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Inactivity and Skeletal Muscle Metabolism: A Vicious Cycle in Old Age.

ABSTRACT: Aging is an inevitable and gradually progressive process affecting all organs and systems. The musculoskeletal system makes no exception, elderly exhibit an increased risk of sarcopenia (low muscle mass),dynapenia (declining muscle strength), and subsequent disability. Whereas in recent years the subject of skeletal muscle metabolic decline in the elderly has been gathering interest amongst researchers, as well as medical professionals, there are many challenges yet to be solved in order to counteract the effects of aging on muscle function efficiently. Noteworthy, it has been shown that aging individuals exhibit a decline in skeletal muscle metabolism, a phenomenon which may be linked to a number of predisposing (risk) factors such as telomere attrition, epigenetic changes, mitochondrial dysfunction, sedentary behavior (leading to body composition alterations), age-related low-grade systemic inflammation (inflammaging), hormonal imbalance, as well as a hypoproteic diet (unable to counterbalance the repercussions of the age-related increase in skeletal muscle catabolism). The present review aims to discuss the relationship between old age and muscle wasting in an effort to highlight the modifications in skeletal muscle metabolism associated with aging and physical activity.

SUBMITTER: Rezus E

PROVIDER: S-EPMC7014434 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Inactivity and Skeletal Muscle Metabolism: A Vicious Cycle in Old Age.

Rezuş Elena E Burlui Alexandra A Cardoneanu Anca A Rezuş Ciprian C Codreanu Cătălin C Pârvu Mirela M Rusu Zota Gabriela G Tamba Bogdan Ionel BI

International journal of molecular sciences 20200116 2

Aging is an inevitable and gradually progressive process affecting all organs and systems. The musculoskeletal system makes no exception, elderly exhibit an increased risk of sarcopenia (low muscle mass),dynapenia (declining muscle strength), and subsequent disability. Whereas in recent years the subject of skeletal muscle metabolic decline in the elderly has been gathering interest amongst researchers, as well as medical professionals, there are many challenges yet to be solved in order to coun ...[more]

PMID: 31963330

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Project description:BackgroundLipid hydroperoxides (LOOH) have been implicated in skeletal muscle atrophy with age and disuse. Lysophosphatidylcholine acyltransferase 3 (LPCAT3), an enzyme of the Lands cycle, conjugates a polyunsaturated fatty acyl chain to a lysophospholipid to form a polyunsaturated fatty acid containing phospholipid (PUFA-PL) molecule, providing substrates for LOOH propagation. Previous studies suggest that inhibition of the Lands cycle is an effective strategy to suppress LOOH. Mice with skeletal muscle-specific tamoxifen-inducible knockout of LPCAT3 (LPCAT3-MKO) were utilized to determine if muscle-specific attenuation of LOOH may alleviate muscle atrophy and weakness with disuse.MethodsLPCAT3-MKO and control mice underwent 7 days of sham or hindlimb unloading (HU model) to study muscle mass and force-generating capacity. LOOH was assessed by quantifying 4-hydroxynonenal (4-HNE)-conjugated peptides. Quantitative PCR and lipid mass spectrometry were used to validate LPCAT3 deletion.ResultsSeven days of HU was sufficient to induce muscle atrophy and weakness concomitant to a ~2-fold increase in 4-HNE (P = 0.0069). Deletion of LPCAT3 reversed HU-induced increase in muscle 4-HNE (P = 0.0256). No difference was found in body mass, body composition, or caloric intake between genotypes. The soleus (SOL) and plantaris (PLANT) muscles of the LPCAT3-MKO mice experienced ~15% and ~40% less atrophy than controls, respectively. (P = 0.0011 and P = 0.0265). Type I and IIa SOL myofibers experienced a ~40% decrease in cross sectional area (CSA), which was attenuated to only 15% in the LPCAT3-MKO mice (P = 0.0170 and P = 0.0411, respectively). Strikingly, SOL muscles were fully protected and extensor digitorum longus (EDL) muscles experienced a ~35% protection from HU-induced reduction in force-generating capacity in the LPCAT3-MKO mice compared with controls (P < 0.0001 for both muscles).ConclusionsOur findings demonstrate that attenuation of skeletal muscle lipid hydroperoxides is sufficient to restore its function, in particular a protection from reduction in muscle specific force. Our findings suggest muscle lipid peroxidation contributes to atrophy and weakness induced by disuse in mice.

Project description:Clinical Scenario: Even though chronological aging is an inevitable phenomenological consequence occurring in every living organism, it is biological aging that may be the most significant factor challenging our quality of life. Development of functional limitations, resulting from improper maintenance and restoration of various organ systems, ultimately leads to reduced health and independence. Skeletal muscle is an organ system that, when challenged, is often injured in response to varying stimuli. Overt muscle-strain injury can be traumatic, clinically diagnosable, properly managed, and a remarkably common event, yet our contemporary understanding of how age and environmental stressors affect the initial and subsequent induction of injury and how the biological processes resulting from this event are modifiable and, eventually, lead to functional restoration and healing of skeletal muscle and adjacent tissues is presently unclear. Even though the secondary injury response to and recovery from "contraction-induced" skeletal-muscle injury are impaired with aging, there is no scientific consensus as to the exact mechanism responsible for this event. Given the multitude of investigative approaches, particular consideration given to the appropriateness of the muscle-injury model, or research paradigm, is critical so that outcomes may be physiologically relevant and translational. In this case, methods implementing stretch-shortening contractions, the most common form of muscle movements used by all mammals during physical movement, work, and activity, are highlighted. CLINICAL RELEVANCE:Understanding the fundamental evidence regarding how aging influences the responsivity of skeletal muscle to strain injury is vital for informing how clinicians approach and implement preventive strategies, as well as therapeutic interventions. From a practical perspective, maintaining or improving the overall health and tissue quality of skeletal muscle as one ages will positively affect skeletal muscle's safety threshold and responsivity, which may reduce incidence of injury, improve recovery time, and lessen overall fiscal burdens.

Dataset Information

Inactivity and Skeletal Muscle Metabolism: A Vicious Cycle in Old Age.

Publications

Inactivity and Skeletal Muscle Metabolism: A Vicious Cycle in Old Age.

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