Exercise conditioning in old mice improves skeletal muscle regeneration

Joanisse, Sophie; Nederveen, Joshua P.; Baker, Jeff; Snijders, Tim; Iacono, Carlo; Parise, Gianni

doi:10.1096/fj.201600143rr

Cited by 60 publications

(59 citation statements)

References 46 publications

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“…This suggests that regeneration is delayed as a response to CR 49 , but why this did not occur at other timepoints is not clear. The notexin injection in these 22 month CR mice elicited less widespread TA muscle injury than in the 6 month CR mice, which may explain the difference.…”

Section: Discussionmentioning

confidence: 96%

“…C57Bl/6 is a commonly used mouse for many studies, including ageing, response to dietary intervention 47 and studies on satellite cells and muscle regeneration 8, 20, 48, 49 , but it should be borne in mind that there may be mutations that act as genetic modifiers to affect the outcome of experiments 50 . Studies on muscle regeneration have been done on C57Bl/6 mice of different sexes 51–54 .…”

Section: Discussionmentioning

confidence: 99%

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The effect of calorie restriction on mouse skeletal muscle is sex, strain and time-dependent

Boldrin¹,

Ross

Whitmore

et al. 2017

Sci Rep

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Loss of skeletal muscle mass and function occurs with increasing age. Calorie restriction (CR) increases the lifespan of C57Bl/6 mice, but not in the shorter-lived DBA/2 strain. There is some evidence that calorie restriction reduces or delays many of the age-related defects that occur in rodent skeletal muscle. We therefore investigated the effect of short (2.5 month) and longer term (8.5 and 18.5 months) CR on skeletal muscle in male and female C57Bl/6 and DBA/2 mice. We found that short-term CR increased the satellite cell number and collagen VI content of muscle, but resulted in a delayed regenerative response to injury.Consistent with this, the in vitro proliferation of satellite cells derived from these muscles was reduced by CR. The percentage of stromal cells, macrophages, hematopoietic stem cells and fibroadipogenic cells in the mononucleated cell population derived from skeletal muscle was reduced by CR at various stages. But overall, these changes are neither consistent over time, nor between strain and sex. The fact that changes induced by CR do not persist with time and the dissimilarities between the two mouse strains, combined with sex differences, urge caution in applying CR to improve skeletal muscle function across the lifespan in humans.

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Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

The effect of calorie restriction on mouse skeletal muscle is sex, strain and time-dependent

Boldrin¹,

Ross

Whitmore

et al. 2017

Sci Rep

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“…Later, this finding was substantiated by work demonstrating that old mice fail to re-establish fibre area 30 days after injury [24,25]. Others have also demonstrated that the early phases of muscle regeneration are also impaired in old compared with young rodents [26,27].…”

Section: Sc and Impaired Muscle Fibre Regeneration Repair And Remodementioning

confidence: 92%

Skeletal Muscle Regeneration, Repair and Remodelling in Aging: The Importance of Muscle Stem Cells and Vascularization

et al. 2016

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Sarcopenia is the age-related loss of skeletal muscle mass and strength. Ultimately, sarcopenia results in the loss of independence, which imposes a large financial burden on healthcare systems worldwide. A critical facet of sarcopenia is the diminished ability for aged muscle to regenerate, repair and remodel. Over the years, research has focused on elucidating underlying mechanisms of sarcopenia and the impaired ability of muscle to respond to stimuli with aging. Muscle-specific stem cells, termed satellite cells (SC), play an important role in maintaining muscle health throughout the lifespan. It is well established that SC are essential in skeletal muscle regeneration, and it has been hypothesized that a reduction and/or dysregulation of the SC pool, may contribute to accelerated loss of skeletal muscle mass that is observed with advancing age. The preservation of skeletal muscle tissue and its ability to respond to stimuli may be impacted by reduced SC content and impaired function observed with aging. Aging is also associated with a reduction in capillarization of skeletal muscle. We have recently demonstrated that the distance between type II fibre-associated SC and capillaries is greater in older compared to younger adults. The greater distance between SC and capillaries in older adults may contribute to the dysregulation in SC activation ultimately impairing muscle's ability to remodel and, in extreme circumstances, regenerate. This viewpoint will highlight the importance of optimal SC activation in addition to skeletal muscle capillarization to maximize the regenerative potential of skeletal muscle in older adults.

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“…Specifically, aged mice submitted to 8-week progressive exercise training (8.5-15 mÁmin À1 , 40 min per session, 3 days a week) showed comparable skeletal muscle regeneration (e.g., assessed by cross-sectional area) with wild-type mice 28 days after cardiotoxin injury [78]. Also, aged mice that performed the exercise training showed more regenerating fibers (e.g., fibers with centrally located nuclei) when compared with the aged group that remained sedentary [78]. This improvement was followed by increased number of Pax7+ cells per muscle fiber and reduced collagen deposition (although not significantly) in the skeletal muscle of the aged exercised mice, suggesting that an enhanced niche improves the satellite cell function.…”

Section: Macrophage Imbalance In Chronic Inflammation and Skeletal Mumentioning

confidence: 96%

“…In general, physical exercise seems to reduce both phenotypes of the infiltrated macrophages in the skeletal muscle [31] or leads to an increase in M2 macrophages [32]. Additionally, although no study has showed the effects of physical exercise in the frequency of FAPs in the skeletal muscle so far, fibrosis markers are reduced after physical exercise in aging [78] and idiopathic inflammatory myopathies [23].…”

Section: Macrophage Imbalance In Chronic Inflammation and Skeletal Mumentioning

confidence: 99%

Chronic inflammation in skeletal muscle impairs satellite cells function during regeneration: can physical exercise restore the satellite cell niche?

et al. 2018

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Chronic inflammation impairs skeletal muscle regeneration. Although many cells are involved in chronic inflammation, macrophages seem to play an important role in impaired muscle regeneration since these cells are associated with skeletal muscle stem cell (namely, satellite cells) activation and fibro-adipogenic progenitor cell (FAP) survival. Specifically, an imbalance of M1 and M2 macrophages seems to lead to impaired satellite cell activation, and these are the main cells that function during skeletal muscle regeneration, after muscle damage. Additionally, this imbalance leads to the accumulation of FAPs in skeletal muscle, with aberrant production of pro-fibrotic factors (e.g., extracellular matrix components), impairing the niche for proper satellite cell activation and differentiation. Treatments aiming to block the inflammatory pro-fibrotic response are partially effective due to their side effects. Therefore, strategies reverting chronic inflammation into a pro-regenerative pattern are required. In this review, we first describe skeletal muscle resident macrophage ontogeny and homeostasis, and explain how macrophages are replenished after muscle injury. We next discuss the potential role of chronic physical activity and exercise in restoring the M1 and M2 macrophage balance and consequently, the satellite cell niche to improve skeletal muscle regeneration after injury.

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Exercise conditioning in old mice improves skeletal muscle regeneration

Abstract: Skeletal muscle possesses the ability to regenerate after injury, but this ability is impaired or delayed with aging.

Cited by 60 publications

References 46 publications

The effect of calorie restriction on mouse skeletal muscle is sex, strain and time-dependent

The effect of calorie restriction on mouse skeletal muscle is sex, strain and time-dependent

Skeletal Muscle Regeneration, Repair and Remodelling in Aging: The Importance of Muscle Stem Cells and Vascularization

Chronic inflammation in skeletal muscle impairs satellite cells function during regeneration: can physical exercise restore the satellite cell niche?

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