Petrick Heather L, Handy Rachel M, Vachon Bayley, Frangos Sara M, Holwerda Andrew M, Gijsen Annemarie P, Senden Joan M, van Loon Luc J C, Holloway Graham P
Department of Human Health and Nutritional Sciences, University of Guelph, Guelph, Ontario, Canada.
Department of Human Biology, NUTRIM School of Nutrition and Translational Research in Metabolism, Maastricht University Medical Centre+, Maastricht, The Netherlands.
J Physiol. 2023 Jun 9. doi: 10.1113/JP284701.
Skeletal muscle disuse reduces muscle protein synthesis rates and induces atrophy, events associated with decreased mitochondrial respiration and increased reactive oxygen species. Given that dietary nitrate can improve mitochondrial bioenergetics, we examined whether nitrate supplementation attenuates disuse-induced impairments in mitochondrial function and muscle protein synthesis rates. Female C57Bl/6N mice were subjected to single-limb casting (3 or 7 days) and consumed drinking water with or without 1 mM sodium nitrate. Compared with the contralateral control limb, 3 days of immobilization lowered myofibrillar fractional synthesis rates (FSR, P < 0.0001), resulting in muscle atrophy. Although FSR and mitophagy-related proteins were higher in subsarcolemmal (SS) compared with intermyofibrillar (IMF) mitochondria, immobilization for 3 days decreased FSR in both SS (P = 0.009) and IMF (P = 0.031) mitochondria. Additionally, 3 days of immobilization reduced maximal mitochondrial respiration, decreased mitochondrial protein content, and increased maximal mitochondrial reactive oxygen species emission, without altering mitophagy-related proteins in muscle homogenate or isolated mitochondria (SS and IMF). Although nitrate consumption did not attenuate the decline in muscle mass or myofibrillar FSR, intriguingly, nitrate completely prevented immobilization-induced reductions in SS and IMF mitochondrial FSR. In addition, nitrate prevented alterations in mitochondrial content and bioenergetics after both 3 and 7 days of immobilization. However, in contrast to 3 days of immobilization, nitrate did not prevent the decline in SS and IMF mitochondrial FSR after 7 days of immobilization. Therefore, although nitrate supplementation was not sufficient to prevent muscle atrophy, nitrate may represent a promising therapeutic strategy to maintain mitochondrial bioenergetics and transiently preserve mitochondrial protein synthesis rates during short-term muscle disuse. KEY POINTS: Alterations in mitochondrial bioenergetics (decreased respiration and increased reactive oxygen species) are thought to contribute to muscle atrophy and reduced protein synthesis rates during muscle disuse. Given that dietary nitrate can improve mitochondrial bioenergetics, we examined whether nitrate supplementation could attenuate immobilization-induced skeletal muscle impairments in female mice. Dietary nitrate prevented short-term (3 day) immobilization-induced declines in mitochondrial protein synthesis rates, reductions in markers of mitochondrial content, and alterations in mitochondrial bioenergetics. Despite these benefits and the preservation of mitochondrial content and bioenergetics during more prolonged (7 day) immobilization, nitrate consumption did not preserve skeletal muscle mass or myofibrillar protein synthesis rates. Overall, although dietary nitrate did not prevent atrophy, nitrate supplementation represents a promising nutritional approach to preserve mitochondrial function during muscle disuse.
骨骼肌废用会降低肌肉蛋白质合成速率并导致萎缩,这些事件与线粒体呼吸减少和活性氧增加有关。鉴于膳食硝酸盐可改善线粒体生物能量学,我们研究了补充硝酸盐是否能减轻废用引起的线粒体功能和肌肉蛋白质合成速率损伤。雌性C57Bl/6N小鼠进行单肢固定(3天或7天),饮用含或不含1 mM硝酸钠的水。与对侧对照肢体相比,固定3天降低了肌原纤维分数合成速率(FSR,P < 0.0001),导致肌肉萎缩。尽管与肌原纤维间(IMF)线粒体相比,肌膜下(SS)线粒体中的FSR和与线粒体自噬相关的蛋白质更高,但固定3天降低了SS(P = 0.009)和IMF(P = 0.031)线粒体中的FSR。此外,固定3天降低了最大线粒体呼吸,减少了线粒体蛋白质含量,并增加了最大线粒体活性氧释放,而未改变肌肉匀浆或分离线粒体(SS和IMF)中与线粒体自噬相关的蛋白质。尽管摄入硝酸盐并未减轻肌肉质量或肌原纤维FSR的下降,但有趣的是,硝酸盐完全阻止了固定引起的SS和IMF线粒体FSR降低。此外,硝酸盐在固定3天和7天后均阻止了线粒体含量和生物能量学的改变。然而,与固定3天不同,硝酸盐未能阻止固定7天后SS和IMF线粒体FSR的下降。因此,尽管补充硝酸盐不足以预防肌肉萎缩,但硝酸盐可能是一种有前景的治疗策略,可在短期肌肉废用期间维持线粒体生物能量学并短暂保持线粒体蛋白质合成速率。要点:线粒体生物能量学的改变(呼吸减少和活性氧增加)被认为是导致肌肉废用期间肌肉萎缩和蛋白质合成速率降低的原因。鉴于膳食硝酸盐可改善线粒体生物能量学,我们研究了补充硝酸盐是否能减轻雌性小鼠固定引起的骨骼肌损伤。膳食硝酸盐可预防短期(3天)固定引起的线粒体蛋白质合成速率下降、线粒体含量标志物减少以及线粒体生物能量学改变。尽管有这些益处以及在更长时间(7天)固定期间线粒体含量和生物能量学得以保留,但摄入硝酸盐并不能保留骨骼肌质量或肌原纤维蛋白质合成速率。总体而言,尽管膳食硝酸盐不能预防萎缩,但补充硝酸盐是在肌肉废用期间保留线粒体功能的一种有前景的营养方法。