Effects of aging on basement membrane of the soleus muscle during recovery following disuse atrophy in rats

Ikegami, Keisuke; Sujino, Mitsugu; Koinuma, Satoshi; Nagano, Mamoru; Oi, Yuki; Onishi, Teruo; Sugiyo, Shinichi; Takeda, Isao; Kaji, Hiroshi; Shigeyoshi, Yasufumi

doi:10.1016/j.exger.2017.08.014

Cited by 34 publications

(50 citation statements)

References 35 publications

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“…In terms of their role in skeletal muscle and exercise induced hypertrophy, only 7 out of these 14 upregulated and hypomethylated genes have been investigated, notably COL4A2, HSPG2, TIAM1, CTTN, PTK2/FAK, PLD1 and PLAUR. Indeed, the responsiveness of COL4A2 (Type IV collagen) to muscle unloading and reloading seems to be impaired in aged muscle of rats 30 . Further, HSPG2 (Perlecan) has been identified to alter mass and metabolism in skeletal muscle 53 .…”

Section: Discussionmentioning

confidence: 99%

“…File 9)). Importantly, some of these ECM/actin structural and remodelling genes have been shown to demonstrate increases after aerobic or resistance exercise at the gene expression, protein abundance or activity level such as; TIMP3 27 , FLNB 28 , COL4A1 29,30 , or are involved in satellite/muscle cell regulation (ITGB3 31 , CTTN 32 , LAMA5 33 , CRK 34,35 ). However, to the authors knowledge there is no evidence to suggest that any of these genes are differentially methylated at the DNA level after skeletal muscle anabolism or hypertrophy.…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

Turner

Seaborne

Sharples

2019

Sci Rep

100

143

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Transcriptome wide changes in human skeletal muscle after acute (anabolic) and chronic resistance exercise (RE) induced hypertrophy have been extensively determined in the literature. We have also recently undertaken DNA methylome analysis (850,000 + CpG sites) in human skeletal muscle after acute and chronic RE, detraining and retraining, where we identified an association between DNA methylation and epigenetic memory of exercise induced skeletal muscle hypertrophy. However, it is currently unknown as to whether all the genes identified in the transcriptome studies to date are also epigenetically regulated at the DNA level after acute, chronic or repeated RE exposure. We therefore aimed to undertake large scale bioinformatical analysis by pooling the publicly available transcriptome data after acute (110 samples) and chronic RE (181 samples) and comparing these large data sets with our genome-wide DNA methylation analysis in human skeletal muscle after acute and chronic RE, detraining and retraining. Indeed, after acute RE we identified 866 up- and 936 down-regulated genes at the expression level, with 270 (out of the 866 up-regulated) identified as being hypomethylated, and 216 (out of 936 downregulated) as hypermethylated. After chronic RE we identified 2,018 up- and 430 down-regulated genes with 592 (out of 2,018 upregulated) identified as being hypomethylated and 98 (out of 430 genes downregulated) as hypermethylated. After KEGG pathway analysis, genes associated with ‘cancer’ pathways were significantly enriched in both bioinformatic analysis of the pooled transcriptome and methylome datasets after both acute and chronic RE. This resulted in 23 (out of 69) and 28 (out of 49) upregulated and hypomethylated and 12 (out of 37) and 2 (out of 4) downregulated and hypermethylated ‘cancer’ genes following acute and chronic RE respectively. Within skeletal muscle tissue, these ‘cancer’ genes predominant functions were associated with matrix/actin structure and remodelling, mechano-transduction (e.g. PTK2/Focal Adhesion Kinase and Phospholipase D- following chronic RE), TGF-beta signalling and protein synthesis (e.g. GSK3B after acute RE). Interestingly, 51 genes were also identified to be up/downregulated in both the acute and chronic RE pooled transcriptome analysis as well as significantly hypo/hypermethylated after acute RE, chronic RE, detraining and retraining. Five genes; FLNB, MYH9, SRGAP1, SRGN, ZMIZ1 demonstrated increased gene expression in the acute and chronic RE transcriptome and also demonstrated hypomethylation in these conditions. Importantly, these 5 genes demonstrated retained hypomethylation even during detraining (following training induced hypertrophy) when exercise was ceased and lean mass returned to baseline (pre-training) levels, identifying them as genes associated with epigenetic memory in skeletal muscle. Importantly, for the first time across the transcriptome and epigenome combined, this study identifies novel differentially methylated genes associated with human skeletal muscle anaboli...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

Turner

Seaborne

Sharples

2019

Sci Rep

100

143

View full text Add to dashboard Cite

show abstract

“…A second possibility is that that the atrophic type I fibers in the mouse gastrocnemius muscle were more vulnerable to reloading-induced damage to the basement membrane and this may have contributed to fragility and slowed repair in old gastrocnemius muscles (Kanazawa, et al 2017). A third possibility is that reduced satellite cell number or function in muscles of old animals (Ballak, et al 2015) might limit muscle growth or repair of injury due to reloading.…”

Section: Discussionmentioning

confidence: 99%

Effects of hindlimb suspension and reloading on gastrocnemius and soleus muscle mass and function in geriatric mice

Oliveira

Mohamed

Myers

et al. 2019

Experimental Gerontology

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Reloading of atrophied muscles after hindlimb suspension (HLS) can induce muscle injury and prolong recovery after disuse in old rats, especially in fast contracting muscles. Less is known about the responses in mice and whether fast and slow muscles from geriatric mice will respond in a similar fashion to HLS unloading and recovery (HLS+R). Furthermore, while slow muscles undergo atrophy with disuse, they typically are more resistant to sarcopenia than fast contracting muscles. Geriatric (28 mo. of age) male C57BL/6 mice were randomly placed into 3 groups. These included HLS for 14 days n=9, and HLS followed by 14 days of reloading recovery (HLS+R; n=9), or normal ambulatory cage controls (n=9). Control mice were not exposed to unloading. Electrically evoked maximal muscle function was assessed in vivo in anesthetized mice at baseline, after 14 days of HLS or HLS+R. As expected, HLS significantly reduced body weight, wet weight of gastrocnemius and soleus muscles and in vivo maximal force. There were no differences in vivo fatigability of the plantar flexor muscles and overall fiber size. There were only minor fiber type distribution and frequency distribution of fiber sizes that differ between HLS+R and control gastrocnemius and soleus muscles. Soleus muscle wet weight had recovered to control levels after reloading, but type I/IIA fibers in the soleus muscles were significantly smaller after HLS+R than control muscles. In contrast, gastrocnemius muscle wet weight did not recover to control levels after reloading. Plantar flexion muscle force (primarily influenced by the gastrocnemius muscles) did not recover in HLS+R conditions as compared to HLS conditions and both were lower than control force production Signaling for apoptosis, autophagy and anabolic markers were not different between control and HLS+R gastrocnemius and soleus muscles in geriatric mice. These results suggest that molecular signaling does not explain attenuated ability to regain muscle wet weight, fiber size or muscle force production after HLS in geriatric mice. It is possible that fluid shifts, reduced blood flow, or shortened muscle fibers which failed to regain control lengths contributed to the attenuation of muscle wet weight after HLS and reloading and this affected force production. Further work is needed to determine if altered/loss of neural activity contributed to the inability of geriatric mice to regain gastrocnemius muscle weight and function after HLS and reloading.

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“…notably COL4A2, HSPG2, TIAM1, CTTN, PTK2/FAK, PLD1 and PLAUR. Indeed, the responsiveness of COL4A2 (Type IV collagen) to muscle unloading and reloading seems to be impaired in aged muscle of rats 28 . Further, HSPG2 (Perlecan) has been identified to alter mass and metabolism in skeletal muscle 51 .…”

Section: Kegg Cancermentioning

confidence: 99%

“…File 8). Importantly, some of these ECM/actin structural and remodelling genes have been shown to demonstrate increases after aerobic or resistance exercise at the gene expression, protein abundance or activity level such as; TIMP3 25 , FLNB 26 , COL4A1 27,28 , or are involved in satellite/muscle cell regulation (ITGB3 29 , CTTN 30 , LAMA5 31 , CRK 32,33 ). However, to the authors knowledge there is no evidence to suggest that any of these genes are differentially methylated at the DNA level in skeletal muscle anabolism or hypertrophy.…”

Section: Kegg Cancermentioning

confidence: 99%

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

Turner

Seaborne

Sharples

2018

Preprint

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38Transcriptome wide changes in human skeletal muscle after acute (anabolic) and chronic resistance exercise 39 (RE) induced hypertrophy have been extensively determined in the literature. We have also recently 40 undertaken DNA methylome analysis (850,000 + CpG sites) in human skeletal muscle after acute and 41 chronic RE, detaining and retraining, where we identified an association between DNA methylation in an 42 epigenetic memory of exercise induced skeletal muscle hypertrophy. However, it is currently unknown as to 43 whether all the genes identified in the transcriptome studies to date are also epigenetically regulated at the 44 DNA level after acute, chronic or repeated RE exposure. We therefore aimed to undertake large scale 45 bioinformatical analysis by pooling the publicly available transcriptome data after acute (110 samples) and 46 chronic RE (181 samples) and comparing these large data sets with our genome-wide DNA methylation 47 analysis in human skeletal muscle after acute and chronic RE, detraining and retraining. Indeed, after acute 48 RE we identified 866 up-and 936 down-regulated genes at the expression level, with 270 (out of the 866 up-49 regulated) identified as being hypomethylated, and 216 (out of 936 downregulated) as hypermethylated. 50After chronic RE we identified 2,018 up-and 430 down-regulated genes with 592 (out of 2,018 upregulated) 51 identified as being hypomethylated and 98 (out of 430 genes downregulated) as hypermethylated. After 52 KEGG pathway analysis, genes associated with 'cancer' pathways were significantly enriched in both 53 bioinformatic analysis of the pooled transcriptome and methylome data after both acute and chronic RE. 54 This resulted in 23 (out of 69) and 28 (out of 49) upregulated and hypomethylated and 12 (out of 37) and 2 55 (out of 4) downregulated and hypermethylated 'cancer' genes following acute and chronic RE respectively. 56Within skeletal muscle tissue, these 'cancer' genes predominant functions were associated with matrix/ actin 57 structure and remodelling, mechano-transduction (including PTK2/Focal Adhesion Kinase and 58 Phospholipase D-following chronic RE only), TGF-beta signalling and protein synthesis (GSK3B after 59 acute RE only). Interestingly, 51 genes were also identified to be up/downregulated in both the acute and 60 chronic RE pooled transcriptome analysis as well as significantly hypo/hypermethylated after acute RE, 61 chronic RE, detraining and retraining. Five genes; FLNB, MYH9, SRGAP1, SRGN, ZMIZ1 demonstrated 62 increased gene expression in the acute and chronic RE transcriptome and also demonstrated 63 hypomethylation in these conditions. Importantly, these 5 genes demonstrated retained hypomethylation 64 even during detraining (following training induced hypertrophy) when exercise was ceased and lean mass 65 returned to baseline (pre-training) levels, identifying them as potential epigenetic memory genes. 66 Importantly, for the first time across the transcriptome and epigenome combined, this study identifies novel 67 diffe...

show abstract

Effects of aging on basement membrane of the soleus muscle during recovery following disuse atrophy in rats

Cited by 34 publications

References 35 publications

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

Effects of hindlimb suspension and reloading on gastrocnemius and soleus muscle mass and function in geriatric mice

Comparative Transcriptome and Methylome Analysis in Human Skeletal Muscle Anabolism, Hypertrophy and Epigenetic Memory

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