Hexosamines regulate sensitivity of glucose-stimulated insulin secretion in β-cells

American Journal of Physiology - Endocrinology and Metabolism

Volumn 290, Issue 2, 2006, Pages

  Cooksey, Robert C ^a   Pusuluri, Sumitha ^a   Hazel, Mark ^a   McClain, Donald A ^a  

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

Author keywords

Desensitization; Glucose sensing; Islet

Indexed keywords

CARBACHOL; CARBON DIOXIDE; FRUCTOSE 6 PHOSPHATE; GLUCOSE; HEXOSAMINE; INSULIN; MESSENGER RNA; MITOCHONDRIAL ENZYME; TRANSFERASE;

ANIMAL TISSUE; ARTICLE; CELL ISOLATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; FEMALE; GLUCOSE OXIDATION; IN VITRO STUDY; INSULIN RELEASE; INSULIN SENSITIVITY; MALE; MOUSE; MOUSE STRAIN; NONHUMAN; PANCREAS ISLET; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; TRANSGENIC MOUSE; WILD TYPE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; GENETICS; INSULIN RESISTANCE; METABOLISM; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; GLUCOSE; HEXOSAMINES; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC;

EID: 33644856434     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00265.2005     Document Type: Article

References (50)

1. Anello M, Spampinato D, Piro S, Purrello F, and Rabuazzo AM. Glucosamine-induced alterations of mitochondrial function in pancreatic β-cells: possible role of protein glycosylation. Am J Physiol Endocrinol Metab 287: E602-E608, 2004.
2. Balkan B and Dunning BE. Glucosamine inhibits glucokinase in vitro and produces a glucose-specific impairment of in vivo insulin secretion in rats. Diabetes 43: 1173-1179, 1994.
3. Baron AD, Zhu JS, Zhu JH, Weldon H, Maianu L, and Garvey WT. Glucosamine induces insulin resistance in vivo by affecting GLUT 4 translocation in skeletal muscle. Implications for glucose toxicity. J Clin Invest 96: 2792-2801, 1995.
4. Cooksey RC, Jouihan HA, Ajioka RS, Hazel MW, Jones DL, Kushner JP, and McClain DA. Oxidative stress, beta-cell apoptosis, and decreased insulin secretory capacity in mouse models of hemochromatosis. Endocrinology 145: 5305-5312, 2004.
5. Crook ED, Daniels MC, Smith TM, and McClain DA. Regulation of insulin-stimulated glycogen synthase activity by overexpression of glutamine: fructose-6-phosphate amidotransferase in rat-1 fibroblasts. Diabetes 42: 1289-1296, 1993.
6. Crook ED and McClain DA. Regulation of glycogen synthase and protein phosphatase-1 by hexosamines. Diabetes 45: 322-327, 1996.
7. Crook ED, Zhou J, Daniels M, Neidigh JL, and McClain DA. Regulation of glycogen synthase by glucose, glucosamine, and glutamine: fructose-6-phosphate amidotransferase. Diabetes 44: 314-320, 1995.
8. D'Alessandris C, Andreozzi F, Federici M, Cardellini M, Brunetti A, Ranalli M, Del Guerra S, Lauro D, Del Prato S, Marchetti P, Lauro R, and Sesti G. Increased O-glycosylation of insulin signaling proteins results in their impaired activation and enhanced susceptibility to apoptosis in pancreatic beta-cells. FASEB J 18: 959-961, 2004.
9. Gao Y, Miyazaki J, and Hart GW. The transcription factor PDX-1 is post-translationally modified by O-linked N-acetylglucosamine and this modification is correlated with its DNA binding activity and insulin secretion in min6 beta-cells. Arch Biochem Biophys 415: 155-163, 2003.
10. Giaccari A, Morviducci L, Zorretta D, Sbraccia P, Leonetti F, Caiola S, Buongiorno A, Bonadonna RC, and Tamburrano G. In vivo effects of glucosamine on insulin secretion and insulin sensitivity in the rat: possible relevance to the maladaptive responses to chronic hyperglycaemia. Diabetologia 38: 518-524, 1995.
11. Hazel M, Cooksey RC, Jones D, Parker G, Neidigh JL, Witherbee B, Gulve EA, and McClain DA. Activation of the hexosamine signaling pathway in adipose tissue results in decreased serum adiponectin and skeletal muscle insulin resistance. Endocrinology 145: 2118-2128, 2004.
12. Hebert LF Jr, Daniels MC, Zhou J, Crook ED, Turner RL, Simmons ST, Neidigh JL, Zhu JS, Baron AD, and McClain DA. Overexpression of glutamine:fructose-6-phosphate amidotransferase in transgenic mice leads to insulin resistance. J Clin Invest 98: 930-936, 1996.
13. Kaneto H, Xu G, Song KH, Suzuma K, Bonner-Weir S, Sharma A, and Weir GC. Activation of the hexosamine pathway leads to deterioration of pancreatic beta-cell function through the induction of oxidative stress. J Biol Chem 276: 31099-31104, 2001.
14. Kreppel LK, Blomberg MA, and Hart GW. Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J Biol Chem 272: 9308-9315, 1997.
15. Lehman DM, Fu DJ, Freeman AB, Hunt KJ, Leach RJ, Johnson-Pais T, Hamlington J, Dyer TD, Arya R, Abboud H, Goring HH, Duggirala R, Blangero J, Konrad RJ, and Stern MP. A single nucleotide polymorphism in MGEA5 encoding O-GlcNAc-selective N-acetyl-beta-D glucosaminidase is associated with type 2 diabetes in Mexican Americans. Diabetes 54: 1214-1221, 2005.
16. Lekanne Deprez RH, Fijnvandraat AC, Ruijter JM, and Moorman AF. Sensitivity and accuracy of quantitative real-time polymerase chain reaction using SYBR green I depends on cDNA synthesis conditions. Anal Biochem 307: 63-69, 2002.
17. Leonard J, Peers B, Johnson T, Ferreri K, Lee S, and Montminy MR. Characterization of somatostatin transactivating factor-1, a novel homeobox factor that stimulates somatostatin expression in pancreatic islet cells. Mol Endocrinol 7: 1275-1283, 1993.
18. Liu K, Paterson AJ, Chin E, and Kudlow JE. Glucose stimulates protein modification by O-linked GlcNAc in pancreatic beta cells: linkage of O-linked GlcNAc to beta cell death. Proc Natl Acad Sci USA 97: 2820-2825, 2000.
19. Liu K, Paterson AJ, Zhang F, McAndrew J, Fukuchi K, Wyss JM, Peng L, Hu Y, and Kudlow JE. Accumulation of protein O-GlcNAc modification inhibits proteasomes in the brain and coincides with neuronal apoptosis in brain areas with high O-GlcNAc metabolism. J Neurochem 89: 1044-1055, 2004.
20. Lubas WA and Hanover JA. Functional expression of O-linked GlcNAc transferase. Domain structure and substrate specificity. J Biol Chem 275: 10983-10988, 2000.
21. Marshall S, Bacote V, and Traxinger RR. Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system. Role of hexosamine biosynthesis in the induction of insulin resistance. J Biol Chem 266: 4706-4712, 1991.
22. McClain DA and Crook ED. Hexosamines and insulin resistance. Diabetes 45: 1003-1009, 1996.
23. McClain DA, Lubas WA, Cooksey RC, Hazel M, Parker GJ, Love DC, and Hanover JA. Altered glycan-dependent signaling induces insulin resistance and hyperleptinemia. Proc Natl Acad Sci USA 99: 10695-10699, 2002.
24. Miller CP, McGehee RE Jr, and Habener JF. IDX-1: a new homeodomain transcription factor expressed in rat pancreatic islets and duodenum that transactivates the somatostatin gene. EMBO J 13: 1145-1156, 1994.
25. Nakamura M, Barber AJ, Antonetti DA, LaNoue KF, Robinson KA, Buse MG, and Gardner TW. Excessive hexosamines block the neuroprotective effect of insulin and induce apoptosis in retinal neurons. J Biol Chem 276: 43748-43755, 2001.
26. Obici S, Wang J, Chowdury R, Feng Z, Siddhanta U, Morgan K, and Rossetti L. Identification of a biochemical link between energy intake and energy expenditure. J Clin Invest 109: 1599-1605, 2002.
27. Ohlsson H, Karlsson K, and Edlund T. IPF1, a homeodomain-containing transactivator of the insulin gene. EMBO J 12: 4251-4259, 1993.
28. Parker GJ, Lund KC, Taylor RP, and McClain DA. Insulin resistance of glycogen synthase mediated by o-linked N-acetylglucosamine. J Biol Chem 278: 10022-10027, 2003.
29. Robinson KA, Sens DA, and Buse MG. Pre-exposure to glucosamine induces insulin resistance of glucose transport and glycogen synthesis in isolated rat skeletal muscles. Study of mechanisms in muscle and in rat-1 fibroblasts overexpressing the human insulin receptor. Diabetes 42: 1333-1346, 1993.
30. Rossetti L. Perspective: hexosamines and nutrient sensing. Endocrinology 141: 1922-1925, 2000.
31. Rossetti L, Giaccari A, and DeFronzo RA. Glucose toxicity. Diabetes Care 13: 610-630, 1990.
32. Rossetti L, Hawkins M, Chen W, Gindi J, and Barzilai N. In vivo glucosamine infusion induces insulin resistance in normoglycemic but not in hyperglycemic conscious rats. J Clin Invest 96: 132-140, 1995.
33. Savage DB, Sewter CP, Klenk ES, Segal DG, Vidal-Puig A, Considine RV, and O'Rahilly S. Resistin/Fizz3 expression in relation to obesity and peroxisome proliferator-activated receptor-gamma action in humans. Diabetes 50: 2199-2202, 2001.
34. Shankar RR, Zhu JS, and Baron AD. Glucosamine infusion in rats mimics the beta-cell dysfunction of non-insulin-dependent diabetes mellitus. Metabolism 47: 573-577, 1998.
35. Tang J, Neidigh JL, Cooksey RC, and McClain DA. Transgenic mice with increased hexosamine flux specifically targeted to beta-cells exhibit hyperinsulinemia and peripheral insulin resistance. Diabetes 49: 1492-1499, 2000.
36. Uldry M, Ibberson M, Hosokawa M, and Thorens B. GLUT2 is a high affinity glucosamine transporter. FEBS Lett 524: 199-203, 2002.
37. Veerababu G, Tang J, Hoffman RT, Daniels MC, Hebert LF Jr, Crook ED, Cooksey RC, and McClain DA. Overexpression of glutamine: fructose-6-phosphate amidotransferase in the liver of transgenic mice results in enhanced glycogen storage, hyperlipidemia, obesity, and impaired glucose tolerance. Diabetes 49: 2070-2078, 2000.
38. Vosseller K, Wells L, Lane MD, and Hart GW. Elevated nucleocytoplasmic glycosylation by O-GlcNAc results in insulin resistance associated with defects in Akt activation in 3T3-L1 adipocytes. Proc Natl Acad Sci USA 99: 5313-5318, 2002.
39. Waeber G, Thompson N, Nicod P, and Bonny C. Transcriptional activation of the GLUT2 gene by the IPF-1/STF-1/IDX-1 homeobox factor. Mol Endocrinol 10: 1327-1334, 1996.
40. Watada H, Kajimoto Y, Miyagawa J, Hanafusa T, Hamaguchi K, Matsuoka T, Yamamoto K, Matsuzawa Y, Kawamori R, and Yamasaki Y. PDX-1 induces insulin and glucokinase gene expressions in alphaTC1 clone 6 cells in the presence of betacellulin. Diabetes 45: 1826-1831, 1996.
41. Wells L and Hart GW. O-GlcNAc turns twenty: functional implications for post-translational modification of nuclear and cytosolic proteins with a sugar. FEBS Lett 546: 154-158, 2003.
42. Wells L, Whelan SA, and Hart GW. O-GlcNAc: a regulatory posttranslational modification. Biochem Biophys Res Commun 302: 435-441, 2003.
43. Whelan SA and Hart GW. Proteomic approaches to analyze the dynamic relationships between nucleocytoplasmic protein glycosylation and phosphorylation. Circ Res 93: 1047-1058, 2003.
44. Yoshikawa H, Tajiri Y, Sako Y, Hashimato T, Umeda F, and Nawata H. Glucosamine-induced beta-cell dysfunction: a possible involvement of glucokinase or glucose-transporter type 2. Pancreas 24: 228-234, 2002.
45. Zawalich WS, Bonnet-Eymard M, and Zawalich KC. Glucose-induced desensitization of the pancreatic β-cell is species dependent. Am J Physiol Endocrinol Metab 275: E917-E924, 1998.
46. Zawalich WS, Diaz VA, and Zawalich KC. Role of phosphoinositide metabolism in induction of memory in isolated perifused rat islets. Am J Physiol Endocrinol Metab 254: E609-E616, 1988.
47. Zawalich WS and Zawalich KC. Glucosamine-induced desensitization of beta-cell responses: possible involvement of impaired information flow in the phosphoinositide cycle. Endocrinology 130: 3135-3142, 1992.
48. Zhang H, Jia Y, Cooper JJ, Hale T, Zhang Z, and Elbein SC. Common variants in glutamine:fructose-6-phosphate amidotransferase 2 (GFPT2) gene are associated with type 2 diabetes, diabetic nephropathy, and increased GFPT2 mRNA levels. J Clin Endocrinol Metab 89: 748-755, 2004.
49. Zitzler J, Link D, Schafer R, Liebetrau W, Kazinski M, Bonin-Debs A, Behl C, Buckel P, and Brinkmann U. High-throughput functional genomics identifies genes that ameliorate toxicity due to oxidative stress in neuronal HT-22 cells: GFPT2 protects cells against peroxide. Mol Cell Proteomics 3: 834-840, 2004.
50. Zraika S, Dunlop M, Proietto J, and Andrikopoulos S. The hexosamine biosynthesis pathway regulates insulin secretion via protein glycosylation in mouse islets. Arch Biochem Biophys 405: 275-279, 2002.