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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.

References

  1. NRC (1998) Nutrient requirement of swine, 10th edn. National Academy Press, Washington

    Google Scholar 

  2. Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17. https://doi.org/10.1007/s00726-009-0269-0

    Article  CAS  PubMed  Google Scholar 

  3. Bonetto A, Penna F, Muscaritoli M, Minero VG, Rossi Fanelli F, Baccino FM, Costelli P (2009) Are antioxidants useful for treating skeletal muscle atrophy? Free Radic Biol Med 47:906–916. https://doi.org/10.1016/j.freeradbiomed.2009.07.002

    Article  CAS  PubMed  Google Scholar 

  4. Kim YI (2005) Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr 135:2703–2709

    Article  CAS  Google Scholar 

  5. Lushchak VI (2012) Glutathione homeostasis and functions: potential targets for medical interventions. J Amino Acids 2012:736837. https://doi.org/10.1155/2012/736837

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lobley GE (2003) Protein turnover—what does it mean for animal production? Can J Anim Sci 83:327–340

    Article  CAS  Google Scholar 

  7. Henriksson J (1990) The possible role of skeletal muscle in the adaptation to periods of energy deficiency. Eur J Clin Nutr 44(Suppl 1):55–64

    PubMed  Google Scholar 

  8. Just A (1982) The net energy value of crude (catabolized) protein for growth in pigs. Livest Prod Sci 9:349–360. https://doi.org/10.1016/0301-6226(82)90041-0

    Article  Google Scholar 

  9. Conde-Aguilera JA, Cobo-Ortega C, Tesseraud S, Mercier Y, van Milgen J (2014) The amino acid composition of tissue protein is affected by the total sulfur amino acid supply in growing pigs. Animal 8:401–409. https://doi.org/10.1017/S1368980008002541

    Article  CAS  PubMed  Google Scholar 

  10. Conde-Aguilera JA, Barea R, Le Floc’h N, Lefaucheur L, van Milgen J (2010) A sulfur amino acid deficiency changes the amino acid composition of body protein in piglets. Animal 4:1349–1358. https://doi.org/10.1017/S1751731110000340

    Article  CAS  PubMed  Google Scholar 

  11. Conde-Aguilera JA, Cobo-Ortega C, Tesseraud S, Lessire M, Mercier Y, van Milgen J (2013) Changes in body composition in broilers by a sulfur amino acid deficiency during growth. Poult Sci 92:1266–1275

    Article  CAS  Google Scholar 

  12. Gahl MJ, Crenshaw TD, Benevenga NJ (1994) Diminishing returns in weight, nitrogen, and lysine gain of pigs fed six levels of lysine from three supplemental sources. J Anim Sci 72:3177–3187

    Article  CAS  Google Scholar 

  13. Hamard A, Seve B, Le Floc’h N (2009) A moderate threonine deficiency differently affects protein metabolism in tissues of early-weaned piglets. Comp Biochem Physiol A 152:491–497. https://doi.org/10.1016/j.cbpa.2008.12.002

    Article  CAS  Google Scholar 

  14. Spangenburg EE, Booth FW (2003) Molecular regulation of individual skeletal muscle fibre types. Acta Physiol Scand 178:413–424

    Article  CAS  Google Scholar 

  15. Gomez-Requeni P, de Vareilles M, Kousoulaki K, Jordal AEO, Conceicao LEC, Ronnestad I (2011) Whole body proteome response to a dietary lysine imbalance in zebrafish Danio rerio. Comp Biochem Physiol D 6:178–186. https://doi.org/10.1016/j.cbd.2011.02.002

    Article  CAS  Google Scholar 

  16. Zhai W, Araujo LF, Burgess SC, Cooksey AM, Pendarvis K, Mercier Y, Corzo A (2012) Protein expression in pectoral skeletal muscle of chickens as influenced by dietary methionine. Poult Sci 91:2548–2555. https://doi.org/10.3382/ps.2012-02213

    Article  CAS  PubMed  Google Scholar 

  17. Conde-Aguilera JA, 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. Eur J Nutr 55:117–126. https://doi.org/10.1007/s00394-014-0830-9

    Article  CAS  PubMed  Google Scholar 

  18. Lefaucheur L (2010) A second look into fibre typing—relation to meat quality. Meat Sci 84:257–270. https://doi.org/10.1016/j.meatsci.2009.05.004

    Article  CAS  PubMed  Google Scholar 

  19. Henry Y (1993) Affinement du concept de la protéine idéale pour le porc en croissance. INRA Prod Anim 6:199–212

    Article  Google Scholar 

  20. Vincent A, Louveau I, Gondret F, Trefeu C, Gilbert H, Lefaucheur L (2015) Divergent selection for residual feed intake affects the transcriptomic and proteomic profiles of pig skeletal muscle. J Anim Sci 93:2745–2758. https://doi.org/10.2527/jas.2015-8928

    Article  CAS  PubMed  Google Scholar 

  21. Huang DW, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37:1–13. https://doi.org/10.1093/nar/gkn923

    Article  CAS  Google Scholar 

  22. Castellano R, Perruchot MH, Conde-Aguilera JA, van Milgen J, Collin A, Tesseraud S, Mercier Y, Gondret F (2015) A methionine deficient diet enhances adipose tissue lipid metabolism and alters anti-oxidant pathways in young growing pigs. PLoS One. https://doi.org/10.1371/journal.pone.0130514

    Article  PubMed  PubMed Central  Google Scholar 

  23. SAS (2004) Statistical analysis system release/STAT 9.1 user’s guide. SAS Institute Inc., Cary

    Google Scholar 

  24. Katsumata M, Kobayashi H, Ashihara A, Ishida A (2018) Effects of dietary lysine levels and lighting conditions on intramuscular fat accumulation in growing pigs. Anim Sci J 89:988–993. https://doi.org/10.1111/asj.13019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Hasek BE, Stewart LK, Henagan TM, Boudreau A, Lenard NR, Black C, Shin J, Huypens P, Malloy VL, Plaisance EP, Krajcik RA, Orentreich N, Gettys TW (2010) Dietary methionine restriction enhances metabolic flexibility and increases uncoupled respiration in both fed and fasted states. Am J Physiol Integr Comp Physiol 299:R728–R739. https://doi.org/10.1152/ajpregu.00837.2009

    Article  CAS  Google Scholar 

  26. Yamashita K, Yoshioka T (1991) Profiles of creatinine-kinase isoenzyme compositions in single muscle-fibers of different types. J Muscle Res Cell Motil 12:37–44. https://doi.org/10.1007/bf01781172

    Article  CAS  PubMed  Google Scholar 

  27. Chin ER, Olson EN, Richardson JA, Yano Q, Humphries C, Shelton JM, Wu H, Zhu WG, Bassel-Duby R, Williams RS (1998) A calcineurin-dependent transcriptional pathway controls skeletal muscle fiber type. Genes Dev 12:2499–2509. https://doi.org/10.1101/gad.12.16.2499

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Katsumata M, Matsumoto M, Kobayashi S-i, Kaji Y (2008) Reduced dietary lysine enhances proportion of oxidative fibers in porcine skeletal muscle. Anim Sci J 79:347–353. https://doi.org/10.1111/j.1740-0929.2008.00536.x27

    Article  CAS  Google Scholar 

  29. Katsumata M, Matsumoto M, Kaji Y (2003) Effects of a low lysine diet on glucose metabolism in skeletal muscle of growing pigs. In: Souffrant WB, Metges CC (eds) Progress in research on energy and protein metabolism. european association for animal production publication, vol 109. Wageningen Academic Publishers, Wageningen, pp 187–190

    Google Scholar 

  30. Gomez-Requeni P, Mingarro M, Kirchner S, Calduch-Giner JA, Medale F, Corraze G, Panserat S, Martin SAM, Houlihan DF, Kaushik SJ, Perez-Sanchez J (2003) Effects of dietary amino acid profile on growth performance, key metabolic enzymes and somatotropic axis responsiveness of gilthead sea bream (Sparus aurata). Aquaculture 220:749–767. https://doi.org/10.1016/s0044-8486(02)00654-3

    Article  CAS  Google Scholar 

  31. Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  CAS  Google Scholar 

  32. Song IS, Kim HK, Jeong SH, Lee SR, Kim N, Rhee BD, Ko KS, Han J (2011) Mitochondrial peroxiredoxin III is a potential target for cancer therapy. Int J Mol Sci 12:7163–7185. https://doi.org/10.3390/ijms12107163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Krishnan N, Dickman MB, Becker DF (2008) Proline modulates the intracellular redox environment and protects mammalian cells against oxidative stress. Free Radic Biol Med 44:671–681. https://doi.org/10.1016/j.freeradbiomed.2007.10.054

    Article  CAS  PubMed  Google Scholar 

  34. Yasuda T, Kaji Y, Agatsuma T, Niki T, Arisawa M, Shuto S, Ariga H, Iguchi-Ariga SM (2013) DJ-1 cooperates with PYCR34 in cell protection against oxidative stress. Biochem Biophys Res Commun 436:289–294

    Article  CAS  Google Scholar 

  35. Del Vesco AP, Gasparino E, Grieser DO, Zancanela V, Gasparin FRS, Constantin J, Oliveira Neto AR (2014) Effects of methionine supplementation on the redox state of acute heat stress-exposed quails. J Anim Sci 92:806–815. https://doi.org/10.2527/jas2013-6829

    Article  CAS  PubMed  Google Scholar 

  36. Paulsen G, Vissing K, Kalhovde JM, Ugelstad I, Bayer ML, Kadi F, Schjerling P, Hallen J, Raastad T (2007) Maximal eccentric exercise induces a rapid accumulation of small heat shock proteins on myofibrils and a delayed HSP70 response in humans. Am J Physiol Regul Integr Comp Physiol 293:R844–R853. https://doi.org/10.1152/ajpregu.00677.2006

    Article  CAS  PubMed  Google Scholar 

  37. Mustafi SB, Chakraborty PK, Dey RS, Raha S (2009) Heat stress upregulates chaperone heat shock protein 70 and antioxidant manganese superoxide dismutase through reactive oxygen species (ROS), p38MAPK, and Akt. Cell Stress Chaperon 14:579–589. https://doi.org/10.1007/s12192-009-0109-x

    Article  CAS  Google Scholar 

  38. Fu L, Liang JJ (2003) Enhanced stability of alpha B-crystallin in the presence of small heat shock protein Hsp27. Biochem Biophys Res Commun 302:710–714

    Article  CAS  Google Scholar 

  39. Gerke V, Moss SE (1997) Annexins and membrane dynamics. Biochim Biophys Acta 1357:129–154. https://doi.org/10.1016/s0167-4889(97)00038-4

    Article  CAS  PubMed  Google Scholar 

  40. Leffler J, Herbert AP, Norstrom E, Schmidt CQ, Barlow PN, Blom AM, Martin M (2010) Annexin-II, DNA, and histones serve as factor H ligands on the surface of apoptotic cells. J Biol Chem 285:3766–3776. https://doi.org/10.1074/jbc.M109.045427

    Article  CAS  PubMed  Google Scholar 

  41. Sauvant D, Perez JM, Tran G (2004) Tables of composition and nutritional value of feed materials. Pigs, poultry, cattle, sheep, goats, rabbits, horses, fish. INRA Editions, Paris, France

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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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Authors and Affiliations

  1. INRA, AGROCAMPUS OUEST, PEGASE, Saint-Gilles, 35590, France

    José Alberto Conde-Aguilera, Louis Lefaucheur, Florence Gondret & Jaap van Milgen

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

    Cristina Delgado-Andrade

  3. Adisseo France SAS, Antony, France

    Yves Mercier

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

    Sophie Tesseraud

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  1. José Alberto Conde-Aguilera
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Correspondence to Jaap van Milgen.

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Electronic supplementary material

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394_2019_2133_MOESM1_ESM.docx

Supplementary material 1: Table S1 Characteristics of the protein spots identified by mass spectrometry in the longissimus muscle of piglets. (DOCX 42 kb)

394_2019_2133_MOESM2_ESM.docx

Supplementary material 2: Table S2 Characteristics of the protein spots identified by mass spectrometry in the rhomboideus muscle of piglets. (DOCX 39 kb)

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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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