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Longissimus, rhomboideus, and semitendinosus muscles

Skeletal muscles account for approximately 50% of the body mass of the animal. For their functioning and development, total sulphur amino acids (TSAA), methionine and cysteine, play a key role as structural components of muscle protein, but they also have important functional roles such as in the antioxidant defense via glutathione (cysteine-glutamate-glycine). Changes in glutathione concentrations as a result of a TSAA deficiency have been reported in splanchnic tissues, but no information is available for skeletal muscles. Moreover, a limiting supply of essential amino acids (AA) changes the balance between protein synthesis and protein degradation, which may explain changes in muscle mass. Also, the dietary AA supply can affect the AA composition of muscle protein. However, it is not known if these all changes are accompanied by changes in the contractile and metabolic properties of skeletal muscles and if muscles respond in a similar way to a deficient TSAA content of the diet.
The aim of this study was therefore to evaluate the changes in composition, and contractile and metabolic properties three morphologically, functionally, and metabolically different skeletal muscles in piglets receiving a diet with a deficient or sufficient TSAA supply.

Different physiological responses depending on muscle type

A deficient TSAA supply of 28% reduced the relative weight, protein mass and synthesis of the longissimus muscle (LM) by 10 to 32%, while the rhomboideus muscle (RM) and the semitendinous muscle (SM) were not affected. The TSAA content of the diet affect the AA composition of muscles. Concentrations of methionine and branched-chain AA (valine, leucine, and isoleucine) were respectively 7% and 3% lower in piglets receiving the deficient TSAA diet (TSAA–) compared with those receiving the control diet. Total and reduced glutathione concentrations were about 2 times greater in RM than in LM or SM, which is consistent with a higher antioxidant capacity of oxidative muscles compared with glycolytic muscles. The glutathione concentration was affected by the TSAA supply and was on average 10% lower in TSAA– pigs than in control pigs. The histidine concentration was 30% higher in LM and SM in TSAA– pigs than in control pigs, and unaffected in RM, which was accompanied by a greater carnosine concentration in the oxidative muscles of TSAA– pigs. Carnosine is an histidine-containing dipeptide, which acts as an antioxidant in muscle and increases the buffering capacity. The decrease in glutathione concentration and the increase in carnosine concentration in TSAA– pigs may indicate that the pigs changed (or: were forced to change) the mechanisms to face oxidative stress. The activity of citrate synthase, a global oxidative potential indicator, was 14% higher in all three muscles of TSAA– pigs. In these deficient pigs, the β-hydroxy-acyl-CoA dehydrogenase activity, an indicator of fatty acid oxidation, was 20% higher in RM compared with control pigs, while the activity of lactate dehydrogenase, an indicator of glycolytic potential, was 21% lower in LM. This result coincided with the shift from type IIB (glycolytic type) to type I fibers (oxidative type) in RM of TSAA– pigs, which could be explained by the observed differences in the AA composition among muscles.

The underlying mechanisms, course to proteomics?

Our study shows that growing piglets responded in a muscle-dependent manner to a deficient TSAA supply. This occurred by reducting growth rate and glycolytic metabolism of LM, and increasesing the oxidative metabolism and capacity to oxidize fatty acids of RM, whereas the glutathione concentration, as an indicator of the antioxidant status, was lower. We hypothesize that the change in AA composition of the tissue protein by a limiting TSAA supply may be the result of changing the proportions of different types of proteins. Further studies involving proteomics could help to understand the underlying mechanisms of how the animal responds to a deficient AA supply. The observation that the animals responds in different ways to a nutrient deficiency also illustrates the limitations of using a single criterion to appreciate nutrient requirements.

These studies were partially funded by the private company Adisseo France SAS and exhibited in numerous scientific and technical presentations in France, Turkey, Brazil and Spain.

For further information

Conde-Aguilera, J. A., Lefaucheur, L., Tesseraud, S., Mercier, Y., Le Floc'h, N., Van Milgen, J. (2015). Skeletal muscles respond differently when piglets are offered a diet 30 % deficient in total sulfur amino acid for 10 days. European Journal of Nutrition. (DOI)

Conde-Aguilera, J. A., Le Floc’h, N., Le Huërou-Luron, I., Mercier, Y., Tesseraud, S., Lefaucheur, L., van Milgen, J. (2015). Splanchnic tissues respond differently when piglets are offered a diet 30 % deficient in total sulfur amino acid for 10 days. European Journal of Nutrition. (DOI)

Conde-Aguilera J.A., C. Cobo-Ortega, S. Tesseraud, Y. Mercier, J. van Milgen. 2014. The amino acid composition of tissue protein is affected by the total sulfur amino acid supply in growing pigs. Animal 8 (3). (DOI)

Conde-Aguilera J.A., R. Barea, N. Le Floc’h, L. Lefaucheur, J. van Milgen. 2010. A sulfur amino acid deficiency changes the amino acid composition of body protein in piglets. Animal 4 (8): 1349-1358. (DOI)

Contact

Alberto Conde-Aguilera, team Feeding and Nutrition (alberto.conde[at]rennes.inra.fr)