Regulation of signal transduction pathways in development by glycosylation

Current Opinion in Structural Biology

Volumn 12, Issue 5, 2002, Pages 593-598

  Haltiwanger, Robert S ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 1,3 N ACETYLGLUCOSAMINYLTRANSFERASE; ENZYME; EPIDERMAL GROWTH FACTOR; FUCOSE; N ACETYLGLUCOSAMINYLTRANSFERASE; NOTCH RECEPTOR; UNCLASSIFIED DRUG;

CARBOHYDRATE ANALYSIS; CELL SURFACE; HUMAN; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION;

EID: 0036816590     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-440X(02)00371-8     Document Type: Review

References (55)

1. Roseman S. Reflections on glycobiology. J Biol Chem. 276:2001;41527-41542.
2. Marth J.D. Glycosylation changes in ontogeny and cell activation. Varki A., Cummings R., Esko J., Freeze H., Hart G., Marth J. Essentials of Glycobiology. 1999;515-536 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
3. Marth J.D. Determining glycan function using genetically modified mice. Varki A., Cummings R., Esko J., Freeze H., Hart G., Marth J. Essentials of Glycobiology. 1999;499-514 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
4. Perrimon N., Berfield M. Specificities of heparan sulphate proteoglycans in developmental processes. Nature. 404:2000;725-728.
5. Bernfield M., Gotte M., Park P.W., Reizes O., Fitzgerald M.L., Lincecum J., Zako M. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 68:1999;729-777.
6. Selleck S.B. Proteoglycans and pattern formation: sugar biochemistry meets developmental genetics. Trends Genet. 16:2000;206-212.
7. Hallgren P., Lundblad A., Svensson S. A new type of carbohydrate-protein linkage in a glycopeptide from normal human urine. J Biol Chem. 250:1975;5312-5314.
8. Kentzer E.J., Buko A.M., Menon G., Sarin V.K. Carbohydrate composition and presence of a fucose-protein linkage in recombinant human pro-urokinase. Biochem Biophys Res Commun. 171:1990;401-406.
9. Harris R.J., Spellman M.W. O-linked fucose and other post-translational modifications unique to EGF modules. Glycobiology. 3:1993;219-224.
10. Campbell I.D., Bork P. Epidermal growth factor-like modules. Curr Opin Struct Biol. 3:1993;385-392.
11. Moloney D.J., Shair L., Lu F.M., Xia J., Locke R., Matta K.L., Haltiwanger R.S. Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J Biol Chem. 275:2000;9604-9611. The original report of O-fucose modifications of Notch.
12. Schiffer S.G., Foley S., Kaffashan A., Hronowski X., Zichittella A., Yeo C.Y., Miatkowski K., Adkins H.B., Damon B., Whitman M., et al. Fucosylation of Cripto is required for its ability to facilitate Nodal signaling. J Biol Chem. 276:2001;37769-37778. The initial report describing O-fucose modification of human Cripto and its essential role in Nodal signaling.
13. Yan Y.T., Liu J.J., Luo Y.E.C., Haltiwanger R.S., Abate-shen C., Shen M.M. Bi-functional activity of Cripto as a ligand and co-receptor in the Nodal signaling pathway. Mol Cell Biol. 22:2002;4439-4449. A recent report describing O-fucose on mouse Cripto and the importance of the O-fucose for Cripto-Nodal interactions.
14. 3.
15. Wang Y., Spellman M.W. Purification and characterization of a GDP-fucose: polypeptide fucosyltransferase from Chinese hamster ovary cells. J Biol Chem. 273:1998;8112-8118.
16. Wang Y., Shao L., Shi S., Harris R.J., Spellman M.W., Stanley P., Haltiwanger R.S. Modification of epidermal growth factor-like repeats with O-fucose: molecular cloning of a novel GDP-fucose: protein O-fucosyltransferase. J Biol Chem. 276:2001;40338-40345.
17. Wang Y., Lee G.F., Kelley R.F., Spellman M.W. Identification of a GDP-L-fucose: polypeptide fucosyltransferase and enzymatic addition of O-linked fucose to EGF domains. Glycobiology. 6:1996;837-842.
18. Kao Y.-H., Lee G.F., Wang Y., Starovasnik M.A., Kelley R.F., Spellman M.W., Lerner L. The effect of O-fucosylation on the first EGF-like domain from human blood coagulation factor VII. Biochemistry. 38:1999;7097-7110.
19. Dear A., Medcalf R.L.: The urokinase-type-plasminogen-activator receptor (CD87) is a pleiotropic molecule. Eur J Biochem. 252:1998;185-193.
20. Rabbani S.A., Mazar A.P., Bernier S.M., Haq M., Bolivar I., Henkin J., Goltzman D. Structural requirements for the growth factor activity of the amino-terminal domain of urokinase. J Biol Chem. 267:1992;14151-14156.
21. Artavanis-Tsakonas S., Rand M.D., Lake R.J.: Notch signaling: cell fate control and signal integration in development. Science. 284:1999;770-776.
22. Mumm J.S., Kopan R. Notch signaling: from the outside in. Dev Biol. 228:2000;151-165.
23. Joutel A., Tournier-Lasserve E. Notch signalling pathway and human diseases. Semin Cell Dev Biol. 9:1998;619-625.
24. Krantz I.D., Smith R., Colliton R.P., Tinkel H., Zackai E.H., Piccoli D.A., Goldmuntz E., Spinner N.B. Jagged1 mutations in patients ascertained with isolated congenital heart defects. Am J Med Genet. 84:1999;56-60.
25. Bulman M.P., Kusumi K., Frayling T.M., McKeown C., Garrett C., Lander E.S., Krumlauf R., Hattersley A.T., Ellard S., Turnpenny P.D. Mutations in the human delta homologue, DLL3, cause axial skeletal defects in spondylocostal dysostosis. Nat Genet. 24:2000;438-441.
26. Irvine K.D. Fringe, Notch, and making developmental boundaries. Curr Opin Genet Dev. 9:1999;434-441.
27. Irvine K.D., Rauskolb C. Boundaries in development: formation and function. Annu Rev Cell Dev Biol. 17:2001;189-214.
28. Cohen B., Bashirullah A., Dagnino L., Campbell C., Fisher W.W., Leow C.C., Whiting E., Ryan D., Zinyk D., Boulianne G., et al. Fringe boundaries coincide with Notch-dependent patterning centres in mammals and alter Notch-dependent development in Drosophila. Nat Genet. 16:1997;283-288.
29. Johnston S.H., Rauskolb C., Wilson R., Prabhakaran B., Irvine K.D., Vogt T.F. A family of mammalian Fringe genes implicated in boundary determination and the Notch pathway. Development. 124:1997;2245-2254.
30. Moloney D.J., Panin V.M., Johnston S.H., Chen J., Shao L., Wilson R., Wang Y., Stanley P., Irvine K.D., Haltiwanger R.S., et al. Fringe is a glycosyltransferase that modifies notch. Nature. 406:2000;369-375. This paper, together with [37••,38••], demonstrates that Fringe is a glycosyltransferase that modifies O-fucose residues on Notch and that the glycosyltransferase activity is essential for Fringe to be able to modulate Notch function.
31. Shimizu K., Chiba S., Saito T., Kumano K., Takahashi T., Hirai H. Manic fringe and lunatic fringe modify different sites of the notch2 extracellular region, resulting in different signaling modulation. J Biol Chem. 276:2001;25753-25758. The authors show that Manic and Lunatic fringe can modulate Notch2-ligand binding and signaling to Notch2 in cell-based assays.
32. Hicks C., Johnston S.H., DiSibio G., Collazo A., Vogt T.F., Weinmaster G. Jagged1 and Delta1 mediated Notch signaling is differentially regulated by lunatic fringe. Nat Cell Biol. 2:2000;515-520. The initial demonstration that Notch regulation by Fringe can be mimicked in a cell-based assay.
33. Evrard Y.A., Lun Y., Aulehla A., Gan L., Johnson R.L. Lunatic fringe is an essential mediator of somite segmentation and patterning. Nature. 394:1998;377-381.
34. Zhang N., Gridley T. Defects in somite formation in lunatic fringe-deficient mice. Nature. 394:1998;374-377.
35. Zhang N., Norton C.R., Gridley T. Segmentation defects of Notch pathway mutants and absence of a synergistic phenotype in lunatic fringe/radical fringe double mutant mice. Genesis. 33:2002;21-28.
36. Moran J.L., Levorse J.M., Vogt T.F. Limbs move beyond the radical fringe. Nature. 399:1999;742-743.
37. Bruckner K., Perez L., Clausen H., Cohen S. Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature. 406:2000;411-415. Together with [30••,38••], this paper demonstrates that Fringe is a glycosyltransferase. The authors provide data suggesting that Fringe alters Notch-Delta binding interactions.
38. Munro S., Freeman M. The notch signalling regulator fringe acts in the Golgi apparatus and requires the glycosyltransferase signature motif DXD. Curr Biol. 10:2000;813-820. Together with [30••,37••], this paper demonstrates that mutations in the putative DxD motif of Fringe prevent its ability to alter Notch signaling.
39. Chen J., Moloney D.J., Stanley P. Fringe modulation of Jagged1-induced Notch signaling requires the action of β4galactosyltransferase-1. Proc Natl Acad Sci USA. 98:2001;13716-13721. The addition of sialic acids is shown not to be essential for Fringe to inhibit Jagged1-induced Notch signaling. By contrast, the addition of β1,4-galactose is required for Fringe to mediate its effects.
40. Haltiwanger R.S., Stanley P. Modulation of receptor signaling by glycosylation: Fringe is an O-fucose-β1,3-N-acetylglucosaminyltransferase. Biochem Biophys Acta 2002, in press. A more detailed review on Fringe, including several potential mechanisms for how altered carbohydrate structures on Notch result in altered Notch activity.
41. Schier A.F., Shen M.M. Nodal signalling in vertebrate development. Nature. 403:2000;385-389.
42. Whitman M. Nodal signaling in early vertebrate embryos: themes and variations. Dev Cell. 1:2001;605-617.
43. Shen M.M., Schier A.F. The EGF-CFC gene family in vertebrate development. Trends Genet. 16:2000;303-309.
44. Hofsteenge J., Huwiler K.G., Macek B., Hess D., Lawler J., Mosher D.F., Peter-Katalinic J. C-mannosylation and O-fucosylation of the thrombospondin type 1 module. J Biol Chem. 276:2001;6485-6498.
45. Adams J.C., Tucker R.P. The thrombospondin type 1 repeat (TSR) superfamily: diverse proteins with related roles in neuronal development. Develop Dynamics. 218:2000;280-299.
46. De Celis J.F., Bray S.J. The Abruptex domain of Notch regulates negative interactions between Notch, its ligands and Fringe. Development. 127:2000;1291-1302.
47. Gohlke M., Baude G., Nuck R., Grunow D., Kannicht C., Bringmann P., Donner P., Reutter W. O-linked L-fucose is present in Desmodus rotundus salivary plasminogen activator. J Biol Chem. 271:1996;7381-7386.
48. Bjoern S., Foster D.C., Thim L., Wiberg F.C., Christensen M., Komiyama Y., Pedersen A.H., Kisiel W. Human plasma and recombinant factor VII: characterization of O-glycosylation at serine residues 52 and 60 and effects of site-directed mutagenesis of serine 52 to alanine. J Biol Chem. 266:1991;11051-11057.
49. Nishimura H., Takao T., Hase S., Shimonishi Y., Iwanaga S. Human factor IX has a tetrasaccharide O-glycosidically linked to serine 61 through the fucose residue. J Biol Chem. 267:1992;17520-17525.
50. Harris R.J., Ling V.T., Spellman M.W. O-linked fucose is present in the first epidermal growth factor domain of factor XII but protein C. J Biol Chem. 267:1992;5102-5107.
51. Krogh T.N., Bachmann E., Teisner B., Skjodt K., Hojrup P. Glycosylation analysis and protein structure determination of murine fetal antigen 1 (mFA1)-The circulating gene product of the delta-like protein (dlk), preadipocyte factor 1 (Pref-1) and stromal-cell-derived protein 1 (SCP-1) cDNAs. Eur J Biochem. 244:1997;334-342.
52. Moloney D.J., Haltiwanger R.S. The O-linked fucose glycosylation pathway: identification and characterization of a UDP-glucose: O-fucose β1,3-glucosyltransferase. Glycobiology. 9:1999;679-687.
53. Sakamoto K., Ohara O., Takagi M., Takeda S., Katsube K. Intracellular cell-autonomous association of Notch and its ligands: a novel mechanism of Notch signal modification. Dev Biol. 241:2002;313-326.
54. Harris R.J., Leonard C.K., Guzzetta A.W., Spellman M.W. Tissue plasminogen activator has an O-linked fucose attached to threonine-61 in the epidermal growth factor domain. Biochemistry. 30:1991;2311-2314.
55. Schwientek T, Keck B, Levery SB, Jensen MA, Pedersen JW, Wandall HH, Stroud M, Cohen SM, Amado M, Clausen H: The Drosophila gene Brainiac encodes a glycosyltransferase putatively involved in glycosphingolipid synthesis. J Biol Chem 2002, in press.