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

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Skeletal muscle proteome of piglets is affected in a muscle‑dependent manner by a limiting total sulfur amino acid supply José Alberto Conde‑Aguilera1 · Louis Lefaucheur1   · Florence Gondret1 · Cristina Delgado‑Andrade2 · Yves Mercier3 · Sophie Tesseraud4 · Jaap van Milgen1 Received: 28 May 2019 / Accepted: 29 October 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019

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. Keywords  Methionine deficiency · Skeletal muscle · Proteome · Energy metabolism · Oxidative stress · Pig

Introduction The supply of dietary amino acids (AA) in right and balanced amounts is needed to improve the efficiency of protein utilization, to increase lean growth rate, and to limit nitrogen Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s0039​4-019-02133​-y) contains supplementary material, which is available to authorized users. * Jaap van Milgen [email protected] 1



INRA, AGROCAMPUS OUEST, PEGASE, Saint‑Gilles 35590, France

2



CSIC, Instituto Nacional de Alimentación y Nutrición (INAN), Armilla, Granada, Spain

3

Adisseo France SAS, Antony, France

4

INRA, BOA, Université de Tours, Nouzilly 37380, France



excretion. After Lys and Thr, total sulfur AA (TSAA, i.e., Met and Cys) are the third limiting AA for muscle deposition in young growing pigs fed cereal-soybean based diets