Deleterious Effect of High-Fat Diet on Skeletal Muscle Performance Is Prevented by High-Protein Intake in Adult Rats but Not in Old Rats.

Eleonora Poggiogalle,Patrice Lebecque,Christophe Giraudet,Christelle Guillet,Olivier Le-Bacquer,Jean-Paul Rigaudière,Véronique Patrac,Aude Carayon,Fanny Rossignon,Vincent Martin,Fréderic Capel,Yves Boirie,Jérôme Salles,Sarah De Saint Vincent,Stéphane Walrand

doi:10.3389/fphys.2021.749049

Abstract

The phenotype of sarcopenic obesity is frequently associated with impaired muscle strength and performance. Ectopic lipid deposition may interfere with muscle anabolic response especially during aging. Evidence is scarce concerning the potential interplay among aging and nutrient imbalance on skeletal muscle functionality. The objective of the present study was to investigate the impact of protein intake in the context of an obesogenic diet on skeletal muscle functional properties and intramuscular lipid infiltration. Two groups of forty-two adult and thirty-seven old male Wistar rats were randomly divided into four groups: isocaloric standard diet (12% protein, 14% lipid, as ST12); isocaloric standard (high-protein) diet (25% protein, 14% lipid, ST25); hypercaloric high-fat (normal-protein) diet (12% protein, 45% lipid, HF12); and hypercaloric high-fat (high-protein) diet (25% protein, 45% lipid, HF25). The nutritional intervention lasted 10 weeks. Total body composition was measured through Echo-MRI. Lipids were extracted from tibialis anterior muscle and analyzed by gas-liquid chromatography. The functional properties of the plantarflexor muscles were evaluated in vivo on an isokinetic dynamometer. Maximal torque was assessed from the torque-frequency relationship in isometric condition and maximal power was evaluated from the torque-velocity relationship in concentric condition. In adult rats high-protein intake combined with high-fat diet determined a lower decrease in relative isometric torque, normalized to either FFM or body weight, compared with adult rats fed a high-fat normal-protein diet. High-fat diet was also detrimental to relative muscle power, as normalized to body weight, that decreased to a larger extent in adult rats fed a high-fat normal-protein diet than their counterparts fed a normal-fat, high-protein diet. The effect of high-fat diet observed in adults, with the enhanced protein intake (25%) conferring some kind of protection against the negative effects of HFD, may be linked to the reduced intramuscular fat in this group, which may have contributed to preserve, at least partly, the contractile properties. A potential role for high-protein diet in preventing ectopic lipid deposition needs to be explored in future research. Detrimental effects of high- fat diet on skeletal muscle performance are mitigated by high- protein intake in adult rats but not in old rats.

Highlights

Sarcopenia is the progressive and generalized loss of skeletal muscle mass and function, frequently reported in older people and in patients with chronic diseases (Cruz-Jentoft et al, 2014; Tournadre et al, 2019)
Despite diets providing higher energy were administered to the HF12 and HF25 groups compared to the two ST groups, rats in the high-fat diet groups self-limited their food intake, and no significant differences were observed in calories ingested
Changes in total adiposity are displayed in Figure 1F: the adult HF12 group exhibited a higher percent increase of fat mass (FM) compared to the ST12 and the ST25 groups (HF12 vs. ST12: p = 0.007; HF12 vs. ST25: p = 0.007); the FM percent augmentation tended to be higher in the adult HF25 group than the adults ST25 group (p = 0.070) and ST12 group (p = 0.086)

Summary

Introduction

Sarcopenia is the progressive and generalized loss of skeletal muscle mass and function, frequently reported in older people and in patients with chronic diseases (Cruz-Jentoft et al, 2014; Tournadre et al, 2019). During aging or chronic diseases, one of the principal determinants of skeletal muscle protein loss is a muscle “anabolic resistance” (Paulussen et al, 2021) This metabolic alteration concerns a reduced sensitivity of muscle protein synthesis response to normal anabolic stimuli, such as nutrients and/or exercise (Guillet et al, 2004; Dardevet et al, 2012; Beals et al, 2018). In models of obesity and aging, the decreased muscle protein anabolism was associated with ectopic accumulation of specific fatty acids and derivatives (such as ceramides) involved in lipotoxicity within skeletal muscle (i.e., myosteatosis) (Tardif et al, 2014). Muscle fat infiltration affects skeletal muscle quality, as evidenced by a lower muscle strength and poor physical performance (Visser et al, 2002; Delmonico et al, 2009)

Objectives

Results

Conclusion