Defective Natriuretic Peptide Receptor Signaling in Skeletal Muscle Links Obesity to Type 2 Diabetes

Coué, Marine; Badin, Pierre Marie; Vila, Isabelle K.; Laurens, Claire; Louche, Katie; Marqués, Marie-Adeline; Bourlier, Virginie; Mouisel, Etienne; Tavernier, Geneviève; Rustan, Arild C.; Galgani, José E.; Joanisse, Denis R.; Smith, Steven R.; Langin, Dominique; Moro, Cédric

doi:10.2337/db15-0305

Cited by 79 publications

(99 citation statements)

References 45 publications

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“…In addition, chronic BNP infusion improved glucose tolerance and insulin signaling in HFD-fed and obese mice, respectively due to a reduction in lipotoxicity within the muscle31. Therefore, it is not surprising that BNP levels are inversely correlated with BMI32, indicating that the possible protective effects of BNP against obesity and diabetes are blunted in obese individuals with lower circulating BNP33.…”

Section: Discussionmentioning

confidence: 99%

Paracrine cross-talk between skeletal muscle and macrophages in exercise by PGC-1α-controlled BNP

Furrer

Eisele

Schmidt

et al. 2017

Sci Rep

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Activation of resident and infiltrating immune cells is a central event in training adaptation and other contexts of skeletal muscle repair and regeneration. A precise orchestration of inflammatory events in muscle fibers and immune cells is required after recurrent contraction-relaxation cycles. However, the mechanistic aspects of this important regulation remain largely unknown. We now demonstrate that besides a dominant role in controlling cellular metabolism, the peroxisome proliferator-activated receptor γ co-activator 1α (PGC-1α) also has a profound effect on cytokine expression in muscle tissue. Muscle PGC-1α expression results in activation of tissue-resident macrophages, at least in part mediated by PGC-1α-dependent B-type natriuretic peptide (BNP) production and secretion. Positive effects of exercise in metabolic diseases and other pathologies associated with chronic inflammation could accordingly involve the PGC-1α-BNP axis and thereby provide novel targets for therapeutic approaches.

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Section: Discussionmentioning

confidence: 99%

Paracrine cross-talk between skeletal muscle and macrophages in exercise by PGC-1α-controlled BNP

Furrer

Eisele

Schmidt

et al. 2017

Sci Rep

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“…Several lines of evidence have pointed at defective ANP signaling being an early event in the progression of metabolic dysfunction (Coué et al, 2015, Kovacova et al, 2016, Pivovarova et al, 2012). Specifically, the ratio of the gene expression levels of the natriuretic peptide receptors type A and C is decreased already at early stages of a dysregulated glucose metabolism (Kovacova et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Effect of Pancreatic Hormones on pro-Atrial Natriuretic Peptide in Humans

et al. 2017

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Plasma concentrations of pro-Atrial natriuretic peptide, proANP, are decreased in obesity and diabetes. Decreased proANP concentrations have also been noted after meal intake, and recently, a glucose-mediated regulation of ANP gene expression was reported. Hence, we evaluated the effects of insulin, glucagon and glucose on plasma proANP in a series of observational and experimental studies.Six healthy men underwent seven days of bed rest. Before and after the bed rest, hyperinsulinemic euglycemic clamps with serial plasma measurements of proANP were performed. Moreover, plasma proANP was quantified in 65 individuals with normal or impaired glucose regulation. Finally, the effects of infusion-induced hyperglucagonemia were examined in ten healthy men.Bed rest decreased insulin sensitivity and plasma proANP. The decrease in proANP was not associated with insulin sensitivity and the peptide concentrations remained constant during euglycemic hyperinsulinemia and hyperglycemic hyperglucagonemia. Impaired glucose regulation was not associated with decreased proANP concentrations.Bed rest per se induces a marked decrease in plasma proANP concentrations whereas insulin resistance and impaired glucose regulation was not associated with lower proANP concentrations. Neither acute hyperinsulinemia nor hyperglucagonemia seems to affect plasma proANP. Our findings thus suggest that decreased plasma proANP concentrations occur late in the development of insulin resistance.

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“…Triacylglycerols and diacylglycerols were determined by gas chromatography, and ceramide and sphingomyelin species by high-performance liquid chromatography-tandem mass spectrometry after total lipid extraction as described elsewhere4546.…”

Section: Methodsmentioning

confidence: 99%

Perilipin 5 fine-tunes lipid oxidation to metabolic demand and protects against lipotoxicity in skeletal muscle

Laurens

Bourlier

Mairal

et al. 2016

Sci Rep

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Lipid droplets (LD) play a central role in lipid homeostasis by controlling transient fatty acid (FA) storage and release from triacylglycerols stores, while preventing high levels of cellular toxic lipids. This crucial function in oxidative tissues is altered in obesity and type 2 diabetes. Perilipin 5 (PLIN5) is a LD protein whose mechanistic and causal link with lipotoxicity and insulin resistance has raised controversies. We investigated here the physiological role of PLIN5 in skeletal muscle upon various metabolic challenges. We show that PLIN5 protein is elevated in endurance-trained (ET) subjects and correlates with muscle oxidative capacity and whole-body insulin sensitivity. When overexpressed in human skeletal muscle cells to recapitulate the ET phenotype, PLIN5 diminishes lipolysis and FA oxidation under basal condition, but paradoxically enhances FA oxidation during forskolin- and contraction- mediated lipolysis. Moreover, PLIN5 partly protects muscle cells against lipid-induced lipotoxicity. In addition, we demonstrate that down-regulation of PLIN5 in skeletal muscle inhibits insulin-mediated glucose uptake under normal chow feeding condition, while paradoxically improving insulin sensitivity upon high-fat feeding. These data highlight a key role of PLIN5 in LD function, first by finely adjusting LD FA supply to mitochondrial oxidation, and second acting as a protective factor against lipotoxicity in skeletal muscle.

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Defective Natriuretic Peptide Receptor Signaling in Skeletal Muscle Links Obesity to Type 2 Diabetes

Cited by 79 publications

References 45 publications

Paracrine cross-talk between skeletal muscle and macrophages in exercise by PGC-1α-controlled BNP

Paracrine cross-talk between skeletal muscle and macrophages in exercise by PGC-1α-controlled BNP

Effect of Pancreatic Hormones on pro-Atrial Natriuretic Peptide in Humans

Perilipin 5 fine-tunes lipid oxidation to metabolic demand and protects against lipotoxicity in skeletal muscle

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