Abstract
This study was conducted to test the hypothesis that different dietary Met levels affect small-intestinal mucosal integrity in post-weaning piglets. Two groups of piglets (n = 6/group) were weaned at 28 days of age and randomly allotted to a basal diet (without extra Met supplementation) or a Met-supplemented diet (with 0.12 % l-Met) for 14 days. The standardized ileal digestible (SID) Met levels were 0.24 and 0.35 %, respectively. At days 7 and 14 of the trial, venous blood samples were obtained from piglets, followed by their euthanasia for tissue collection. Piglets fed the diet supplemented with l-Met had a higher average daily gain during days 7–14 and improved feed efficiency during the entire period. Concentrations of sulfur amino acids (SAA), glutamate acid (Glu), glutamine (Gln), and taurine in the plasma and tissues were higher for the piglets in the Met-supplemented group. Met supplementation increased cysteine (Cys) and glutathione (GSH) concentrations in the plasma and tissues, leading to reductions in plasma Cys/CySS redox potential and tissue GSH/GSSH redox potential. The small-intestinal mucosa of Met-supplemented piglets exhibited improved villus architecture, compared with control piglets. Met supplementation increased transepithelial electrical resistance of the jejunal mucosa. Transport of Met, Gln and Cys across the jejunal mucosa did not differ between control and Met-supplemented piglets. The abundance occludin was higher, whereas the abundance of active caspase-3 was lower, in the jejunum of the Met-supplemented piglets. Collectively, adequate dietary Met is required for optimal protein synthesis and mucosal integrity in the small intestine of post-weaning piglets.
Similar content being viewed by others
Abbreviations
- ADG:
-
Average daily gain
- ADFI:
-
Average daily feed intake
- EDTA:
-
Ethylene diaminetetraacetic acid
- FCR:
-
Feed conversion ratio
- GSH:
-
Glutathione
- Isc:
-
Transepithelial short circuit current
- KHB:
-
Krebs–Ringer bicarbonate
- MHA-FA:
-
Methionine hydroxyl analog-free acid
- PBS:
-
Phosphate-buffered saline
- SAA:
-
Sulfur amino acids
- SAM:
-
S-adenosylmethionine
- SID:
-
Standardized ileal digestible
- TEER:
-
Transepithelial electrical resistance
- TJ:
-
Tight junctions
References
AOAC (2003) Official Methods of Analysis. Association of Office Analytical Chemists, Arlington
Bauchart-Thevert C, Stoll B, Chacko S et al (2009a) Sulfur amino acid deficiency upregulates intestinal methionine cycle activity and suppresses epithelial growth in neonatal pigs. Am J Physiol Endocrinol Metab 296:E1239–E1250
Bauchart-Thevert C, Stoll B, Burrin DG (2009b) Intestinal metabolism of sulfur amino acids. Nutr Res Rev 22:175–187
Boudry G (2005) The Ussing chamber technique to evaluate alternatives to in-feed antibiotics for young pigs. Anim Res 54:718–733
Brosnan JT, Brosnan ME (2006) The sulfur-containing amino acids: an overview. J Nutr 136:1636S–1640S
Brosnan JT, Brosnan ME, Bertolo RF et al (2007a) Methionine: a metabolically unique amino acid. Livest Sci 122:2–7
Brosnan JT, da Silva R, Brosnan ME (2007b) Amino acids and the regulation of methyl balance in humans. Curr Opin Clin Nutr Metab Care 10:52–57
Burrin DG, Stoll B, Jiang R et al (2000) GLP-2 stimulates intestinal growth in premature TPN-fed pigs by suppressing proteolysis and apoptosis. Am J Physiol Gastrointest Liver Physiol 279:G1249–G1256
Conde-Aguilera JA, Barea R, Le Floc’h N et al (2010) A sulfur amino acid deficiency changes the amino acid composition of body protein in piglets. Animal 4:1349–1358
Dahm LJ, Jones DP (2000) Rat jejunum controls luminal thiol-disulfide redox. J Nutr 130:2739–2745
Dibner JJ, Ivey FJ (1992) Capacity in the liver of the broiler chick for conversion of supplement methionine activity to l-methionine. Poult Sci 71:1695–1699
Fang ZF, Yao K, Zhang XL et al (2010) Nutrition and health relevant regulation of intestinal sulfur amino acid metabolism. Amino Acids 39:633–640
Gaines AM, Yi GF, Ratliff BW et al (2005) Estimation of the ideal ratio of true ileal digestible sulfur amino acids: lysine in 8- to 26-kg nursery pigs. J Anim Sci 84:1709–1721
Gu X, Li D, She R (2002) Effect of weaning on small intestinal structure and function in the piglet. Arch Anim Nutr 56:275–286
Guo X, Rao J, Liu L et al (2003) Regulation of adherens junctions and epithelial paracellular permeability: a novel function for polyamines. Am J Physiol Cell Physiol 285:C1174–C1187
Guo X, Rao J, Liu L et al (2005) Polyamines are necessary for synthesis and stability of occludin protein in intestinal epithelial cells. Am J Physiol Cell Physiol 288:G1159–G1169
Haynes TE, Li P, Li X et al (2009) l-Glutamine or l-alanyl-l-glutamine prevents oxidant- or endotoxin- induced death of neonatal enterocytes. Amino Acids 37:131–142
He LQ, Yin YL, Li TJ et al (2013) Use of the Ussing chamber technique to study nutrient transport by epithelial tissues. Front Biosci 18:1266–1274
Hoehler D, Rademacher M, Mosenthin R (2005) Methionine requirement and commercial Methionine sources in growing pigs. Adv Pork Prod 16:109–117
Hou Y, Wang L, Zhang W et al (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242
Hou YQ, Wang L, Yi D et al (2013) N-acetylcysteine reduces inflammation in the small intestine by regulating redox, EGF and TLR4 signaling. Amino Acids 45:513–522
Jones DP (2002) Redox potential of GSH/GSSH couple: assay and biological significance. Methods Enzymol 348:93–112
Jones DP, Carlson JL, Mody VC et al (2000) Redox state of glutathione in human plasma. Free Radic Biol Med 28:625–635
Kino K, Okumura J (1986) The effect of single essential amino acid deprivation on chick growth and nitrogen and energy balance at ad libitum- and equalized-food intakes. Poult Sci 65:1728–1735
Martín-Venegas R, Rodríguez-Lagunas MJ, Mercier Y et al (2009) Effect of pH on l- and d-methionine uptake across the apical membrane of Caco-2 cells. Am J Physiol Cell Physiol 296:C632–C638
Martín-Venegas R, Brufau MT, Guerrero-Zamora AM et al (2013) The methionine precursor DL-2-hydroxy-(4-methylthio)butanoic acid protects intestinal epithelial barrier function. Food Chem 141:1702–1709
Mato JM, Martínez-Chantar ML, Lu SC (2013) S-adenosylemthionine metabolism and liver disease. Ann Hepatol 12:183–189
McCormack SA, Johnson LR (1991) Role of polyamines in gastrointestinal mucosal growth. Am J Physiol Gastrointest Liver Physiol 260:G795–G806
Miller EL (1967) Determination of the tryptophan content of feedingstuffs with particular reference to cereals. J Sci Food Agri 18:381–386
Nkabyo YS, Gu LH, Jones DP et al (2006) Thiol/disulfide redox status is oxidized in plasma and small intestinal and colonic mucosa of rats with inadequate sulfur amino acid intake. J Nutr 136:1242–1248
NRC (1998) Nutrient requirements of swine, 10th edn. Natl. Acad Press, Washington, DC
Opapeju FO, Htoo JK, Dapoza C et al (2012) Bioavailability of methionine hydroxy analog-calcium salt relative to dl-methionine to support nitrogen retention and growth in starter pigs. Animal 6:1750–1756
Owen KQ, Nelssen JL, Goodband RD et al (1995) Added dietary methionine in starter pig diets containing spray-dried blood products. J Anim Sci 73:2647–2654
Porte AG, Jänicke RU (1999) Emerging roles of caspase-3 in apoptosis. Cell Death Differ 6:99–104
Ramalingam A, Wang X, Gabello M et al (2010) Dietary methionine restriction improves colon tight junction barrier function and alters claudin expression pattern. Am J Physiol Cell Physiol 299:C1028–C1035
Rezaei R, Knabe DA, Tekwe CD et al (2013a) Dietary supplementation with monosodium glutamate is safe and improves growth performance in postweaning pigs. Amino Acids 44:911–923
Rezaei R, Wang WW, Wu ZL et al (2013b) Biochemical and physiological bases for utilization of dietary amino acids by young pigs. J Anim Sci Biotech 4:7
Rhoads JM, Wu G (2009) Glutamine, arginine, and leucine signaling in the intestine. Amino Acids 37:111–122
Riedijk MA, Stoll B, Chacko S et al (2007) Methionine transmethylation and transsulfuration in the piglet gastrointestinal tract. Proc Natl Acad Sci 104:3408–3413
Seiler N, Raul F (2005) Polyamines and apoptosis. J Cell Mol Med 9:623–642
Sholly DM (2009) Dietary fiber in swine diets: Impact on fiber degradation, disaccharidase activity, nutrient digestibility, uptake, and intestinal histology along the gastrointestinal tract. Ph.D. dissertation. Indiana: Purdue University
Shoveller AK, Stoll B, Ball RO et al (2005) Nutritional and functional importance of intestinal sulfur amino acid metabolism. J Nutr 135:1609–1612
Steed E, Balda MS, Matter K (2010) Dynamics and functions of tight junctions. Trends Cell Biol 20:142–149
Stipanuk MH (2004) Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24:539–577
Tan B, Yin YL, Kong XF et al (2010) l-Argnine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids 38:1227–1235
Tesseraud S, Coustard SM, Collin A et al (2009) Role of sulfur amino acid in controlling nutrient metabolism and cell functions: implication for nutrition. Br J Nutr 101:1132–1139
Tsukita S, Furuse M (2000) The structure and function of claudins, cell adhesion molecules at tight junctions. Ann NY Acad Sci 915:129–135
Wang JY (2007) Polyamines and mRNA stability in regulation of intestinal mucosal growth. Amino Acids 33:241–252
Wang JJ, Chen LX, Li P et al (2008) Gene expression is altered in piglet small intestinal by weaning and dietary glutamine supplementation. J Nutr 138:1025–1032
Wang WW, Qiao SY, Li DF (2009a) Amino acids and gut function. Amino Acids 37:105–110
Wang XQ, Ou DY, Yin JD et al (2009b) Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets. Amino Acids 37:209–218
Wang WW, Wu ZL, Dai ZL et al (2013) Glycine metabolism in animals and humans: implications for nutrition and health. Amino Acids 45:463–477
Wijtten PJ, ver der Meulen J, Verstegen MW (2011) Intestinal barrier function and absorption in pigs after weaning: a review. Br J Nutr 105:967–981
Williams KT, Schalinske KL (2007) New insights into the regulation of methyl group and homocysteine metabolism. J Nutr 137:311–314
Wu G (1998) Intestinal mucosal amino acid catabolism. J Nutr 128:1249–1252
Wu G (2010) Recent advances in swine amino acid nutrition. J Anim Sci Biotech 1:49–61
Wu G (2013a) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton
Wu G (2013b) Functional amino acids in nutrition and health. Amino Acids 45:407–411
Wu G, Knabe DA (1994) Free and protein-bound amino acid in sow’s colostrum and milk. J Nutr 124:415–424
Wu G, Davis PK, Flynn NE et al (1997) Endogenous synthesis of arginine plays an important role in maintaining arginine homeostasis in postweaning growing pigs. J Nutr 127:2342–2349
Wu G, Pond WG, Flynn SP et al (1998) Maternal dietary protein deficiency decreases nitric oxide synthase and ornithine decarboxylase activities in placenta and endometrium of pigs during early gestation. J Nutr 128:2395–2402
Wu G, Flynn NE, Knabe DA (2000) Enhanced intestinal synthesis of polyamines from proline in cortisol-treated piglets. Am J Physiol Endocrinol Metab 279:E395–E402
Wu G, Fang Y, Sheng Y et al (2004) Glutathione metabolism and its implications for health. J Nutr 134:489–492
Wu G, Bazer FW, Burghardt RC et al (2011a) Proline and hydroxyproline metabolism: implications for animal and human nutrition. Amino Acids 40:1053–1063
Wu G, Bazer FW, Johnson GA et al (2011b) Important roles for l-glutamine in swine nutrition and production. J Anim Sci 89:2017–2030
Wu G, Wu ZL, Dai ZL et al (2013) Dietary requirements of “nutritionally nonessential amino acids” by animals and humans. Amino Acids 44:1107–1113
Zhou X, Li DF, Yin JD et al (2007) CLA differently regulates adipogenesis in stromal vascular cells from porcine subcutaneous adipose and skeletal muscle. J Lipid Res 48:1701–1709
Acknowledgments
The research was financially supported by the National Natural Science Foundation of China (No. 31072040), and the CJ Corporation, Seoul, Korea.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Chen, Y., Li, D., Dai, Z. et al. l-Methionine supplementation maintains the integrity and barrier function of the small-intestinal mucosa in post-weaning piglets. Amino Acids 46, 1131–1142 (2014). https://doi.org/10.1007/s00726-014-1675-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-014-1675-5