Autophagy controls neonatal myogenesis by regulating the GH-IGF1 system through a NFE2L2- and DDIT3-mediated mechanism

Zecchini, Silvia; Giovarelli, Matteo; Perrotta, Cristiana; Morisi, Federica; Touvier, Thierry; Renzo, Ilaria Di; Moscheni, Claudia; Bassi, Maria Teresa; Cervia, Davide; Sandri, Marco; Clementi, Emilio; Palma, Clara De

doi:10.1080/15548627.2018.1507439

Cited by 44 publications

(27 citation statements)

References 64 publications

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“…Recently, it was shown that muscle specific deletion of Atg7, a key upstream marker for the autophagic regulation, led to a severe retardation of postnatal skeletal muscle development (Zecchini et al . ), suggesting an important role of autophagic system for neonatal muscle growth. Furthermore, ablation of either fusion (Papanicolaou et al .…”

Section: Discussionmentioning

confidence: 97%

Protein composition of the muscle mitochondrial reticulum during postnatal development

Kim

Yang

Katti

2019

The Journal of Physiology

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Key pointsr Muscle mitochondrial networks changed from a longitudinal, fibre parallel orientation to a perpendicular configuration during postnatal development.r Mitochondrial dynamics, mitophagy and calcium uptake proteins were abundant during early postnatal development.r Mitochondrial biogenesis and oxidative phosphorylation proteins were upregulated throughout muscle development.r Postnatal muscle mitochondrial network formation is accompanied by a change in protein expression profile from mitochondria designed for co-ordinated cellular assembly to mitochondria highly specialized for cellular energy metabolism.Abstract Striated muscle mitochondria form connected networks capable of rapid cellular energy distribution. However, the mitochondrial reticulum is not formed at birth and the mechanisms driving network development remain unclear. In the present study, we aimed to establish the network formation timecourse and protein expression profile during postnatal development of the murine muscle mitochondrial reticulum. Two-photon microscopy was used to observe mitochondrial network orientation in tibialis anterior (TA) muscles of live mice at postnatal days (P) 1, 7, 14, 21 and 42, respectively. All muscle fibres maintained a longitudinal, fibre parallel mitochondrial network orientation early in development (P1-7). Mixed networks were most common at P14 but, by P21, almost all fibres had developed the perpendicular mitochondrial orientation observed in mature, glycolytic fibres. Tandem mass tag proteomics were then applied to examine changes in 6869 protein abundances in developing TA muscles. Mitochondrial proteins increased by 32% from P1 to P42. In addition, both nuclear-and mitochondrial-DNA encoded oxidative phosphorylation (OxPhos) components were increased during development, whereas OxPhos assembly factors decreased. Although mitochondrial dynamics and mitophagy were induced at P1-7, mitochondrial biogenesis was enhanced after P14. Moreover, calcium signalling Y. Kim and others J Physiol 597.10 proteins and the mitochondrial calcium uniporter had the highest expression early in postnatal development. In conclusion, mitochondrial networks transform from a fibre parallel to perpendicular orientation during the second and third weeks after birth in murine glycolytic skeletal muscle. This structural transition is accompanied by a change in protein expression profile from mitochondria designed for co-ordinated cellular assembly to mitochondria highly specialized for cellular energy metabolism.

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Section: Discussionmentioning

confidence: 97%

Protein composition of the muscle mitochondrial reticulum during postnatal development

Kim

Yang

Katti

2019

The Journal of Physiology

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“…The noncanonical KEAP1-NRF2 pathway has been suggested to have a role in development, disease and, specifically, cancer. For example, a deficiency of Atg7 in paired box 7 (Pax7)-positive muscle satellite cells (Atg7 F/F ;Pax7-Cre mice) results in dwarfism and decreased skeletal muscle mass in male mice only after P14, both of which are due to cell proliferation defects through decreased NRF2-target gene expression in the satellite cells (Zecchini et al, 2018). In this study, we found that an activated noncanonical KEAP1-NRF2 pathway resulted in a maturation defect of the GCTs in the SMGs of Insig1/2 cKO and Atg7 cKO mice through suppressed Foxa1 expression.…”

Section: Discussionmentioning

confidence: 99%

Cholesterol metabolism plays a crucial role in the regulation of autophagy for cell differentiation of granular convoluted tubules in male mouse submandibular glands

et al. 2019

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It has been long appreciated that sex hormone receptors are expressed in various non-gonadal organs. However, it remains unclear how sex hormones regulate the morphogenesis of these nongonadal organs. To address this issue, we used a male mouse model of androgen-dependent salivary gland morphogenesis. Mice with excessive cholesterol synthesis in the salivary glands exhibited defects in the maturation of granular convoluted tubules (GCTs), which is regulated through sex hormone-dependent cascades. We found that excessive cholesterol synthesis resulted in autophagy failure specifically in the duct cells of salivary glands, followed by the accumulation of NRF2, a transcription factor known as one of the specific substrates for autophagy. The accumulated NRF2 suppressed the expression of Foxa1, which forms a transcriptional complex with the androgen receptor to regulate target genes. Taken together, our results indicate that cholesterol metabolism plays a crucial role in GCT differentiation through autophagy.

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“…Another potential mechanism whereby IGF-1 affects SC function is via regulation of autophagy. Zecchini et al showed that autophagy is required for neonatal myogenesis and muscle development [ 137 ]. Atg7 is an E1-like activating enzyme that regulates fusion of peroxisomal and vacuolar membranes during autophagy, and Atg7 knockdown in SCs caused severe reduction in neonatal myogenesis.…”

Section: Igf-1 Satellite Cells and Skeletal Muscle Regenerationmentioning

confidence: 99%

Mechanisms of IGF-1-Mediated Regulation of Skeletal Muscle Hypertrophy and Atrophy

Yoshida

Delafontaine

2020

Cells

385

209

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Insulin-like growth factor-1 (IGF-1) is a key growth factor that regulates both anabolic and catabolic pathways in skeletal muscle. IGF-1 increases skeletal muscle protein synthesis via PI3K/Akt/mTOR and PI3K/Akt/GSK3β pathways. PI3K/Akt can also inhibit FoxOs and suppress transcription of E3 ubiquitin ligases that regulate ubiquitin proteasome system (UPS)-mediated protein degradation. Autophagy is likely inhibited by IGF-1 via mTOR and FoxO signaling, although the contribution of autophagy regulation in IGF-1-mediated inhibition of skeletal muscle atrophy remains to be determined. Evidence has suggested that IGF-1/Akt can inhibit muscle atrophy-inducing cytokine and myostatin signaling via inhibition of the NF-κΒ and Smad pathways, respectively. Several miRNAs have been found to regulate IGF-1 signaling in skeletal muscle, and these miRs are likely regulated in different pathological conditions and contribute to the development of muscle atrophy. IGF-1 also potentiates skeletal muscle regeneration via activation of skeletal muscle stem (satellite) cells, which may contribute to muscle hypertrophy and/or inhibit atrophy. Importantly, IGF-1 levels and IGF-1R downstream signaling are suppressed in many chronic disease conditions and likely result in muscle atrophy via the combined effects of altered protein synthesis, UPS activity, autophagy, and muscle regeneration.

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Autophagy controls neonatal myogenesis by regulating the GH-IGF1 system through a NFE2L2- and DDIT3-mediated mechanism

Cited by 44 publications

References 64 publications

Protein composition of the muscle mitochondrial reticulum during postnatal development

Protein composition of the muscle mitochondrial reticulum during postnatal development

Cholesterol metabolism plays a crucial role in the regulation of autophagy for cell differentiation of granular convoluted tubules in male mouse submandibular glands

Mechanisms of IGF-1-Mediated Regulation of Skeletal Muscle Hypertrophy and Atrophy

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