Skip to main content
SpringerLink
Log in

Splanchnic tissues respond differently when piglets are offered a diet 30 % deficient in total sulfur amino acid for 10 days

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

A deficient total sulfur amino acid (TSAA) supply has been reported to differently affect the amino acid composition of tissues, but limited information is available about its effects on the morphology and metabolic properties of splanchnic tissues.

Methods

The amino acid composition, protein metabolism, glutathione concentration of the liver, proximal and distal jejunum, ileum and kidneys, and intestinal architecture were compared in 42-day-old piglets pair-fed either a diet deficient (TSAA−; 28 % deficiency) or sufficient (TSAA+) in TSAA for 10 days.

Results

The supply of TSAA had no effect on tissue weights, but influenced the amino acid composition in a tissue-dependent manner. Compared with animals receiving diet TSAA+, the concentrations of Met and Ser were higher in liver protein of TSAA− animals while the Cys concentration in protein was lower in the liver but higher in the distal jejunum. The TSAA supply had no effect on protein synthesis and proteolytic activities of tissues. Villus width and surface, and crypt surface were lower in the proximal jejunum of TSAA− versus TSAA+ pigs. Crypt surface in the ileum of TSAA− pigs was higher. Pigs receiving diet TSAA− had lower GSH and GSSG concentrations in the liver and proximal jejunum, but the GSH/GSSG ratio was decreased only in the liver.

Conclusions

A greater nutritional priority appears to be given to splanchnic tissues so that its growth and protein metabolism can be maintained when the TSAA supply is limiting. The amino acid composition, glutathione status, and intestinal mucosa architecture are affected in a tissue-dependent manner.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

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

    Google Scholar 

  2. Chung TK, Baker DH (1992) Efficiency of dietary methionine utilization by young pigs. J Nutr 122(9):1862–1869

    CAS  Google Scholar 

  3. Kim YI (2005) Nutritional epigenetics: impact of folate deficiency on DNA methylation and colon cancer susceptibility. J Nutr 135(11):2703–2709

    CAS  Google Scholar 

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

    Article  Google Scholar 

  5. 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(8):1349–1358. doi:10.1017/S1751731110000340

    Article  CAS  Google Scholar 

  6. Seve B, Ponter AA (1997) Nutrient-hormone signals regulating muscle protein turnover in pigs. Proc Nutr Soc 56(2):565–580. doi:10.1079/pns19970058

    Article  CAS  Google Scholar 

  7. Lobley GE (1993) Species comparisons of tissue protein-metabolim—effects of age and hormonal action. J Nutr 123(2):337–343

    CAS  Google Scholar 

  8. Sugden PH, Fuller SJ (1991) Regulation of protein turnover in skeletal and cardiac muscle. Biochem J 273(Pt 1):21–37

    Article  CAS  Google Scholar 

  9. Tesseraud S, Peresson R, Lopes J, Chagneau AM (1996) Dietary lysine deficiency greatly affects muscle and liver protein turnover in growing chickens. Br J Nutr 75(6):853–865

    Article  CAS  Google Scholar 

  10. 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 Mol Integr Physiol 152(4):491–497. doi:10.1016/j.cbpa.2008.12.002

    Article  Google Scholar 

  11. Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136(6 Suppl):1636S–1640S

    CAS  Google Scholar 

  12. Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577

    Article  CAS  Google Scholar 

  13. Shoveller AK, Stoll B, Ball RO, Burrin DG (2005) Nutritional and functional importance of intestinal sulfur amino acid metabolism. J Nutr 135(7):1609–1612

    CAS  Google Scholar 

  14. Riedijk MA, Stoll B, Chacko S, Schierbeek H, Sunehag AL, van Goudoever JB, Burrin DG (2007) Methionine transmethylation and transsulfuration in the piglet gastrointestinal tract. Proc Natl Acad Sci USA 104(9):3408–3413. doi:10.1073/pnas.0607965104

    Article  CAS  Google Scholar 

  15. Bauchart-Thevret C, Cottrell J, Stoll B, Burrin DG (2011) First-pass splanchnic metabolism of dietary cysteine in weanling pigs. J Anim Sci 89:4093–4099. doi:10.2527/jas.2011-3944

    Article  CAS  Google Scholar 

  16. Bauchart-Thevret C, Stoll B, Chacko S, Burrin DG (2009) Sulfur amino acid deficiency upregulates intestinal methionine cycle activity and suppresses epithelial growth in neonatal pigs. Am J Physiol Endocrinol Metab 296(6):E1239–E1250. doi:10.1152/ajpendo.91021.2008

    Article  CAS  Google Scholar 

  17. Hamard A, Mazurais D, Boudry G, Le Huerou-Luron I, Seve B, Le Floc’h N (2010) A moderate threonine deficiency affects gene expression profile, paracellular permeability and glucose absorption capacity in the ileum of piglets. J Nutr Biochem 21(10):914–921. doi:10.1016/j.jnutbio.2009.07.004

    Article  CAS  Google Scholar 

  18. Ebner S, Schoknecht P, Reeds P, Burrin D (1994) Growth and metabolism of gastrointestinal and skeletal muscle tissues in protein-malnourished neonatal pigs. Am J Physiol 266(6 Pt 2):R1736–R1743

    CAS  Google Scholar 

  19. 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. doi:10.1007/s00394-014-0830-9

    Google Scholar 

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

    Google Scholar 

  21. Seve B, Ballevre O, Ganier P, Noblet J, Prugnaud J, Obled C (1993) Recombinant porcine somatotropin and dietary protein enhance protein synthesis in growing pigs. J Nutr 123(3):529–540

    CAS  Google Scholar 

  22. Griffith OW (1980) Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal Biochem 106(1):207–212. doi:10.1016/0003-2697(80)90139-6

    Article  CAS  Google Scholar 

  23. Goodlad RA, Levi S, Lee CY, Mandir N, Hodgson H, Wright NA (1991) Morphometry and cell-proliferation in endoscopic biopsies—evaluation of a technique. Gastroenterology 101(5):1235–1241

    Article  CAS  Google Scholar 

  24. SAS (2004) SAS/STAT 9.1 user’s guide. SAS Institute Inc., Cary

    Google Scholar 

  25. Buddington RK, Elnif J, Puchal-Gardiner AA, Sangild PT (2001) Intestinal apical amino acid absorption during development of the pig. Am J Physiol Regul Integr Comp Physiol 280(1):R241–R247

    CAS  Google Scholar 

  26. Faure M, Moennoz D, Montigon F, Mettraux C, Breuille D, Ballevre O (2005) Dietary threonine restriction specifically reduces intestinal mucin synthesis in rats. J Nutr 135(3):486–491

    CAS  Google Scholar 

  27. Rivera-Ferre MG, Aguilera JF, Nieto R (2006) Differences in whole-body protein turnover between Iberian and Landrace pigs fed adequate or lysine-deficient diets. J Anim Sci 84(12):3346–3355. doi:10.2527/jas.2005-405

    Article  CAS  Google Scholar 

  28. Wang X, Qiao SY, Yin YL, Yue LY, Wang ZY, Wu GY (2007) A deficiency or excess of dietary threonine reduces protein synthesis in jejunum and skeletal muscle of young pigs. J Nutr 137(6):1442–1446

    CAS  Google Scholar 

  29. Sève B, Reeds PJ, Fuller MF, Cadenhead A, Hay SM (1986) Protein synthesis and retention in some tissues of the young-pig as influenced by dietary-protein intake after early-weaning. Possible connection to the energy metabolism. Reprod Nutr Dev 26(3):849–861. doi:10.1051/rnd:19860509

    Article  Google Scholar 

  30. Ponter AA, Cortamira NO, Seve B, Salter DN, Morgan LM (1994) The effects of energy source and tryptophan on the rate of protein synthesis and on hormones of the entero-insular axis in the piglet. Br J Nutr 71(5):661–674

    Article  CAS  Google Scholar 

  31. Schaart MW, Schierbeek H, van der Schoor SRD, Stoll B, Burrin DG, Reeds PJ, van Goudoever JB (2005) Threonine utilization is high in the intestine of piglets. J Nutr 135(4):765–770

    CAS  Google Scholar 

  32. Le Floc’h N, Seve B (2005) Catabolism through the threonine dehydrogenase pathway does not account for the high first-pass extraction rate of dietary threonine by the portal drained viscera in pigs. Br J Nutr 93(4):447–456. doi:10.1079/bjn20051375

    Article  Google Scholar 

  33. Chen Y, Li DF, Dai ZL, Piao XS, Wu ZL, Wang B, Zhu YH, Zeng ZK (2014) l-Methionine supplementation maintains the integrity and barrier function of the small-intestinal mucosa in post-weaning piglets. Amino Acids 46(4):1131–1142. doi:10.1007/s00726-014-1675-5

    Article  CAS  Google Scholar 

  34. 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(3):401–409. doi:10.1017/S1368980008002541

    Article  CAS  Google Scholar 

  35. Marion J, Biernat M, Thomas F, Savary G, Le Breton Y, Zabielski R, Le Huerou-Luron I, Le Dividich J (2002) Small intestine growth and morphometry in piglets weaned at 7 days of age. Effects of level of energy intake. Reprod Nutr Dev 42(4):339–354. doi:10.1051/rnd:2002030

    Article  CAS  Google Scholar 

  36. Hamard A, Seve B, Le Floc’h N (2007) Intestinal development and growth performance of early-weaned piglets fed a low-threonine diet. Animal 1(8):1134–1142. doi:10.1017/S1751731107000560

    Article  CAS  Google Scholar 

  37. Boudry G, Peron V, Le Huerou-Luron I, Lalles JP, Seve B (2004) Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. J Nutr 134(9):2256–2262

    CAS  Google Scholar 

  38. Kansagra K, Stoll B, Rognerud C, Niinikoski H, Ou CN, Harvey R, Burrin D (2003) Total parenteral nutrition adversely affects gut barrier function in neonatal piglets. Am J Physiol Gastrointest Liver Physiol 285(6):G1162–G1170. doi:10.1152/ajpgi.00243.2003

    Article  CAS  Google Scholar 

  39. Aw TY (1999) Molecular and cellular responses to oxidative stress and changes in oxidation-reduction imbalance in the intestine. Am J Clin Nutr 70(4):557–565

    CAS  Google Scholar 

  40. Bauchart-Thevret C, Stoll B, Burrin DG (2009) Intestinal metabolism of sulfur amino acids. Nutr Res Rev 22(2):175–187. doi:10.1017/S0954422409990138

    Article  CAS  Google Scholar 

  41. Jonas CR, Ziegler TR, Gu LH, Jones DP (2002) Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma (Caco2) cell line. Free Radic Biol Med 33(11):1499–1506

    Article  CAS  Google Scholar 

  42. Noda T, Iwakiri R, Fujimoto K, Aw TY (2001) Induction of mild intracellular redox imbalance inhibits proliferation of CaCo-2 cells. FASEB J 15(12):2131–2139. doi:10.1096/fj.01-0131com

    Article  CAS  Google Scholar 

  43. Lash LH (2011) Renal membrane transport of glutathione in toxicology and disease. Vet Pathol 48(2):408–419. doi:10.1177/0300985810375811

    Article  CAS  Google Scholar 

  44. Anderson ME, Meister A (1980) Dynamic state of glutathione in blood plasma. J Biol Chem 255(20):9530–9533

    CAS  Google Scholar 

  45. Griffith OW, Meister A (1979) Glutathione: interorgan translocation, turnover, and metabolism. Proc Natl Acad Sci USA 76(11):5606–5610

    Article  CAS  Google Scholar 

  46. Morand C, Rios L, Moundras C, Besson C, Remesy C, Demigne C (1997) Influence of methionine availability on glutathione synthesis and delivery by the liver. J Nutr Biochem 8(5):246–255. doi:10.1016/s0955-2863(97)89661-1

    Article  CAS  Google Scholar 

  47. Richie JP, Komninou D, Leutzinger Y, Kleinman W, Orentreich N, Malloy V, Zimmerman JA (2004) Tissue glutathione and cysteine levels in methionine-restricted rats. Nutrition 20(9):800–805. doi:10.1016/j.nut.2004.05.009

    Article  CAS  Google Scholar 

  48. Lu SC (2009) Regulation of glutathione synthesis. Mol Aspects Med 30(1–2):42–59. doi:10.1016/j.mam.2008.05.005

    Article  CAS  Google Scholar 

  49. Miller LT, Watson WH, Kirlin WG, Ziegler TR, Jones DP (2002) Oxidation of the glutathione/glutathione disulfide redox state is induced by cysteine deficiency in human colon carcinoma HT29 cells. J Nutr 132(8):2303–2306

    CAS  Google Scholar 

  50. Perez-Vilar J, Hill R (2004) Mucin family of glycoproteins. In: Lennarz WJ, Lane E (eds) Encyclopedia of biological chemistry. Academic Press/Elsevier, Oxford, pp 758–764

    Chapter  Google Scholar 

  51. Van Klinken BJ, Dekker J, Buller HA, de Bolos C, Einerhand AW (1997) Biosynthesis of mucins (MUC2-6) along the longitudinal axis of the human gastrointestinal tract. Am J Physiol 273(2 Pt 1):G296–G302

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Rhodimet Research Grant 2010 from Adisseo SAS (France). The authors gratefully acknowledge Nadine Mézière, Colette Mustière, Yolande Jaguelin, Armelle Cahu, Michèle Formal, Jean Noël Thibault and Philippe Ganier for their excellent assistance with sampling and laboratory analyses, Alain Chauvin, Regis Janvier, Francis Le Gouevec and Vincent Piedvache, for surgical procedures and animal care, Maurice Alix, Georges Guillemois, Jérôme Liger and Jean-François Rouaud for diet preparation and slaughter procedures (INRA, Saint-Gilles, France). J.A.C-A., N.L.F., I.LH-L., L.L., Y.M., S.T. and J.V.M. designed and conducted the research, wrote the paper and had primary responsibility for the final content; J.A.C-A. analyzed the data. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. UMR1348 PEGASE, INRA, 35590, Saint-Gilles, France

    José Alberto Conde-Aguilera, Nathalie Le Floc’h, Louis Lefaucheur & Jaap van Milgen

  2. UMR1348 PEGASE, Agrocampus Ouest, 35000, Rennes, France

    José Alberto Conde-Aguilera, Nathalie Le Floc’h, Louis Lefaucheur & Jaap van Milgen

  3. UR 1341, ADNC, INRA, 35590, Saint-Gilles, France

    Isabelle Le Huërou-Luron

  4. Adisseo France SAS, 92160, Antony, France

    Yves Mercier

  5. UR83 Recherches Avicoles, INRA, 37380, Nouzilly, France

    Sophie Tesseraud

Authors
  1. José Alberto Conde-Aguilera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nathalie Le Floc’h
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Isabelle Le Huërou-Luron
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yves Mercier
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sophie Tesseraud
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Louis Lefaucheur
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jaap van Milgen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jaap van Milgen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Conde-Aguilera, J.A., Le Floc’h, N., Le Huërou-Luron, I. et al. Splanchnic tissues respond differently when piglets are offered a diet 30 % deficient in total sulfur amino acid for 10 days. Eur J Nutr 55, 2209–2219 (2016). https://doi.org/10.1007/s00394-015-1031-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-015-1031-x

Keywords

Search

Navigation