NextGen Precision Health, University of Missouri System, Columbia, MO, USA; Department of Physical Medicine and Rehabilitation University of Missouri, Columbia, MO, USA.
Ohio Musculoskeletal and Neurological Institute (OMNI) Ohio University, Athens, OH, USA; Department of Biomedical Sciences, Ohio University, Athens, OH, USA.
Ageing Res Rev. 2023 Aug;89:101966. doi: 10.1016/j.arr.2023.101966. Epub 2023 Jun 1.
Sarcopenia, or age-related decline in muscle form and function, exerts high personal, societal, and economic burdens when untreated. Integrity and function of the neuromuscular junction (NMJ), as the nexus between the nervous and muscular systems, is critical for input and dependable neural control of muscle force generation. As such, the NMJ has long been a site of keen interest in the context of skeletal muscle function deficits during aging and in the context of sarcopenia. Historically, changes of NMJ morphology during aging have been investigated extensively but primarily in aged rodent models. Aged rodents have consistently shown features of NMJ endplate fragmentation and denervation. Yet, the presence of NMJ changes in older humans remains controversial, and conflicting findings have been reported. This review article describes the physiological processes involved in NMJ transmission, discusses the evidence that supports NMJ transmission failure as a possible contributor to sarcopenia, and speculates on the potential of targeting these defects for therapeutic development. The technical approaches that are available for assessment of NMJ transmission, whether each approach has been applied in the context of aging and sarcopenia, and the associated findings are summarized. Like morphological studies, age-related NMJ transmission deficits have primarily been studied in rodents. In preclinical studies, isolated synaptic electrophysiology recordings of endplate currents or potentials have been mostly used, and paradoxically, have shown enhancement, rather than failure, with aging. Yet, in vivo assessment of single muscle fiber action potential generation using single fiber electromyography and nerve-stimulated muscle force measurements show evidence of NMJ failure in aged mice and rats. Together these findings suggest that endplate response enhancement may be a compensatory response to post-synaptic mechanisms of NMJ transmission failure in aged rodents. Possible, but underexplored, mechanisms of this failure are discussed including the simplification of post-synaptic folding and altered voltage-gated sodium channel clustering or function. In humans, there is limited clinical data that has selectively investigated single synaptic function in the context of aging. If sarcopenic older adults turn out to exhibit notable impairments in NMJ transmission (this has yet to be examined but based on available evidence appears to be plausible) then these NMJ transmission defects present a well-defined biological mechanism and offer a well-defined pathway for clinical implementation. Investigation of small molecules that are currently available clinically or being testing clinically in other disorders may provide a rapid route for development of interventions for older adults impacted by sarcopenia.
肌肉减少症,或与年龄相关的肌肉形态和功能下降,如果不加以治疗,会给个人、社会和经济带来沉重负担。神经肌肉接头(NMJ)的完整性和功能是神经系统和肌肉系统之间的连接,对于肌肉力量产生的输入和可靠的神经控制至关重要。因此,NMJ 一直是骨骼肌肉功能随着年龄衰退以及肌肉减少症研究的重点。从历史上看,NMJ 形态在衰老过程中的变化已经被广泛研究,但主要是在老年啮齿动物模型中。老年啮齿动物一直表现出 NMJ 终板碎片化和去神经支配的特征。然而,老年人 NMJ 变化的存在仍然存在争议,并且有相互矛盾的发现报告。本文综述了 NMJ 传递过程中的生理过程,讨论了支持 NMJ 传递失败可能是肌肉减少症的一个促成因素的证据,并推测了针对这些缺陷进行治疗开发的可能性。本文还概述了用于评估 NMJ 传递的技术方法,每种方法是否已应用于衰老和肌肉减少症的背景下,以及相关发现。与形态学研究一样,与年龄相关的 NMJ 传递缺陷主要在啮齿动物中进行了研究。在临床前研究中,主要使用了分离突触电生理学记录终板电流或电位的方法,具有讽刺意味的是,这些方法随着年龄的增长显示出增强,而不是失败。然而,使用单纤维肌电图和神经刺激肌肉力量测量来评估单个肌肉纤维动作电位的产生,表明 NMJ 在老年小鼠和大鼠中失败。这些发现表明,终板反应增强可能是老年啮齿动物 NMJ 传递失败的突触后机制的代偿反应。讨论了这种失败的可能机制,但尚未探索,包括突触后折叠的简化以及电压门控钠通道聚集或功能的改变。在人类中,关于衰老背景下单个突触功能的临床数据有限。如果肌肉减少症的老年人表现出明显的 NMJ 传递受损(这尚未得到检验,但根据现有证据似乎是合理的),那么这些 NMJ 传递缺陷提供了一个明确的生物学机制,并为临床实施提供了一个明确的途径。目前临床上可用或其他疾病中正在进行临床试验的小分子的研究可能为受肌肉减少症影响的老年人开发干预措施提供快速途径。