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Increasing whole-body energetic stress does not augment fasting-induced changes in human skeletal muscle

  • Muscle physiology
  • Published:
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Abstract

Fasting rapidly (≤ 6 h) activates mitochondrial biogenic pathways in rodent muscle, an effect that is absent in human muscle following prolonged (10–72 h) fasting. We tested the hypotheses that fasting-induced changes in human muscle occur shortly after food withdrawal and are modulated by whole-body energetic stress. Vastus lateralis biopsies were obtained from ten healthy males before, during (4 h), and after (8 h) two supervised fasts performed with (FAST+EX) or without (FAST) 2 h of arm ergometer exercise (~ 400 kcal of added energy expenditure). PGC-1α mRNA (primary outcome measure) was non-significantly reduced (p = 0.065 [ηp2 = 0.14]) whereas PGC-1α protein decreased (main effect of time: p < 0.01) during both FAST and FAST+EX. P53 acetylation increased in both conditions (main effect of time: p < 0.01) whereas ACC and SIRT1 phosphorylation were non-significantly decreased (both p < 0.06 [ηp2 = 0.15]). Fasting-induced increases in NFE2L2 and NRF1 protein were observed (main effects of time: p < 0.03), though TFAM and COXIV protein remained unchanged (p > 0.05). Elevating whole-body energetic stress blunted the increase in p53 mRNA, which was apparent during FAST only (condition × time interaction: p = 0.04). Select autophagy/mitophagy regulators (LC3BI, LC3BII, BNIP3) were non-significantly reduced at the protein level (p ≤ 0.09 [ηp2 > 0.13]) but the LC3II:I ratio was unchanged (p > 0.05). PDK4 mRNA (p < 0.01) and intramuscular triglyceride content in type IIA fibers (p = 0.04) increased similarly during both conditions. Taken together, human skeletal muscle signaling, mRNA/protein expression, and substrate storage appear to be unaffected by whole-body energetic stress during the initial hours of fasting.

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Acknowledgments

We would like to thank all participants for their time and effort.

Funding

This work was supported by funding provided to B.J.G. from the Natural Sciences and Engineering Research Council of Canada (NSERC; grant no. 402635). H.I. was supported by a post-graduate scholarship (Doctoral) from NSERC.

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Authors and Affiliations

  1. School of Kinesiology and Health Studies, Queen’s University, Kingston, Ontario, Canada

    Hashim Islam, Alessandra Amato, Jacob T. Bonafiglia, Nicholas Preobrazenski, Craig A. Simpson & Brendon J. Gurd

  2. Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada

    Fasih A. Rahman, Andrew Ma & Joe Quadrilatero

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Contributions

H.I., A.A., and B.J.G conceptualized and designed the study. H.I., A.A., C.A.S., and B.J.G. collected the data. H.I., A.A., J.T.B., F.A.R., N.P., A.M., J.Q., and B.J.G. contributed to data analysis and interpretation. H.I. drafted the first version of the manuscript. All authors contributed to manuscript revisions and approved the final version of the manuscript.

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Correspondence to Brendon J. Gurd.

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Fig S1

Representative images for GAPDH and amido black staining for total protein. (PNG 78 kb)

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Fig S2

NFE2L2 (A), LRP130 (B) and SIRT1 (C) mRNA expression in the vastus lateralis before (PRE), during (MID; 4 hours) and after (POST; 8 hours) an acute fast performed with (FAST+EX; grey boxes) or without (FAST; white boxes) 2-hours of low-intensity arm ergometer exercise (n=10). Note: Boxes, whiskers, horizontal lines, and crosses indicate interquartile ranges, min/max values, medians, and means, respectively (PNG 127 kb)

High Resolution (TIFF 204 kb)

Fig S3

Expression of protein involved in intracellular signaling (A), mitochondrial biogenesis (B- D), and autophagy/mitophagy (E-I) in the vastus lateralis before (PRE), during (MID; 4 hours) and after (POST; 8 hours) an acute fast performed with (FAST+EX; grey boxes) or without (FAST; white boxes) 2-hours of low-intensity arm ergometer exercise (n = 10). Note: Boxes, whiskers, horizontal lines, and crosses indicate interquartile ranges, min/max values, medians, and means, respectively. Significant/near- significant main effects and interactions (two-way RM- ANOVA) are reported below graphs where appropriate. Symbols denote significant (* p < 0.05) or near- significant (# p < 0.10) difference versus PRE (Bonferroni post-hoc). (PNG 559 kb)

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Islam, H., Amato, A., Bonafiglia, J.T. et al. Increasing whole-body energetic stress does not augment fasting-induced changes in human skeletal muscle. Pflugers Arch - Eur J Physiol 473, 241–252 (2021). https://doi.org/10.1007/s00424-020-02499-7

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