Integrated physiological, whole transcriptomic and functional analysis reveals the regulatory mechanism in the liver of rainbow trout (Oncorhynchus mykiss) in response to short-term and chronic hypoxia stress

被引:3
作者
Wu, Shenji [1 ]
Huang, Jinqiang [1 ]
Li, Yongjuan [1 ,2 ]
Zhao, Lu [1 ]
机构
[1] Gansu Agr Univ, Coll Anim Sci & Technol, Lanzhou 730070, Peoples R China
[2] Gansu Agr Univ, Coll Sci, Lanzhou 730070, Peoples R China
基金
中国国家自然科学基金;
关键词
Rainbow trout; Hypoxia; Biochemical parameters; ceRNA network; Functional analysis; LIPID-PEROXIDATION; IMMUNE-RESPONSES; EXPRESSION; ANTIOXIDANT; METABOLISM; EXPOSURE; TILAPIA; GENES;
D O I
10.1016/j.aquaculture.2024.741250
中图分类号
S9 [水产、渔业];
学科分类号
0908 ;
摘要
The frequency of fish encountering hypoxia has risen dramatically as global warming and water pollution intensify, posing a serious threat to survival. Rainbow trout (Oncorhynchus mykiss), which is an economically important fish worldwide, belongs to a typical hypoxia-sensitive fish. However, little is known about the differences in response mechanisms employed by rainbow trout to short-term and chronic hypoxia stress and the roles of non-coding RNAs (ncRNAs) in the response of rainbow trout to hypoxia stress. In this study, we systematically analyzed the changes of liver biochemical parameters in rainbow trout exposed to moderate hypoxic conditions (DO: 4.5 +/- 0.1 mg/L) for different durations (4, 8, 12, 24 h and 1 month) and 24 h reoxygenation, and histologic and transcriptome profiles (lncRNA, miRNA and mRNA) under hypoxia stress for 12 h (Tm12L) and 1 month (TmlL) compared with control (normoxia, DO: 8.5 +/- 0.1 mg/L), and target and regulatory relationships between LOC110520201, miR-2188-y and superoxide dismutase 1 (sod1) were verified by dual-luciferase reporter, overexpression and silencing assays. Histological observations revealed that liver showed no pathological changes in TmlL. Integrating biochemical parameters and mRNA expression profiles, we found that exposure to short-term hypoxia stress resulted in enhanced immune response, aerobic and anaerobic glycolysis and lipid metabolism. In TmlL, increased anaerobic glycolysis and decreased aerobic glycolysis were observed, and antioxidant and immune capacity has returned to normal. Additionally, several key hypoxia-related genes (epo, vegfc, epor, sod1, ppara, foxo1a, gk, dusp1, nlrc3 and nlrp3) and ceRNA regulatory networks were identified from 2711 differentially expressed (DE) mRNAs, 575 DElncRNAs and 395 DEmiRNAs, including LOC110520201-miR2188-y-sod1, LOC110533332-miR-144-y-vegfc, LOC110526066-miR-465-x-ppara and LOC110535032-miR-743y-nlrp3. The analysis of expression patterns in rainbow trout liver and liver cells treated with hypoxia suggested that changes in LOC110520201, miR-2188-y and sod1 showed a ceRNA regulatory relationship. Further experiments demonstrated that sod1 was a target of miR-2188-y, and LOC110520201 silencing increased the expression of miR-2188-y and inhibited sod1 expression. These results facilitate our understanding of the molecular mechanisms of hypoxia response in rainbow trout and provide genetic resources for breeding hypoxiatolerant varieties.
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页数:16
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共 72 条
  • [1] Lipid Metabolism in Inflammation and Immune Function
    Andersen, Catherine J.
    [J]. NUTRIENTS, 2022, 14 (07)
  • [2] Genome-wide identification of novel long non-coding RNAs and their possible roles in hypoxic zebrafish brain
    Banerjee, Bodhisattwa
    Koner, Debaprasad
    Karasik, David
    Saha, Nirmalendu
    [J]. GENOMICS, 2021, 113 (01) : 29 - 43
  • [3] Hepatic transcriptomic and metabolic responses of hybrid striped bass (Morone saxatilis x Morone chrysops) to acute and chronic hypoxic insult
    Beck, Benjamin H.
    Fuller, S. Adam
    Li, Chao
    Green, Bartholomew W.
    Zhao, Honggang
    Rawles, Steven D.
    Webster, Carl D.
    Peatman, Eric
    [J]. COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY D-GENOMICS & PROTEOMICS, 2016, 18 : 1 - 9
  • [4] Bhoopalan Senthil Velan, 2020, F1000Res, V9, DOI 10.12688/f1000research.26648.1
  • [5] Oxidation Resistance of the Sulfur Amino Acids: Methionine and Cysteine
    Bin, Peng
    Huang, Ruilin
    Zhou, Xihong
    [J]. BIOMED RESEARCH INTERNATIONAL, 2017, 2017
  • [6] Hypoxia acclimation alters reactive oxygen species homeostasis and oxidative status in estuarine killifish (Fundulus heteroclitus)
    Borowiec, Brittney G.
    Scott, Graham R.
    [J]. JOURNAL OF EXPERIMENTAL BIOLOGY, 2020, 223 (13)
  • [7] Long noncoding RNA MARL regulates antiviral responses through suppression miR-122-dependent MAVS downregulation in lower vertebrates
    Chu, Qing
    Xu, Tianjun
    Zheng, Weiwei
    Chang, Renjie
    Zhang, Lei
    [J]. PLOS PATHOGENS, 2020, 16 (07)
  • [8] Biomarkers for the toxicity of sublethal concentrations of triclosan to the early life stages of carps
    Dar, Owias Iqbal
    Sharma, Sunil
    Singh, Kirpal
    Sharma, Anket
    Bhardwaj, Renu
    Kaur, Arvinder
    [J]. SCIENTIFIC REPORTS, 2020, 10 (01)
  • [9] Long term salinity disrupts the hepatic function, intestinal health, and gills antioxidative status in Nile tilapia stressed with hypoxia
    Dawood, Mahmoud A. O.
    Noreldin, Ahmed E.
    Sewilam, Hani
    [J]. ECOTOXICOLOGY AND ENVIRONMENTAL SAFETY, 2021, 220
  • [10] Teleost innate immunity, an intricate game between immune cells and parasites of fish organs: who wins, who loses
    Dezfuli, Bahram Sayyaf
    Lorenzoni, Massimo
    Carosi, Antonella
    Giari, Luisa
    Bosi, Giampaolo
    [J]. FRONTIERS IN IMMUNOLOGY, 2023, 14