao, Yueling Zhang, Xian-Wei Wang
Format: Article
Language:English
Published: Elsevier 2025-06-01
Series:Comparative Immunology Reports
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2950311625000138
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850136166690455552
author Kai-Min Zhou
Bao-Rui Zhao
Jie Gao
Yongzhen Zhao
Yueling Zhang
Xian-Wei Wang
author_facet Kai-Min Zhou
Bao-Rui Zhao
Jie Gao
Yongzhen Zhao
Yueling Zhang
Xian-Wei Wang
author_sort Kai-Min Zhou
collection DOAJ
description The Mindin/Spondin family, as host extracellular matrix components, comprises key immune-related molecules in both mammals and Drosophila. While the detailed mechanisms of Mindin's function and its role in initiating an effective immune response have been elucidated in model animals, its immune regulatory function in invertebrates remains largely unknown. In the present study, we identified and characterized a Mindin homolog from kuruma shrimp (Marsupenaeus japonicus), which was significantly up-regulated upon Vibrio anguillarum infection. Our findings revealed that Mindin plays a crucial protective role in the antibacterial response by regulating dual oxidase 2 (Duox2) expression. Mechanistically, Mindin recognizes V. anguillarum through its Tsp domain and simultaneously interacts with cell membrane integrin via its SpN domain. This dual interaction triggers the phosphorylation of extracellular regulated kinase (Erk), leading to the activation and phosphorylation of transcription factor Atf2. The phosphorylated Atf2 translocates to the nucleus where it induces the expression of Duox2, resulting in the production of reactive oxygen species (ROS) that effectively inhibit bacterial growth. By establishing the Mindin/Integrin/Erk/Atf2/Duox2 signaling axis, this study unveils a novel antibacterial mechanism in shrimp and provides new insights into the functional role of Mindin in invertebrate immunity.
format Article
id doaj-art-8d9c2e9c72b34a3d8260f235162a9dc1
institution OA Journals
issn 2950-3116
language English
publishDate 2025-06-01
publisher Elsevier
record_format Article
series Comparative Immunology Reports
spelling doaj-art-8d9c2e9c72b34a3d8260f235162a9dc12025-08-20T02:31:12ZengElsevierComparative Immunology Reports2950-31162025-06-01820020710.1016/j.cirep.2025.200207Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicusKai-Min Zhou0Bao-Rui Zhao1Jie Gao2Yongzhen Zhao3Yueling Zhang4Xian-Wei Wang5Shandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, ChinaGuangxi Academy of Fishery Sciences, Guangxi Key Laboratory of Aquatic Genetic Breeding and Healthy Aquaculture, Nanning 530021, ChinaGuangdong Provincial Key Laboratory of Marine Biotechnology, Institute of Marine Sciences, Shantou University, Shantou 515063, ChinaShandong Provincial Key Laboratory of Animal Cells and Developmental Biology, School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China; Corresponding author at: School of Life Sciences, Shandong University, Qingdao, Shandong 266237, China.The Mindin/Spondin family, as host extracellular matrix components, comprises key immune-related molecules in both mammals and Drosophila. While the detailed mechanisms of Mindin's function and its role in initiating an effective immune response have been elucidated in model animals, its immune regulatory function in invertebrates remains largely unknown. In the present study, we identified and characterized a Mindin homolog from kuruma shrimp (Marsupenaeus japonicus), which was significantly up-regulated upon Vibrio anguillarum infection. Our findings revealed that Mindin plays a crucial protective role in the antibacterial response by regulating dual oxidase 2 (Duox2) expression. Mechanistically, Mindin recognizes V. anguillarum through its Tsp domain and simultaneously interacts with cell membrane integrin via its SpN domain. This dual interaction triggers the phosphorylation of extracellular regulated kinase (Erk), leading to the activation and phosphorylation of transcription factor Atf2. The phosphorylated Atf2 translocates to the nucleus where it induces the expression of Duox2, resulting in the production of reactive oxygen species (ROS) that effectively inhibit bacterial growth. By establishing the Mindin/Integrin/Erk/Atf2/Duox2 signaling axis, this study unveils a novel antibacterial mechanism in shrimp and provides new insights into the functional role of Mindin in invertebrate immunity.http://www.sciencedirect.com/science/article/pii/S2950311625000138Innate immunityInvertebrateMindinReactive oxygen species
spellingShingle Kai-Min Zhou
Bao-Rui Zhao
Jie Gao
Yongzhen Zhao
Yueling Zhang
Xian-Wei Wang
Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
Comparative Immunology Reports
Innate immunity
Invertebrate
Mindin
Reactive oxygen species
title Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
title_full Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
title_fullStr Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
title_full_unstemmed Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
title_short Mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp Marsupenaeus japonicus
title_sort mindin promotes the production of reactive oxygen species to regulate intestinal microbiota in kuruma shrimp marsupenaeus japonicus
topic Innate immunity
Invertebrate
Mindin
Reactive oxygen species
url http://www.sciencedirect.com/science/article/pii/S2950311625000138
work_keys_str_mv AT kaiminzhou mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus
AT baoruizhao mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus
AT jiegao mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus
AT yongzhenzhao mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus
AT yuelingzhang mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus
AT xianweiwang mindinpromotestheproductionofreactiveoxygenspeciestoregulateintestinalmicrobiotainkurumashrimpmarsupenaeusjaponicus