ACTA THERIOLOGICA SINICA ›› 2023, Vol. 43 ›› Issue (6): 710-722.DOI: 10.16829/j.slxb.150822

• ORIGINAL PAPERS • Previous Articles     Next Articles

Effect of exposure to high temperature on energy metabolism and oxidative stress in striped hamsters

ZHANG Ruihan, LUO Dan, LUO Xinxin, HU Chenxiao, LIN Long, CHEN Qian, CAO Jing, ZHAO Zhijun   

  1. College of Life and Environmental Science, Zhejiang Provincial Key Laboratory for Water Environment and Marine Biological Resources Protection, Wenzhou University, Wenzhou 325035, China
  • Received:2023-06-30 Revised:2023-08-07 Online:2023-11-30 Published:2023-11-22

高温暴露对黑线仓鼠能量代谢和组织氧化应激的影响

张锐涵, 罗丹, 罗欣欣, 胡陈晓, 林珑, 陈倩, 曹静, 赵志军   

  1. 温州大学生命与环境科学学院, 浙江省水环境与海洋生物资源保护重点实验室, 温州 325035
  • 通讯作者: 赵志军, E-mail:zhao73@foxmail.com
  • 作者简介:张锐涵(2002-),女,本科生,主要从事动物生理生态学研究.
  • 基金资助:
    国家自然科学基金(31670417);国家级大学生创新创业训练计划项目(202310351047);浙江省大学生科技创新活动计划暨新苗人才计划项目(2023R451028)

Abstract: The adaptive regulation of animal energy metabolism affects life history characteristics such as growth, development, reproduction, and aging. Metabolic rate and tissue mitochondrial respiration rate are related to free radical levels, which are important factors influencing the aging of the organism. In this study, we investigated the intrinsic link among energy metabolism, tissue respiration rates of major metabolically active organs, free radical levels, and antioxidant capacity in response to high ambient temperature. We used as a model species striped hamsters (Cricetulus barabensis) that were previously acclimated to room temperature (21 ℃) and warm temperature (32.5 ℃) for 4 weeks and then were acutely exposed to extremely high temperature (37 ℃) for 48 h. The energy intake, metabolic rate, body temperature, mitochondrial respiration rate, and uncoupling protein (UCP) gene (ucp) expression of brown adipose tissue (BAT), liver and skeletal muscle were measured. The levels of protein carbonyl and malondialdehyde (MDA), and the activity of superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) were also determined. The results showed that the acclimation to 32.5℃ and acute exposure to 37℃ resulted in significant reductions in gross and digestive energy intake, basal metabolic rate, and non-shivering thermogenesis. Cytochrome c oxidase (COX) activity was reduced after acclimation to 32.5℃ by 84.2%, 50.0%, and 56.6% in BAT, liver, and muscle, respectively. The liver COX activity decreased further by 23.3% after exposure to 37℃, but COX activity in BAT and muscle was not significantly changed. The acute exposure to 37℃ deceased BAT ucp1 expression by 89.5%, liver ucp2 by 76.2%, and muscle ucp3 by 58.8% in the hamster previously acclimated to 21℃, but it had no significant effect on the gene expression in the hamsters previously acclimated to 32.5℃. Acclimation to 32.5℃ significantly decreased MDA levels in heart, lung, kidney, and muscle, but not in liver and brain, and it significantly increased protein carbonyl levels in the kidney only. Acute exposure to 37℃ significantly reduced protein carbonyl levels in liver and heart, but it had no significant effect on MDA levels in all tissues. In addition, acclimation to 32.5℃ significantly reduced SOD activity in liver and muscle, but did not affect heart, lung, kidney, or brain; and it decreased GSH-Px activity in heart, lung, and kidney, but increased GSH-Px activity in muscle, and had no effect in liver. These findings suggest that (1) the effects of acute exposure to high temperatures on energy metabolism and mitochondrial respiration rate are related to habitat ambient temperature, with the animals at lower ambient temperature being more affected by high temperature; (2) after being acclimated to the warm and acutely exposed to high temperature, the metabolic rate of the organism and mitochondria respiratory decreased, while the liver, heart, lung, kidneys, skeletal muscle, and brain do not show considerable oxidative stress and damage, being inconsistent with the‘free radical hypothesis’ .

Key words: Energy metabolism, High-temperature exposure, Metabolic rate, Oxidative stress, Uncoupling protein, Striped hamsters

摘要: 动物能量代谢的适应性调节影响动物生长、发育、繁殖、衰老等生活史特征。代谢率和组织线粒体呼吸率与自由基水平有关,是影响机体衰老的重要因素。为了探讨高温环境下能量代谢、主要代谢活性器官组织呼吸率、自由基水平和抗氧化能力的内在联系,我们将室温(21℃)和暖温(32.5℃)驯化4周的黑线仓鼠(Cricetulus barabensis)分别进行急性高温暴露(37℃)48 h,分别测定摄入能、代谢率,以及褐色脂肪组织(brown adiposetissue,BAT)、肝脏和肌肉的线粒体呼吸率,解偶联蛋白(uncoupling protein,UCP)基因(ucp)表达,蛋白羰基和丙二醛(malondialdehyde,MDA)水平,以及超氧化物歧化酶(superoxide dismutase,SOD)和谷胱甘肽过氧化物酶(glutathione peroxidase,GSH-Px)活性。结果显示,暖温驯化和急性高温暴露使摄入能、消化能、基础代谢率和非颤抖性产热显著降低。暖温驯化后BAT、肝脏和肌肉的细胞色素c氧化酶(cytochrome c oxidase,COX)活性分别降低了84.2%、50.0%和56.6%,急性高温暴露后肝脏COX活性降低了23.3%,但BAT和肌肉COX活性未发生显著变化。21℃组黑线仓鼠在急性高温暴露后BAT中ucp1表达下调89.5%、肝脏ucp2下调76.2%、肌肉ucp3下调58.8%,而32.5℃组在急性高温暴露后未发生显著变化。暖温驯化使心脏、肺脏、肾脏和肌肉组织MDA水平显著降低,而未影响肝脏和脑MDA水平;使肾脏蛋白羰基水平显著升高,但对其他组织影响不显著。急性高温暴露对各组织MDA水平的影响不显著,但显著降低了肝脏和心脏蛋白羰基水平。暖温驯化使肝脏和肌肉SOD活性显著降低,但未影响心脏、肺脏、肾脏和脑组织SOD活性。暖温驯化使心脏、肺脏、肾脏GSH-Px活性显著降低,使肌肉GSH-Px活性显著升高,而对肝脏无显著影响。结果表明:(1)急性高温暴露对能量代谢和线粒体呼吸率的影响与动物生存的环境温度有关,生存的环境温度越低,受高温的影响越大;(2)在暖温驯化和急性高温暴露条件下,机体代谢率与线粒体呼吸率降低,但心脏、肝脏、肺脏、肾脏、肌肉和脑未出现显著的氧化应激和损伤,与“自由基假说”不一致。

关键词: 能量代谢, 高温暴露, 代谢率, 氧化应激, 解偶联蛋白, 黑线仓鼠

CLC Number: