cAMP-dependent protein kinase inhibits FoxO activity and regulates skeletal muscle plasticity in mice

Although we have shown that catecholamines suppress the activity of the Ubiquitin-Proteasome System (UPS) and atrophy-related genes expression through a cAMP-dependent manner in skeletal muscle from rodents, the underlying mechanisms remain unclear. Here, we report that a single injection of norepin...

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Published inThe FASEB journal Vol. 34; no. 9; p. 12946
Main Authors Silveira, Wilian A, Gonçalves, Dawit A, Machado, Juliano, Lautherbach, Natalia, Lustrino, Danilo, Paula-Gomes, Silvia, Pereira, Marcelo G, Miyabara, Elen H, Sandri, Marco, Kettelhut, Isis C, Navegantes, Luiz C
Format Journal Article
LanguageEnglish
Published United States 01.09.2020
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Abstract Although we have shown that catecholamines suppress the activity of the Ubiquitin-Proteasome System (UPS) and atrophy-related genes expression through a cAMP-dependent manner in skeletal muscle from rodents, the underlying mechanisms remain unclear. Here, we report that a single injection of norepinephrine (NE; 1 mg kg ; s.c) attenuated the fasting-induced up-regulation of FoxO-target genes in tibialis anterior (TA) muscles by the stimulation of PKA/CREB and Akt/FoxO1 signaling pathways. In addition, muscle-specific activation of PKA by the overexpression of PKA catalytic subunit (PKAcat) suppressed FoxO reporter activity induced by (1) a wild-type; (2) a non-phosphorylatable; (3) a non-phosphorylatable and non-acetylatable forms of FoxO1 and FoxO3; (4) downregulation of FoxO protein content, and probably by (5) PGC-1α up-regulation. Consistently, the overexpression of the PKAcat inhibitor (PKI) up-regulated FoxO activity and the content of Atrogin-1 and MuRF1, as well as induced muscle fiber atrophy, the latter effect being prevented by the overexpression of a dominant negative (d. n.) form of FoxO (d.n.FoxO). The sustained overexpression of PKAcat induced fiber-type transition toward a smaller, slower, and more oxidative phenotype and improved muscle resistance to fatigue. Taken together, our data provide the first evidence that endogenous PKA activity is required to restrain the basal activity of FoxO and physiologically important to maintain skeletal muscle mass.
AbstractList Although we have shown that catecholamines suppress the activity of the Ubiquitin-Proteasome System (UPS) and atrophy-related genes expression through a cAMP-dependent manner in skeletal muscle from rodents, the underlying mechanisms remain unclear. Here, we report that a single injection of norepinephrine (NE; 1 mg kg ; s.c) attenuated the fasting-induced up-regulation of FoxO-target genes in tibialis anterior (TA) muscles by the stimulation of PKA/CREB and Akt/FoxO1 signaling pathways. In addition, muscle-specific activation of PKA by the overexpression of PKA catalytic subunit (PKAcat) suppressed FoxO reporter activity induced by (1) a wild-type; (2) a non-phosphorylatable; (3) a non-phosphorylatable and non-acetylatable forms of FoxO1 and FoxO3; (4) downregulation of FoxO protein content, and probably by (5) PGC-1α up-regulation. Consistently, the overexpression of the PKAcat inhibitor (PKI) up-regulated FoxO activity and the content of Atrogin-1 and MuRF1, as well as induced muscle fiber atrophy, the latter effect being prevented by the overexpression of a dominant negative (d. n.) form of FoxO (d.n.FoxO). The sustained overexpression of PKAcat induced fiber-type transition toward a smaller, slower, and more oxidative phenotype and improved muscle resistance to fatigue. Taken together, our data provide the first evidence that endogenous PKA activity is required to restrain the basal activity of FoxO and physiologically important to maintain skeletal muscle mass.
Author Miyabara, Elen H
Lautherbach, Natalia
Machado, Juliano
Paula-Gomes, Silvia
Sandri, Marco
Lustrino, Danilo
Pereira, Marcelo G
Navegantes, Luiz C
Gonçalves, Dawit A
Kettelhut, Isis C
Silveira, Wilian A
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  givenname: Dawit A
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  fullname: Gonçalves, Dawit A
  organization: Venetian Institute of Molecular Medicine, Padova, Italy
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Keywords ubiquitin-proteasome system
skeletal muscle plasticity
skeletal muscle atrophy
adrenergic signaling
protein metabolism
Language English
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Snippet Although we have shown that catecholamines suppress the activity of the Ubiquitin-Proteasome System (UPS) and atrophy-related genes expression through a...
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StartPage 12946
SubjectTerms Animals
Cell Line
Cyclic AMP-Dependent Protein Kinases - metabolism
Forkhead Box Protein O1 - metabolism
Forkhead Box Protein O3 - metabolism
Male
Mice
Mice, Inbred C57BL
Muscle, Skeletal - enzymology
Muscle, Skeletal - pathology
Muscular Atrophy - metabolism
Myoblasts, Skeletal - enzymology
Signal Transduction
Title cAMP-dependent protein kinase inhibits FoxO activity and regulates skeletal muscle plasticity in mice
URI https://www.ncbi.nlm.nih.gov/pubmed/32772437
Volume 34
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