Sulfur amino acid deficiency upregulates intestinal methionine cycle activity and suppresses epithelial growth in neonatal pigs

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 6, 2009, Pages

  Bauchart Thevret, Caroline ^b   Stoll, Barbara ^b   Chacko, Shaji ^b   Burrin, Douglas G ^a  

^a CHILDREN S NUTRITION RESEARCH CENTER   (United States)

^b NONE

Author keywords

Homocysteine; Remethylation; Transmethylation; Transsulfuration

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; CYSTEINE; HOMOCYSTEINE; METHIONINE; METHIONINE ADENOSYLTRANSFERASE; METHIONINE SYNTHASE; S ADENOSYLMETHIONINE; SULFUR AMINO ACID; TAURINE;

AMINO ACID BLOOD LEVEL; AMINO ACID DEFICIENCY; AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CRYPT CELL; ENZYME ACTIVITY; FEMALE; GOBLET CELL; INTESTINE MUCOSA; MORPHOMETRICS; NONHUMAN; OXIDATION REDUCTION REACTION; PIGLET; PRIORITY JOURNAL; PROTEIN SYNTHESIS; STEADY STATE; WEIGHT GAIN;

AMINO ACIDS, SULFUR; ANIMALS; ANIMALS, NEWBORN; CELL DIVISION; CYSTEINE; ENTERAL NUTRITION; EPITHELIAL CELLS; FEMALE; GLUTATHIONE; GOBLET CELLS; HOMOCYSTEINE; INTESTINAL MUCOSA; IODINE RADIOISOTOPES; METHIONINE; METHIONINE ADENOSYLTRANSFERASE; METHYLATION; MODELS, BIOLOGICAL; NITROGEN ISOTOPES; ORGAN SIZE; OXIDATION-REDUCTION; SUS SCROFA; TRITIUM; UP-REGULATION;

EID: 66849115545     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.91021.2008     Document Type: Article

References (45)

1. Anderson CL, Iyer SS, Ziegler TR, Jones DP. Control of extracellular cysteine/cystine redox state by HT-29 cells is independent of cellular glutathione. Am J Physiol Regul Integr Comp Physiol 293: R1069-R1075, 2007. (Pubitemid 47358926)
2. Atmaca G. Antioxidant effects of sulfur-containing amino acids. Yonsei Med J 45: 776-788, 2004. (Pubitemid 39545364)
3. Aw TY. Cellular redox: a modulator of intestinal epithelial cell proliferation. News Physiol Sci 18: 201-204, 2003. (Pubitemid 37356867)
4. Bettuzzi S, Davalli P, Astancolle S, Pinna C, Roncaglia R, Boraldi F, Tiozzo R, Sharrard M, Corti A. Coordinate changes of polyamine metabolism regulatory proteins during the cell cycle of normal human dermal fibroblasts. FEBS Lett 446: 18-22, 1999. (Pubitemid 29127241)
5. Bouckenooghe T, Remacle C, Reusens B. Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care 9: 728-733, 2006. (Pubitemid 44624621)
6. Brosnan JT, Brosnan ME. The sulfur-containing amino acids: an overview. J Nutr 136: 1636S-1640S, 2006. (Pubitemid 43765374)
7. Burrin DG, Shulman RJ, Langston C, Storm MC. Supplemental alanylglutamine, organ growth, and nitrogen metabolism in neonatal pigs fed by total parenteral nutrition. JPEN J Parenter Enteral Nutr 18: 313-319, 1994. (Pubitemid 24222345)
8. Burrin DG, Stoll B. Emerging aspects of gut sulfur amino acid metabolism. Curr Opin Clin Nutr Metab Care 10: 63-68, 2007. (Pubitemid 44901136)
9. Burrin DG, Stoll B, Jiang R, Chang X, Hartmann B, Holst JJ, Greeley GH Jr, Reeds PJ. Minimal enteral nutrient requirements for intestinal growth in neonatal piglets: how much is enough? Am J Clin Nutr 71: 1603-1610, 2000. (Pubitemid 30395911)
10. Burrin DG, Stoll B, Jiang R, Petersen Y, Elnif J, Buddington RK, Schmidt M, Holst JJ, Hartmann B, Sangild PT. GLP-2 stimulates intestinal growth in premature TPN-fed pigs by suppressing proteolysis and apoptosis. Am J Physiol Gastrointest Liver Physiol 279: G1249-G1256, 2000.
11. Chen H, Xia M, Lin M, Yang H, Kuhlenkamp J, Li T, Sodir NM, Chen YH, Josef-Lenz H, Laird PW, Clarke S, Mato JM, Lu SC. Role of methionine adenosyltransferase 2A and S-adenosylmethionine in mitogen-induced growth of human colon cancer cells. Gastroenterology 133: 207-218, 2007. (Pubitemid 47039238)
12. Davis SR, Stacpoole PW, Williamson J, Kick LS, Quinlivan EP, Coats BS, Shane B, Bailey LB, Gregory JF 3rd. Tracer-derived total and folate-dependent homocysteine remethylation and synthesis rates in humans indicate that serine is the main one-carbon donor. Am J Physiol Endocrinol Metab 286: E272-E279, 2004. (Pubitemid 38140319)
13. Deplancke B, Gaskins HR. Redox control of the transsulfuration and glutathione biosynthesis pathways. Curr Opin Clin Nutr Metab Care 5: 85-92, 2002.
14. Farrar C, Clarke S. Altered levels of S-adenosylmethionine and S-adenosylhomocysteine in the brains of L-isoaspartyl (D-aspartyl) O-methyltransferase-deficient mice. J Biol Chem 277: 27856-27863, 2002. (Pubitemid 34966731)
15. Jahoor F, Badaloo A, Reid M, Forrester T. Sulfur amino acid metabolism in children with severe childhood undernutrition: methionine kinetics. Am J Clin Nutr 84: 1400-1405, 2006. (Pubitemid 44912824)
16. Jahoor F, Jackson A, Gazzard B, Philips G, Sharpstone D, Frazer ME, Heird W. Erythrocyte glutathione deficiency in symptom-free HIV infection is associated with decreased synthesis rate. Am J Physiol Endocrinol Metab 276: E205-E211, 1999. (Pubitemid 29065611)
17. Jonas CR, Ziegler TR, Gu LH, Jones DP. Extracellular thiol/disulfide redox state affects proliferation rate in a human colon carcinoma (Caco2) cell line. Free Radic Biol Med 33: 1499-1506, 2002. (Pubitemid 35351593)
18. Jones DP. Extracellular redox state: refining the definition of oxidative stress in aging. Rejuvenation Res 9: 169-181, 2006. (Pubitemid 43856805)
19. Jones DP, Carlson JL, Mody VC, Cai J, Lynn MJ, Sternberg P. Redox state of glutathione in human plasma. Free Radic Biol Med 28: 625-635, 2000. (Pubitemid 30136044)
20. Lambert BD, Titgemeyer EC, Stokka GL, DeBey BM, Loest CA. Methionine supply to growing steers affects hepatic activities of methionine synthase and betaine-homocysteine methyltransferase, but not cystathionine synthase. J Nutr 132: 2004-2009, 2002. (Pubitemid 34742891)
21. Lyons J, Rauh-Pfeiffer A, Yu YM, Lu XM, Zurakowski D, Tompkins RG, Ajami AM, Young VR, Castillo L. Blood glutathione synthesis rates in healthy adults receiving a sulfur amino acid-free diet. Proc Natl Acad Sci USA 97: 5071-5076, 2000. (Pubitemid 30313673)
22. MacCoss MJ, Fukagawa NK, Matthews DE. Measurement of intracellular sulfur amino acid metabolism in humans. Am J Physiol Endocrinol Metab 280: E947-E955, 2001. (Pubitemid 32553236)
23. Martensson J, Jain A, Meister A. Glutathione is required for intestinal function. Proc Natl Acad Sci USA 87: 1715-1719, 1990. (Pubitemid 20098041)
24. Martinez-Lopez N, Varela-Rey M, Ariz U, Embade N, Vazquez-Chantada M, Fernandez-Ramos D, Gomez-Santos L, Lu SC, Mato JM, Martinez-Chantar ML. S-adenosylmethionine and proliferation: new pathways, new targets. Biochem Soc Trans 36: 848-852, 2008.
25. Mato JM, Corrales FJ, Lu SC, Avila MA. S-adenosylmethionine: a control switch that regulates liver function. FASEB J 16: 15-26, 2002. (Pubitemid 34027946)
26. 13C]leucine infusion in man: a method for measuring human intracellular leucine tracer enrichment. Metabolism 31: 1105-1112, 1982.
27. Metayer S, Seiliez I, Collin A, Duchene S, Mercier Y, Geraert PA, Tesseraud S. Mechanisms through which sulfur amino acids control protein metabolism and oxidative status. J Nutr Biochem 19: 207-215, 2008.
28. Moinard C, Cynober L, de Bandt JP. Polyamines: metabolism and implications in human diseases. Clin Nutr 24: 184-197, 2005. (Pubitemid 40392801)
29. Nkabyo YS, Gu LH, Jones DP, Ziegler TR. 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, 2006.
30. Noda T, Iwakiri R, Fujimoto K, Aw TY. Induction of mild intracellular redox imbalance inhibits proliferation of CaCo-2 cells. FASEB J 15: 2131-2139, 2001. (Pubitemid 32927930)
31. Noda T, Iwakiri R, Fujimoto K, Rhoads CA, Aw TY. Exogenous cysteine and cystine promote cell proliferation in CaCo-2 cells. Cell Prolif 35: 117-129, 2002. (Pubitemid 34603858)
32. Pias EK, Aw TY. Apoptosis in mitotic competent undifferentiated cells is induced by cellular redox imbalance independent of reactive oxygen species production. FASEB J 16: 781-790, 2002. (Pubitemid 34615126)
33. Prudova A, Bauman Z, Braun A, Vitvitsky V, Lu SC, Banerjee R. S-adenosylmethionine stabilizes cystathionine β-synthase and modulates redox capacity. Proc Natl Acad Sci USA 103: 6489-6494, 2006.
34. Riedijk MA, Stoll B, Chacko S, Schierbeek H, Sunehag AL, van Goudoever JB, Burrin DG. Methionine transmethylation and transsulfuration in the piglet gastrointestinal tract. Proc Natl Acad Sci USA 104: 3408-3413, 2007. (Pubitemid 46364172)
35. Shoveller AK, Brunton JA, Pencharz PB, Ball RO. The methionine requirement is lower in neonatal piglets fed parenterally than in those fed enterally. J Nutr 133: 1390-1397, 2003. (Pubitemid 36548711)
36. Stipanuk MH. Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine. Annu Rev Nutr 24: 539-577, 2004. (Pubitemid 38938803)
37. Stoll B, Chang X, Fan MZ, Reeds PJ, Burrin DG. Enteral nutrient intake level determines intestinal protein synthesis and accretion rates in neonatal pigs. Am J Physiol Gastrointest Liver Physiol 279: G288-G294, 2000.
38. 3]methionine kinetics in humans: methionine conservation and cystine sparing. Am J Physiol Endocrinol Metab 258: E790-E798, 1990.
39. Tappaz ML. Taurine biosynthetic enzymes and taurine transporter: molecular identification and regulations. Neurochem Res 29: 83-96, 2004. (Pubitemid 38181701)
40. van Goudoever JB, Stoll B, Henry JF, Burrin DG, Reeds PJ. Adaptive regulation of intestinal lysine metabolism. Proc Natl Acad Sci USA 97: 11620-11625, 2000.
41. Van Klinken BJ, Einerhand AW, Buller HA, Dekker J. Strategic biochemical analysis of mucins. Anal Biochem 265: 103-116, 1998. (Pubitemid 28541799)
42. Wolfe RR, Chinkes DL. Determination of isotopic enrichment. In: Isotope Tracer in Metabolic Research: Principles and Practice of Kinetic Analysis. Hoboken, NJ: Wiley, 2005, p. 93-132.
43. Wu G, Davis PK, Flynn NE, Knabe DA, Davidson JT. Endogenous synthesis of arginine plays an important role in maintaining arginine homeostasis in postweaning growing pigs. J Nutr 127: 2342-2349, 1997. (Pubitemid 28018910)
44. Wu G, Fang YZ, Yang S, Lupton JR, Turner ND. Glutathione metabolism and its implications for health. J Nutr 134: 489-492, 2004. (Pubitemid 38298485)
45. Wu G, Knabe DA. Free and protein-bound amino acids in sow's colostrum and milk. J Nutr 124: 415-424, 1994. (Pubitemid 24096493)