Glutamine enhances heat shock protein 70 expression via increased hexosamine biosynthetic pathway activity

American Journal of Physiology - Cell Physiology

Volumn 297, Issue 6, 2009, Pages

  Hamiel, Christine R ^a   Pinto, Shanti ^b   Hau, Ann ^a   Wischmeyer, Paul E ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cell injury; Cell protection; Cell survival; Heat shock factor 1; Heat shock proteins; O GlcNAc; O glycosylation

Indexed keywords

ENZYME; GLUTAMINE; HEAT SHOCK PROTEIN 70; HEAT SHOCK TRANSCRIPTION FACTOR 1; HEXOSAMINE; LUCIFERASE; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE; POLYPEPTIDE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SP; URIDINE DIPHOSPHATE N ACETYLGLUCOSAMINE; BETA N ACETYLHEXOSAMINIDASE; DNA BINDING PROTEIN; HEXOSAMINIDASE C; HSF1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ARTICLE; ATTENUATION; BIOSYNTHESIS; CELL PROTECTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FIBROBLAST; GLYCOSYLATION; HEAT STRESS; IMMUNOPRECIPITATION; MOUSE; MOUSE EMBRYO; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; TRANSCRIPTION INITIATION; WESTERN BLOTTING; ANIMAL; ANIMAL EMBRYO; CELL CULTURE; CELL NUCLEUS; DRUG ANTAGONISM; GENE SILENCING; GENETICS; HEAT; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROMOTER REGION; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BETA-N-ACETYLHEXOSAMINIDASES; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELLS, CULTURED; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; GENE SILENCING; GLUTAMINE; GLYCOSYLATION; HEXOSAMINES; HOT TEMPERATURE; HSP70 HEAT-SHOCK PROTEINS; MICE; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROMOTER REGIONS, GENETIC; RNA, SMALL INTERFERING; SP1 TRANSCRIPTION FACTOR; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

EID: 73449137269     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00240.2009     Document Type: Article

References (30)

1. Bevilacqua A, Fiorenza MT, Mangia F. A developmentally regulated GAGA box-binding factor and Sp1 are required for transcription of the hsp70.1 gene at the onset of mouse zygotic genome activation. Development 127: 1541-1551, 2000.
2. Brasse-Lagnel C, Fairand A, Lavoinne A, Husson A. Glutamine stimulates argininosuccinate synthetase gene expression through cytosolic O-glycosylation of Sp1 in Caco-2 cells. J Biol Chem 278: 52504-52510, 2003.
3. Hu S, Ciancio MJ, Lahav M, Fujiya M, Lichtenstein L, Anant S, Musch MW, Chang EB. Translational inhibition of colonic epithelial heat shock proteins by IFN-gamma and TNF-alpha in intestinal inflammation. Gastroenterology 133: 1893-1904, 2007.
4. Kudlow JE. Post-translational modification by O-GlcNAc: another way to change protein function. J Cell Biochem 98: 1062-1075, 2006.
5. Liu J, Marchase RB, Chatham JC. Glutamine-induced protection of isolated rat heart from ischemia/reperfusion injury is mediated via the hexosamine biosynthesis pathway and increased protein O-GlcNAc levels. J Mol Cell Cardiol 42: 177-185, 2007.
6. Liu J, Pang Y, Chang T, Bounelis P, Chatham JC, Marchase RB. Increased hexosamine biosynthesis and protein O-GlcNAc levels associated with myocardial protection against calcium paradox and ischemia. J Mol Cell Cardiol 40: 303-312, 2006.
7. Majumdar G, Harrington A, Hungerford J, Martinez-Hernandez A, Gerling IC, Raghow R, Solomon S. Insulin dynamically regulates calmodulin gene expression by sequential o-glycosylation and phosphorylation of sp1 and its subcellular compartmentalization in liver cells. J Biol Chem 281: 3642-3650, 2006.
8. Mestril R, Chi SH, Sayen MR, O'Reilly K, Dillmann WH. Expression of inducible stress protein 70 in rat heart myogenic cells confers protection against simulated ischemia-induced injury. J Clin Invest 93: 759-767, 1994.
9. Morrison AL, Dinges M, Singleton KD, Odoms K, Wong HR, Wischmeyer PE. Glutamine's protection against cellular injury is dependent on heat shock factor-1. Am J Physiol Cell Physiol 290: C1625-C1632, 2006.
10. Oesterreich S, Hickey E, Weber LA, Fuqua SA. Basal regulatory promoter elements of the hsp27 gene in human breast cancer cells. Biochem Biophys Res Commun 222: 155-163, 1996.
11. Parry-Billings M, Evans J, Calder PC, Newsholme EA. Does glutamine contribute to immunosuppression after major burns? Lancet 336: 523-525, 1990.
12. Pirkkala L, Nykanen P, Sistonen L. Roles of the heat shock transcription factors in regulation of the heat shock response and beyond. FASEB J 15: 1118-1131, 2001.
13. Plumier JC, Ross BM, Currie RW, Angelidis CE, Kazlaris H, Kollias G, Pagoulatos GN. Transgenic mice expressing the human heat shock protein 70 have improved post-ischemic myocardial recovery. J Clin Invest 95: 1854-1860, 1995.
14. Porter W, Wang F, Wang W, Duan R, Safe S. Role of estrogen receptor/Sp1 complexes in estrogen-induced heat shock protein 27 gene expression. Mol Endocrinol 10: 1371-1378, 1996.
15. Rumberger JM, Wu T, Hering MA, Marshall S. Role of hexosamine biosynthesis in glucose-mediated up-regulation of lipogenic enzyme mRNA levels: effects of glucose, glutamine, and glucosamine on glycero-phosphate dehydrogenase, fatty acid synthase, and acetyl-CoA carboxylase mRNA levels. J Biol Chem 278: 28547-28552, 2003.
16. Singleton KD, Serkova N, Beckey VE, Wischmeyer PE. Glutamine attenuates lung injury and improves survival after sepsis: role of enhanced heat shock protein expression. Crit Care Med 33: 1206-1213, 2005.
17. Singleton KD, Wischmeyer PE. Glutamine induces heat shock protein expression via O-glycosylation and phosphorylation of HSF-1 and Sp1. JPEN J Parenter Enteral Nutr 32: 371-376, 2008.
18. Singleton KD, Wischmeyer PE. Glutamine's protection against sepsis and lung injury is dependent on heat shock protein 70 expression. Am J Physiol Regul Integr Comp Physiol 292: R1839-R1845, 2007.
19. Villar J, Edelson JD, Post M, Mullen JB, Slutsky AS. Induction of heat stress proteins is associated with decreased mortality in an animal model of acute lung injury. Am Rev Respir Dis 147: 177-181, 1993.
20. Villar J, Ribeiro SP, Mullen JB, Kuliszewski M, Post M, Slutsky AS. Induction of the heat shock response reduces mortality rate and organ damage in a sepsis-induced acute lung injury model. Crit Care Med 22: 914-921, 1994.
21. Weiss YG, Bouwman A, Gehan B, Schears G, Raj N, Deutschman CS. Cecal ligation and double puncture impairs heat shock protein 70 (HSP-70) expression in the lungs of rats. Shock 13: 19-23, 2000.
22. Wischmeyer PE, Jayakar D, Williams U, Singleton KD, Riehm J, Bacha EA, Jeevanandam V, Christians U, Serkova N. Single dose of glutamine enhances myocardial tissue metabolism, glutathione content, and improves myocardial function after ischemia-reperfusion injury. JPEN J Parenter Enteral Nutr 27: 396-403, 2003.
23. 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.
24. 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.
25. Yang S, Zou LY, Bounelis P, Chaudry I, Chatham JC, Marchase RB. Glucosamine administration during resuscitation improves organ function after trauma hemorrhage. Shock 25: 600-607, 2006.
26. Zachara NE, Hart GW. Cell signaling, the essential role of O-GlcNAc! Biochim Biophys Acta 1761: 599-617, 2006.
27. Zachara NE, Hart GW. O-GlcNAc a sensor of cellular state: the role of nucleocytoplasmic glycosylation in modulating cellular function in response to nutrition and stress. Biochim Biophys Acta 1673: 13-28, 2004.
28. Zachara NE, Hart GW. O-GlcNAc modification: a nutritional sensor that modulates proteasome function. Trends Cell Biol 14: 218 -221, 2004.
29. Zachara NE, O'Donnell N, Cheung WD, Mercer JJ, Marth JD, Hart GW. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J Biol Chem 279: 30133-30142, 2004.
30. Ziegler TR, Ogden LG, Singleton KD, Luo M, Fernandez-Estivariz C, Griffith DP, Galloway JR, Wischmeyer PE. Parenteral glutamine increases serum heat shock protein 70 in critically ill patients. Intensive Care Med 31: 1079-1086, 2005.