High temperature induces oxidative damage, immune modulation, and atrophy in the gills and skeletal muscle of the teleost fish black cusk-eel (Genypterus maculatus)

IF 2.4 3区 农林科学 Q1 FISHERIES Developmental and comparative immunology Pub Date : 2025-03-01 Epub Date: 2025-01-30 DOI:10.1016/j.dci.2025.105332
Sofia Becerra , Marcia Arriagada-Solimano , Sebastian Escobar-Aguirre , Jaime Palomino , Jorge Aedo , Juan Manuel Estrada , Veronica Barra-Valdebenito , Rodrigo Zuloaga , Juan Antonio Valdes , Phillip Dettleff
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Abstract

The high temperature associated with heat waves is a relevant abiotic factor that could impact the biology of teleost fish. The innate immune response, muscular growth, and oxidative stress status are relevant functions in fish tissues that could be affected by increased temperature. In this study, black cusk-eel (Genypterus maculatus) juveniles were subjected to increased temperature, to experimentally replicate heat waves registered from the South Pacific Ocean for five days. The results showed that thermal stress modulated the immune response in gills, with up-regulation of antibacterial peptides, pro-inflammatory cytokines, and Toll-like receptors genes, including hepcidin, gzma, tnfa, cxcl8, and tlr5, with no effect on complement system genes. In skeletal muscle, high temperature triggered atrophy-related gene expression, with up-regulation of foxo1, foxo3, fbxo32, murf1, and atg16l. Increased temperature also generated an up-regulation of transcripts encoding heat shock protein (hsp60 and hsp70) in gills and skeletal muscle, generating oxidative stress in both tissues, with increased expression of the antioxidant genes sod1 and gpx1 in gills and skeletal muscle, respectively, with oxidative damage observed at the DNA level (AP sites), protein (carbonyl content), and lipoperoxidation (HNE content) in both tissues. The present study shows that short-term increases in temperature like those observed in heat waves could affect the immune response in gills, induced atrophy in skeletal muscle, and generate oxidative stress in a teleost species important for Chilean aquaculture diversification, information relevant under the context of climate change scenario.
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高温诱导硬骨鱼黑尾鳗(Genypterus maculatus)的鳃和骨骼肌氧化损伤、免疫调节和萎缩。
与热浪相关的高温是影响硬骨鱼生物学的相关非生物因素。先天免疫反应、肌肉生长和氧化应激状态是鱼类组织的相关功能,可能受到温度升高的影响。在这项研究中,黑尾鳗(Genypterus maculatus)幼鱼被置于温度升高的环境中,以实验性地复制来自南太平洋的五天热浪。结果表明,热应激可调节鳃的免疫反应,上调抗菌肽、促炎细胞因子和toll样受体基因,包括hepcidin、gzma、tnfa、cxcl8和tlr5,而对补体系统基因无影响。在骨骼肌中,高温触发了萎缩相关基因的表达,foxo1、foxo3、fbxo32、murf1和atg16l表达上调。温度升高还导致鳃和骨骼肌中编码热休克蛋白(hsp60和hsp70)的转录本上调,在两种组织中产生氧化应激,分别增加了鳃和骨骼肌中抗氧化基因sod1和gpx1的表达,并在两种组织中观察到DNA水平(AP位点)、蛋白质(羰基含量)和脂质过氧化(HNE含量)的氧化损伤。目前的研究表明,像热浪中观察到的短期温度升高可能会影响鳃的免疫反应,诱导骨骼肌萎缩,并产生氧化应激,这对智利水产养殖多样化至关重要,这是气候变化情景下相关信息。
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来源期刊
CiteScore
6.20
自引率
6.90%
发文量
206
审稿时长
49 days
期刊介绍: Developmental and Comparative Immunology (DCI) is an international journal that publishes articles describing original research in all areas of immunology, including comparative aspects of immunity and the evolution and development of the immune system. Manuscripts describing studies of immune systems in both vertebrates and invertebrates are welcome. All levels of immunological investigations are appropriate: organismal, cellular, biochemical and molecular genetics, extending to such fields as aging of the immune system, interaction between the immune and neuroendocrine system and intestinal immunity.
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