Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging
Abstract
:1. Introduction
Oxidative Stress and Inflammation, Constituents of the Background of Aging
2. Aging-Related Changes in Skeletal Muscle and Cardiovascular System
2.1. Skeletal Muscle
2.1.1. Anabolic Resistance
2.1.2. Mitochondrial Dysfunction
2.1.3. Oxidative Stress
2.1.4. Inflammation
2.1.5. Myokines
2.2. Cardiovascular System
2.2.1. Oxidative Stress
2.2.2. Inflammation
3. Impact of Physical Activity/Exercise on Aged Skeletal Muscle and Cardiovascular System
3.1. Skeletal Muscle
3.2. Cardiovascular System
4. Impact of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging
4.1. Skeletal Muscle
4.2. Cardiovascular System
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Biological System | Signaling Pathway | Tissue Effect | Evidence in Animals | Evidence in Humans | Effect of Exercise |
---|---|---|---|---|---|
Skeletal muscle | Increased ROS/RNS | Cellular damage Defective redox signaling Increased proteolysis | SOD-1 KO mice lost muscle mass and function [77] | Signals of increased oxidative stress was related to functional outcomes in the elderly [26] | Increased catalase expression in trained older subjects [218] Exercise increased SOD and GPX [219] Decreased oxidative stress by exercise was associated with muscle size and strength in older individuals with COPD [217] |
Reduced PGC-1α | Reduced mitochondrial biogenesis Mitochondrial dysfunction | Associated with sarcopenia in mice [59] | PGC-1α was related to reduced physical activity and muscle atrophy in older humans [57,61] | Endurance exercise induced PGC-1α expression in skeletal muscle in aged animals and humans [223] 12-weeks resistance training increased PGC-1α levels in elderly men [225] | |
Reduced Nrf2 | Increased oxidative stress | Reduced muscle strength and increased fatigue in mice [75,76] | Positive association of Nrf2 with gait speed in older subjects [82] | Long-term exercise increased Nrf2 expression in aged mice related to attenuation of sarcopenia phenotype in vivo [226] Physical activity increased Nrf2 expression promoting protection against ROS-induced damage in skeletal muscle [227,228] | |
Vascular system | Increased ROS/RNS | Reduced NO availability | Inhibition of peroxynitrite normalized vasorelaxation in resistance arteries of aged rats [122] | Increased superoxide anion and peroxynitrite were detected in aged human vessels with defective endothelial vasodilation [121] | Expression of SOD2 and activity of SOD3 were greater in exercising vs. sedentary older subjects [249] |
Uncoupled eNOS/BH4 deficiency | Reduced NO availability Increased ROS production | Reduced levels of BH4 were associated with impaired endothelial vasodilation in aged rat arterioles [123] | Vascular reduction in BH4 was related to arterial stiffness and endothelial dysfunction in postmenopausal women [124] | Old age reduced and exercise training restored levels of BH4 in rat soleus feed arterioles related to improved flow-mediated dilation [252] | |
Increased NOX | Increased ROS production | Age-dependent increase in blood pressure, cardiomyocyte hypertrophy, coronary remodeling and cardiac fibrosis was associated with increased NOX2 activity [130] Attenuation of NOX activity improved endothelial dysfunction in aged coronary arteries [126] | NOX was overexpressed in arteries from older subjects while NOX inhibition improved endothelial vasodilation [121] | Exercise was related to reduced endothelial NOX expression in elderly subjects [249] | |
Reduced Nrf2 | Defective antioxidant response Increased oxidative damage | Increased oxidative stress in hearts from old mice correlates with Nrf2 dysregulation and is reversed by sulforaphane [81] | Short-term pharmacological activation decreased age-related impairment of endothelium-dependent and ROS-induced vasodilation in rat and human vascular tissues [132] | Exercise increases Nrf2 expression in mouse cardiac fibroblasts [259] and in human peripheral blood mononuclear cells [230] |
Biological System | Signaling Pathway | Tissue Effect | Evidence in Animals | Evidence in Humans | Effect of Exercise |
---|---|---|---|---|---|
Skeletal muscle | Increased pro-inflammatory cytokines | Muscle inflammation (increased NF-κB) Increased proteolysis | Blockade of TNF-α prevents sarcopenia in aged mice [82] | Increased TNF-α and IL-6 correlates with muscle mass loss in older subjects [90]. Associated with poor physical performance and reduced muscular strength in older subjects [85] | Multicomponent exercise program downregulated expressions of IL-6 and TNF-α in frail obese elderly subjects [232] Physical activity resulted in a reduction in systemic concentrations of IL-6, TNF-α, CRP in middle aged and older subjects and postmenopausal women [233,234] Moderate-intensity aerobic exercise reduced the expression of inflammasome constituents (NLRP3, TLR4) and IL-1β, IL-6, and TNF-α [235] |
Reduced anti-inflammatory cytokines | Muscle inflammation | Muscle overexpression of IL-10 was associated with a low level of muscle inflammation and insulin resistance [94] IL-10 KO mice was proposed as a model of frailty with reduced muscle strength [95] | Increased IL-6/IL-10 ratio in older subjects with sarcopenia [92] | Physical activity was associated with higher levels of IL-10 and adiponectin [236] | |
Myokine alteration | Apelin increases mitocondriogenesis and reduces inflammation Myostatin inhibits muscle synthesis and promotes muscle catabolism and is inhibited by follistatin Adiponectin increases mitochondrial function and augments oxidative fibers Irisin improves mitochondrial function decreases ROS production and protects skeletal muscle from metabolic stresses | Apelin restoration prevented muscle wasting in aged mice [92] Adiponectin signaling improves skeletal muscle function in aged mice [97] | Elevated myostatin has been related to sarcopenia in humans [43] Circulating irisin was decreased in older subjects losing muscle strength [243] | Serum irisin levels increased in response to exercise in aged humans [243] Improvement in muscle strength by resistance training was related to decreased myostatin and increased follistatin in sarcopenic older adults [244] Production of apelin in response to muscle contraction contributes to the positive feedback of physical activity and muscle function [98] | |
Vascular system | Activated NF-κB | Vascular inflammation Transcription of inflammatory cytokines and mediators of inflammation Vascular remodeling | Inhibition of vascular NF-κB improved blood flow regulation and decreased systemic inflammation [126] | Enhanced activation of NF-κB in vessels from aged humans which correlated with endothelial dysfunction [121] | Voluntary wheel running by old mice decreased aortic NF-κB activation [248] |
Increased pro-inflammatory cytokines | Endothelial dysfunction Vascular remodeling | Abrogation of inflammasome (NLRP3) preserved cardiac function in old mice and increased the lifespan [137] Anti-inflammatory cytokine, IL-37, improved vascular endothelial function in old mice [142] | CRP and IL-6 have been positively related to aortic stiffness and inversely correlated to endothelial function in older adults [125] | Voluntary wheel running by old mice decreased aortic expression of inflammatory cytokines and macrophage infiltration and reversed impaired NO-mediated endothelial dilation [248] | |
Myokine alteration | Irisin improves vascular function Apelin could increase NO production | Higher concentrations of irisin were detected in centenarian people without CVD [113] | Aerobic exercise training increased apelin concentrations along with higher NO production and lower aortic stiffness in middle-aged and older subjects [254] |
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El Assar, M.; Álvarez-Bustos, A.; Sosa, P.; Angulo, J.; Rodríguez-Mañas, L. Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging. Int. J. Mol. Sci. 2022, 23, 8713. https://doi.org/10.3390/ijms23158713
El Assar M, Álvarez-Bustos A, Sosa P, Angulo J, Rodríguez-Mañas L. Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging. International Journal of Molecular Sciences. 2022; 23(15):8713. https://doi.org/10.3390/ijms23158713
Chicago/Turabian StyleEl Assar, Mariam, Alejandro Álvarez-Bustos, Patricia Sosa, Javier Angulo, and Leocadio Rodríguez-Mañas. 2022. "Effect of Physical Activity/Exercise on Oxidative Stress and Inflammation in Muscle and Vascular Aging" International Journal of Molecular Sciences 23, no. 15: 8713. https://doi.org/10.3390/ijms23158713