Epidermal growth factor receptor expression and signaling are essential in glutamine's cytoprotective mechanism in heat-stressed intestinal epithelial-6 cells

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 304, Issue 5, 2013, Pages

  Niederlechner, Stefanie ^a   Baird, Christine ^a   Petrie, Benjamin ^a   Wischmeyer, Erhard ^b   Wischmeyer, Paul E ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Akt; Apoptosis; ERK1 2; p38MAPK; Phosphatidylinositol 3 kinase

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 (3 CHLOROANILINO) 6,7 DIMETHOXYQUINAZOLINE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CASPASE 3; EPIDERMAL GROWTH FACTOR RECEPTOR; GLUTAMINE; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; SMALL INTERFERING RNA;

APOPTOSIS; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; HEAT INJURY; INTESTINE EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SUPPLEMENTATION; WESTERN BLOTTING;

EID: 84874633206     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00418.2012     Document Type: Article

References (61)

1. Alam N, Goel HL, Zarif MJ, Butterfield JE, Perkins HM, Sansoucy BG, Sawyer TK, Languino LR. The integrin-growth factor receptor duet. J Cell Physiol 213: 649-653, 2007.
2. Alexander RJ, Panja A, Kaplan-Liss E, Mayer L, Raicht RF. Expression of growth factor receptor-encoded mRNA by colonic epithelial cells is altered in inflammatory bowel disease. Dig Dis Sci 40: 485-494, 1995.
3. Alwan HA, van Zoelen EJ, van Leeuwen JE. Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination. J Biol Chem 278: 35781-35790, 2003.
4. Anderson RA, Boronenkov IV, Doughman SD, Kunz J, Loijens JC. Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem 274: 9907-9910, 1999.
5. Avissar NE, Sax HC, Toia L. In human enterocytes, GLN transport and ASCT2 surface expression induced by short-term EGF are MAPK, PI3K, and Rho-dependent. Dig Dis Sci 53: 2113-2125, 2008.
6. Bae SS, Choi JH, Oh YS, Perry DK, Ryu SH, Suh PG. Proteolytic cleavage of epidermal growth factor receptor by caspases. FEBS Lett 491: 16-20, 2001.
7. Bang OS, Ha BG, Park EK, Kang SS. Activation of Akt is induced by heat shock and involved in suppression of heat-shock-induced apoptosis of NIH3T3 cells. Biochem Biophys Res Commun 278: 306-311, 2000.
8. Bonni A, Brunet A, West AE, Datta SR, Takasu MA, Greenberg ME. Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and-independent mechanisms. Science 286: 1358-1362, 1999.
9. Cantley LC. The phosphoinositide 3-kinase pathway. Science 296: 1655-1657, 2002.
10. Carpenter CL, Cantley LC. Phosphoinositide kinases. Curr Opin Cell Biol 8: 153-158, 1996.
11. Clark EC, Patel SD, Chadwick PR, Warhurst G, Curry A, Carlson GL. Glutamine deprivation facilitates tumour necrosis factor induced bacterial translocation in Caco-2 cells by depletion of enterocyte fuel substrate. Gut 52: 224-230, 2003.
12. Cybulsky AV, McTavish AJ, Cyr MD. Extracellular matrix modulates epidermal growth factor receptor activation in rat glomerular epithelial cells. J Clin Invest 94: 68-78, 1994.
13. Dittmann K, Mayer C, Kehlbach R, Rodemann HP. Radiation-induced caveolin-1 associated EGFR internalization is linked with nuclear EGFR transport and activation of DNA-PK. Mol Cancer 7: 69, 2008.
14. Dube PE, Yan F, Punit S, Girish N, McElroy SJ, Washington MK, Polk DB. Epidermal growth factor receptor inhibits colitis-associated cancer in mice. J Clin Invest 122: 2780-2792, 2012.
15. Edinger AL, Thompson CB. Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol Biol Cell 13: 2276-2288, 2002.
16. Egger B, Buchler MW, Lakshmanan J, Moore P, Eysselein VE. Mice harboring a defective epidermal growth factor receptor (waved-2) have an increased susceptibility to acute dextran sulfate-induced colitis. Scand J Gastroenterol 35: 1181-1187, 2000.
17. Egger B, Carey HV, Procaccino F, Chai NN, Sandgren EP, Lakshmanan J, Buslon VS, French SW, Buchler MW, Eysselein VE. Reduced susceptibility of mice overexpressing transforming growth factor-α to dextran sodium sulphate induced colitis. Gut 43: 64-70, 1998.
18. Egger B, Procaccino F, Lakshmanan J, Reinshagen M, Hoffmann P, Patel A, Reuben W, Gnanakkan S, Liu L, Barajas L, Eysselein VE. Mice lacking transforming growth factor-α have an increased susceptibility to dextran sulfate-induced colitis. Gastroenterology 113: 825-832, 1997.
19. Galadari S, Thayyullathil F, Hago A, Patel M, Chathoth S. Akt depletion is an important determinant of L929 cell death following heat stress. Ann NY Acad Sci 1138: 385-392, 2008.
20. Gianotti L, Alexander JW, Gennari R, Pyles T, Babcock GF. Oral glutamine decreases bacterial translocation and improves survival in experimental gut-origin sepsis. JPEN J Parenter Enteral Nutr 19: 69-74, 1995.
21. Hamiel CR, Pinto S, Hau A, Wischmeyer PE. Glutamine enhances heat shock protein 70 expression via increased hexosamine biosynthetic pathway activity. Am J Physiol Cell Physiol 297: C1509-C1519, 2009.
22. Hoffmann EK, Lambert IH, Pedersen SF. Physiology of cell volume regulation in vertebrates. Physiol Rev 89: 193-277, 2009.
23. Jimenez JJ, Roberts SM, Mejia J, Mauro LM, Munson JW, Elgart GW, Connelly EA, Chen Q, Zou J, Goldenberg C, Voellmy R. Prevention of chemotherapy-induced alopecia in rodent models. Cell Stress Chaperones 13: 31-38, 2008.
24. Junttila MR, Li SP, Westermarck J. Phosphatase-mediated crosstalk between MAPK signaling pathways in the regulation of cell survival. FASEB J 22: 954-965, 2008.
25. Kallweit AR, Baird CH, Stutzman DK, Wischmeyer PE. Glutamine prevents apoptosis in intestinal epithelial cells and induces differential protective pathways in heat and oxidant injury models. JPEN J Parenter Enteral Nutr 36: 551-555, 2012.
26. Karin M. Signal transduction from cell surface to nucleus in development and disease. FASEB J 6: 2581-2590, 1992.
27. Klimberg VS, Salloum RM, Kasper M, Plumley DA, Dolson DJ, Hautamaki RD, Mendenhall WR, Bova FC, Bland KI, Copeland EM 3rd, et al. Oral glutamine accelerates healing of the small intestine and improves outcome after whole abdominal radiation. Arch Surg 125: 1040-1045, 1990.
28. Kohno M, Pouyssegur J. Pharmacological inhibitors of the ERK signaling pathway: application as anticancer drugs. Prog Cell Cycle Res 5: 219-224, 2003.
29. Kyriakis JM, Avruch J. Protein kinase cascades activated by stress and inflammatory cytokines. Bioessays 18: 567-577, 1996.
30. 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.
31. Lin SY, Makino K, Xia W, Matin A, Wen Y, Kwong KY, Bourguignon L, Hung MC. Nuclear localization of EGF receptor and its potential new role as a transcription factor. Nat Cell Biol 3: 802-808, 2001.
32. Liu F, Yin J, Du M, Yan P, Xu J, Zhu X, Yu J. Heat-stress-induced damage to porcine small intestinal epithelium associated with downregulation of epithelial growth factor signaling. J Anim Sci 87: 1941-1949, 2009.
33. Liu S, Calderwood DA, Ginsberg MH. Integrin cytoplasmic domainbinding proteins. J Cell Sci 113: 3563-3571, 2000.
34. Matsumoto T, Turesson I, Book M, Gerwins P, Claesson-Welsh L. p38 MAP kinase negatively regulates endothelial cell survival, proliferation, and differentiation in FGF-2-stimulated angiogenesis. J Cell Biol 156: 149-160, 2002.
35. Nair RR, Warner BB, Warner BW. Role of epidermal growth factor and other growth factors in the prevention of necrotizing enterocolitis. Semin Perinatol 32: 107-113, 2008.
36. Niederlechner S, Klawitter J, Baird C, Kallweit AR, Christians U, Wischmeyer PE. Signaling is required for L-glutamine's protection against gut injury. PLos One 7: e50185, 2012.
37. Oehler R, Roth E. Glutamine metabolism. In: Metabolic and Therapeutic Aspects of Amino Acids in Clinical Nutrition, edited by Cynober LA. Boca Raton, FL: CRC, 2004, p. 169-180.
38. Oudemans-van Straaten HM, Bosman RJ, Treskes M, van der Spoel HJ, Zandstra DF. Plasma glutamine depletion and patient outcome in acute ICU admissions. Intensive Care Med 27: 84-90, 2001.
39. Parry-Billings M, Evans J, Calder PC, Newsholme EA. Does glutamine contribute to immunosuppression after major burns? Lancet 336: 523-525, 1990.
40. Paul G, Marchelletta RR, McCole DF, Barrett KE. Interferon-alters downstream signaling originating from epidermal growth factor receptor in intestinal epithelial cells: functional consequences for ion transport. J Biol Chem 287: 2144-2155, 2012.
41. Playford RJ, Wright NA. Why is epidermal growth factor present in the gut lumen? Gut 38: 303-305, 1996.
42. Reeds PJ, Burrin DG. Glutamine and the bowel. J Nutr 131: 2505S-2508S, 2001.
43. 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.
44. Rhoads M. Glutamine signaling in intestinal cells. JPEN J Parenter Enteral Nutr 23: S38-S40, 1999.
45. Sakiyama T, Musch MW, Ropeleski MJ, Tsubouchi H, Chang EB. Glutamine increases autophagy under basal and stressed conditions in intestinal epithelial cells. Gastroenterology 136: 924-932, 2009.
46. Sartor RB. Induction of mucosal immune responses by bacteria and bacterial components. Curr Opin Gastroenterol 17: 555-561, 2001.
47. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J 9: 726-735, 1995.
48. Seth A, Basuroy S, Sheth P, Rao RK. L-Glutamine ameliorates acetaldehyde-induced increase in paracellular permeability in Caco-2 cell monolayer. Am J Physiol Gastrointest Liver Physiol 287: G510-G517, 2004.
49. Sheng G, Guo J, Warner BW. Epidermal growth factor receptor signaling modulates apoptosis via p38α MAPK-dependent activation of Bax in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 293: G599-G606, 2007.
50. Souba WW. Glutamine: a key substrate for the splanchnic bed. Annu Rev Nutr 11: 285-308, 1991.
51. Tappenden KA. Mechanisms of enteral nutrient-enhanced intestinal adaptation. Gastroenterology 130: S93-S99, 2006.
52. Weitzel LR, Wischmeyer PE. Glutamine in critical illness: the time has come, the time is now. Crit Care Clin 26: 515-525, 2010.
53. Wells A. EGF receptor. Int J Biochem Cell Biol 31: 637-643, 1999.
54. Wischmeyer P. Nutritional pharmacology in surgery and critical care: "you must unlearn what you have learned. " Curr Opin Anaesthesiol 24: 381-388, 2011.
55. Wischmeyer PE. Glutamine and heat shock protein expression. Nutrition 18: 225-228, 2002.
56. 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.
57. Xue H, Sufit AJ, Wischmeyer PE. Glutamine therapy improves outcome of in vitro and in vivo experimental colitis models. JPEN J Parenter Enteral Nutr 35: 188-197, 2011.
58. Yamaoka T, Yan F, Cao H, Hobbs SS, Dise RS, Tong W, Polk DB. Transactivation of EGF receptor and ErbB2 protects intestinal epithelial cells from TNF-induced apoptosis. Proc Natl Acad Sci USA 105: 11772-11777, 2008.
59. Yan F, Cao H, Chaturvedi R, Krishna U, Hobbs SS, Dempsey PJ, Peek RM Jr, Cover TL, Washington MK, Wilson KT, Polk DB. Epidermal growth factor receptor activation protects gastric epithelial cells from Helicobacter pylori-induced apoptosis. Gastroenterology 136: 1297-1307, 2009.
60. Zapata-Sirvent RL, Hansbrough JF, Ohara MM, Rice-Asaro M, Nyhan WL. Bacterial translocation in burned mice after administration of various diets including fiber-and glutamine-enriched enteral formulas. Crit Care Med 22: 690-696, 1994.
61. Ziegler TR, Bazargan N, Leader LM, Martindale RG. Glutamine and the gastrointestinal tract. Curr Opin Clin Nutr Metab Care 3: 355-362, 2000.