Tools for probing and perturbing O-GlcNAc in cells and in vivo

Current Opinion in Chemical Biology

Volumn 17, Issue 5, 2013, Pages 719-728

  Cecioni, Samy ^a   Vocadlo, David J ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; AZIDE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYSTEINE; DEHYDROALANINE; HEXOSAMINE; KETONE; LECTIN; N ACETYLGLUCOSAMINE; NUCLEOPORIN; PROTEOME;

CAENORHABDITIS ELEGANS; CARBOHYDRATE ANALYSIS; HUMAN; IN VIVO STUDY; INTRACELLULAR SIGNALING; MASS SPECTROMETRY; METABOLIC ENGINEERING; MICHAEL ADDITION; NONHUMAN; PROTEIN CROSS LINKING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; SITE DIRECTED MUTAGENESIS; TETRATRICOPEPTIDE REPEAT; TOBACCO;

ACETYLGLUCOSAMINE; ANIMALS; GLYCOSYLATION; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 84887135413     PISSN: 13675931     EISSN: 18790402     Source Type: Journal    
DOI: 10.1016/j.cbpa.2013.06.030     Document Type: Review

References (76)

1. Torres C.R., Hart G.W. Topography and polypeptide distribution of terminal N-acetylglucosamine residues on the surfaces of intact lymphocytes, Evidence for O-linked GlcNAc. J Biol Chem 1984, 259:3308-3317.
2. Haltiwanger R.S., Holt G.D., Hart G.W. Enzymatic addition of O-GlcNAc to nuclear and cytoplasmic proteins. Identification of a uridine diphospho-N-acetylglucosamine:peptide β-N-acetylglucosaminyltransferase. J Biol Chem 1990, 265:2563-2568.
3. Dong D.L., Hart G.W. Purification and characterization of an O-GlcNAc selective N-acetyl-β-d-glucosaminidase from rat spleen cytosol. J Biol Chem 1994, 269:19321-19330.
4. Vocadlo D.J. O-GlcNAc processing enzymes: catalytic mechanisms, substrate specificity, and enzyme regulation. Curr Opin Chem Biol 2012, 16:488-497.
5. Hart G.W., Housley M.P., Slawson C. Cycling of O-linked β-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 2007, 446:1017-1022.
6. Zeidan Q., Hart G.W. The intersections between O-GlcNAcylation and phosphorylation: implications for multiple signaling pathways. J Cell Sci 2010, 123:13-22.
7. Wang Z., Gucek M., Hart G.W. Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc. Proc Natl Acad Sci U S A 2008, 105:13793-13798.
8. 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 Gen Subj 2010, 1800:96-106.
9. Tarrant M.K., Rho H.-S., Xie Z., Jiang Y.L., Gross C., Culhane J.C., Yan G., Qian J., Ichikawa Y., Matsuoka T., et al. Regulation of CK2 by phosphorylation and O-GlcNAcylation revealed by semisynthesis. Nat Chem Biol 2012, 8:262-269.
10. Kim E.J. Chemical arsenal for the study of O-GlcNAc. Molecules 2011, 16:1987-2022.
11. Yang Y.R., Song M., Lee H., Jeon Y., Choi E.-J., Jang H.-J., Moon H.Y., Byun H.-Y., Kim E.-K., Kim D.H., et al. O-GlcNAcase is essential for embryonic development and maintenance of genomic stability. Aging Cell 2012, 11:439-448.
12. 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 U S A 2000, 97:5735-5739.
13. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res 2009, 37:D233-D238.
14. Lazarus M.B., Nam Y., Jiang J., Sliz P., Walker S. Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 2011, 469:564-567.
15. Lazarus M.B., Jiang J., Gloster T.M., Zandberg W.F., Whitworth G.E., Vocadlo D.J., Walker S. Structural snapshots of the reaction coordinate for O-GlcNAc transferase. Nat Chem Biol 2012, 8:966-968.
16. Schimpl M., Zheng X., Borodkin V.S., Blair D.E., Ferenbach A.T., Schüttelkopf A.W., Navratilova I., Aristotelous T., Albarbarawi O., Robinson D.A., et al. O-GlcNAc transferase invokes nucleotide sugar pyrophosphate participation in catalysis. Nat Chem Biol 2012, 8:969-974.
17. Gloster T.M., Zandberg W.F., Heinonen J.E., Shen D.L., Deng L., Vocadlo D.J. Hijacking a biosynthetic pathway yields a glycosyltransferase inhibitor within cells. Nat Chem Biol 2011, 7:174-181.
18. Ma Z., Vocadlo D.J., Vosseller K. Hyper-O-GlcNAcylation is anti-apoptotic and maintains constitutive NF-κB activity in pancreatic cancer cells. J Biol Chem 2013.
19. Ruan H.-B., Han X., Li M.-D., Singh Jay P., Qian K., Azarhoush S., Zhao L., Bennett Anton M., Samuel Varman T., Wu J., et al. O-GlcNAc transferase/host cell factor C1 complex regulates gluconeogenesis by modulating PGC-1α stability. Cell Metab 2012, 16:226-237.
20. Capotosti F., Guernier S., Lammers F., Waridel P., Cai Y., Jin J., Conaway J.W., Conaway R.C., Herr W. O-GlcNAc transferase catalyzes site-specific proteolysis of HCF-1. Cell 2011, 144:376-388.
21. Dennis R.J., Taylor E.J., Macauley M.S., Stubbs K.A., Turkenburg J.P., Hart S.J., Black G.N., Vocadlo D.J., Davies G.J. Structure and mechanism of a bacterial β-glucosaminidase having O-GlcNAcase activity. Nat Struct Mol Biol 2006, 13:365-371.
22. Rao F.V., Dorfmueller H.C., Villa F., Allwood M., Eggleston I.M., van Aalten D.M.F. Structural insights into the mechanism and inhibition of eukaryotic O-GlcNAc hydrolysis. EMBO J 2006, 25:1569-1578.
23. 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., et al. A potent mechanism-inspired O-GlcNAcase inhibitor that blocks phosphorylation of tau in vivo. Nat Chem Biol 2008, 4:483-490.
24. Dorfmueller H.C., Borodkin V.S., Schimpl M., Shepherd S.M., Shpiro N.A., van Aalten D.M.F. GlcNAcstatin: a Picomolar, selective O-GlcNAcase inhibitor that modulates intracellular O-GlcNAcylation levels. J Am Chem Soc 2006, 128:16484-16485.
25. Mariappa D., Sauert K., Marino K., Turnock D., Webster R., van Aalten D.M.F., Ferguson M.A.J., Muller H.-A.J. Protein O-GlcNAcylation is required for fibroblast growth factor signaling in Drosophila. Sci Signal 2011, 4:ra89.
26. Yuzwa S.A., Shan X., Macauley M.S., Clark T., Skorobogatko Y., Vosseller K., Vocadlo D.J. Increasing O-GlcNAc slows neurodegeneration and stabilizes tau against aggregation. Nat Chem Biol 2012, 8:393-399.
27. Vosseller K., Trinidad J.C., Chalkley R.J., Specht C.G., Thalhammer A., Lynn A.J., Snedecor J.O., Guan S., Medzihradszky K.F., Maltby D.A., et al. O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affinity chromatography and mass spectrometry. Mol Cell Proteomics 2006, 5:923-934.
28. Chalkley R.J., Thalhammer A., Schoepfer R., Burlingame A.L. Identification of protein O-GlcNAcylation sites using electron transfer dissociation mass spectrometry on native peptides. Proc Natl Acad Sci U S A 2009, 106:8894-8899.
29. Schouppe D., Ghesquière B., Menschaert G., De Vos W.H., Bourque S., Trooskens G., Proost P., Gevaert K., Van Damme E.J.M. Interaction of the tobacco lectin with histone proteins. Plant Physiol 2011, 155:1091-1102.
30. Zachara N.E., Vosseller K., Hart G.W. Detection and analysis of proteins modified by O-linked N-acetylglucosamine. Current Protocols in Molecular Biology 2011, John Wiley & Sons, Inc.
31. 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.
32. Fujiki R., Hashiba W., Sekine H., Yokoyama A., Chikanishi T., Ito S., Imai Y., Kim J., He H.H., Igarashi K., et al. GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 2011, 480:557-560.
33. Yuzwa S.A., Yadav A.K., Skorobogatko Y., Clark T., Vosseller K., Vocadlo D. Mapping O-GlcNAc modification sites on tau and generation of a site-specific O-GlcNAc tau antibody. Amino Acids 2011, 40:857-868.
34. Klein A.L., Berkaw M.N., Buse M.G., Ball L.E. O-linked N-acetylglucosamine modification of insulin receptor substrate-1 occurs in close proximity to multiple SH2 domain binding motifs. Mol Cell Proteomics 2009, 8:2733-2745.
35. Overath T., Kuckelkorn U., Henklein P., Strehl B., Bonar D., Kloss A., Siele D., Kloetzel P.-M., Janek K. Mapping of O-GlcNAc Sites of 20 S proteasome subunits and Hsp90 by a novel biotin-cystamine tag. Mol Cell Proteomics 2012, 11:467-477.
36. 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.
37. Vosseller K., Hansen K.C., Chalkley R.J., Trinidad J.C., Wells L., Hart G.W., Burlingame A.L. Quantitative analysis of both protein expression and serine/threonine post-translational modifications through stable isotope labeling with dithiothreitol. Proteomics 2005, 5:388-398.
38. Sletten E.M., Bertozzi C.R. From mechanism to mouse: a tale of two bioorthogonal reactions. Acc Chem Res 2011, 44:666-676.
39. Mahal L.K., Yarema K.J., Bertozzi C.R. Engineering chemical reactivity on cell surfaces through oligosaccharide biosynthesis. Science 1997, 276:1125-1128.
40. Vocadlo D.J., Hang H.C., Kim E.-J., Hanover J.A., Bertozzi C.R. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc Natl Acad Sci U S A 2003, 100:9116-9121.
41. Boyce M., Carrico I.S., Ganguli A.S., Yu S.-H., Hangauer M.J., Hubbard S.C., Kohler J.J., Bertozzi C.R. Metabolic cross-talk allows labeling of O-linked β-N-acetylglucosamine-modified proteins via the N-acetylgalactosamine salvage pathway. Proc Natl Acad Sci U S A 2011, 108:3141-3146.
42. Zaro B.W., Yang Y.-Y., Hang H.C., Pratt M.R. Chemical reporters for fluorescent detection and identification of O-GlcNAc-modified proteins reveal glycosylation of the ubiquitin ligase NEDD4-1. Proc Natl Acad Sci U S A 2011, 108:8146-8151.
43. Bateman L.A., Zaro B.W., Chuh K.N., Pratt M.R. N-Propargyloxycarbamate monosaccharides as metabolic chemical reporters of carbohydrate salvage pathways and protein glycosylation. Chem Commun 2013, 49:4328-4330.
44. Burnham-Marusich A.R., Snodgrass C.J., Johnson A.M., Kiyoshi C.M., Buzby S.E., Gruner M.R., Berninsone P.M. Metabolic labeling of Caenorhabditis elegans primary embryonic cells with azido-sugars as a tool for glycoprotein discovery. PLoS One 2012, 7:e49020.
45. Gurcel C., Vercoutter-Edouart A.-S., Fonbonne C., Mortuaire M., Salvador A., Michalski J.-C., Lemoine J. Identification of new O-GlcNAc modified proteins using a click-chemistry-based tagging. Anal Bioanal Chem 2008, 390:2089-2097.
46. Sprung R., Nandi A., Chen Y., Kim S.C., Barma D., Falck J.R., Zhao Y. Tagging-via-substrate strategy for probing O-GlcNAc modified proteins. J Proteome Res 2005, 4:950-957.
47. Nandi A., Sprung R., Barma D.K., Zhao Y., Kim S.C., Falck J.R., Zhao Y. Global identification of O-GlcNAc-modified proteins. Anal Chem 2005, 78:452-458.
48. Hahne H., Sobotzki N., Nyberg T., Helm D., Borodkin V.S., van Aalten D.M.F., Agnew B., Kuster B. Proteome wide purification and identification of O-GlcNAc-modified proteins using click chemistry and mass spectrometry. J Proteome Res 2013, 12:927-936.
49. 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.
50. Fairbanks B.D., Sims E.A., Anseth K.S., Bowman C.N. Reaction rates and mechanisms for radical, photoinitated addition of thiols to alkynes, and implications for thiol-yne photopolymerizations and click reactions. Macromolecules 2010, 43:4113-4119.
51. Conte M.L., Staderini S., Marra A., Sanchez-Navarro M., Davis B.G., Dondoni A. Multi-molecule reaction of serum albumin can occur through thiol-yne coupling. Chem Commun 2011, 47:11086-11088.
52. van Geel R., Pruijn G.J.M., van Delft F.L., Boelens W.C. Preventing thiol-yne addition improves the specificity of strain-promoted azide-alkyne cycloaddition. Bioconjug Chem 2012, 23:392-398.
53. Devaraj N.K., Weissleder R., Hilderbrand S.A. Tetrazine-based cycloadditions: application to pretargeted live cell imaging. Bioconjug Chem 2008, 19:2297-2299.
54. Devaraj N.K., Weissleder R. Biomedical applications of tetrazine cycloadditions. Acc Chem Res 2011, 44:816-827.
55. Patterson D.M., Nazarova L.A., Xie B., Kamber D.N., Prescher J.A. Functionalized cyclopropenes as bioorthogonal chemical reporters. J Am Chem Soc 2012, 134:18638-18643.
56. Khidekel N., Arndt S., Lamarre-Vincent N., Lippert A., Poulin-Kerstien K.G., Ramakrishnan B., Qasba P.K., Hsieh-Wilson L.C. A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications. J Am Chem Soc 2003, 125:16162-16163.
57. Boeggeman E., Ramakrishnan B., Kilgore C., Khidekel N., Hsieh-Wilson L.C., Simpson J.T., Qasba P.K. Direct identification of nonreducing GlcNAc residues on N-glycans of glycoproteins using a novel chemoenzymatic method. Bioconjug Chem 2007, 18:806-814.
58. Wang Z., Udeshi N.D., O'Malley M., Shabanowitz J., Hunt D.F., Hart G.W. Enrichment and site mapping of O-linked N-acetylglucosamine by a combination of chemical/enzymatic tagging, photochemical cleavage, and electron transfer dissociation mass spectrometry. Mol Cell Proteomics 2010, 9:153-160.
59. 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.
60. Alfaro J.F., Gong C.-X., Monroe M.E., Aldrich J.T., Clauss T.R.W., Purvine S.O., Wang Z., Camp D.G., Shabanowitz J., Stanley P., et al. Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc Natl Acad Sci U S A 2012, 109:7280-7285.
61. Sakaidani Y., Nomura T., Matsuura A., Ito M., Suzuki E., Murakami K., Nadano D., Matsuda T., Furukawa K., Okajima T. O-Linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell-matrix interactions. Nat Commun 2011, 2:583.
62. Drougat L., Olivier-Van Stichelen S., Mortuaire M., Foulquier F., Lacoste A.-S., Michalski J.-C., Lefebvre T., Vercoutter-Edouart A.-S. Characterization of O-GlcNAc cycling and proteomic identification of differentially O-GlcNAcylated proteins during G1/S transition. Biochim Biophys Acta Gen Subj 2012, 1820:1839-1848.
63. Hughes C., Krijgsveld J. Developments in quantitative mass spectrometry for the analysis of proteome dynamics. Trends Biotechnol 2012, 30:668-676.
64. Myers S.A., Panning B., Burlingame A.L. Polycomb repressive complex 2 is necessary for the normal site-specific O-GlcNAc distribution in mouse embryonic stem cells. Proc Natl Acad Sci U S A 2011, 108:9490-9495.
65. Skorobogatko Y., Deuso J., Adolf-Bergfoyle J., Nowak M., Gong Y., Lippa C., Vosseller K. Human Alzheimer's disease synaptic O-GlcNAc site mapping and iTRAQ expression proteomics with ion trap mass spectrometry. Amino Acids 2011, 40:765-779.
66. Khidekel N., Ficarro S.B., Clark P.M., Bryan M.C., Swaney D.L., Rexach J.E., Sun Y.E., Coon J.J., Peters E.C., Hsieh-Wilson L.C. Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics. Nat Chem Biol 2007, 3:339-348.
67. Breidenbach M.A., Palaniappan K.K., Pitcher A.A., Bertozzi C.R. Mapping Yeast N-Glycosites with Isotopically Recoded Glycans. Mol Cell Proteomics 2012, 11.
68. Rexach J.E., Rogers C.J., Yu S.-H., Tao J., Sun Y.E., Hsieh-Wilson L.C. Quantification of O-glycosylation stoichiometry and dynamics using resolvable mass tags. Nat Chem Biol 2010, 6:645-651.
69. Rexach J.E., Clark P.M., Mason D.E., Neve R.L., Peters E.C., Hsieh-Wilson L.C. Dynamic O-GlcNAc modification regulates CREB-mediated gene expression and memory formation. Nat Chem Biol 2012, 8:253-261.
70. Yi W., Clark P.M., Mason D.E., Keenan M.C., Hill C., Goddard W.A., Peters E.C., Driggers E.M., Hsieh-Wilson L.C. Phosphofructokinase 1 glycosylation regulates cell growth and metabolism. Science 2012, 337:975-980.
71. Hahne H., Gholami A.M., Kuster B. Discovery of O-GlcNAc-modified proteins in published large-scale proteome data. Mol Cell Proteomics 2012, 11:843-850.
72. Myers S.A., Daou S., Affar E.B., Burlingame A. Electron transfer dissociation (ETD): the mass spectrometric breakthrough essential for O-GlcNAc protein site assignments-a study of the O-GlcNAcylated protein Host Cell Factor C1. Proteomics 2013, 13:982-991.
73. Zhao P., Viner R., Teo C.F., Boons G.-J., Horn D., Wells L. Combining high-energy C-trap dissociation and electron transfer dissociation for protein O-GlcNAc modification site assignment. J Proteome Res 2011, 10:4088-4104.
74. Yu S.-H., Boyce M., Wands A.M., Bond M.R., Bertozzi C.R., Kohler J.J. Metabolic labeling enables selective photocrosslinking of O-GlcNAc-modified proteins to their binding partners. Proc Natl Acad Sci U S A 2012, 109:4834-4839.
75. Carrillo L.D., Krishnamoorthy L., Mahal L.K. A cellular FRET-based sensor for β-O-GlcNAc, a dynamic carbohydrate modification involved in signaling. J Am Chem Soc 2006, 128:14768-14769.
76. Carrillo L.D., Froemming J.A., Mahal L.K. Targeted in vivo O-GlcNAc sensors reveal discrete compartment-specific dynamics during signal transduction. J Biol Chem 2011, 286:6650-6658.