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Reduced insulin/insulin-like growth factor-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans

Geert Depuydt (UGent) , Fang Xie, Vladislav A Petyuk, Nilesh Shanmugam (UGent) , Arne Smolders (UGent) , Ineke Dhondt (UGent) , Heather M Brewer, David G Camp, Richard D Smith and Bart Braeckman (UGent)
(2013) MOLECULAR & CELLULAR PROTEOMICS. 12(12). p.3624-3639
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Abstract
Reduced signaling through the C. elegans insulin/IGF-1-like tyrosine kinase receptor daf-2 and dietary restriction via bacterial dilution are two well-characterized lifespan-extending interventions that operate in parallel or through (partially) independent mechanisms. Using accurate mass and time tag LC-MS/MS quantitative proteomics we detected that the abundance of a large number of ribosomal subunits is decreased in response to dietary restriction as well as in the daf-2(e1370) insulin/IGF-1-receptor mutant. In addition, general protein synthesis levels in these long-lived worms are repressed. Surprisingly, ribosomal transcript levels were not correlated to actual protein abundance, suggesting that post-transcriptional regulation determines ribosome content. Proteomics also revealed increased presence of many structural muscle cell components in long-lived worms, which appears to result from prioritized preservation of muscle cell volume in nutrient-poor conditions or low insulin-like signaling. Activation of DAF-16, but not diet-restriction, stimulates mRNA expression of muscle-related genes to prevent muscle atrophy. Important daf-2-specific proteome changes include overexpression of aerobic metabolism enzymes and a general activation of stress responsive and immune defense systems, while increased abundance of many protein subunits of the proteasome core complex is a DR-specific characteristic.
Keywords
Physiology, Caenorhabditis elegans, Mass Spectrometry, Ribosomes, Gene Expression, Translation, DAUER LARVAE, POSTTRANSCRIPTIONAL MECHANISMS, INDUCED LONGEVITY, RIBOSOMAL-PROTEINS, SACCHAROMYCES-CEREVISIAE, Electron Microscopy, GENE-EXPRESSION, C-ELEGANS, CHAIN AMINO-ACIDS, LIFE-SPAN EXTENSION, MESSENGER-RNA TRANSLATION, Aging, Molecular biology

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Citation

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MLA
Depuydt, Geert, Fang Xie, Vladislav A Petyuk, et al. “Reduced Insulin/insulin-like Growth Factor-1 Signaling and Dietary Restriction Inhibit Translation but Preserve Muscle Mass in Caenorhabditis Elegans.” MOLECULAR & CELLULAR PROTEOMICS 12.12 (2013): 3624–3639. Print.
APA
Depuydt, G., Xie, F., Petyuk, V. A., Shanmugam, N., Smolders, A., Dhondt, I., Brewer, H. M., et al. (2013). Reduced insulin/insulin-like growth factor-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans. MOLECULAR & CELLULAR PROTEOMICS, 12(12), 3624–3639.
Chicago author-date
Depuydt, Geert, Fang Xie, Vladislav A Petyuk, Nilesh Shanmugam, Arne Smolders, Ineke Dhondt, Heather M Brewer, David G Camp, Richard D Smith, and Bart Braeckman. 2013. “Reduced Insulin/insulin-like Growth Factor-1 Signaling and Dietary Restriction Inhibit Translation but Preserve Muscle Mass in Caenorhabditis Elegans.” Molecular & Cellular Proteomics 12 (12): 3624–3639.
Chicago author-date (all authors)
Depuydt, Geert, Fang Xie, Vladislav A Petyuk, Nilesh Shanmugam, Arne Smolders, Ineke Dhondt, Heather M Brewer, David G Camp, Richard D Smith, and Bart Braeckman. 2013. “Reduced Insulin/insulin-like Growth Factor-1 Signaling and Dietary Restriction Inhibit Translation but Preserve Muscle Mass in Caenorhabditis Elegans.” Molecular & Cellular Proteomics 12 (12): 3624–3639.
Vancouver
1.
Depuydt G, Xie F, Petyuk VA, Shanmugam N, Smolders A, Dhondt I, et al. Reduced insulin/insulin-like growth factor-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans. MOLECULAR & CELLULAR PROTEOMICS. 2013;12(12):3624–39.
IEEE
[1]
G. Depuydt et al., “Reduced insulin/insulin-like growth factor-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans,” MOLECULAR & CELLULAR PROTEOMICS, vol. 12, no. 12, pp. 3624–3639, 2013.
@article{4166172,
  abstract     = {Reduced signaling through the C. elegans insulin/IGF-1-like tyrosine kinase receptor daf-2 and dietary restriction via bacterial dilution are two well-characterized lifespan-extending interventions that operate in parallel or through (partially) independent mechanisms. Using accurate mass and time tag LC-MS/MS quantitative proteomics we detected that the abundance of a large number of ribosomal subunits is decreased in response to dietary restriction as well as in the daf-2(e1370) insulin/IGF-1-receptor mutant. In addition, general protein synthesis levels in these long-lived worms are repressed. Surprisingly, ribosomal transcript levels were not correlated to actual protein abundance, suggesting that post-transcriptional regulation determines ribosome content. Proteomics also revealed increased presence of many structural muscle cell components in long-lived worms, which appears to result from prioritized preservation of muscle cell volume in nutrient-poor conditions or low insulin-like signaling. Activation of DAF-16, but not diet-restriction, stimulates mRNA expression of muscle-related genes to prevent muscle atrophy. Important daf-2-specific proteome changes include overexpression of aerobic metabolism enzymes and a general activation of stress responsive and immune defense systems, while increased abundance of many protein subunits of the proteasome core complex is a DR-specific characteristic.},
  author       = {Depuydt, Geert and Xie, Fang and Petyuk, Vladislav A and Shanmugam, Nilesh and Smolders, Arne and Dhondt, Ineke and Brewer, Heather M and Camp, David G and Smith, Richard D and Braeckman, Bart},
  issn         = {1535-9476},
  journal      = {MOLECULAR & CELLULAR PROTEOMICS},
  keywords     = {Physiology,Caenorhabditis elegans,Mass Spectrometry,Ribosomes,Gene Expression,Translation,DAUER LARVAE,POSTTRANSCRIPTIONAL MECHANISMS,INDUCED LONGEVITY,RIBOSOMAL-PROTEINS,SACCHAROMYCES-CEREVISIAE,Electron Microscopy,GENE-EXPRESSION,C-ELEGANS,CHAIN AMINO-ACIDS,LIFE-SPAN EXTENSION,MESSENGER-RNA TRANSLATION,Aging,Molecular biology},
  language     = {eng},
  number       = {12},
  pages        = {3624--3639},
  title        = {Reduced insulin/insulin-like growth factor-1 signaling and dietary restriction inhibit translation but preserve muscle mass in Caenorhabditis elegans},
  url          = {http://dx.doi.org/10.1074/mcp.M113.027383},
  volume       = {12},
  year         = {2013},
}
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