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Structural basis of Notch O-glucosylation and O-xylosylation by mammalian protein-O-glucosyltransferase 1 (POGLUT1).

Li Z, Fischer M, Satkunarajah M, Zhou D, Withers SG, Rini JM
Nat Commun 8 185 (2017)
Related entries: 5l0r, 5l0s, 5l0u, 5l0v, 5ub5

Cited: 24 times
EuropePMC logo PMID: 28775322

Abstract

Protein O-glucosyltransferase 1/Rumi-mediated glucosylation of Notch epidermal growth factor-like (EGF-like) domains plays an important role in Notch signaling. Protein O-glucosyltransferase 1 shows specificity for folded EGF-like domains, it can only glycosylate serine residues in the C1XSXPC2 motif, and it possesses an uncommon dual donor substrate specificity. Using several EGF-like domains and donor substrate analogs, we have determined the structures of human Protein O-glucosyltransferase 1 substrate/product complexes that provide mechanistic insight into the basis for these properties. Notably, we show that Protein O-glucosyltransferase 1's requirement for folded EGF-like domains also leads to its serine specificity and that two distinct local conformational states are likely responsible for its ability to transfer both glucose and xylose. We also show that Protein O-glucosyltransferase 1 possesses the potential to xylosylate a much broader range of EGF-like domain substrates than was previously thought. Finally, we show that Protein O-glucosyltransferase 1 has co-evolved with EGF-like domains of the type found in Notch.POGLUT1 is a protein-O-glucosyltransferase that transfers glucose and xylose to the EGF-like domains of Notch and other signaling receptors. Here the authors report the structure of human POGLUT1 in complexes with 3 different EGF-like domains and donor substrates and shed light on the enzyme's substrate specificity and catalytic mechanism.

Articles - 5l0t mentioned but not cited (2)

  1. Structural basis of Notch O-glucosylation and O-xylosylation by mammalian protein-O-glucosyltransferase 1 (POGLUT1). Li Z, Fischer M, Satkunarajah M, Zhou D, Withers SG, Rini JM. Nat Commun 8 185 (2017)
  2. Letter Altered Notch Signaling in Dowling-Degos Disease: Additional Mutations in POGLUT1 and Further Insights into Disease Pathogenesis. Ralser DJ, Takeuchi H, Fritz G, Basmanav FB, Effern M, Sivalingam S, El-Shabrawi-Caelen L, Degirmentepe EN, Kocatürk E, Singh M, Booken N, Spierings NMK, Schnabel V, Heineke A, Knuever J, Wolf S, Wehner M, Tronnier M, Leverkus M, Tantcheva-Poór I, Wenzel J, Oji V, Has C, Hölzel M, Frank J, Haltiwanger RS, Betz RC. J Invest Dermatol 139 960-964 (2019)


Reviews citing this publication (8)

  1. Meta-heterogeneity: Evaluating and Describing the Diversity in Glycosylation Between Sites on the Same Glycoprotein. Čaval T, Heck AJR, Reiding KR. Mol Cell Proteomics 20 100010 (2021)
  2. Emerging structural insights into glycosyltransferase-mediated synthesis of glycans. Moremen KW, Haltiwanger RS. Nat Chem Biol 15 853-864 (2019)
  3. Glycomics, Glycoproteomics, and Glycogenomics: An Inter-Taxa Evolutionary Perspective. West CM, Malzl D, Hykollari A, Wilson IBH. Mol Cell Proteomics 20 100024 (2021)
  4. Meeting Between Rumi and Shams in Notch Signaling; Implications for Pain Management: A Narrative Review. Rajaei S, Fatahi Y, Dabbagh A. Anesth Pain Med 9 e85279 (2019)
  5. Current Views on the Roles of O-Glycosylation in Controlling Notch-Ligand Interactions. Saiki W, Ma C, Okajima T, Takeuchi H. Biomolecules 11 (2021)
  6. Modulation of Notch Signaling by Small-Molecular Compounds and Its Potential in Anticancer Studies. Czerwonka A, Kałafut J, Nees M. Cancers (Basel) 15 4563 (2023)
  7. Significant Roles of Notch O-Glycosylation in Cancer. Wang W, Okajima T, Takeuchi H. Molecules 27 1783 (2022)
  8. Structure, function, and pathology of protein O-glucosyltransferases. Mehboob MZ, Lang M. Cell Death Dis 12 71 (2021)

Articles citing this publication (14)

  1. Two novel protein O-glucosyltransferases that modify sites distinct from POGLUT1 and affect Notch trafficking and signaling. Takeuchi H, Schneider M, Williamson DB, Ito A, Takeuchi M, Handford PA, Haltiwanger RS. Proc Natl Acad Sci U S A 115 E8395-E8402 (2018)
  2. POGLUT1 biallelic mutations cause myopathy with reduced satellite cells, α-dystroglycan hypoglycosylation and a distinctive radiological pattern. Servián-Morilla E, Cabrera-Serrano M, Johnson K, Pandey A, Ito A, Rivas E, Chamova T, Muelas N, Mongini T, Nafissi S, Claeys KG, Grewal RP, Takeuchi M, Hao H, Bönnemann C, Lopes Abath Neto O, Medne L, Brandsema J, Töpf A, Taneva A, Vilchez JJ, Tournev I, Haltiwanger RS, Takeuchi H, Jafar-Nejad H, Straub V, Paradas C. Acta Neuropathol 139 565-582 (2020)
  3. Structural Basis for the Initiation of Glycosaminoglycan Biosynthesis by Human Xylosyltransferase 1. Briggs DC, Hohenester E. Structure 26 801-809.e3 (2018)
  4. On-tissue spatially resolved glycoproteomics guided by N-glycan imaging reveal global dysregulation of canine glioma glycoproteomic landscape. Malaker SA, Quanico J, Raffo-Romero A, Kobeissy F, Aboulouard S, Tierny D, Bertozzi CR, Fournier I, Salzet M. Cell Chem Biol 29 30-42.e4 (2022)
  5. Xylosyl Extension of O-Glucose Glycans on the Extracellular Domain of NOTCH1 and NOTCH2 Regulates Notch Cell Surface Trafficking. Urata Y, Saiki W, Tsukamoto Y, Sago H, Hibi H, Okajima T, Takeuchi H. Cells 9 (2020)
  6. A β-hairpin epitope as novel structural requirement for protein arginine rhamnosylation. Yakovlieva L, Wood TM, Kemmink J, Kotsogianni I, Koller F, Lassak J, Martin NI, Walvoort MTC. Chem Sci 12 1560-1567 (2020)
  7. Identification of a novel genetic locus associated with immune-mediated thrombotic thrombocytopenic purpura. Stubbs MJ, Coppo P, Cheshire C, Veyradier A, Dufek S, Levine AP, Thomas M, Patel V, Connolly JO, Hubank M, Benhamou Y, Galicier L, Poullin P, Kleta R, Gale DP, Stanescu H, Scully MA. Haematologica 107 574-582 (2022)
  8. A comprehensive role evaluation and mechanism exploration of POGLUT2 in pan-cancer. Xu X, Xie G, Xie M, Liu Q. Front Oncol 12 962540 (2022)
  9. Coagulation factor IX analysis in bioreactor cell culture supernatant predicts quality of the purified product. Zacchi LF, Roche-Recinos D, Pegg CL, Phung TK, Napoli M, Aitken C, Sandford V, Mahler SM, Lee YY, Schulz BL, Howard CB. Commun Biol 4 390 (2021)
  10. HIT-2: Implementing machine learning algorithms to treat bound ions in biomolecules. Sun S, Xu H, Xie Y, Sanchez JE, Guo W, Liu D, Li L. Comput Struct Biotechnol J 21 1383-1389 (2023)
  11. Ligand-Induced Conformational and Dynamical Changes in a GT-B Glycosyltransferase: Molecular Dynamics Simulations of Heptosyltransferase I Complexes. Hassan BA, Milicaj J, Ramirez-Mondragon CA, Sham YY, Taylor EA. J Chem Inf Model 62 324-339 (2022)
  12. Multifaceted regulation of Notch signaling by glycosylation. Pandey A, Niknejad N, Jafar-Nejad H. Glycobiology 31 8-28 (2021)
  13. Other Types of Glycosylation. Tsukamoto Y, Takeuchi H. Adv Exp Med Biol 1325 117-135 (2021)
  14. Structure of the human heparan sulfate polymerase complex EXT1-EXT2. Leisico F, Omeiri J, Le Narvor C, Beaudouin J, Hons M, Fenel D, Schoehn G, Couté Y, Bonnaffé D, Sadir R, Lortat-Jacob H, Wild R. Nat Commun 13 7110 (2022)


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