Glutamine protects against apoptosis via downregulation of Sp3 in intestinal epithelial cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 299, Issue 6, 2010, Pages

  Ban, Kechen ^a   Kozar, Rosemary A ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

Bax; Bcl 2; Caspase; DNA fragmentation; Hypoxia reoxygenation; Specificity protein 3

Indexed keywords

BCL2 RELATED PROTEIN A1; CASPASE 3; CASPASE 8; CASPASE 9; GLUTAMINE; MESSENGER RNA; PROTEIN BAX; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP3;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE SILENCING; HYPOXIA; INTESTINE EPITHELIUM CELL; MICROARRAY ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REOXYGENATION; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CASPASES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE SILENCING; GENES, BCL-2; GLUTAMINE; INTESTINAL MUCOSA; RATS; RNA, SMALL INTERFERING; SP3 TRANSCRIPTION FACTOR;

EID: 78649744171     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00334.2010     Document Type: Article

References (65)

1. Abdelrahim M, Smith R 3rd, Burghardt R, Safe S. Role of Sp proteins in regulation of vascular endothelial growth factor expression and proliferation of pancreatic cancer cells. Cancer Res 64: 6740-6749, 2004.
2. Bhattacharya S, Ray RM, Johnson LR. Prevention of TNF-α-induced apoptosis in polyamine-depleted IEC-6 cells is mediated through the activation of ERK1/2. Am J Physiol Gastrointest Liver Physiol 286: G479-G490, 2004.
3. Brantley S, Pierce J. Effects of enteral glutamine on trauma patients (Abstract). Nutr Clin Pract 15: S13, 2000.
4. Brasse-Lagnel CG, Lavoinne AM, Husson AS. Amino acid regulation of mammalian gene expression in the intestine. Biochimie 92: 729-735, 2010.
5. Chang WK, Yang KD, Chuang H, Jan JT, Shaio MF. Glutamine protects activated human T cells from apoptosis by up-regulating glutathione and Bcl-2 levels. Clin Immunol 104: 151-160, 2002.
6. Chipuk JE, Moldoveanu T, Llambi F, Parsons MJ, Green DR. The BCL2 family reunion. Mol Cell 37: 299-310, 2010.
7. Coëffier M, Le Pessot F, Leplingard A, Marion R, Lerebours E, Ducrotté P, Déchelotte P. Acute enteral glutamine infusion enhances heme oxygenase-1 expression in human duodenal mucosa. J Nutr 132: 2570-2573, 2002.
8. Coëffier M, Claeyssens S, Hecketsweiler B, Lavoinne A, Ducrotté P, Déchelotte P. Enteral glutamine stimulates protein synthesis and decreases ubiquitin mRNA level in human gut mucosa. Am J Physiol Gastrointest Liver Physiol 285: G266-G273, 2003.
9. Coëffier M, Marion R, Ducrotté P, Déchelotte P. Modulating effect of glutamine on IL-1beta-induced cytokine production by human gut. Clin Nutr 22: 407-413, 2003.
10. Creagh EM, Conroy H, Martin SJ. Caspase-activation pathways in apoptosis and immunity. Immunol Rev 193: 10-21, 2003.
11. Deldicque L, Sanchez Canedo C, Horman S, De Potter I, Bertrand L, Hue L, Francaux M. Antagonistic effects of leucine and glutamine on the mTOR pathway in myogenic C2C12 cells. Amino Acids 35: 147-155, 2008.
12. Deniel N, Marion-Letellier R, Charlionet R, Tron F, Leprince J, Vaudry H, Ducrotté P, Déchelotte P, Thébault S. Glutamine regulates the human epithelial intestinal HCT-8 cell proteome under apoptotic conditions. Mol Cell Proteomics 6: 1671-1679, 2007.
13. Erbil Y, Oztezcan S, Giriş M, Barbaros U, Olgaç V, Bilge H, Küçücük H, Toker G. The effect of glutamine on radiation-induced organ damage. Life Sci 78: 376-382, 2005.
14. Essafi-Benkhadir K, Grosso S, Puissant A, Robert G, Essafi M, Deckert M, Chamorey E, Dassonville O, Milano G, Auberger P, Pagès G. Dual role of Sp3 transcription factor as an inducer of apoptosis and a marker of tumour aggressiveness. PLoS One 4: e4478, 2009.
15. Evans ME, Jones DP, Ziegler TR. Glutamine prevents cytokine-induced apoptosis in human colonic epithelial cells. J Nutr 133: 3065-3071, 2003.
16. Evans ME, Jones DP, Ziegler TR. Glutamine inhibits cytokine-induced apoptosis in human colonic epithelial cells via the pyrimidine pathway. Am J Physiol Gastrointest Liver Physiol 289: G388-G396, 2005.
17. Garrel D, Patenaude J, Nedelec B, Samson L, Dorais J, Champoux J, D'Elia M, Bernier J. Decreased mortality and infectious morbidity in adult burn patients given enteral glutamine supplements: a prospective, controlled, randomized clinical trial. Crit Care Med 31: 2444-2449, 2003.
18. Grimble RF. Immunonutrition. Curr Opin Gastroenterol 21: 216-222, 2005.
19. Hall JC, Dobb G, Hall J, de Sousa R, Brennan L, McCauley R. A prospective randomized trial of enteral glutamine in critical illness. Intensive Care Med 29: 1710-1716, 2003.
20. Heyland DK, Dhaliwal R, Day AG, Muscedere J, Drover J, Suchner U, Cook D, Canadian Critical Care Trials Group. Reducing Deaths due to Oxidative Stress (The REDOXS Study): rationale and study design for a randomized trial of glutamine and antioxidant supplementation in critically-ill patients. Proc Nutr Soc 65: 250-263, 2006.
21. Heyland DK, Dhaliwalm R, Day A, Drover J, Cote H, Wischmeyer P. Optimizing the dose of glutamine dipeptides and antioxidants in critically ill patients: a phase I dose-finding study. JPEN J Parenter Enteral Nutr 31: 109-118, 2007.
22. Hinshaw DB, Burger JM. Protective effect of glutamine on endothelial cell ATP in oxidant injury. J Surg Res 49: 222-227, 1990.
23. Houdijk AP, Rijnsburger ER, Jansen J, Wesdorp RI, Weiss JK, McCamish MA, Teerlink T, Meuwissen SG, Haarman HJ, Thijs LG, van Leeuwen PA. Randomised trial of glutamine-enriched enteral nutrition on infectious morbidity in patients with multiple trauma. Lancet 352: 772-776, 1998.
24. Koubi D, Jiang H, Zhang L, Tang W, Kuo J, Rodriguez AI, Hunter TJ, Seidman MD, Corcoran GB, Levine RA. Role of Bcl-2 family of proteins in mediating apoptotic death of PC12 cells exposed to oxygen and glucose deprivation. Neurochem Int 46: 73-81, 2005.
25. Kozar RA, Schultz SG, Hassoun HT, Desoignie R, Weisbrodt NW, Haber MM, Moore FA. The type of sodium-coupled solute modulates small bowel mucosal injury, transport function, and ATP after ischemia/reperfusion injury in rats. Gastroenterology 123: 810-816, 2002.
26. Kozar RA, Schultz SG, Bick RJ, Poindexter BJ, DeSoignie R, Moore FA. Enteral glutamine but not alanine maintains small bowel barrier function after ischemia/reperfusion injury in rats. Shock 21: 433-437, 2004.
27. Kurokawa M, Kornbluth S. Caspases and kinases in a death grip. Cell 138: 838-854, 2009.
28. Kypriotou M, Beauchef G, Chadjichristos C, Widom R, Renard E, Jimenez SA, Korn J, Maquart FX, Oddos T, Von Stetten O, Pujol JP, Galéra P. Human collagen Krox up-regulates type I collagen expression in normal and scleroderma fibroblasts through interaction with Sp1 and Sp3 transcription factors. J Biol Chem 282: 32000-32014, 2007.
29. Labow BI, Souba WW. Glutamine. World J Surg 24: 1503-1513, 2000.
30. Lagranha CJ, Doi SQ, Pithon-Curi TC, Curi R, Sellitti DF. Glutamine enhances glucose-induced mesangial cell proliferation. Amino Acids 34: 683-685, 2008.
31. Larson SD, Li J, Chung DH, Evers BM. Molecular mechanisms contributing to glutamine-mediated intestinal cell survival. Am J Physiol Gastrointest Liver Physiol 293: G1262-G1271, 2007.
32. Li L, He S, Sun JM, Davie JR. Gene regulation by Sp1 and Sp3. Biochem Cell Biol 82: 460-471, 2004.
33. Li N, Liboni K, Fang MZ, Samuelson D, Lewis P, Patel R, Neu J. Glutamine decreases lipopolysaccharide-induced intestinal inflammation in infant rats. Am J Physiol Gastrointest Liver Physiol 286: G914-G921, 2004.
34. Majello B, De Luca P, Lania L. Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J Biol Chem 272: 4021-4026, 1997.
35. Marion R, Coëffier MM, Gargala G, Ducrotté P, Déchelotte PP. Glutamine and CXC chemokines IL-8, Mig, IP-10 and I-TAC in human intestinal epithelial cells. Clin Nutr 23: 579-585, 2004.
36. Marion R, Coëffier M, Leplingard A, Favennec L, Ducrotté P, Déchelotte P. Cytokine-stimulated nitric oxide production and inducible NOsynthase mRNA level in human intestinal cells: lack of modulation by glutamine. Clin Nutr 22: 523-528, 2003.
37. McQuiggan M, Kozar R, Sailors RM, Ahn C, McKinley B, Moore F. Enteral glutamine during active shock resuscitation is safe and enhances tolerance of enteral feeding. JPEN J Parenter Enteral Nutr 32: 28-35, 2008.
38. Medeiros AC, Chacon DA, Sales VS, Egito ES, Brandão-Neto J, Pinheiro LA, Carvalho MR. Glucan and glutamine reduce bacterial translocation in rats subjected to intestinal ischemia-reperfusion. J Invest Surg 19: 39-46, 2006.
39. Nakajima Y, Shimazawa M, Mishima S, Hara H. Neuroprotective effects of Brazilian green propolis and its main constituents against oxygen-glucose deprivation stress, with a gene-expression analysis. Phytother Res 23: 1431-1438, 2009.
40. Nakamura E, Hagen SJ. Role of glutamine and arginase in protection against ammonia-induced cell death in gastric epithelial cells. Am J Physiol Gastrointest Liver Physiol 283: G1264-G1275, 2002.
41. Papaconstantinou HT, Chung DH, Zhang W, Ansari NH, Hellmich MR, Townsend CM Jr, Ko TC. Prevention of mucosal atrophy: role of glutamine and caspases in apoptosis in intestinal epithelial cells. J Gastrointest Surg 4: 416-423, 2000.
42. Peng X, Yan H, You Z, Wang P, Wang S. Effects of enteral supplementation with glutamine granules on intestinal mucosal barrier function in severe burned patients. Burns 30: 135-139, 2004.
43. Philipsen S, Suske G. A tale of three fingers: the family of mammalian Sp/XKLF transcription factors. Nucleic Acids Res 27: 2991-3000, 1999.
44. Ray SK, Leiter AB. The basic helix-loop-helix transcription factor NeuroD1 facilitates interaction of Sp1 with the secretin gene enhancer. Mol Cell Biol 27: 7839-7847, 2007.
45. Reeds PJ, Burrin DG. Glutamine and the bowel. J Nutr 131, Suppl 9: 2505S-2508S, 2001.
46. Rhoads JM, Argenzio RA, Chen W, Rippe RA, Westwick JK, Cox AD, Berschneider HM, Brenner DA. L-glutamine stimulates intestinal cell proliferation and activates mitogen-activated protein kinases. Am J Physiol Gastrointest Liver Physiol 272: G943-G953, 1997.
47. Rhoads JM, Argenzio RA, Chen W, Graves LM, Licato LL, Blikslager AT, Smith J, Gatzy J, Brenner DA. Glutamine metabolism stimulates intestinal cell MAPKs by a cAMP-inhibitable, Raf-independent mechanism. Gastroenterology 118: 90-100, 2000.
48. Robinson EK, Kelly DP, Mercer DW, Kozar RA. Differential effects of luminal arginine and glutamine on metalloproteinase production in the postischemic gut. JPEN J Parenter Enteral Nutr 32: 433-438, 2008.
49. Ropeleski MJ, Riehm J, Baer KA, Musch MW, Chang EB. Antiapoptotic effects of L-glutamine-mediated transcriptional modulation of the heat shock protein 72 during heat shock. Gastroenterology 129: 170-184, 2005.
50. Santoso JT, Lucci JA 3rd, Coleman RL, Hatch S, Wong P, Miller D, Mathis JM. Does glutamine supplementation increase radioresistance in squamous cell carcinoma of the cervix? Gynecol Oncol 71: 359-563, 1998.
51. Sato N, Moore FA, Kone BC, Zou L, Smith MA, Childs MA, Moore-Olufemi S, Schultz SG, Kozar RA. Differential induction of PPAR-γ by luminal glutamine and iNOS by luminal arginine in the rodent postischemic small bowel. Am J Physiol Gastrointest Liver Physiol 290: G616-G623, 2006.
52. Suske G. The Sp-family of transcription factors. Gene 238: 291-300, 1999.
53. Tabakman R, Jiang H, Levine RA, Kohen R, Lazarovici P. Apoptotic characteristics of cell death and the neuroprotective effect of homocarnosine on pheochromocytoma PC12 cells exposed to ischemia. J Neurosci Res 75: 499-507, 2004.
54. Valin A, Gill G. Regulation of the dual-function transcription factor Sp3 by SUMO. Biochem Soc Trans 35: 1393-1396, 2007.
55. Wang JY. Polyamines and mRNA stability in regulation of intestinal mucosal growth. Amino Acids 33: 241-252, 2007.
56. Wang W, Dong L, Saville B, Safe S. Transcriptional activation of E2F1 gene expression by 17beta-estradiol in MCF-7 cells is regulated by NF-Y-Sp1/estrogen receptor interactions. Mol Endocrinol 13: 1373-1387, 1999.
57. Wang ZB, Liu YQ, Cui YF. Pathways to caspase activation. Cell Biol Int 29: 489-496, 2005.
58. Wilson AJ, Chueh AC, Tögel L, Corner GA, Ahmed N, Goel S, Byun DS, Nasser S, Houston MA, Jhawer M, Smartt HJ, Murray LB, Nicholas C, Heerdt BG, Arango D, Augenlicht LH, Mariadason JM. Apoptotic sensitivity of colon cancer cells to histone deacetylase inhibitors is mediated by an Sp1/Sp3-activated transcriptional program involving immediate-early gene induction. Cancer Res 70: 609-620, 2010.
59. Wischmeyer PE. Glutamine and heat shock protein expression. Nutrition 18: 225-228, 2002.
60. Wischmeyer PE, Kahana M, Wolfson R, Ren H, Musch MM, Chang EB. Glutamine induces heat shock protein and protects against endotoxin shock in the rat. J Appl Physiol 90: 2403-2410, 2001.
61. Wischmeyer PE, Musch MW, Madonna MB, Thisted R, Chang EB. Glutamine protects intestinal epithelial cells: role of inducible HSP70. Am J Physiol Gastrointest Liver Physiol 272: G879-G884, 1997.
62. Zelko IN, Mueller MR, Folz RJ. Transcription factors sp1 and sp3 regulate expression of human extracellular superoxide dismutase in lung fibroblasts. Am J Respir Cell Mol Biol 39: 243-251, 2008.
63. Zhao C, Meng A. Sp1-like transcription factors are regulators of embryonic development in vertebrates. Dev Growth Differ 47: 201-211, 2005.
64. Zhou YP, Jiang ZM, Sun YH, Wang XR, Ma EL, Wilmore D. The effect of supplemental enteral glutamine on plasma levels, gut function, and outcome in severe burns: a randomized, double-blind, controlled clinical trial. JPEN J Parenter Enteral Nutr 27: 241-245, 2003.
65. Ziegler TR, Bazargan N, Leader LM, Martindale RG. Glutamine and the gastrointestinal tract. Curr Opin Clin Nutr Metab Care 3: 355-362, 2000.