Characteristic increase in nucleocytoplasmic protein glycosylation by O-GlcNAc in 3T3-L1 adipocyte differentiation

Biochemical and Biophysical Research Communications

Volumn 398, Issue 3, 2010, Pages 489-494

  Ishihara, Katsunori ^a   Takahashi, Isao ^a   Tsuchiya, Yuichi ^a   Hasegawa, Makoto ^a   Kamemura, Kazuo ^a  

^a NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

3T3 L1; Adipocyte; Differentiation; Glycosylation; O GlcNAc

Indexed keywords

6 DIAZO 5 OXONORLEUCINE; CCAAT ENHANCER BINDING PROTEIN ALPHA; CELL PROTEIN; LONG CHAIN FATTY ACID COENZYME A LIGASE; N ACETYLGLUCOSAMINE; NUCLEOPORIN; PYRUVATE CARBOXYLASE; VIMENTIN;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN GLYCOSYLATION;

3T3-L1 CELLS; ACETYLGLUCOSAMINE; ADIPOCYTES; ADIPOGENESIS; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-ALPHA; CELL NUCLEUS; CYTOPLASM; GLYCOSYLATION; MICE; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS;

EID: 77955270120     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.06.105     Document Type: Article

References (37)

1. Zeidan Q., Hart G.W. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J. Cell Sci. 2010, 123:13-22.
2. Vosseller K., Wells L., Lane M.D., Hart G.W. 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 2002, 99:5313-5318.
3. Whelan S.A., Lane M.D., Hart G.W. Regulation of the O-linked β-N-acetylglucosamine transferase by insulin signaling. J. Biol. Chem. 2008, 283:21411-21417.
4. Slawson C., Zachara N.E., Vosseller K., Cheung W.D., Lane M.D., Hart G.W. Perturbations in O-linked β-N-acetylglucosamine protein modification cause severe defects in mitotic progression and cytokinesis. J. Biol. Chem. 2005, 280:32944-32956.
5. Wang Z., Udeshi N.D., Slawson C., Compton P.D., Sakabe K., Cheung W.D., Shabanowitz J., Hunt D.F., Hart G.W. Extensive crosstalk between O-GlcNAcylation and phosphorylation regulates cytokinesis. Sci. Signal. 2010, 3:ra2.
6. Hart G.W., Housley M.P., Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 2007, 446:1017-1022.
7. Zhang F., Su K., Yang X., Bowe D.B., Paterson A.J., Kudlow J.E. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell 2003, 115:715-725.
8. Guinez C., Mir A.-M., Dehennaut V., Cacan R., Harduin-Lepers A., Michalski J.-C., Lefebvre T. Protein ubiquitination is modulated by O-GlcNAc glycosylation. FASEB J. 2008, 22:2901-2911.
9. Zachara N.E., O'Donnell N., Cheung W.D., Mercer J.J., Marth J.D., Hart G.W. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress: a survival response of mammalian cells. J. Biol. Chem. 2004, 279:30133-30142.
10. Ohn T., Kedersha N., Hickman T., Tisdale S., Anderson P. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 2008, 10:1224-1231.
11. Shafi R., Iyer S.P.N., Ellies L.G., O'Donnell N., Marek K.W., Chui D., Hart G.W., Marth J.D. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc. Natl. Acad. Sci. USA 2000, 97:5735-5739.
12. O'Donnell N., Zachara N.E., Hart G.W., Marth J.D. Ogt-dependent X-chromosome-linked protein glycosylation is a requisite modification in somatic cell function and embryo viability. Mol. Cell. Biol. 2004, 24:1680-1690.
13. Marshall S., Bacote V., Traxinger R.R. 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. 1991, 266:4706-4712.
14. Butkinaree C., Park K., Hart G.W. O-Linked β-N-acetylglucosamine (O-GlcNAc): extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim. Biophys. Acta 2010, 1800:96-106.
15. Lefebvre T., Dehennaut V., Guinez C., Olivier S., Drougat L., Mir A.-M., Mortuaire M., Vercoutter-Edouart A.-S., Michalski J.-C. Dysregulation of the nutrient/stress sensor O-GlcNAcylation is involved in the etiology of cardiovascular disorders, type-2 diabetes and Alzheimer's disease. Biochim. Biophys. Acta 2010, 1800:67-79.
16. Lehman D.M., Fu D.J., Freeman A.B., Hunt K.J., Leach R.J., Johnson-Pais T., Hamlington J., Dyer T.D., Arya R., Abboud H., Goring H.H., Duggirala R., Blangero J., Konrad R.J., Stern M.P. A single nucleotide polymorphism in MGEA5 encoding O-GlcNAc-selective N-acetyl-β-d-glucosaminidase is associated with type 2 diabetes in Mexican-Americans. Diabetes 2005, 54:1214-1221.
17. Forsythe M.E., Love D.C., Lazarus B.D., Kim E.J., Prinz W.A., Ashwell G.A., Krause M.W., Hanover J.A. Caenorhabditis elegans ortholog of a diabetes susceptibility locus: oga-1 (O-GlcNAcase) knockout impacts O-GlcNAc cycling, metabolism, and dauer. Proc. Natl. Acad. Sci. USA 2006, 103:11952-11957.
18. Hanover J.A., Krause M.W., Love D.C. The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim. Biophys. Acta 2010, 1800:80-95.
19. Buse M.G. Hexosamines, insulin resistance, and the complications of diabetes: current status. Am. J. Physiol. Endocrinol. Metab. 2006, 290:E1-E8.
20. Mandrup S., Lane M.D. Regulating adipogenesis. J. Biol. Chem. 1997, 272:5367-5370.
21. Yuzwa S.A., Macauley M.S., Heinonen J.E., Shan X., Dennis R.J., He Y., Whitworth G.E., Stubbs K.A., McEachern E.J., Davies G.J., Vocadlo D.J. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat. Chem. Biol. 2008, 4:483-490.
22. Wang Z., Pandey A., Hart G.W. Dynamic interplay between O-linked N-acetylglucosaminylation and glycogen synthase kinase-3-dependent phosphorylation. Mol. Cell. Proteomics 2007, 6:1365-1379.
23. Davis L.I., Blobel G. Nuclear pore complex contains a family of glycoproteins that includes p62: glycosylation through a previously unidentified cellular pathway. Proc. Natl. Acad. Sci. USA 1987, 84:7552-7556.
24. Teo C.F., Ingale S., Wolfert M.A., Elsayed G.A., Nöt L.G., Chatham J.C., Wells L., Boons G.-J. Glycopeptide-specific monoclonal antibodies suggest new roles for O-GlcNAc. Nat. Chem. Biol. 2010, 6:338-343.
25. Wells L., Vosseller K., Cole R.N., Cronshaw J.M., Matunis M.J., Hart G.W. Mapping sites of O-GlcNAc modification using affinity tags for serine and threonine post-translational modifications. Mol. Cell. Proteomics 2002, 1:791-804.
26. Mackall J.C., Lane M.D. Role of pyruvate carboxylase in fatty acid synthesis: alterations during preadipocyte differentiation. Biochem. Biophys. Res. Commun. 1977, 79:720-725.
27. Freytag S.O., Utter M.F. Induction of pyruvate carboxylase apoenzyme and holoenzyme in 3T3-L1 cells during differentiation. Proc. Natl. Acad. Sci. USA 1980, 77:1321-1325.
28. Sayeski P.P., Kudlow J.E. Glucose metabolism to glucosamine is necessary for glucose stimulation of transforming growth factor-α gene transcription. J. Biol. Chem. 1996, 271:15237-15243.
29. Franke W.W., Hergt M., Grund C. Rearrangement of the vimentin cytoskeleton during adipose conversion: formation of an intermediate filament cage around lipid globules. Cell 1987, 49:131-141.
30. Love D.C., Kochan J., Cathey R.L., Shin S.H., Hanover J.A. Mitochondrial and nucleocytoplasmic targeting of O-linked GlcNAc transferase. J. Cell Sci. 2003, 116:647-654.
31. Hu Y., Suarez J., Fricovsky E., Wang H., Scott B.T., Trauger S.A., Han W., Hu Y., Oyeleye M.O., Dilmann W.H. Increased enzymatic O-GlcNAcylation of mitochondrial proteins impairs mitochondrial function in cardiac myocytes exposed to high glucose. J. Biol. Chem. 2009, 284:547-555.
32. Ordóñez J.L., Osuna D., Herrero D., de Alava E., Madoz-Gúrpide J. Advances in Ewing's sarcoma research: where are we now and what lies ahead?. Cancer Res. 2009, 69:7140-7150.
33. Bachmaier R., Aryee D.N.T., Jug G., Kauer M., Kreppel M., Lee K.A., Kovar H. O-GlcNAcylation is involved in the transcriptional activity of EWS-FLI1 in Ewing's sarcoma. Oncogene 2009, 28:1280-1284.
34. Araya N., Hirota K., Shimamoto Y., Miyagishi M., Yoshida E., Ishida J., Kaneko S., Kaneko M., Nakajima T., Fukamizu A. Cooperative interaction of EWS with CREB-binding protein selectively activates hepatocyte nuclear factor 4-mediated transcription. J. Biol. Chem. 2003, 278:5427-5432.
35. Li H., Watford W., Li C., Parmelee A., Bryant M.A., Deng C., O'Shea J., Lee S.B. Ewing sarcoma gene EWS is essential for meiosis and B lymphocyte development. J. Clin. Invest. 2007, 117:1314-1323.
36. Lefterova M.I., Lazar M.A. New developments in adipogenesis. Trends Endocrinol. Metab. 2009, 20:107-114.
37. Li X., Molina H., Huang H., Zhang Y.-Y., Liu M., Qian S.-W., Slawson C., Dias W.B., Pandey A., Hart G.W., Lane M.D., Tang Q.-Q. O-Linked N-acetylglucosamine modification on CCAAT enhancer-binding protein β: role during adipocyte differentiation. J. Biol. Chem. 2009, 284:19248-19254.