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Fringe-mediated extension of O-linked fucose in the ligand-binding region of Notch1 increases binding to mammalian Notch ligands.

Taylor P, Takeuchi H, Sheppard D, Chillakuri C, Lea SM, Haltiwanger RS, Handford PA
Proc Natl Acad Sci U S A 111 7290-5 (2014)
Related entries: 4cud, 4cuf, 4d0e, 4d0f

Cited: 62 times
EuropePMC logo PMID: 24803430

Abstract

The Notch signaling pathway is essential for many aspects of development, cell fate determination, and tissue homeostasis. Notch signaling can be modulated by posttranslational modifications to the Notch receptor, which are known to alter both ligand binding and receptor activation. We have modified the ligand-binding region (EGF domains 11-13) of human Notch1 (hN1) with O-fucose and O-glucose glycans and shown by flow cytometry and surface plasmon resonance that the Fringe-catalyzed addition of GlcNAc to the O-fucose at T466 in EGF12 substantially increases binding to Jagged1 and Delta-like 1 (DLL1) ligands. We have subsequently determined the crystal structures of EGF domains 11-13 of hN1 modified with either the O-fucose monosaccharide or the GlcNAc-fucose disaccharide at T466 of EGF12 and observed no change in backbone structure for each variant. Collectively, these data demonstrate a role for GlcNAc in modulating the ligand-binding site in hN1 EGF12, resulting in an increased affinity of this region for ligands Jagged1 and DLL1. We propose that this finding explains the Fringe-catalyzed enhancement of Notch-Delta signaling observed in flies and humans, but suggest that the inhibitory effect of Fringe on Jagged/Serrate mediated signaling involves other regions of Notch.

Articles - 4cue mentioned but not cited (3)

  1. Fringe-mediated extension of O-linked fucose in the ligand-binding region of Notch1 increases binding to mammalian Notch ligands. Taylor P, Takeuchi H, Sheppard D, Chillakuri C, Lea SM, Haltiwanger RS, Handford PA. Proc Natl Acad Sci U S A 111 7290-7295 (2014)
  2. Non-Linear and Flexible Regions of the Human Notch1 Extracellular Domain Revealed by High-Resolution Structural Studies. Weisshuhn PC, Sheppard D, Taylor P, Whiteman P, Lea SM, Handford PA, Redfield C. Structure 24 555-566 (2016)
  3. Small molecule activation of NOTCH signaling inhibits acute myeloid leukemia. Ye Q, Jiang J, Zhan G, Yan W, Huang L, Hu Y, Su H, Tong Q, Yue M, Li H, Yao G, Zhang Y, Liu H. Sci Rep 6 26510 (2016)


Reviews citing this publication (15)

  1. The notch ligand JAGGED1 as a target for anti-tumor therapy. Li D, Masiero M, Banham AH, Harris AL. Front Oncol 4 254 (2014)
  2. Significance of glycosylation in Notch signaling. Takeuchi H, Haltiwanger RS. Biochem Biophys Res Commun 453 235-242 (2014)
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  5. The Diverse Contributions of Fucose Linkages in Cancer. Keeley TS, Yang S, Lau E. Cancers (Basel) 11 E1241 (2019)
  6. Multiple roles for O-glycans in Notch signalling. Varshney S, Stanley P. FEBS Lett 592 3819-3834 (2018)
  7. The multiple roles of epidermal growth factor repeat O-glycans in animal development. Haltom AR, Jafar-Nejad H. Glycobiology 25 1027-1042 (2015)
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  12. A Review of Advances in Hematopoietic Stem Cell Mobilization and the Potential Role of Notch2 Blockade. Albakri M, Tashkandi H, Zhou L. Cell Transplant 29 963689720947146 (2020)
  13. Astrogliosis in multiple sclerosis and neuro-inflammation: what role for the notch pathway? Mora P, Chapouly C. Front Immunol 14 1254586 (2023)
  14. Just a spoonful of sugar: Short glycans affect protein properties and functions. Bello C, Rovero P, Papini AM. J Pept Sci 25 e3167 (2019)
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Articles citing this publication (44)

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  2. Structural biology. Structural basis for Notch1 engagement of Delta-like 4. Luca VC, Jude KM, Pierce NW, Nachury MV, Fischer S, Garcia KC. Science 347 847-853 (2015)
  3. Deciphering the Fringe-Mediated Notch Code: Identification of Activating and Inhibiting Sites Allowing Discrimination between Ligands. Kakuda S, Haltiwanger RS. Dev Cell 40 193-201 (2017)
  4. O-Glycosylation modulates the stability of epidermal growth factor-like repeats and thereby regulates Notch trafficking. Takeuchi H, Yu H, Hao H, Takeuchi M, Ito A, Li H, Haltiwanger RS. J Biol Chem 292 15964-15973 (2017)
  5. 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)
  6. Notch-modifying xylosyltransferase structures support an SNi-like retaining mechanism. Yu H, Takeuchi M, LeBarron J, Kantharia J, London E, Bakker H, Haltiwanger RS, Li H, Takeuchi H. Nat Chem Biol 11 847-854 (2015)
  7. A proactive role of water molecules in acceptor recognition by protein O-fucosyltransferase 2. Valero-González J, Leonhard-Melief C, Lira-Navarrete E, Jiménez-Osés G, Hernández-Ruiz C, Pallarés MC, Yruela I, Vasudevan D, Lostao A, Corzana F, Takeuchi H, Haltiwanger RS, Hurtado-Guerrero R. Nat Chem Biol 12 240-246 (2016)
  8. Cis-activation in the Notch signaling pathway. Nandagopal N, Santat LA, Elowitz MB. Elife 8 e37880 (2019)
  9. Mapping Sites of O-Glycosylation and Fringe Elongation on Drosophila Notch. Harvey BM, Rana NA, Moss H, Leonardi J, Jafar-Nejad H, Haltiwanger RS. J Biol Chem 291 16348-16360 (2016)
  10. Inhibition of Delta-induced Notch signaling using fucose analogs. Schneider M, Kumar V, Nordstrøm LU, Feng L, Takeuchi H, Hao H, Luca VC, Garcia KC, Stanley P, Wu P, Haltiwanger RS. Nat Chem Biol 14 65-71 (2018)
  11. Lunatic, Manic, and Radical Fringe Each Promote T and B Cell Development. Song Y, Kumar V, Wei HX, Qiu J, Stanley P. J Immunol 196 232-243 (2016)
  12. Structure of human POFUT1, its requirement in ligand-independent oncogenic Notch signaling, and functional effects of Dowling-Degos mutations. McMillan BJ, Zimmerman B, Egan ED, Lofgren M, Xu X, Hesser A, Blacklow SC. Glycobiology 27 777-786 (2017)
  13. Structural and functional dissection of the interplay between lipid and Notch binding by human Notch ligands. Suckling RJ, Korona B, Whiteman P, Chillakuri C, Holt L, Handford PA, Lea SM. EMBO J 36 2204-2215 (2017)
  14. Lunatic fringe-mediated Notch signaling regulates adult hippocampal neural stem cell maintenance. Semerci F, Choi WT, Bajic A, Thakkar A, Encinas JM, Depreux F, Segil N, Groves AK, Maletic-Savatic M. Elife 6 e24660 (2017)
  15. Impaired O-linked N-acetylglucosaminylation in the endoplasmic reticulum by mutated epidermal growth factor (EGF) domain-specific O-linked N-acetylglucosamine transferase found in Adams-Oliver syndrome. Ogawa M, Sawaguchi S, Kawai T, Nadano D, Matsuda T, Yagi H, Kato K, Furukawa K, Okajima T. J Biol Chem 290 2137-2149 (2015)
  16. Radical and lunatic fringes modulate notch ligands to support mammalian intestinal homeostasis. Kadur Lakshminarasimha Murthy P, Srinivasan T, Bochter MS, Xi R, Varanko AK, Tung KL, Semerci F, Xu K, Maletic-Savatic M, Cole SE, Shen X. Elife 7 e35710 (2018)
  17. Canonical Notch ligands and Fringes have distinct effects on NOTCH1 and NOTCH2. Kakuda S, LoPilato RK, Ito A, Haltiwanger RS. J Biol Chem 295 14710-14722 (2020)
  18. Notch ligand delta-like1: X-ray crystal structure and binding affinity. Kershaw NJ, Church NL, Griffin MD, Luo CS, Adams TE, Burgess AW. Biochem J 468 159-166 (2015)
  19. Variant in human POFUT1 reduces enzymatic activity and likely causes a recessive microcephaly, global developmental delay with cardiac and vascular features. Takeuchi H, Wong D, Schneider M, Freeze HH, Takeuchi M, Berardinelli SJ, Ito A, Lee H, Nelson SF, Haltiwanger RS. Glycobiology 28 276-283 (2018)
  20. Glycosylation of Specific Notch EGF Repeats by O-Fut1 and Fringe Regulates Notch Signaling in Drosophila. Pandey A, Harvey BM, Lopez MF, Ito A, Haltiwanger RS, Jafar-Nejad H. Cell Rep 29 2054-2066.e6 (2019)
  21. Notch Signaling-Induced Oscillatory Gene Expression May Drive Neurogenesis in the Developing Retina. Ivanov D. Front Mol Neurosci 12 226 (2019)
  22. Combining genetic and biophysical approaches to probe the structure and function relationships of the notch receptor. Baron M. Mol Membr Biol 34 33-49 (2017)
  23. 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 E1220 (2020)
  24. NOTCH activation promotes glycosyltransferase expression in human myeloid leukemia cells. Wang S, Itoh M, Shiratori E, Ohtaka M, Tohda S. Hematol Rep 10 7576 (2018)
  25. Protein O-Glucosyltransferase 1 Expression Influences Formation of Differentiated Myotubes in C2C12 Cell Line. Pélisse M, Der Vartanian A, Germot A, Maftah A. DNA Cell Biol 37 359-372 (2018)
  26. Congress The Notch meeting: an odyssey from structure to function. Chitnis A, Balle-Cuif L. Development 143 547-553 (2016)
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  29. Glycosylation of FGFR4 in cholangiocarcinoma regulates receptor processing and cancer signaling. Phillips AJ, Lobl MB, Hafeji YA, Safranek HR, Mohr AM, Mott JL. J Cell Biochem 123 568-580 (2022)
  30. (1)H, (13)C and (15)N assignments of EGF domains 4 to 7 of human Notch-1. Weisshuhn PC, Handford PA, Redfield C. Biomol NMR Assign 9 275-279 (2015)
  31. (1)H, (13)C and (15)N assignments of EGF domains 8-11 of human Notch-1. Weisshuhn PC, Handford PA, Redfield C. Biomol NMR Assign 9 375-379 (2015)
  32. CIGB-300-Regulated Proteome Reveals Common and Tailored Response Patterns of AML Cells to CK2 Inhibition. Rosales M, Rodríguez-Ulloa A, Pérez GV, Besada V, Soto T, Ramos Y, González LJ, Zettl K, Wiśniewski JR, Yang K, Perera Y, Perea SE. Front Mol Biosci 9 834814 (2022)
  33. Cleaved Delta like 1 intracellular domain regulates neural development via Notch signal-dependent and -independent pathways. Okubo Y, Ohtake F, Igarashi K, Yasuhiko Y, Hirabayashi Y, Saga Y, Kanno J. Development 148 dev193664 (2021)
  34. Protein O-Fucosyltransferase 1 Undergoes Interdomain Flexibility in Solution. Lira-Navarrete E, Pallarés MC, Castello F, Ruedas-Rama MJ, Orte A, Lostao A, Hurtado-Guerrero R. Molecules 26 2105 (2021)
  35. Mouse WIF1 Is Only Modified with O-Fucose in Its EGF-like Domain III Despite Two Evolutionarily Conserved Consensus Sites. Pennarubia F, Pinault E, Al Jaam B, Brun CE, Maftah A, Germot A, Legardinier S. Biomolecules 10 E1250 (2020)
  36. Other Types of Glycosylation. Tsukamoto Y, Takeuchi H. Adv Exp Med Biol 1325 117-135 (2021)
  37. Signal Transduction: Notch catches a Jagged edge. Blacklow SC. Nat Chem Biol 13 570-571 (2017)
  38. Twinkle twinkle brittle star: the draft genome of Ophioderma brevispinum (Echinodermata: Ophiuroidea) as a resource for regeneration research. Mashanov V, Machado DJ, Reid R, Brouwer C, Kofsky J, Janies DA. BMC Genomics 23 574 (2022)
  39. 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)
  40. Mutations observed in somatic evolution reveal underlying gene mechanisms. Hall MWJ, Shorthouse D, Alcraft R, Jones PH, Hall BA. Commun Biol 6 753 (2023)
  41. Notch1 and Notch4 core binding domain peptibodies exhibit distinct ligand-binding and anti-angiogenic properties. Sargis T, Youn SW, Thakkar K, Naiche LA, Paik NY, Pajcini KV, Kitajewski JK. Angiogenesis 26 249-263 (2023)
  42. O-Fucose and Fringe-modified NOTCH1 extracellular domain fragments as decoys to release niche-lodged hematopoietic progenitor cells. Yu S, Wang W, Albakri M, Yu X, Majihail G, Lim S, Lopilato RK, Ito A, Letterio J, Haltiwanger RS, Zhou L. Glycobiology 31 582-592 (2021)
  43. Single-cell fucosylation breakdown: Switching fucose to europium. Liu Z, Liang Y, Zhou Y, Ge F, Yan X, Yang L, Wang Q. iScience 24 102397 (2021)
  44. Two NOTCH1 O-fucose sites have opposing functions in mouse retinal angiogenesis. LoPilato RK, Kroeger H, Mohan SK, Lauderdale JD, Grimsey N, Haltiwanger RS. Glycobiology 33 661-672 (2023)


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