Muscle-specific activation of Ca2+/calmodulin-dependent protein kinase IV increases whole-body insulin action in mice

Aims/hypothesis Aerobic exercise increases muscle glucose and improves insulin action through numerous pathways, including activation of Ca 2+ /calmodulin-dependent protein kinases (CAMKs) and peroxisome proliferator γ coactivator 1α (PGC-1α). While overexpression of PGC-1α increases muscle mitochon...

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Published inDiabetologia Vol. 57; no. 6; pp. 1232 - 1241
Main Authors Lee, Hui-Young, Gattu, Arijeet K., Camporez, João-Paulo G., Kanda, Shoichi, Guigni, Blas, Kahn, Mario, Zhang, Dongyan, Galbo, Thomas, Birkenfeld, Andreas L., Jornayvaz, Francois R., Jurczak, Michael J., Choi, Cheol Soo, Yan, Zhen, Williams, R. Sanders, Shulman, Gerald I., Samuel, Varman T.
Format Journal Article
LanguageEnglish
Published Berlin/Heidelberg Springer Berlin Heidelberg 01.06.2014
Springer
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Abstract Aims/hypothesis Aerobic exercise increases muscle glucose and improves insulin action through numerous pathways, including activation of Ca 2+ /calmodulin-dependent protein kinases (CAMKs) and peroxisome proliferator γ coactivator 1α (PGC-1α). While overexpression of PGC-1α increases muscle mitochondrial content and oxidative type I fibres, it does not improve insulin action. Activation of CAMK4 also increases the content of type I muscle fibres, PGC-1α level and mitochondrial content. However, it remains unknown whether CAMK4 activation improves insulin action on glucose metabolism in vivo. Methods The effects of CAMK4 activation on skeletal muscle insulin action were quantified using transgenic mice with a truncated and constitutively active form of CAMK4 (CAMK4 ● ) in skeletal muscle. Tissue-specific insulin sensitivity was assessed in vivo using a hyperinsulinaemic–euglycaemic clamp and isotopic measurements of glucose metabolism. Results The rate of insulin-stimulated whole-body glucose uptake was increased by ∼25% in CAMK4 ● mice. This was largely attributed to an increase of ∼60% in insulin-stimulated glucose uptake in the quadriceps, the largest hindlimb muscle. These changes were associated with improvements in insulin signalling, as reflected by increased phosphorylation of Akt and its substrates and an increase in the level of GLUT4 protein. In addition, there were extramuscular effects: CAMK4 ● mice had improved hepatic and adipose insulin action. These pleiotropic effects were associated with increased levels of PGC-1α-related myokines in CAMK4 ● skeletal muscle. Conclusions/interpretation Activation of CAMK4 enhances mitochondrial biogenesis in skeletal muscle while also coordinating improvements in whole-body insulin-mediated glucose.
AbstractList Aims/hypothesis Aerobic exercise increases muscle glucose and improves insulin action through numerous pathways, including activation of Ca 2+ /calmodulin-dependent protein kinases (CAMKs) and peroxisome proliferator γ coactivator 1α (PGC-1α). While overexpression of PGC-1α increases muscle mitochondrial content and oxidative type I fibres, it does not improve insulin action. Activation of CAMK4 also increases the content of type I muscle fibres, PGC-1α level and mitochondrial content. However, it remains unknown whether CAMK4 activation improves insulin action on glucose metabolism in vivo. Methods The effects of CAMK4 activation on skeletal muscle insulin action were quantified using transgenic mice with a truncated and constitutively active form of CAMK4 (CAMK4 ● ) in skeletal muscle. Tissue-specific insulin sensitivity was assessed in vivo using a hyperinsulinaemic–euglycaemic clamp and isotopic measurements of glucose metabolism. Results The rate of insulin-stimulated whole-body glucose uptake was increased by ∼25% in CAMK4 ● mice. This was largely attributed to an increase of ∼60% in insulin-stimulated glucose uptake in the quadriceps, the largest hindlimb muscle. These changes were associated with improvements in insulin signalling, as reflected by increased phosphorylation of Akt and its substrates and an increase in the level of GLUT4 protein. In addition, there were extramuscular effects: CAMK4 ● mice had improved hepatic and adipose insulin action. These pleiotropic effects were associated with increased levels of PGC-1α-related myokines in CAMK4 ● skeletal muscle. Conclusions/interpretation Activation of CAMK4 enhances mitochondrial biogenesis in skeletal muscle while also coordinating improvements in whole-body insulin-mediated glucose.
Author Choi, Cheol Soo
Gattu, Arijeet K.
Guigni, Blas
Kahn, Mario
Zhang, Dongyan
Shulman, Gerald I.
Camporez, João-Paulo G.
Williams, R. Sanders
Samuel, Varman T.
Jornayvaz, Francois R.
Jurczak, Michael J.
Galbo, Thomas
Birkenfeld, Andreas L.
Kanda, Shoichi
Yan, Zhen
Lee, Hui-Young
AuthorAffiliation 3 Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, Korea
5 Department of Endocrinology, Charite – University School of Medicine, Berlin, Germany
4 Veteran’s Affairs Medical Center, West Haven, CT, USA
7 J. David Gladstone Institutes, San Francisco, CA, USA
1 Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520, USA
2 Howard Hughes Medical Institute, Yale University School of Medicine, New Haven, CT, USA
8 Department of Cellular & Molecular Physiology, Yale University School of Medicine, New Haven, CT
6 Department of Medicine, University of Virginia, Charlottesville, VA, USA
AuthorAffiliation_xml – name: 5 Department of Endocrinology, Charite – University School of Medicine, Berlin, Germany
– name: 3 Lee Gil Ya Cancer and Diabetes Institute, Gachon University of Medicine and Science, Incheon, Korea
– name: 1 Department of Internal Medicine, Yale University School of Medicine, New Haven, CT 06520, USA
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  givenname: Varman T.
  surname: Samuel
  fullname: Samuel, Varman T.
  email: varman.samuel@yale.edu
  organization: Department of Internal Medicine, Yale University School of Medicine, Veteran’s Affairs Medical Center
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Issue 6
Keywords Myokines
Muscle insulin resistance
Hyperinsulinaemic–euglycaemic clamp
Endocrinopathy
Pancreatic hormone
Calcium
Enzyme
Transferases
Diabetes mellitus
Non-specific serine/threonine protein kinase
Rodentia
Metabolic diseases
Hyperinsulinaemic-euglycaemic clamp
Inorganic element
Insulin
Target tissue resistance
Vertebrata
Mammalia
Mouse
Animal
Insulin resistance
Muscle
Calmodulin
Language English
License CC BY 4.0
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PublicationSubtitle Clinical and Experimental Diabetes and Metabolism
PublicationTitle Diabetologia
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Snippet Aims/hypothesis Aerobic exercise increases muscle glucose and improves insulin action through numerous pathways, including activation of Ca 2+...
SourceID pubmedcentral
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springer
SourceType Open Access Repository
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Index Database
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StartPage 1232
SubjectTerms Biological and medical sciences
Diabetes. Impaired glucose tolerance
Endocrine pancreas. Apud cells (diseases)
Endocrinopathies
Etiopathogenesis. Screening. Investigations. Target tissue resistance
Human Physiology
Internal Medicine
Medical sciences
Medicine
Medicine & Public Health
Metabolic Diseases
Title Muscle-specific activation of Ca2+/calmodulin-dependent protein kinase IV increases whole-body insulin action in mice
URI https://link.springer.com/article/10.1007/s00125-014-3212-1
https://pubmed.ncbi.nlm.nih.gov/PMC5634138
Volume 57
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