Tokarska-Schlattner Malgorzata, Kay Laurence, Perret Pascale, Isola Raffaella, Attia Stéphane, Lamarche Frédéric, Tellier Cindy, Cottet-Rousselle Cécile, Uneisi Amjad, Hininger-Favier Isabelle, Foretz Marc, Dubouchaud Hervé, Ghezzi Catherine, Zuppinger Christian, Viollet Benoit, Schlattner Uwe
Inserm U1055, Laboratory of Fundamental and Applied Bioenergetics (LBFA), University of Grenoble Alpes, Grenoble, France.
Inserm U1039, Radiopharmaceutiques Biocliniques, Faculté de Médecine, University of Grenoble Alpes, Grenoble, France.
Front Cell Dev Biol. 2021 Oct 18;9:731015. doi: 10.3389/fcell.2021.731015. eCollection 2021.
AMP-activated protein kinase (AMPK) is a key regulator of energy homeostasis under conditions of energy stress. Though heart is one of the most energy requiring organs and depends on a perfect match of energy supply with high and fluctuating energy demand to maintain its contractile performance, the role of AMPK in this organ is still not entirely clear, in particular in a non-pathological setting. In this work, we characterized cardiomyocyte-specific, inducible AMPKα1 and α2 knockout mice (KO), where KO was induced at the age of 8 weeks, and assessed their phenotype under physiological conditions. In the heart of KO mice, both AMPKα isoforms were strongly reduced and thus deleted in a large part of cardiomyocytes already 2 weeks after tamoxifen administration, persisting during the entire study period. AMPK KO had no effect on heart function at baseline, but alterations were observed under increased workload induced by dobutamine stress, consistent with lower endurance exercise capacity observed in AMPK KO mice. AMPKα deletion also induced a decrease in basal metabolic rate (oxygen uptake, energy expenditure) together with a trend to lower locomotor activity of AMPK KO mice 12 months after tamoxifen administration. Loss of AMPK resulted in multiple alterations of cardiac mitochondria: reduced respiration with complex I substrates as measured in isolated mitochondria, reduced activity of complexes I and IV, and a shift in mitochondrial cristae morphology from lamellar to mixed lamellar-tubular. A strong tendency to diminished ATP and glycogen level was observed in older animals, 1 year after tamoxifen administration. Our study suggests important roles of cardiac AMPK at increased cardiac workload, potentially limiting exercise performance. This is at least partially due to impaired mitochondrial function and bioenergetics which degrades with age.
AMP激活的蛋白激酶(AMPK)是能量应激条件下能量稳态的关键调节因子。尽管心脏是最需要能量的器官之一,依赖于能量供应与高且波动的能量需求完美匹配以维持其收缩功能,但AMPK在该器官中的作用仍不完全清楚,尤其是在非病理状态下。在这项研究中,我们对心肌细胞特异性、可诱导的AMPKα1和α2基因敲除小鼠(KO)进行了表征,其中KO在8周龄时诱导产生,并评估了它们在生理条件下的表型。在KO小鼠的心脏中,两种AMPKα亚型均显著减少,因此在给予他莫昔芬后仅2周,大部分心肌细胞中的该亚型就已缺失,并在整个研究期间持续存在。AMPK基因敲除在基线时对心脏功能没有影响,但在多巴酚丁胺应激诱导的工作量增加情况下观察到了变化,这与在AMPK基因敲除小鼠中观察到的耐力运动能力降低一致。在给予他莫昔芬12个月后,AMPKα缺失还导致基础代谢率(摄氧量、能量消耗)降低,同时AMPK基因敲除小鼠的运动活动有降低趋势。AMPK缺失导致心脏线粒体发生多种改变:在分离的线粒体中测量,以复合体I底物进行的呼吸作用降低,复合体I和IV的活性降低,线粒体嵴形态从板层状转变为混合的板层 - 管状。在给予他莫昔芬1年后的老年动物中,观察到ATP和糖原水平有显著降低的趋势。我们的研究表明,心脏AMPK在心脏工作量增加时发挥重要作用,可能会限制运动表现。这至少部分是由于线粒体功能和生物能量学受损,且随着年龄增长而退化。