Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics

Nature Chemical Biology - Tập 3 Số 6 - Trang 339-348 - 2007
Nelly Khidekel1, Scott B. Ficarro2, Peter M. Clark3, Marian C. Bryan3, Danielle L. Swaney4, Jessica E. Rexach5, Yi Eve Sun5, Joshua J. Coon4, Eric C. Peters2, Linda C. Hsieh‐Wilson3
1Division of Chemistry and Chemical Engineering and Howard Hughes Medical Institute, California Institute of Technology, Pasadena, California, 91125, USA.
2Genomics Institute of the Novartis Research Foundation, San Diego, USA
3Division of Chemistry and Chemical Engineering and Howard Hughes Medical Institute, California Institute of Technology, Pasadena, USA
4Department of Chemistry, University of Wisconsin-Madison, Madison, USA
5University of California, Los Angeles, Los Angeles, United States

Tóm tắt

Từ khóa


Tài liệu tham khảo

Khidekel, N. & Hsieh-Wilson, L.C. A 'molecular switchboard'–covalent modifications to proteins and their impact on transcription. Org. Biomol. Chem. 2, 1–7 (2004).

Greengard, P. The neurobiology of slow synaptic transmission. Science 294, 1024–1030 (2001).

Love, D.C. & Hanover, J.A. The hexosamine signaling pathway: deciphering the “O-GlcNAc code”. Sci. STKE 2005, re13 (2005).

Khidekel, N., Ficarro, S.B., Peters, E.C. & Hsieh-Wilson, L.C. Exploring the O-GlcNAc proteome: direct identification of O-GlcNAc-modified proteins from the brain. Proc. Natl. Acad. Sci. USA 101, 13132–13137 (2004).

Vosseller, K. et al. O-linked N-acetylglucosamine proteomics of postsynaptic density preparations using lectin weak affinity chromatography and mass spectrometry. Mol. Cell. Proteomics 5, 923–934 (2006).

Kneass, Z.T. & Marchase, R.B. Neutrophils exhibit rapid agonist-induced increases in protein-associated O-GlcNAc. J. Biol. Chem. 279, 45759–45765 (2004).

Zachara, N.E. et al. Dynamic O-GlcNAc modification of nucleocytoplasmic proteins in response to stress. A survival response of mammalian cells. J. Biol. Chem. 279, 30133–30142 (2004).

Cheng, X. & Hart, G.W. Alternative O-glycosylation/O-phosphorylation of serine-16 in murine estrogen receptor beta: post-translational regulation of turnover and transactivation activity. J. Biol. Chem. 276, 10570–10575 (2001).

Chou, T.Y., Hart, G.W. & Dang, C.V. c-Myc is glycosylated at threonine 58, a known phosphorylation site and a mutational hot spot in lymphomas. J. Biol. Chem. 270, 18961–18965 (1995).

Iyer, S.P. & Hart, G.W. Dynamic nuclear and cytoplasmic glycosylation: enzymes of O-GlcNAc cycling. Biochemistry 42, 2493–2499 (2003).

Cole, R.N. & Hart, G.W. Cytosolic O-glycosylation is abundant in nerve terminals. J. Neurochem. 79, 1080–1089 (2001).

Iyer, S.P.N. & Hart, G.W. Dynamic nuclear and cytoplasmic glycosylation: enzymes of O- GlcNAc cycling. Biochemistry 42, 2493–2499 (2003).

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. 24, 1680–1690 (2004).

Lamarre-Vincent, N. & Hsieh-Wilson, L.C. Dynamic glycosylation of the transcription factor CREB: a potential role in gene regulation. J. Am. Chem. Soc. 125, 6612–6613 (2003).

Griffith, L.S. & Schmitz, B. O-linked N-acetylglucosamine levels in cerebellar neurons respond reciprocally to perturbations of phosphorylation. Eur. J. Biochem. 262, 824–831 (1999).

Khidekel, N. et al. A chemoenzymatic approach toward the rapid and sensitive detection of O-GlcNAc posttranslational modifications. J. Am. Chem. Soc. 125, 16162–16163 (2003).

Ong, S.E., Mittler, G. & Mann, M. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat. Methods 1, 119–126 (2004).

Ross, P.L. et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 3, 1154–1169 (2004).

Tai, H.C., Khidekel, N., Ficarro, S.B., Peters, E.C. & Hsieh-Wilson, L.C. Parallel identification of O-GlcNAc-modified proteins from cell lysates. J. Am. Chem. Soc. 126, 10500–10501 (2004).

Cieniewski-Bernard, C. et al. Identification of O-linked N-acetylglucosamine proteins in rat skeletal muscle using two-dimensional gel electrophoresis and mass spectrometry. Mol. Cell. Proteomics 3, 577–585 (2004).

Hsu, J.L., Huang, S.Y., Chow, N.H. & Chen, S.H. Stable-isotope dimethyl labeling for quantitative proteomics. Anal. Chem. 75, 6843–6852 (2003).

Chalkley, R.J. & Burlingame, A.L. Identification of GlcNAcylation sites of peptides and alpha-crystallin using Q-TOF mass spectrometry. J. Am. Soc. Mass Spectrom. 12, 1106–1113 (2001).

Makarov, A., Denisov, E., Lange, O. & Horning, S. Dynamic range of mass accuracy in LTQ orbitrap hybrid mass spectrometer. J. Am. Soc. Mass Spectrom. 17, 977–982 (2006).

Roquemore, E.P., Chevrier, M.R., Cotter, R.J. & Hart, G.W. Dynamic O-GlcNAcylation of the small heat shock protein alpha B-crystallin. Biochemistry 35, 3578–3586 (1996).

Zhang, R., Sioma, C.S., Wang, S. & Regnier, F.E. Fractionation of isotopically labeled peptides in quantitative proteomics. Anal. Chem. 73, 5142–5149 (2001).

Haltiwanger, R.S., Grove, K. & Philipsberg, G.A. Modulation of O-linked N-acetylglucosamine levels on nuclear and cytoplasmic proteins in vivo using the peptide O-GlcNAc-beta-N-acetylglucosaminidase inhibitor O-(2-acetamido-2-deoxy-D-glucopyranosylidene)amino-N-phenylcarbamate. J. Biol. Chem. 273, 3611–3617 (1998).

Syka, J.E., Coon, J.J., Schroeder, M.J., Shabanowitz, J. & Hunt, D.F. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 101, 9528–9533 (2004).

Coon, J.J., Syka, J.E.P., Schwartz, J.C., Shabanowitz, J. & Hunt, D.F. Anion dependence in the partitioning between proton and electron transfer in ion/ion reactions. Int. J. Mass Spectrom. 236, 33–42 (2004).

Hogan, J.M., Pitteri, S.J., Chrisman, P.A. & McLuckey, S.A. Complementary structural information from a tryptic N-linked glycopeptide via electron transfer ion/ion reactions and collision-induced dissociation. J. Proteome Res. 4, 628–632 (2005).

Swaney, D.L. et al. Supplemental activation method for high-efficiency electron-transfer dissociation of doubly protonated peptide precursors. Anal. Chem. 79, 477–485 (2007).

Lazarus, B.D., Love, D.C. & Hanover, J.A. Recombinant O-GlcNAc transferase isoforms: identification of O-GlcNAcase, yes tyrosine kinase, and tau as isoform-specific substrates. Glycobiology 16, 415–421 (2006).

Whisenhunt, T.R. et al. Disrupting the enzyme complex regulating O-GlcNAcylation blocks signaling and development. Glycobiology 16, 551–563 (2006).

Nedivi, E., Hevroni, D., Naot, D., Israeli, D. & Citri, Y. Numerous candidate plasticity-related genes revealed by differential cDNA cloning. Nature 363, 718–722 (1993).

Ben-Ari, Y. & Cossart, R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci. 23, 580–587 (2000).

Beckmann, A.M., Davidson, M.S., Goodenough, S. & Wilce, P.A. Differential expression of Egr-1-like DNA-binding activities in the naive rat brain and after excitatory stimulation. J. Neurochem. 69, 2227–2237 (1997).

Nandi, A. et al. Global identification of O-GlcNAc-modified proteins. Anal. Chem. 78, 452–458 (2006).

Kamemura, K., Hayes, B.K., Comer, F.I. & Hart, G.W. Dynamic interplay between O-glycosylation and O-phosphorylation of nucleocytoplasmic proteins: alternative glycosylation/phosphorylation of THR-58, a known mutational hot spot of c-Myc in lymphomas, is regulated by mitogens. J. Biol. Chem. 277, 19229–19235 (2002).

Ludemann, N. et al. O-glycosylation of the tail domain of neurofilament protein M in human neurons and in spinal cord tissue of a rat model of amyotrophic lateral sclerosis (ALS). J. Biol. Chem. 280, 31648–31658 (2005).

Vosseller, K. et al. Quantitative analysis of both protein expression and serine/ threonine post-translational modifications through stable isotope labeling with dithiothreitol. Proteomics 5, 388–398 (2005).

Brackertz, M., Gong, Z., Leers, J. & Renkawitz, R. p66alpha and p66beta of the Mi-2/NuRD complex mediate MBD2 and histone interaction. Nucleic Acids Res. 34, 397–406 (2006).

Yang, X. et al. O-linkage of N-acetylglucosamine to Sp1 activation domain inhibits its transcriptional capability. Proc. Natl. Acad. Sci. USA 98, 6611–6616 (2001).

Gong, Z., Brackertz, M. & Renkawitz, R. SUMO modification enhances p66-mediated transcriptional repression of the Mi-2/NuRD complex. Mol. Cell. Biol. 26, 4519–4528 (2006).

Ule, J. & Darnell, R.B. RNA binding proteins and the regulation of neuronal synaptic plasticity. Curr. Opin. Neurobiol. 16, 102–110 (2006).

Elvira, G., Massie, B. & DesGroseillers, L. The zinc-finger protein ZFR is critical for Staufen 2 isoform specific nucleocytoplasmic shuttling in neurons. J. Neurochem. 96, 105–117 (2006).

Bastos, R., Lin, A., Enarson, M. & Burke, B. Targeting and function in mRNA export of nuclear pore complex protein Nup153. J. Cell Biol. 134, 1141–1156 (1996).

Jones, M.W. et al. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 4, 289–296 (2001).

Thiel, G. & Cibelli, G. Regulation of life and death by the zinc finger transcription factor Egr-1. J. Cell. Physiol. 193, 287–292 (2002).

James, A.B., Conway, A.M. & Morris, B.J. Genomic profiling of the neuronal target genes of the plasticity-related transcription factor – Zif268. J. Neurochem. 95, 796–810 (2005).

Wang, Q., Yu, S., Simonyi, A., Sun, G.Y. & Sun, A.Y. Kainic acid-mediated excitotoxicity as a model for neurodegeneration. Mol. Neurobiol. 31, 3–16 (2005).

Marin, P. et al. Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J. Neurosci. 17, 3445–3454 (1997).

Datta, R., Choudhury, P., Ghosh, A. & Datta, B. A glycosylation site, 60SGTS63, of p67 is required for its ability to regulate the phosphorylation and activity of eukaryotic initiation factor 2α. Biochemistry 42, 5453–5460 (2003).

Collins, M.O. et al. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 280, 5972–5982 (2005).

Gu, Y., Hamajima, N. & Ihara, Y. Neurofibrillary tangle-associated collapsin response mediator protein-2 (CRMP-2) is highly phosphorylated on Thr-509, Ser-518, and Ser-522. Biochemistry 39, 4267–4275 (2000).

Liu, F., Iqbal, K., Grundke-Iqbal, I., Hart, G.W. & Gong, C.X. O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc. Natl. Acad. Sci. USA 101, 10804–10809 (2004).

Gama, C.I. et al. Sulfation patterns of glycosaminoglycans encode molecular recognition and activity. Nat. Chem. Biol. 2, 467–473 (2006).