Chemical Dissection of the Link between Streptozotocin, O-GlcNAc, and Pancreatic Cell Death

Chemistry and Biology

Volumn 15, Issue 8, 2008, Pages 799-807

  Pathak, Shalini ^a   Dorfmueller, Helge C ^a   Borodkin, Vladimir S ^a   van Aalten, Daan M F ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

CHEMBIO; SIGNALING

Indexed keywords

ANTINEOPLASTIC AGENT; BETA N ACETYLHEXOSAMINIDASE; HEXOSAMINIDASE C; N ACETYLGLUCOSAMINE; STREPTOZOCIN;

ANIMAL; APOPTOSIS; ARTICLE; BINDING COMPETITION; CELL DEATH; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; INSULINOMA; METABOLISM; MOUSE; PANCREAS ISLET BETA CELL; PATHOLOGY; TUMOR CELL LINE;

ACETYLGLUCOSAMINE; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BETA-N-ACETYLHEXOSAMINIDASES; BINDING, COMPETITIVE; CELL DEATH; CELL LINE, TUMOR; CELL SURVIVAL; INSULIN-SECRETING CELLS; INSULINOMA; MICE; STREPTOZOCIN;

EID: 49449101898     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2008.06.010     Document Type: Article

References (43)

1. Akimoto Y., Kreppel L., Hirano H., and Hart G. Localization of the O-linked N-acetylglucosamine transferase in rat pancreas. Diabetes 48 (1999) 2407-2413
2. Bolzán A.D., and Bianchi M.S. Genotoxicity of streptozotocin. Mutat. Res. 512 (2002) 121-134
3. Brentjens R., and Saltz L. Islet cell tumors of the pancreas: the medical oncologist's perspective. Surg. Clin. North Am. 81 (2001) 527-542
4. Dong D.L.Y., and Hart G.W. Purification and characterization of an O-GlcNAc selective N-acetyl-β-D-glucosaminidase from rat spleen cytosol. J. Biol. Chem. 269 (1994) 19321-19330
5. Dorfmueller H.C., Borodkin V.S., Schimpl M., Shepherd S.M., Shpiro N.A., and van Aalten D.M.F. GlcNAcstatin: a picomolar, selective O-GlcNAcase inhibitor that modulates intracellular O-GlcNAcylation levels. J. Am. Chem. Soc. 128 (2006) 16484-16485
6. Duke R.C., Chervenak R., and Cohen J.J. Endogenous endonuclease-induced DNA fragmentation: an early event in cell-mediated cytolysis. Proc. Natl. Acad. Sci. USA 80 (1983) 6361-6365
7. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60 (2004) 2126-2132
8. Gao Y., Parker G.J., and Hart G.W. Streptozotocin-induced β-cell death is independent of its inhibition of O-GlcNAcase in pancreatic Min6 cells. Arch. Biochem. Biophys. 383 (2000) 296-302
9. Gao Y., Wells L., Comer F.I., Parker G.J., and Hart G.W. Dynamic O-glycosylation of nuclear and cytosolic proteins-cloning and characterization of a neutral, cytosolic β-N-acetylglucosaminidase from human brain. J. Biol. Chem. 276 (2001) 9838-9845
10. Gichner T., Velemínský J., and Krepinský J. Strong mutagenic activity of streptozotocin-an antibiotic with an alkylnitroso group. Mol. Gen. Genet. 102 (1968) 184-186
11. Haltiwanger R.S., Blomberg M., and Hart G. Glycosylation of nuclear and cytoplasmic proteins. Purification and characterization of a uridine diphospho-N-acetylglucosamine:polypeptide β-N-acetylglucosaminyltransferase. J. Biol. Chem. 267 (1992) 9005-9013
12. Haltiwanger R.S., Grove K., and Philipsberg G.A. Modulation of O-linked N-acetylglucosamine levels on nuclear and cytoplasmic proteins in vivo using the peptide O-GlcNAc-β-N-acetylglucosaminidase inhibitor O-(2-acetamido-2-deoxy-D-glucopyranosylidene)amino-N-phenylcarbamate. J. Biol. Chem. 273 (1998) 3611-3617
13. Hanover J., Lai Z., Lee G., Lubas W., and Sato S. Elevated O-linked N-acetylglucosamine metabolism in pancreatic β-cells. Arch. Biochem. Biophys. 362 (1999) 38-45
14. Hart G.W., Housley M.P., and Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446 (2007) 1017-1022
15. Hu P., Berkowitz P., Madden V., and Rubenstein D. Stabilization of plakoglobin and enhanced keratinocyte cell-cell adhesion by intracellular O-glycosylation. J. Biol. Chem. 281 (2006) 12786-12791
16. Kaneto H., Fujii J., Seo H., Suzuki K., Matsuoka T., Nakamura M., Tatsumi H., Yamasaki Y., Kamada T., and Taniguchi N. Apoptotic cell death triggered by nitric oxide in pancreatic β-cells. Diabetes 44 (1995) 733-738
17. Kaneto H., Xu G., Song K.H., Suzuma K., Bonner-Weir S., Sharma A., and Weir G.C. Activation of the hexosamine pathway leads to deterioration of pancreatic β-cell function through the induction of oxidative stress. J. Biol. Chem. 276 (2001) 31099-31104
18. Konrad R.J., Mikolaenko I., Tolar J.F., Liu K., and Kudlow J.E. The potential mechanism of the diabetogenic action of streptozotocin: inhibition of pancreatic β-cell O-GlcNAc-selective N-acetyl-β-D-glucosaminidase. Biochem. J. 356 (2001) 31-41
19. Leatherbarrow R.J. GraFit version 5 (2001), Erithacus Software Ltd, Horley, UK
20. Lee T.N., Alborn W.E., Knierman M.D., and Konrad R.J. Alloxan is an inhibitor of O-GlcNAc-selective N-acetyl-β-D-glucosaminidase. Biochem. Biophys. Res. Commun. 350 (2006) 1038-1043
21. Liu K., Paterson A.J., Chin E., and Kudlow J.E. Glucose stimulates protein modification by O-linked GlcNAc in pancreatic β cells: linkage of O-linked GlcNAc to β cell death. Proc. Natl. Acad. Sci. USA 97 (2000) 2820-2825
22. Liu K., Paterson A., Zhang F., McAndrew J., Fukuchi K., Wyss J., Peng L., Hu Y., and Kudlow J. 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 (2004) 1044-1055
23. Lubas W., Frank D., Krause M., and Hanover J. O-linked GlcNAc transferase is a conserved nucleocytoplasmic protein containing tetratricopeptide repeats. J. Biol. Chem. 272 (1997) 9316-9324
24. Mansford K.R., and Opie L. Comparison of metabolic abnormalities in diabetes mellitus induced by streptozotocin or by alloxan. Lancet 1 (1968) 670-671
25. Martinez J., Oiry J., Imbach J., and Winternitz F. Activated N-nitrosocarbamates for regioselective synthesis of N-nitrosoureas. J. Med. Chem. 25 (1982) 178-182
26. Matthews J., Belof J., Acevedo-Duncan M., and Potter R. Glucosamine-induced increase in Akt phosphorylation corresponds to increased endoplasmic reticulum stress in astroglial cells. Mol. Cell. Biochem. 298 (2007) 109-123
27. Miyazaki J., Araki K., Yamato E., Ikegami H., Asano T., Shibasaki Y., Oka Y., and Yamamura K. Establishment of a pancreatic β cell line that retains glucose-inducible insulin secretion: special reference to expression of glucose transporter isoforms. Endocrinology 127 (1990) 126-132
28. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
29. Okuyama R., and Yachi M. Cytosolic O-GlcNAc accumulation is not involved in β-cell death in HIT-T15 or Min6. Biochem. Biophys. Res. Commun. 287 (2001) 366-371
30. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
31. Ran C., Pantazopoulos P., Medarova Z., and Moore A. Synthesis and testing of β-cell-specific streptozotocin-derived near-infrared imaging probes. Angew. Chem. Int. Ed. Engl. 46 (2007) 8998-9001
32. Rao F.V., Dorfmueller H.C., Villa F., Allwood M., Eggleston I.M., and van Aalten D.M.F. Structural insights into the mechanism and inhibition of eukaryotic O-GlcNAc hydrolysis. EMBO J. 25 (2006) 1569-1578
33. Roos M., Xie W., Su K., Clark J., Yang X., Chin E., Paterson A., and Kudlow J. Streptozotocin, an analog of N-acetylglucosamine, blocks the removal of O-GlcNAc from intracellular proteins. Proc. Assoc. Am. Physicians 110 (1998) 422-432
34. Schnedl W.J., Ferber S., Johnson J.H., and Newgard C.B. STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 43 (1994) 1326-1333
35. Slawson C., Zachara N.E., Vosseller K., Cheung W.D., Lane M.D., and Hart G.W. Perturbations in O-linked β-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis. J. Biol. Chem. 280 (2005) 32944-32956
36. Toleman C., Paterson A.J., Shin R., and Kudlow J.E. Streptozotocin inhibits O-GlcNAcase via the production of a transition state analog. Biochem. Biophys. Res. Commun. 340 (2006) 526-534
37. Turk J., Corbett J.A., Ramanadham S., Bohrer A., and Mcdaniel M.L. Biochemical evidence for nitric oxide formation from streptozotocin in isolated pancreatic islets. Biochem. Biophys. Res. Commun. 197 (1993) 1458-1464
38. Vavra J.J., Deboer C., Dietz A., Hanka L.J., and Sokolski W.T. Streptozotocin, a new antibacterial antibiotic. Antibiot. Annu. 7 (1959) 230-235
39. Whitworth G., Macauley M., Stubbs K., Dennis R., Taylor E., Davies G., Greig I., and Vocadlo D. Analysis of PUGNAc and NAG-thiazoline as transition state analogues for human O-GlcNAcase: mechanistic and structural insights into inhibitor selectivity and transition state poise. J. Am. Chem. Soc. 129 (2007) 635-644
40. Yamamoto H., Uchigata Y., and Okamoto H. Streptozotocin and alloxan induce DNA strand breaks and poly(ADP-ribose) synthetase in pancreatic islets. Nature 294 (1981) 284-286
41. Yang W., Kim J., Nam H., Ju J., Kim H., Kim Y., and Cho J. Modification of p53 with O-linked N-acetylglucosamine regulates p53 activity and stability. Nat. Cell Biol. 8 (2006) 1074-1083
42. Yang X., Ongusaha P., Miles P., Havstad J., Zhang F., So W., Kudlow J., Michell R., Olefsky J., Field S., and Evans R. Phosphoinositide signalling links O-GlcNAc transferase to insulin resistance. Nature 451 (2008) 964-969
43. Zachara N.E., and Hart G.W. Cell signaling, the essential role of O-GlcNAc!. Biochim. Biophys. Acta 1761 (2006) 599-617