Hexosamine biosynthesis pathway flux promotes endoplasmic reticulum stress, lipid accumulation, and inflammatory gene expression in hepatic cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 3, 2010, Pages

  Sage, Andrew T ^a   Walter, Lisa A ^b   Shi, Yuanyuan ^c   Khan, Mohammad I ^c   Kaneto, Hideaki ^d   Capretta, Alfredo ^b   Werstuck, Geoff H ^a,c  

^a MCMASTER UNIVERSITY   (Canada)

^b MCMASTER UNIVERSITY   (Canada)

^c HENDERSON RESEARCH CENTRE   (Canada)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Atherosclerosis; Diabetes mellitus; Fructose 6 phosphate amidotransferase; Glucosamine; Glutamine

Indexed keywords

6 DIAZO 5 OXONORLEUCINE; CALRETICULIN; CHOLESTEROL; GLUCOSAMINE; GLUCOSE REGULATED PROTEIN 78; GLUCOSE REGULATED PROTEIN 94; GLUTAMINE FRUCTOSE 6 PHOSPHATE AMINOTRANSFERASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEXOSAMINE; MARKER;

ADENOVIRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BIOSYNTHESIS; CELL LINE; CELL STRAIN HEPG2; CELL STRESS; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; FATTY LIVER; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IMMUNOBLOTTING; IN VITRO STUDY; INFLAMMATION; LIPID STORAGE; LIPOGENESIS; LIVER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STAINING; STRESS;

ANIMALS; CELL LINE; CYTOKINES; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; GENE EXPRESSION; HEPATOCYTES; HEXOSAMINES; HUMANS; LIPID METABOLISM; MICE; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 77349122076     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00507.2009     Document Type: Article

References (54)

1. Allen JR, Nguyen LX, Sargent KE, Lipson KL, Hackett A, Urano F. High ER stress in beta-cells stimulates intracellular degradation of misfolded insulin. Biochem Biophys Res Commun 324: 166-170, 2004.
2. Araki E, Oyadomari S, Mori M. Impact of endoplasmic reticulum stress pathway on pancreatic beta-cells and diabetes mellitus. Exp Biol Med (Maywood) 228: 1213-1217, 2003.
3. Bian Q, Fernandes AF, Taylor A, Wu M, Pereira P, Shang F. Expression of K6W-ubiquitin in lens epithelial cells leads to upregulation of a broad spectrum of molecular chaperones. Mol Vision 14: 403-412, 2008.
4. Bowes AJ, Khan MI, Shi Y, Robertson L, Werstuck GH. Valproate attenuates accelerated atherosclerosis in hyperglycemic apoE-deficient mice: evidence in support of a role for endoplasmic reticulum stress and glycogen synthase kinase-3 in lesion development and hepatic steatosis. Am J Pathol 174: 330-342, 2009.
5. Buse MG. Hexosamines, insulin resistance, and the complications of diabetes: current status. Am J Physiol Endocrinol Metab 290: E1-E8, 2006.
6. Cassader M, Gambino R, Musso G, Depetris N, Mecca F, Cavallo-Perin P, Pacini G, Rizzetto M, Pagano G. Postprandial triglyceride-rich lipoprotein metabolism and insulin sensitivity in nonalcoholic steatohepatitis patients. Lipids 36: 1117-1124, 2001.
7. Cox JS, Shamu CE, Walter P. Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73: 1197-1206, 1993.
8. DeHaven JE, Robinson KA, Nelson BA, Buse MG. A novel variant of glutamine:fructose-6-phosphate amidotransferase-1 (GFAT1) mRNA is selectively expressed in striated muscle. Diabetes 50: 2419-2424, 2001.
9. Durand P, Golinelli-Pimpaneau B, Mouilleron S, Badet B, Badet-Denisot MA. Highlights of glucosamine-6P synthase catalysis. Arch Biochem Biophys 474: 302-317, 2008.
10. Gouze JN, Gouze E, Palmer GD, Kaneto H, Ghivizzani SC, Grodzinsky AJ, Evans CH. Adenovirus-mediated gene transfer of glutamine: fructose-6-phosphate amidotransferase antagonizes the effects of interleukin-1beta on rat chondrocytes. Osteoarthritis Cartilage 12: 217-224, 2004.
11. Haffner SJ, Cassells H. Hyperglycemia as a cardiovascular risk factor. Am J Med 115, Suppl 8A: 6S-11S, 2003.
12. Hanriot D, Bello G, Ropars A, Seguin-Devaux C, Poitevin G, Grosjean S, Latger-Cannard V, Devaux Y, Zannad F, Regnault V, Lacolley P, Mertes PM, Hess K, Longrois D. C-reactive protein induces pro- and anti-inflammatory effects, including activation of the liver X receptor alpha, on human monocytes. Thromb Haemost 99: 558-569, 2008.
13. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274, 1999.
14. Hebert LF Jr, Daniels MC, Zhou J, Crook ED, Turner RL, Simmons ST, Neidigh JL, Zhu JS, Baron AD, McClain DA. Overexpression of glutamine:fructose-6-phosphate amidotransferase in transgenic mice leads to insulin resistance. J Clin Invest 98: 930-936, 1996.
15. Helenius A. How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum. Mol Biol Cell 5: 253-265, 1994.
16. Hsiao JR, Chang KC, Chen CW, Wu SY, Su IJ, Hsu MC, Jin YT, Tsai ST, Takada K, Chang Y. Endoplasmic reticulum stress triggers XBP-1-mediated up-regulation of an EBV oncoprotein in nasopharyngeal carcinoma. Cancer Res 69: 4461-4467, 2009.
17. Huang X, Tsuji N, Miyoshi T, Motobu M, Islam MK, Alim MA, Fujisaki K. Characterization of glutamine: fructose-6-phosphate aminotransferase from the ixodid tick, Haemaphysalis longicornis, and its critical role in host blood feeding. Int J Parasitol 37: 383-392, 2007.
18. Ikesugi K, Mulhern ML, Madson CJ, Hosoya K, Terasaki T, Kador PF, Shinohara T. Induction of endoplasmic reticulum stress in retinal pericytes by glucose deprivation. Curr Eye Res 31: 947-953, 2006.
19. Inoue H, Tanizawa Y, Wasson J, Behn P, Kalidas K, Bernal-Mizrachi E, Mueckler M, Marshall H, Donis-Keller H, Crock P, Rogers D, Mikuni M, Kumashiro H, Higashi K, Sobue G, Oka Y, Permutt MA. A gene encoding a transmembrane protein is mutated in patients with diabetes mellitus and optic atrophy (Wolfram syndrome). Nat Genet 20: 143-148, 1998.
20. Jackson KG, Maitin V, Leake DS, Yaqoob P, Williams CM. Saturated fat-induced changes in Sf 60-400 particle composition reduces uptake of LDL by HepG2 cells. J Lipid Res 47: 393-403, 2006.
21. James LR, Fantus IG, Goldberg H, Ly H, Scholey JW. Overexpression of GFAT activates PAI-1 promoter in mesangial cells. Am J Physiol Renal Physiol 279: F718-F727, 2000.
22. James LR, Tang D, Ingram A, Ly H, Thai K, Cai L, Scholey JW. Flux through the hexosamine pathway is a determinant of nuclear factor kappaB- dependent promoter activation. Diabetes 51: 1146-1156, 2002.
23. Kammoun HL, Chabanon H, Hainault I, Luquet S, Magnan C, Koike T, Ferre P, Foufelle F. GRP78 expression inhibits insulin and ER stress-induced SREBP-1c activation and reduces hepatic steatosis in mice. J Clin Invest 119: 1201-1215, 2009.
24. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Devel 13: 1211-1233, 1999.
25. Kim AJ, Shi Y, Austin RC, Werstuck GH. Valproate protects cells from ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3. J Cell Sci 118: 89-99, 2005.
26. Lautamaki R, Borra R, Iozzo P, Komu M, Lehtimaki T, Salmi M, Jalkanen S, Airaksinen KE, Knuuti J, Parkkola R, Nuutila P. Liver steatosis coexists with myocardial insulin resistance and coronary dysfunction in patients with type 2 diabetes. Am J Physiol Endocrinol Metab 291: E282-E290, 2006.
27. Lee JN, Ye J. Proteolytic activation of sterol regulatory element-binding protein induced by cellular stress through depletion of Insig-1. J Biol Chem 279: 45257-45265, 2004.
28. Li Y, Lopez P, Durand P, Ouazzani J, Badet B, Badet-Denisot MA. An enzyme-coupled assay for amidotransferase activity of glucosamine-6-phosphate synthase. Anal Biochem 370: 142-146, 2007.
29. Liu G, Sun Y, Li Z, Song T, Wang H, Zhang Y, Ge Z. Apoptosis induced by endoplasmic reticulum stress involved in diabetic kidney disease. Biochem Biophys Res Commun 370: 651-656, 2008.
30. Loria P, Lonardo A, Targher G. Is liver fat detrimental to vessels? Intersections in the pathogenesis of NAFLD and atherosclerosis. Clin Sci (Lond) 115: 1-12, 2008.
31. Milewski S. Glucosamine-6-phosphate synthase-the multi-facets enzyme. Biochim Biophys Acta 1597: 173-192, 2002.
32. Niimi M, Ogawara T, Yamashita T, Yamamoto Y, Ueyama A, Kambe T, Okamoto T, Ban T, Tamanoi H, Ozaki K, Fujiwara T, Fukui H, Takahashi EI, Kyushiki H, Tanigami A. Identification of GFAT1-L, a novel splice variant of human glutamine:fructose-6-phosphate amidotransferase (GFAT1) that is expressed abundantly in skeletal muscle. J Hum Genet 46: 566-571, 2001.
33. Oyadomari S, Koizumi A, Takeda K, Gotoh T, Akira S, Araki E, Mori M. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J Clin Invest 109: 525-532, 2002.
34. Oyadomari S, Takeda K, Takiguchi M, Gotoh T, Matsumoto M, Wada I, Akira S, Araki E, Mori M. Nitric oxide-induced apoptosis in pancreatic beta cells is mediated by the endoplasmic reticulum stress pathway. Proc Natl Acad Sci USA 98: 10845-10850, 2001.
35. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461, 2004.
36. Pahl HL. Signal transduction from the endoplasmic reticulum to the cell nucleus. Physiol Rev 79: 683-701, 1999.
37. Qiu W, Avramoglu RK, Rutledge AC, Tsai J, Adeli K. Mechanisms of glucosamine-induced suppression of the hepatic assembly and secretion of apolipoprotein B-100-containing lipoproteins. J Lipid Res 47: 1749-1761, 2006.
38. Qiu W, Kohen-Avramoglu R, Mhapsekar S, Tsai J, Austin RC, Adeli K. Glucosamine-induced endoplasmic reticulum stress promotes ApoB100 degradation: evidence for Grp78-mediated targeting to proteasomal degradation. Arterioscler Thromb Vasc Biol 25: 571-577, 2005.
39. Raman P, Krukovets I, Marinic TE, Bornstein P, Stenina OI. Glycosylation mediates up-regulation of a potent antiangiogenic and proatherogenic protein, thrombospondin-1, by glucose in vascular smooth muscle cells. J Biol Chem 282: 5704-5714, 2007.
40. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev 8: 519-529, 2007.
41. 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 glycerophosphate dehydrogenase, fatty acid synthase, and acetyl-CoA carboxylase mRNA levels. J Biol Chem 278: 28547-28552, 2003.
42. Schroder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res 569: 29-63, 2005.
43. Shang J, Gao N, Kaufman RJ, Ron D, Harding HP, Lehrman MA. Translation attenuation by PERK balances ER glycoprotein synthesis with lipid-linked oligosaccharide flux. J Cell Biol 176: 605-616, 2007.
44. Socha L, Silva D, Lesage S, Goodnow C, Petrovsky N. The role of endoplasmic reticulum stress in nonimmune diabetes: NOD. k iHEL, a novel model of beta cell death. Ann NY Acad Sci 1005: 178-183, 2003.
45. Srinivasan V, Sandhya N, Sampathkumar R, Farooq S, Mohan V, Balasubramanyam M. Glutamine fructose-6-phosphate amidotransferase (GFAT) gene expression and activity in patients with type 2 diabetes: inter-relationships with hyperglycaemia and oxidative stress. Clin Biochem 40: 952-957, 2007.
46. Toledo FG, Sniderman AD, Kelley DE. Influence of hepatic steatosis (fatty liver) on severity and composition of dyslipidemia in type 2 diabetes. Diabetes Care 29: 1845-1850, 2006.
47. Wang J, Takeuchi T, Tanaka S, Kubo SK, Kayo T, Lu D, Takata K, Koizumi A, Izumi T. A mutation in the insulin 2 gene induces diabetes with severe pancreatic beta-cell dysfunction in the Mody mouse. J Clin Invest 103: 27-37, 1999.
48. Weigert C, Brodbeck K, Lehmann R, Haring HU, Schleicher ED. Overexpression of glutamine:fructose-6-phosphate-amidotransferase induces transforming growth factor-beta1 synthesis in NIH-3T3 fibroblasts. FEBS Lett 488: 95-99, 2001.
49. Werstuck GH, Khan MI, Femia G, Kim AJ, Tedesco V, Trigatti B, Shi Y. Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model. Diabetes 55: 93-101, 2006.
50. Werstuck GH, Kim AJ, Brenstrum T, Ohnmacht SA, Panna E, Capretta A. Examining the correlations between GSK-3 inhibitory properties and anti-convulsant efficacy of valproate and valproate-related compounds. Bioorg Med Chem Lett 14: 5465-5467, 2004.
51. Werstuck GH, Lentz SR, Dayal S, Hossain GS, Sood SK, Shi YY, Zhou J, Maeda N, Krisans SK, Malinow MR, Austin RC. Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways. J Clin Invest 107: 1263-1273, 2001.
52. Zhou J, Lhotak S, Hilditch BA, Austin RC. Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice. Circulation 111: 1814-1821, 2005.
53. Zhou P, Teruya-Feldstein J, Lu P, Fleisher M, Olshen A, Comenzo RL. Calreticulin expression in the clonal plasma cells of patients with systemic light-chain (AL-) amyloidosis is associated with response to high-dose melphalan. Blood 111: 549-557, 2008.
54. Zinszner H, Kuroda M, Wang X, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev 12: 982-995, 1998.