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Synergy of peptide and sugar in O-GlcNAcase substrate recognition.

<div class='caption-title'>OGA Binds Different O-GlcNAc Glycopeptides with Similar Conformation but Different Affinities</div>
Schimpl M, Borodkin VS, Gray LJ, van Aalten DM
OpenAccess logo Chem Biol 19 173-8 (2012)
Related entries: 2ydq, 2yds

Cited: 37 times
EuropePMC logo PMID: 22365600

Abstract

Protein O-GlcNAcylation is an essential reversible posttranslational modification in higher eukaryotes. O-GlcNAc addition and removal is catalyzed by O-GlcNAc transferase and O-GlcNAcase, respectively. We report the molecular details of the interaction of a bacterial O-GlcNAcase homolog with three different synthetic glycopeptides derived from characterized O-GlcNAc sites in the human proteome. Strikingly, the peptides bind a conserved O-GlcNAcase substrate binding groove with similar orientation and conformation. In addition to extensive contacts with the sugar, O-GlcNAcase recognizes the peptide backbone through hydrophobic interactions and intramolecular hydrogen bonds, while avoiding interactions with the glycopeptide side chains. These findings elucidate the molecular basis of O-GlcNAcase substrate specificity, explaining how a single enzyme achieves cycling of the complete O-GlcNAc proteome. In addition, this work will aid development of O-GlcNAcase inhibitors that target the peptide binding site.

Reviews - 2ydr mentioned but not cited (1)

  1. p53 Proteoforms and Intrinsic Disorder: An Illustration of the Protein Structure-Function Continuum Concept. Uversky VN. Int J Mol Sci 17 E1874 (2016)

Articles - 2ydr mentioned but not cited (5)

  1. Structures of human O-GlcNAcase and its complexes reveal a new substrate recognition mode. Li B, Li H, Lu L, Jiang J. Nat Struct Mol Biol 24 362-369 (2017)
  2. Synergy of peptide and sugar in O-GlcNAcase substrate recognition. Schimpl M, Borodkin VS, Gray LJ, van Aalten DM. Chem Biol 19 173-178 (2012)
  3. Modeling of RAS complexes supports roles in cancer for less studied partners. Engin HB, Carlin D, Pratt D, Carter H. BMC Biophys 10 5 (2017)
  4. Defining the structural origin of the substrate sequence independence of O-GlcNAcase using a combination of molecular docking and dynamics simulation. Martin JC, Fadda E, Ito K, Woods RJ. Glycobiology 24 85-96 (2014)
  5. Leveraging protein quaternary structure to identify oncogenic driver mutations. Ryslik GA, Cheng Y, Modis Y, Zhao H. BMC Bioinformatics 17 137 (2016)


Reviews citing this publication (15)

  1. Protein O-GlcNAcylation: emerging mechanisms and functions. Yang X, Qian K. Nat Rev Mol Cell Biol 18 452-465 (2017)
  2. A little sugar goes a long way: the cell biology of O-GlcNAc. Bond MR, Hanover JA. J Cell Biol 208 869-880 (2015)
  3. O-GlcNAc and the cardiovascular system. Dassanayaka S, Jones SP. Pharmacol Ther 142 62-71 (2014)
  4. O-GlcNAc processing enzymes: catalytic mechanisms, substrate specificity, and enzyme regulation. Vocadlo DJ. Curr Opin Chem Biol 16 488-497 (2012)
  5. Structural characterization of the O-GlcNAc cycling enzymes: insights into substrate recognition and catalytic mechanisms. Joiner CM, Li H, Jiang J, Walker S. Curr Opin Struct Biol 56 97-106 (2019)
  6. Chemical approaches to study O-GlcNAcylation. Banerjee PS, Hart GW, Cho JW. Chem Soc Rev 42 4345-4357 (2013)
  7. The role of O-GlcNAc signaling in the pathogenesis of diabetic retinopathy. Semba RD, Huang H, Lutty GA, Van Eyk JE, Hart GW. Proteomics Clin Appl 8 218-231 (2014)
  8. Insights into the role of maladaptive hexosamine biosynthesis and O-GlcNAcylation in development of diabetic cardiac complications. Qin CX, Sleaby R, Davidoff AJ, Bell JR, De Blasio MJ, Delbridge LM, Chatham JC, Ritchie RH. Pharmacol Res 116 45-56 (2017)
  9. O-GlcNAcase: promiscuous hexosaminidase or key regulator of O-GlcNAc signaling? Alonso J, Schimpl M, van Aalten DM. J Biol Chem 289 34433-34439 (2014)
  10. Role and Function of O-GlcNAcylation in Cancer. Lee JB, Pyo KH, Kim HR. Cancers (Basel) 13 5365 (2021)
  11. Deciphering the Functions of Protein O-GlcNAcylation with Chemistry. Worth M, Li H, Jiang J. ACS Chem Biol 12 326-335 (2017)
  12. Demystifying O-GlcNAcylation: hints from peptide substrates. Shi J, Ruijtenbeek R, Pieters RJ. Glycobiology 28 814-824 (2018)
  13. Integration of O-GlcNAc into Stress Response Pathways. Fahie KMM, Papanicolaou KN, Zachara NE. Cells 11 3509 (2022)
  14. Tools for functional dissection of site-specific O-GlcNAcylation. Gorelik A, van Aalten DMF. RSC Chem Biol 1 98-109 (2020)
  15. In Vitro Biochemical Assays for O-GlcNAc-Processing Enzymes. Kim EJ. Chembiochem 18 1462-1472 (2017)

Articles citing this publication (16)

  1. Removal of Abnormal Myofilament O-GlcNAcylation Restores Ca2+ Sensitivity in Diabetic Cardiac Muscle. Ramirez-Correa GA, Ma J, Slawson C, Zeidan Q, Lugo-Fagundo NS, Xu M, Shen X, Gao WD, Caceres V, Chakir K, DeVine L, Cole RN, Marchionni L, Paolocci N, Hart GW, Murphy AM. Diabetes 64 3573-3587 (2015)
  2. Nutrient-driven O-GlcNAc cycling - think globally but act locally. Harwood KR, Hanover JA. J Cell Sci 127 1857-1867 (2014)
  3. Insights into activity and inhibition from the crystal structure of human O-GlcNAcase. Elsen NL, Patel SB, Ford RE, Hall DL, Hess F, Kandula H, Kornienko M, Reid J, Selnick H, Shipman JM, Sharma S, Lumb KJ, Soisson SM, Klein DJ. Nat Chem Biol 13 613-615 (2017)
  4. Structure of a bacterial putative acetyltransferase defines the fold of the human O-GlcNAcase C-terminal domain. Rao FV, Schüttelkopf AW, Dorfmueller HC, Ferenbach AT, Navratilova I, van Aalten DM. Open Biol 3 130021 (2013)
  5. A mutant O-GlcNAcase enriches Drosophila developmental regulators. Selvan N, Williamson R, Mariappa D, Campbell DG, Gourlay R, Ferenbach AT, Aristotelous T, Hopkins-Navratilova I, Trost M, van Aalten DMF. Nat Chem Biol 13 882-887 (2017)
  6. Structural basis of O-GlcNAc recognition by mammalian 14-3-3 proteins. Toleman CA, Schumacher MA, Yu SH, Zeng W, Cox NJ, Smith TJ, Soderblom EJ, Wands AM, Kohler JJ, Boyce M. Proc Natl Acad Sci U S A 115 5956-5961 (2018)
  7. Genetic recoding to dissect the roles of site-specific protein O-GlcNAcylation. Gorelik A, Bartual SG, Borodkin VS, Varghese J, Ferenbach AT, van Aalten DMF. Nat Struct Mol Biol 26 1071-1077 (2019)
  8. Structural insights into the substrate binding adaptability and specificity of human O-GlcNAcase. Li B, Li H, Hu CW, Jiang J. Nat Commun 8 666 (2017)
  9. A mutant O-GlcNAcase as a probe to reveal global dynamics of protein O-GlcNAcylation during Drosophila embryonic development. Mariappa D, Selvan N, Borodkin V, Alonso J, Ferenbach AT, Shepherd C, Navratilova IH, vanAalten DMF. Biochem J 470 255-262 (2015)
  10. Loss of O-GlcNAcase catalytic activity leads to defects in mouse embryogenesis. Muha V, Authier F, Szoke-Kovacs Z, Johnson S, Gallagher J, McNeilly A, McCrimmon RJ, Teboul L, van Aalten DMF. J Biol Chem 296 100439 (2021)
  11. Evidence for a Functional O-Linked N-Acetylglucosamine (O-GlcNAc) System in the Thermophilic Bacterium Thermobaculum terrenum. Ostrowski A, Gundogdu M, Ferenbach AT, Lebedev AA, van Aalten DM. J Biol Chem 290 30291-30305 (2015)
  12. O-GlcNAcase contributes to cognitive function in Drosophila. Muha V, Fenckova M, Ferenbach AT, Catinozzi M, Eidhof I, Storkebaum E, Schenck A, van Aalten DMF. J Biol Chem 295 8636-8646 (2020)
  13. O-GlcNAcase Fragment Discovery with Fluorescence Polarimetry. Borodkin VS, Rafie K, Selvan N, Aristotelous T, Navratilova I, Ferenbach AT, van Aalten DMF. ACS Chem Biol 13 1353-1360 (2018)
  14. Enzymatic characterization of recombinant enzymes of O-GlcNAc cycling. Kim EJ, Hanover JA. Methods Mol Biol 1022 129-145 (2013)
  15. Can Glycosylation Mask the Detection of MHC Expressing p53 Peptides by T Cell Receptors? Nguyen TB, Lane DP, Verma CS. Biomolecules 11 1056 (2021)
  16. Native detection of protein O-GlcNAcylation by gel electrophoresis. Fu C, van Aalten DMF. Analyst 145 6826-6830 (2020)


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