Effects of aging and maternal protein restriction on the muscle fibers morphology and neuromuscular junctions of rats after nutritional recovery

Confortim, Heloísa Deola; Jerônimo, Leslie Cazetta; Centenaro, Lígia Aline; Pinheiro, Patrícia Fernanda Felipe; Brancalhão, Rose Meire Costa; Matheus, Selma Maria Michelin; Torrejais, Márcia Miranda

doi:10.1016/j.micron.2014.12.006

Cited by 17 publications

(13 citation statements)

References 34 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As with the restriction of total energy, these observations were fibre type and muscle group dependent where the number and density of fast‐twitch fibres in the soleus were found to be reduced in the offspring after early (0–7 days), mid (8–14 days)‐ and late (15–22 days) restriction, whereas in the gastrocnemius, only a reduction in the density of slow‐twitch fibres occurred at mid (8–14 days)‐restriction (Mallinson et al ., ). A more recent study suggested that a more severe maternal protein restriction at mid (7–14 days)‐gestation (6% of total calories from protein vs. 17% in control group) reduced type I fibre diameter by 20% together with a reduction in type IIa fibres by 5%, while type IIb fibres actually increased by 5% vs. the aged matched control group in aged rat offspring (365 days old) (Confortim et al ., ). Finally, in the same study it was shown that protein restriction during gestation results in a reduction in size of neuromuscular junctions; as age‐related decline in muscle is associated with denervation (Confortim et al ., ), these fascinating findings suggest an important role for early‐life encounters on muscle size and function into old age, which is discussed later in this review.…”

Section: Emergence Of Evidence For Skeletal Muscle Memorymentioning

confidence: 97%

“…A more recent study suggested that a more severe maternal protein restriction at mid (7–14 days)‐gestation (6% of total calories from protein vs. 17% in control group) reduced type I fibre diameter by 20% together with a reduction in type IIa fibres by 5%, while type IIb fibres actually increased by 5% vs. the aged matched control group in aged rat offspring (365 days old) (Confortim et al ., ). Finally, in the same study it was shown that protein restriction during gestation results in a reduction in size of neuromuscular junctions; as age‐related decline in muscle is associated with denervation (Confortim et al ., ), these fascinating findings suggest an important role for early‐life encounters on muscle size and function into old age, which is discussed later in this review. Therefore once again, although there are some discrepancies in the specific fibre‐type changes following protein restriction, on a background of differences in muscle groups studied, timing of protein restriction and sampling of the offspring, it is clear that the general consensus is that muscle size is reduced following maternal protein restriction.…”

Section: Emergence Of Evidence For Skeletal Muscle Memorymentioning

confidence: 97%

See 1 more Smart Citation

Does skeletal muscle have an ‘epi’‐memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise

2016

View full text Add to dashboard Cite

SummarySkeletal muscle mass, quality and adaptability are fundamental in promoting muscle performance, maintaining metabolic function and supporting longevity and healthspan. Skeletal muscle is programmable and can ‘remember’ early‐life metabolic stimuli affecting its function in adult life. In this review, the authors pose the question as to whether skeletal muscle has an ‘epi’‐memory? Following an initial encounter with an environmental stimulus, we discuss the underlying molecular and epigenetic mechanisms enabling skeletal muscle to adapt, should it re‐encounter the stimulus in later life. We also define skeletal muscle memory and outline the scientific literature contributing to this field. Furthermore, we review the evidence for early‐life nutrient stress and low birth weight in animals and human cohort studies, respectively, and discuss the underlying molecular mechanisms culminating in skeletal muscle dysfunction, metabolic disease and loss of skeletal muscle mass across the lifespan. We also summarize and discuss studies that isolate muscle stem cells from different environmental niches in vivo (physically active, diabetic, cachectic, aged) and how they reportedly remember this environment once isolated in vitro. Finally, we will outline the molecular and epigenetic mechanisms underlying skeletal muscle memory and review the epigenetic regulation of exercise‐induced skeletal muscle adaptation, highlighting exercise interventions as suitable models to investigate skeletal muscle memory in humans. We believe that understanding the ‘epi’‐memory of skeletal muscle will enable the next generation of targeted therapies to promote muscle growth and reduce muscle loss to enable healthy aging.

show abstract

Section: Emergence Of Evidence For Skeletal Muscle Memorymentioning

confidence: 97%

Section: Emergence Of Evidence For Skeletal Muscle Memorymentioning

confidence: 97%

Does skeletal muscle have an ‘epi’‐memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise

2016

View full text Add to dashboard Cite

show abstract

“…It was indicated that some effects of prior training were retained and attenuated the responses to unloading in fast-twitch muscles, in which the epigenetic changes were induced by running training. Interestingly, maternal protein restriction during gestation decreased the size of type I fibers, while that of type IIb fibers increased, in aged offspring (7). These type-specific effects remaining within skeletal muscles throughout a lifetime also imply different epigenetic mechanisms underlying the adaptation of fast-twitch and slow-twitch muscles.…”

Section: Responses To Unloadingmentioning

confidence: 99%

“…Liu et al (26) reported that a low-protein maternal diet in pigs increased the gene expression of myostatin, which is known to be a negative regulator of muscle mass, and its receptor in 35-day-old offspring, suggesting that alterations in protein synthetic/degradative pathways in utero impact muscle composition in later life. Furthermore, it was reported that severe protein restriction at midgestation reduced the diameter of type I fibers in aged rat offspring (7). Hypertension, insulin resistance, and obesity were observed in the adult offspring of obese mice (37,40).…”

mentioning

confidence: 97%

Running training experience attenuates disuse atrophy in fast-twitch skeletal muscles of rats

Nakamura

Ohsawa

Masuzawa

et al. 2017

Journal of Applied Physiology

View full text Add to dashboard Cite

Responsiveness to physiological stimuli, such as exercise and muscular inactivation, differs in individuals. However, the mechanisms responsible for these individual differences remain poorly understood. We tested whether a prior experience of exercise training affects the responses of skeletal muscles to unloading. Young rats were assigned to perform daily running training with a treadmill for 8 wk. After an additional 8 wk of normal habitation, the rats were hindlimb unloaded by tail suspension for 1 wk. Fast-twitch plantaris, gastrocnemius, and tibialis anterior muscles did not atrophy after unloading in rats with training experience, although soleus muscle lost weight similar to sedentary rats. We also analyzed the transcriptome in plantaris muscle with RNA sequencing followed by hierarchical clustering analysis and found that a subset of genes that were generally upregulated in sedentary rats after unloading were less responsive in rats with training experience. The distribution of histone 3 was diminished at the loci of these genes during the training period. Although the deposition of histone 3 was restored after an additional period of normal habitation, the incorporation of H3.3 variant was promoted in rats with training experience. This remodeling of nucleosomes closely correlated to the conformational changes of chromatin and suppressed gene expression in response to unloading. These results suggest that exercise training stimulated the early turnover of histone components, which may alter the responsiveness of gene transcription to physiological stimuli. The present study demonstrates that disuse atrophy was suppressed in fast-twitch skeletal muscles of rats with training experience in early life. We also found a subset of genes that were less responsive to unloading in the muscle of rats with training experience. It was further determined that exercise training caused an early turnover of nucleosome components, which may alter the responsiveness of genes to stimulus in later life.

show abstract

“…This is highlighted in studies of ovine fetuses (Zhu et al, 2004) and offspring (Zhu et al, 2006) exposed to a suboptimal in utero environment, which demonstrate low birth weight as well as dysregulation of muscle development, including changes in the number and composition of myofibers. Numbers of myofibers and neuromuscular junctions are also altered in a rat model of maternal protein restriction (Confortim et al, 2016) and this effect is long-lasting, into old age (Confortim et al, 2015). There is also evidence that a suboptimal early environment (nutrient restriction) in the mouse can impact on muscle metabolism/function and molecular changes, including decreased mitochondrial content (Beauchamp et al, 2015) and reduced expression of mitochondrial genes, especially those involved in oxidative phosphorylation (Mortensen et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Poor maternal nutrition and accelerated postnatal growth induces an accelerated aging phenotype and oxidative stress in skeletal muscle of male rats

Tarry-Adkins

Fernandez‐Twinn

Chen

et al. 2016

Disease Models &Amp; Mechanisms

View full text Add to dashboard Cite

ABSTRACT‘Developmental programming’, which occurs as a consequence of suboptimal in utero and early environments, can be associated with metabolic dysfunction in later life, including an increased incidence of cardiovascular disease and type 2 diabetes, and predisposition of older men to sarcopenia. However, the molecular mechanisms underpinning these associations are poorly understood. Many conditions associated with developmental programming are also known to be associated with the aging process. We therefore utilized our well-established rat model of low birth weight and accelerated postnatal catch-up growth (termed ‘recuperated’) in this study to establish the effects of suboptimal maternal nutrition on age-associated factors in skeletal muscle. We demonstrated accelerated telomere shortening (a robust marker of cellular aging) as evidenced by a reduced frequency of long telomeres (48.5-8.6 kb) and an increased frequency of short telomeres (4.2-1.3 kb) in vastus lateralis muscle from aged recuperated offspring compared to controls. This was associated with increased protein expression of the DNA-damage-repair marker 8-oxoguanine-glycosylase (OGG1) in recuperated offspring. Recuperated animals also demonstrated an oxidative stress phenotype, with decreased citrate synthase activity, increased electron-transport-complex activities of complex I, complex II-III and complex IV (all markers of functional mitochondria), and increased xanthine oxidase (XO), p67phox and nuclear-factor kappa-light-chain-enhancer of activated B-cells (NF-κB). Recuperated offspring also demonstrated increased antioxidant defense capacity, with increased protein expression of manganese superoxide dismutase (MnSOD), copper-zinc superoxide dismutase (CuZnSOD), catalase and heme oxygenase-1 (HO1), all of which are known targets of NF-κB and can be upregulated as a consequence of oxidative stress. Recuperated offspring also had a pro-inflammatory phenotype, as evidenced by increased tumor necrosis factor-α (TNFα) and interleukin-1β (IL1β) protein levels. Taken together, we demonstrate, for the first time to our knowledge, an accelerated aging phenotype in skeletal muscle in the context of developmental programming. These findings may pave the way for suitable interventions in at-risk populations.

show abstract

Effects of aging and maternal protein restriction on the muscle fibers morphology and neuromuscular junctions of rats after nutritional recovery

Cited by 17 publications

References 34 publications

Does skeletal muscle have an ‘epi’‐memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise

Does skeletal muscle have an ‘epi’‐memory? The role of epigenetics in nutritional programming, metabolic disease, aging and exercise

Running training experience attenuates disuse atrophy in fast-twitch skeletal muscles of rats

Poor maternal nutrition and accelerated postnatal growth induces an accelerated aging phenotype and oxidative stress in skeletal muscle of male rats

Contact Info

Product

Resources

About