Uncovering the chromatin-mediated transcriptional regulatory network governing cold stress responses in fish immune cells

He Jiao; Songqian Huang; Minghao Zhang; Qiao Huang; Chenyu Yan; Jingting Qi; Jiangbo Cheng; Yuan Xu; Xue Zhai; Xinwen Li; Siyao Zhan; Wei Li; Zhichao Wu; Jiulin Chan; Liangbiao Chen; Peng Hu

doi:10.1016/j.jgg.2025.01.008

Volume 52 Issue 8

Aug. 2025

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Uncovering the chromatin-mediated transcriptional regulatory network governing cold stress responses in fish immune cells

doi: 10.1016/j.jgg.2025.01.008

He Jiao^a,b,
Songqian Huang^a,b,
Minghao Zhang^a,b,
Qiao Huang^a,b,c,
Chenyu Yan^a,b,
Jingting Qi^a,b,
Jiangbo Cheng^d,
Yuan Xu^a,b,
Xue Zhai^a,b,
Xinwen Li^a,b,
Siyao Zhan^a,b,
Wei Li^a,b,
Zhichao Wu^a,b,
Jiulin Chan^a,b,
Liangbiao Chen^a,b,
Peng Hu^a,b,e

a. Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Ministry of Education, Shanghai Ocean University, Shanghai 201306, China;
b. International Research Center for Marine Biosciences, Ministry of Science and Technology, Shanghai Ocean University, Shanghai 201306, China;
c. The Hunan Provincial Key Laboratory of the TCM Agricultural Biogenomics, Changsha Medical University, Changsha, Hunan 410219, China;
d. The State Key Laboratory of Grassland Agro-ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, Gansu 730020, China;
e. Marine Biomedical Science and Technology Innovation Platform of Lin-gang Special Area, Shanghai 201306, China

Funds:

This work was supported by the National Natural Science Foundation of China (32130109 and 32373113), the National Natural Science Foundation of Shanghai (23ZR1426800), and SciTech Funding by CSPFTZ Lingang Special Area Marine Biomedical Innovation Platform. We are grateful to all members of the Hu lab for the helpful discussion.

Received Date: 2024-11-29
Accepted Date: 2025-01-13
Rev Recd Date: 2025-01-12
Publish Date: 2025-01-21

Abstract

Abstract

Temperature fluctuations challenge ectothermic species, particularly tropical fish dependent on external temperatures for physiological regulation. However, the molecular mechanisms through which low-temperature stress impacts immune responses in these species, especially in relation to chromatin accessibility and epigenetic regulation, remain poorly understood. In this study, we investigate chromatin and transcriptional changes in the head kidney and thymus tissues of Nile tilapia (Oreochromis niloticus), a tropical fish of significant economic importance, under cold stress. By analyzing cis-regulatory elements in open chromatin regions and their associated transcription factors (TFs), we construct a comprehensive transcriptional regulatory network (TRN) governing immune responses, including DNA damage-induced apoptosis. Our analysis identifies 119 TFs within the TRN, with Stat1 emerging as a central hub exhibiting distinct binding dynamics under cold stress, as revealed by footprint analysis. Overexpression of Stat1 in immune cells leads to apoptosis and increases the expression of apoptosis-related genes, many of which contain Stat1-binding sites in their regulatory regions, emphasizing its critical role in immune cell survival during cold stress. These results provide insights into the transcriptional and epigenetic regulation of immune responses to cold stress in tilapia and highlight Stat1 as a promising target for enhancing cold tolerance in tropical fish species.
- Cold stress,
- TRN,
- Chromatin accessibility,
- Stat1,
- Tilapia,
- Immune cells

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