Shared and unique phosphoproteomics responses in skeletal muscle from exercise models and in hyperammonemic myotubes
Skeletal muscle generation of ammonia, an endogenous cytotoxin, is increased during exercise. Perturbations in ammonia metabolism consistently occur in chronic diseases, and may blunt beneficial skeletal muscle molecular responses and protein homeostasis with exercise. Phosphorylation of skeletal mu...
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| Published in: | iScience Vol. 25; no. 11; p. 105325 |
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| Abstract | Skeletal muscle generation of ammonia, an endogenous cytotoxin, is increased during exercise. Perturbations in ammonia metabolism consistently occur in chronic diseases, and may blunt beneficial skeletal muscle molecular responses and protein homeostasis with exercise. Phosphorylation of skeletal muscle proteins mediates cellular signaling responses to hyperammonemia and exercise. Comparative bioinformatics and machine learning-based analyses of published and experimentally derived phosphoproteomics data identified differentially expressed phosphoproteins that were unique and shared between hyperammonemic murine myotubes and skeletal muscle from exercise models. Enriched processes identified in both hyperammonemic myotubes and muscle from exercise models with selected experimental validation included protein kinase A (PKA), calcium signaling, mitogen-activated protein kinase (MAPK) signaling, and protein homeostasis. Our approach of feature extraction from comparative untargeted “omics” data allows for selection of preclinical models that recapitulate specific human exercise responses and potentially optimize functional capacity and skeletal muscle protein homeostasis with exercise in chronic diseases.
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•Hyperammonemia occurs in a number of chronic diseases and physical exercise•Beneficial responses to exercise may be blunted by increased muscle ammoniagenesis•Comparative phosphoproteomics show potential modifiable shared molecular responses•Exercise capacity in chronic disease may be improved by targeting hyperammonemia
Biological sciences; Cell biology; Functional aspects of cell biology; Omics; Proteomics. |
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| AbstractList | Skeletal muscle generation of ammonia, an endogenous cytotoxin, is increased during exercise. Perturbations in ammonia metabolism consistently occur in chronic diseases, and may blunt beneficial skeletal muscle molecular responses and protein homeostasis with exercise. Phosphorylation of skeletal muscle proteins mediates cellular signaling responses to hyperammonemia and exercise. Comparative bioinformatics and machine learning-based analyses of published and experimentally derived phosphoproteomics data identified differentially expressed phosphoproteins that were unique and shared between hyperammonemic murine myotubes and skeletal muscle from exercise models. Enriched processes identified in both hyperammonemic myotubes and muscle from exercise models with selected experimental validation included protein kinase A (PKA), calcium signaling, mitogen-activated protein kinase (MAPK) signaling, and protein homeostasis. Our approach of feature extraction from comparative untargeted "omics" data allows for selection of preclinical models that recapitulate specific human exercise responses and potentially optimize functional capacity and skeletal muscle protein homeostasis with exercise in chronic diseases. Skeletal muscle generation of ammonia, an endogenous cytotoxin, is increased during exercise. Perturbations in ammonia metabolism consistently occur in chronic diseases, and may blunt beneficial skeletal muscle molecular responses and protein homeostasis with exercise. Phosphorylation of skeletal muscle proteins mediates cellular signaling responses to hyperammonemia and exercise. Comparative bioinformatics and machine learning-based analyses of published and experimentally derived phosphoproteomics data identified differentially expressed phosphoproteins that were unique and shared between hyperammonemic murine myotubes and skeletal muscle from exercise models. Enriched processes identified in both hyperammonemic myotubes and muscle from exercise models with selected experimental validation included protein kinase A (PKA), calcium signaling, mitogen-activated protein kinase (MAPK) signaling, and protein homeostasis. Our approach of feature extraction from comparative untargeted “omics” data allows for selection of preclinical models that recapitulate specific human exercise responses and potentially optimize functional capacity and skeletal muscle protein homeostasis with exercise in chronic diseases. • Hyperammonemia occurs in a number of chronic diseases and physical exercise • Beneficial responses to exercise may be blunted by increased muscle ammoniagenesis • Comparative phosphoproteomics show potential modifiable shared molecular responses • Exercise capacity in chronic disease may be improved by targeting hyperammonemia Biological sciences; Cell biology; Functional aspects of cell biology; Omics; Proteomics. Skeletal muscle generation of ammonia, an endogenous cytotoxin, is increased during exercise. Perturbations in ammonia metabolism consistently occur in chronic diseases, and may blunt beneficial skeletal muscle molecular responses and protein homeostasis with exercise. Phosphorylation of skeletal muscle proteins mediates cellular signaling responses to hyperammonemia and exercise. Comparative bioinformatics and machine learning-based analyses of published and experimentally derived phosphoproteomics data identified differentially expressed phosphoproteins that were unique and shared between hyperammonemic murine myotubes and skeletal muscle from exercise models. Enriched processes identified in both hyperammonemic myotubes and muscle from exercise models with selected experimental validation included protein kinase A (PKA), calcium signaling, mitogen-activated protein kinase (MAPK) signaling, and protein homeostasis. Our approach of feature extraction from comparative untargeted “omics” data allows for selection of preclinical models that recapitulate specific human exercise responses and potentially optimize functional capacity and skeletal muscle protein homeostasis with exercise in chronic diseases. [Display omitted] •Hyperammonemia occurs in a number of chronic diseases and physical exercise•Beneficial responses to exercise may be blunted by increased muscle ammoniagenesis•Comparative phosphoproteomics show potential modifiable shared molecular responses•Exercise capacity in chronic disease may be improved by targeting hyperammonemia Biological sciences; Cell biology; Functional aspects of cell biology; Omics; Proteomics. |
| ArticleNumber | 105325 |
| Author | Sekar, Jinendiran Attaway, Amy H. Dasarathy, Srinivasan Li, Ling Hornberger, Troy A. Mansuri, M. Shahid Mishra, Saurabh Bellar, Annette Welch, Nicole Singh, Shashi Shekhar Chelluboyina, Aruna K. Musich, Ryan Willard, Belinda |
| Author_xml | – sequence: 1 givenname: Nicole surname: Welch fullname: Welch, Nicole organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 2 givenname: Shashi Shekhar surname: Singh fullname: Singh, Shashi Shekhar organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 3 givenname: Ryan surname: Musich fullname: Musich, Ryan organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 4 givenname: M. Shahid surname: Mansuri fullname: Mansuri, M. Shahid organization: Department of Molecular Biophysics and Biochemistry, Yale University, New Haven, CT 06520, USA – sequence: 5 givenname: Annette surname: Bellar fullname: Bellar, Annette organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 6 givenname: Saurabh surname: Mishra fullname: Mishra, Saurabh organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 7 givenname: Aruna K. surname: Chelluboyina fullname: Chelluboyina, Aruna K. organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 8 givenname: Jinendiran surname: Sekar fullname: Sekar, Jinendiran organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 9 givenname: Amy H. surname: Attaway fullname: Attaway, Amy H. organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 10 givenname: Ling surname: Li fullname: Li, Ling organization: Proteomics Core, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 11 givenname: Belinda surname: Willard fullname: Willard, Belinda organization: Proteomics Core, Cleveland Clinic, Cleveland, OH 44195, USA – sequence: 12 givenname: Troy A. surname: Hornberger fullname: Hornberger, Troy A. organization: Department of Comparative Biosciences, School of Veterinary Medicine, University of Wisconsin, Madison, WI 53706, USA – sequence: 13 givenname: Srinivasan orcidid: 0000-0003-1774-0104 surname: Dasarathy fullname: Dasarathy, Srinivasan email: dasaras@ccf.org organization: Department of Inflammation and Immunity, Cleveland Clinic, Cleveland, OH 44195, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/36345342$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_jhep_2023_03_025 |
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| Keywords | Cell biology Biological sciences Functional aspects of cell biology Omics Proteomics |
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| Title | Shared and unique phosphoproteomics responses in skeletal muscle from exercise models and in hyperammonemic myotubes |
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