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

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 20, 2014, Pages 7290-7295

  Taylor, Paul ^a   Takeuchi, Hideyuki ^b   Sheppard, Devon ^c   Chillakuri, Chandramouli ^a   Lea, Susan M ^c   Haltiwanger, Robert S ^b   Handford, Penny A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b STONY BROOK UNIVERSITY   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE 1 LIGAND; DISACCHARIDE; ENZYME; FRINGE ENZYME; FUCOSE; GLUCOSE; JAGGED1; LIGAND; MONOSACCHARIDE; N ACETYLGLUCOSAMINE; NOTCH1 RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; CHO CELL LINE; CONTROLLED STUDY; CRYSTAL STRUCTURE; EGF12 DOMAIN; ENZYME MODIFICATION; FLOW CYTOMETRY; HUMAN; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SURFACE PLASMON RESONANCE; X RAY CRYSTALLOGRAPHY;

GLYCOSYLATION; MASS SPECTROMETRY; X-RAY;

ANIMALS; BINDING SITES; CALCIUM-BINDING PROTEINS; CATALYSIS; EPIDERMAL GROWTH FACTOR; FUCOSE; GLYCOSYLATION; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIGANDS; MEMBRANE PROTEINS; MICE; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION;

EID: 84901045153     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1319683111     Document Type: Article

References (49)

1. Artavanis-Tsakonas S, Rand MD, Lake RJ (1999) Notch signaling: Cell fate control and signal integration in development. Science 284(5415):770-776.
2. Blaumueller CM, Qi H, Zagouras P, Artavanis-Tsakonas S (1997) Intracellular cleavage of Notch leads to a heterodimeric receptor on the plasma membrane. Cell 90(2): 281-291.
3. Sanchez-Irizarry C, et al. (2004) Notch subunit heterodimerization and prevention of ligand-independent proteolytic activation depend, respectively, on a novel domain and the LNR repeats. Mol Cell Biol 24(21):9265-9273.
4. Fehon RG, et al. (1990) Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell 61(3):523-534.
5. Rebay I, et al. (1991) Specific EGF repeats of Notch mediate interactions with Delta and Serrate: Implications for Notch as a multifunctional receptor. Cell 67(4):687-699.
6. Shimizu K, et al. (1999) Mouse jagged1 physically interacts with notch2 and other notch receptors. Assessment by quantitative methods. J Biol Chem 274(46):32961-32969.
7. Fleming RJ (1998) Structural conservation of Notch receptors and ligands. Semin Cell Dev Biol 9(6):599-607.
8. Kopan R, Ilagan MX (2009) The canonical Notch signaling pathway: Unfolding the activation mechanism. Cell 137(2):216-233.
9. Brou C, et al. (2000) A novel proteolytic cleavage involved in Notch signaling: The role of the disintegrin-metalloprotease TACE. Mol Cell 5(2):207-216.
10. De Strooper B, et al. (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398(6727):518-522.
11. Mumm JS, et al. (2000) A ligand-induced extracellular cleavage regulates gammasecretase- like proteolytic activation of Notch1. Mol Cell 5(2):197-206.
12. Schroeter EH, Kisslinger JA, Kopan R (1998) Notch-1 signaling requires ligand-induced proteolytic release of intracellular domain. Nature 393(6683):382-386.
13. Jarriault S, et al. (1995) Signaling downstream of activated mammalian Notch. Nature 377(6547):355-358.
14. Moloney DJ, et al. (2000) Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J Biol Chem 275(13):9604-9611.
15. Rana NA, Haltiwanger RS (2011) Fringe benefits: Functional and structural impacts of O-glycosylation on the extracellular domain of Notch receptors. Curr Opin Struct Biol 21(5):583-589.
16. Rana NA, et al. (2011) O-glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J Biol Chem 286(36):31623-31637.
17. Shao L, Moloney DJ, Haltiwanger R (2003) Fringe modifies O-fucose on mouse Notch1 at epidermal growth factor-like repeats within the ligand-binding site and the Abruptex region. J Biol Chem 278(10):7775-7782.
18. Okajima T, Irvine KD (2002) Regulation of notch signaling by o-linked fucose. Cell 111(6):893-904.
19. Shi S, Stanley P (2003) Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci USA 100(9):5234-5239.
20. Acar M, et al. (2008) Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132(2):247-258.
21. Fernandez-Valdivia R, et al. (2011) Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development 138(10):1925-1934.
22. Stahl M, et al. (2008) Roles of Pofut1 and O-fucose in mammalian Notch signaling. J Biol Chem 283(20):13638-13651.
23. Yao D, et al. (2011) Protein O-fucosyltransferase 1 (Pofut1) regulates lymphoid and myeloid homeostasis through modulation of Notch receptor ligand interactions. Blood 117(21):5652-5662.
24. Johnston SH, et al. (1997) A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development 124(11):2245-2254.
25. Rampal R, et al. (2005) Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J Biol Chem 280(51):42454-42463.
26. Shimizu K, et al. (2001) Manic fringe and lunatic fringe modify different sites of the Notch2 extracellular region, resulting in different signaling modulation. J Biol Chem 276(28):25753-25758.
27. Yang LT, et al. (2005) Fringe glycosyltransferases differentially modulate Notch1 proteolysis induced by Delta1 and Jagged1. Mol Biol Cell 16(2):927-942.
28. Moloney DJ, et al. (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406(6794):369-375.
29. Hicks C, et al. (2000) Fringe differentially modulates Jagged1 and Delta1 signaling through Notch1 and Notch2. Nat Cell Biol 2(8):515-520.
30. Chen J, Moloney DJ, Stanley P (2001) Fringe modulation of Jagged1-induced Notch signaling requires the action of beta 4galactosyltransferase-1. Proc Natl Acad Sci USA 98(24):13716-13721.
31. Hou X, Tashima Y, Stanley P (2012) Galactose differentially modulates lunatic and manic fringe effects on Delta1-induced NOTCH signaling. J Biol Chem 287(1):474-483.
32. Whiteman P, et al. (2013) Molecular basis for Jagged-1/Serrate ligand recognition by the Notch receptor. J Biol Chem 288(10):7305-7312.
33. Takeuchi H, et al. (2012) Site-specific O-glucosylation of the epidermal growth factorlike (EGF) repeats of notch: Efficiency of glycosylation is affected by proper folding and amino acid sequence of individual EGF repeats. J Biol Chem 287(41):33934-33944.
34. Yamamoto S, et al. (2012) A mutation in EGF repeat-8 of Notch discriminates between Serrate/Jagged and Delta family ligands. Science 338(6111):1229-1232.
35. Cordle J, et al. (2008) A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-Activation and cis-inhibition. Nat Struct Mol Biol 15(8):849-857.
36. Lei L, Xu A, Panin VM, Irvine KD (2003) An O-fucose site in the ligand binding domain inhibits Notch activation. Development 130(26):6411-6421.
37. Ge C, Stanley P (2008) The O-fucose glycan in the ligand-binding domain of Notch1 regulates embryogenesis and T cell development. Proc Natl Acad Sci USA 105(5): 1539-1544.
38. Rampal R, Arboleda-Velasquez JF, Nita-Lazar A, Kosik KS, Haltiwanger RS (2005) Highly conserved O-fucose sites have distinct effects on Notch1 function. J Biol Chem 280(37):32133-32140.
39. Andrawes MB, et al. (2013) Intrinsic selectivity of Notch 1 for Delta-like 4 over Deltalike 1. J Biol Chem 288(35):25477-25489.
40. Hiruma-Shimizu K, et al. (2010) Chemical synthesis, folding, and structural insights into O-fucosylated epidermal growth factor-like repeat 12 of mouse Notch-1 receptor. J Am Chem Soc 132(42):14857-14865.
41. Hambleton S, et al. (2004) Structural and functional properties of the human notch-1 ligand binding region. Structure 12(12):2173-2183.
42. Yang D, Kay LE (1996) Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: Application to protein folding. J Mol Biol 263(2):369-382.
43. Akke M, Skelton NJ, Kördel J, Palmer AG, 3rd, Chazin WJ (1993) Effects of ion binding on the backbone dynamics of calbindin D9k determined by 15N NMR relaxation. Biochemistry 32(37):9832-9844.
44. Shi S, et al. (2007) The threonine that carries fucose, but not fucose, is required for Cripto to facilitate Nodal signaling. J Biol Chem 282(28):20133-20141.
45. Aricescu AR, Lu W, Jones EY (2006) A time- and cost-efficient system for high-level protein production in mammalian cells. Acta Crystallogr D Biol Crystallogr 62(Pt 10):1243-1250.
46. Leonhard-Melief C, Haltiwanger RS (2010) O-fucosylation of thrombospondin type 1 repeats. Methods Enzymol 480:401-416.
47. Winter G (2010) xia2: An expert system for macromolecular crystallography data reduction. J Appl Cryst 43:186-190.
48. Bricogne G, et al. (2011) BUSTER (Global Phasing Ltd. Cambridge, U.K).
49. Chen VB, et al. (2010) MolProbity: All-Atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66(Pt 1):12-21.