Skeletal muscle proteome of piglets is affected in a muscle-dependent manner by a limiting total sulfur amino acid supply

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Abstract

Purpose

A total sulfur amino acid (TSAA) deficient diet can affect the amino acid composition of skeletal muscles. However, it is unknown how the different muscle proteins are affected by the TSAA deficiency.

Methods

The proteomic profiles of the fast-twitch glycolytic longissimus (LM) and the slow-twitch oxidative rhomboideus (RM) muscles were compared in 42-day-old piglets fed either a 28% deficient (TSAA−) or a sufficient (TSAA+) diet in TSAA for 10 days. Differentially regulated proteins were identified and submitted to Gene Ontology Pathways Analysis to identify biological processes affected by TSAA deficiency.

Results

A total of 36 proteins in LM and 24 proteins in RM differed in abundance between the two dietary treatments. In both muscles, an increased oxidative energy metabolism was observed in TSAA− piglets. However, a greater mitochondrial oxidation of pyruvate generated from glycolysis was observed in LM of TSAA− piglets, whereas fatty acid β-oxidation and glycogen sparing were favored in RM. This suggests a muscle-specific reorientation of energy metabolism in response to a TSAA− deficiency. In both muscles, the protein abundance and enzyme activity of superoxide dismutase were increased in TSAA− piglets. Other enzymes involved in antioxidant defense, heat shock proteins coping with cellular stress, and annexins involved in the regulation of apoptosis were generally found to be more expressed in the LM of TSAA− piglets, with no or minor changes in RM.

Conclusions

Skeletal muscle proteome in young growing piglets was modulated in a muscle-dependent manner by a deficient TSAA supply, with accentuated changes in fast-twitch glycolytic muscle.

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Data availability

All relevant data are within the paper and its supplementary material Tables S1 and S2.

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Acknowledgements

This research was supported by the Rhodimet Research Grant 2010 from Adisseo SAS (France). The authors gratefully acknowledge P. Ecolan and S. Tacher for their excellent assistance with sampling and laboratory analyses; G. Guillemois, J.-F. Rouaud, M. Alix, and J. Liger for diet preparation and slaughter procedures; J.-F. Rouaud, P. Touanel, F. Guerin, B. Carrissant, and H. Demay (INRA, Saint-Gilles, France) for expert animal care; and I. Louveau for her helpful scientific discussions. JACA, LL, FG, YM, ST, and JvM conceived and designed the experiments; JACA performed the experiments; JACA, LL, CD-A, YM, ST, and JvM analyzed the data; JACA, LL, FG, CD-A, YM, ST, and JvM wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Jaap van Milgen.

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Table S1

Supplementary material 1: Characteristics of the protein spots identified by mass spectrometry in the longissimus muscle of piglets. (DOCX 42 kb)

Table S2

Supplementary material 2: Characteristics of the protein spots identified by mass spectrometry in the rhomboideus muscle of piglets. (DOCX 39 kb)

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Cite this article

Conde-Aguilera, J.A., Lefaucheur, L., Gondret, F. et al. Skeletal muscle proteome of piglets is affected in a muscle-dependent manner by a limiting total sulfur amino acid supply. Eur J Nutr 59, 2939–2951 (2020). https://doi.org/10.1007/s00394-019-02133-y

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Keywords

  • Methionine deficiency
  • Skeletal muscle
  • Proteome
  • Energy metabolism
  • Oxidative stress
  • Pig