Insulin/IGF1 signalling mediates the effects of β2‐adrenergic agonist on muscle proteostasis and growth
Open accessAbstract
Background: Stimulation of β 2‐adrenoceptors can promote muscle hypertrophy and fibre type shift, and it can counteract atrophy and weakness. The underlying mechanisms remain elusive. Methods: Fed wild type (WT), 2‐day fasted WT, muscle‐specific insulin (INS) receptor (IR) knockout (M‐IR−/−), and MKR mice were studied with regard to acute effects of the β 2‐agonist formoterol (FOR) on protein metabolism and signalling events. MKR mice express a dominant negative IGF1 receptor, which blocks both INS/IGF1 signalling. All received one injection of FOR (300 μg kg−1 subcutaneously) or saline. Skeletal muscles and serum samples were analysed from 30 to 240 min. For the study of chronic effects of FOR on muscle plasticity and function as well as intracellular signalling pathways, fed WT and MKR mice were treated with formoterol (300 μg kg−1 day−1) for 30 days. Results: In fed and fasted mice, one injection of FOR inhibited autophagosome formation (LC3‐II content, 65%, P ≤ 0.05) that was paralleled by an increase in serum INS levels (4‐fold to 25‐fold, P ≤ 0.05) and the phosphorylation of Akt (4.4‐fold to 6.5‐fold, P ≤ 0.05) and ERK1/2 (50% to two‐fold, P ≤ 0.05). This led to the suppression (40–70%, P ≤ 0.05) of the master regulators of atrophy, FoxOs, and the mRNA levels of their target genes. FOR enhanced (41%, P ≤ 0.05) protein synthesis only in fed condition and stimulated (4.4‐fold to 35‐fold, P ≤ 0.05) the prosynthetic Akt/mTOR/p70S6K pathway in both fed and fasted states. FOR effects on Akt signalling during fasting were blunted in both M‐IR−/− and MKR mice. Inhibition of proteolysis markers by FOR was prevented only in MKR mice. Blockade of PI3K/Akt axis and mTORC1, but not ERK1/2, in fasted mice also suppressed the acute FOR effects on proteolysis and autophagy. Chronic stimulation of β 2‐adrenoceptors in fed WT mice increased body (11%, P ≤ 0.05) and muscle (15%, P ≤ 0.05) growth and downregulated atrophy‐related genes (30–40%, P ≤ 0.05), but these effects were abolished in MKR mice. Increases in muscle force caused by FOR (WT, 24%, P ≤ 0.05) were only partially impaired in MKR mice (12%, P ≤ 0.05), and FOR‐induced slow‐to‐fast fibre type shift was not blocked at all in these animals. In MKR mice, FOR also restored the lower levels of muscle SDH activity to basal WT values and caused a marked reduction (57%, P ≤ 0.05) in the number of centrally nucleated fibers. Conclusions: NS/IGF1 signalling is necessary for the anti‐proteolytic and hypertrophic effects of in vivo β 2‐adrenergic stimulation and appears to mediate FOR‐induced enhancement of protein synthesis. INS/IGF1 signalling only partially contributes to gain in strength and does not mediate fibre type transition induced by FOR.
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β2-adrenergic signaling at least partially impinges on insulin/IGF1 receptor signaling and not on the ERK1 pathway.
“Recent data suggest that β2-adrenergic signaling, at least partially, impinges on insulin/IGF1 receptor signaling and not on the ERK1 pathway25.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [25]
Clenbuterol or formoterol enhance protein synthesis and inhibit protein degradation.
“Clenbuterol or formoterol are β2-adrenoreceptor agonists that in addition to stimulating the breakdown of glycogen and lipids, enhance protein synthesis and inhibit protein degradation25.”
From Mechanisms of muscle atrophy and hypertrophy: implications in health and disease (2021) · cites this paper as [25]
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Self-citation
- Authors
- Gonçalves, D. A., Silveira, W. A., Manfredi, L. H., Graça, F. A., Armani, A., Bertaggia, E., O´Neill, B. T., Lautherbach, N., Machado, J., Nogara, L., Pereira, M. G., Arcidiacono, D., Realdon, S., Kahn, C. R., Sandri, M., Kettelhut, I. C., & Navegantes, L. C. C.
- Affiliations
- University of Padua (IT)
- Universidade de São Paulo (BR)
- Section on Integrative Physiology and Metabolism, Joslin Diabetes Center Harvard Medical School Boston MA USA
- Istituto Oncologico Veneto (IT)
- Joslin Diabetes Center (US)
- Department of Physiology Ribeirão Preto Medical School/University of São Paulo Ribeirão Preto SP Brazil
- Corresponding author
- Gonçalves, Dawit A.
- Navegantes, Luiz Carlos C.
- ORCID
- Venue
- Journal of Cachexia, Sarcopenia and Muscle
- Publisher
- Wiley
- Published
- 2019-04
- Volume
- 10
- Issue
- 2
- Pages
- 455-475
- ISSN
- 2190-5991 (ISSN-L)
- 2190-6009
- PMC
- PMC6463755
- OpenAlex
- W2929263901
- Cited by
- 56
- References
- 72
- Citations by year
- 2026: 1 · 2025: 9 · 2024: 14 · 2023: 6 · 2022: 7 · 2021: 12 · 2020: 5 · 2019: 2
- FWCI
- 2.15
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Journal of Cachexia Sarcopenia and Muscle (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, other-oa)
- Funders
- National Institutes of Health (K08DK100543, R01DK031036 and R01DK033201)
- Chicago Committee on High Rise Buildings (645648)
- Fondation Leducq (17388)
- Association Française contre les Myopathies (19524)
- Conselho Nacional de Desenvolvimento Científico e Tecnológico (167033/2017‐4)
- Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (306624/2015‐0, 233261/2014‐1, PNPD20131672)
- Fundação de Amparo à Pesquisa do Estado de São Paulo (12/24524‐6, 10/11015‐0, 15/21112‐7, 12/18861‐0, 18/10089‐2)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Muscle metabolism and nutrition
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Keywords
- beta2-adrenergic agonists, formoterol, muscle atrophy, muscle hypertrophy, autophagy, mTORC1, Akt signaling, ERK1/2, FOXO, IGF-1 receptor, insulin receptor, fasting, protein synthesis, phosphatidylinositol 3-kinase
- MeSH terms
- Proteostasis, Animals, Autophagy, Insulin, Insulin-Like Growth Factor I, Lysosomes, Male, Muscle Proteins, Signal Transduction, Mice, Knockout, Muscle, Skeletal, Phosphatidylinositol 3-Kinases, Proto-Oncogene Proteins c-akt, Mice, Muscle Strength, Adrenergic beta-2 Receptor Agonists, Proteolysis
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