Structural analysis of Notch-regulating Rumi reveals basis for pathogenic mutations

Nature Chemical Biology

Volumn 12, Issue 9, 2016, Pages 735-740

  Yu, Hongjun ^a   Takeuchi, Hideyuki ^b   Takeuchi, Megumi ^b   Liu, Qun ^a   Kantharia, Joshua ^c   Haltiwanger, Robert S ^b   Li, Huilin ^a,c  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD CLOTTING FACTOR 9; JAGGED1; NECDIN; NOTCH RECEPTOR; REGULATOR PROTEIN; RUMI PROTEIN; SERINE; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; GLUCOSYLTRANSFERASE; RUMI PROTEIN, DROSOPHILA;

ARTICLE; CATALYSIS; DISULFIDE BOND; DROSOPHILA; ENZYME ACTIVE SITE; ENZYME ACTIVITY; GLYCOSYLATION; HYDROPHOBICITY; MALIGNANT ATROPHIC PAPULOSIS; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STRUCTURE; ANIMAL; BIOCATALYSIS; CHEMISTRY; DROSOPHILA MELANOGASTER; GENETICS; HUMAN; METABOLISM; MOUSE; MUTATION; PROTEIN CONFORMATION;

ANIMALS; BIOCATALYSIS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GLUCOSYLTRANSFERASES; HUMANS; MICE; MUTATION; PROTEIN CONFORMATION;

EID: 84978760284     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.2135     Document Type: Article

References (52)

1. Rana, N.A. & Haltiwanger, R.S. Fringe benefits: functional and structural impacts of O-glycosylation on the extracellular domain of Notch receptors. Curr. Opin. Struct. Biol. 21, 583-589 (2011).
2. Kopan, R. & Ilagan, M.X. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233 (2009).
3. Acar, M. et al. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132, 247-258 (2008).
4. Fernandez-Valdivia, R. et al. Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development 138, 1925-1934 (2011).
5. Leonardi, J., Fernandez-Valdivia, R., Li, Y.D., Simcox, A.A. & Jafar-Nejad, H. Multiple O-glucosylation sites on Notch function as a buffer against temperature-dependent loss of signaling. Development 138, 3569-3578 (2011).
6. Lee, T.V. et al. Negative regulation of notch signaling by xylose. PLoS Genet. 9, e1003547 (2013).
7. Haltom, A.R. et al. The protein O-glucosyltransferase Rumi modifies eyes shut to promote rhabdomere separation in Drosophila. PLoS Genet. 10, e1004795 (2014).
8. Ramkumar, N. et al. Protein O-glucosyltransferase 1 (POGLUT1) promotes mouse gastrulation through modification of the apical polarity protein CRUMBS2. PLoS Genet. 11, e1005551 (2015).
9. Thakurdas, S.M. et al. Jagged1 heterozygosity in mice results in a congenital cholangiopathy which is reversed by concomitant deletion of one copy of Poglut1 (Rumi). Hepatology 63, 550-565 (2016).
10. Basmanav, F.B. et al. Mutations in POGLUT1, encoding protein O-glucosyltransferase 1, cause autosomal-dominant Dowling-Degos disease. Am. J. Hum. Genet. 94, 135-143 (2014).
11. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P.M. & Henrissat, B. The carbohydrate-Active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490-D495 (2014).
12. Lazarus, M.B. et al. Structural snapshots of the reaction coordinate for O-GlcNAc transferase. Nat. Chem. Biol. 8, 966-968 (2012).
13. Lazarus, M.B., Nam, Y., Jiang, J., Sliz, P. & Walker, S. Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469, 564-567 (2011).
14. Lizak, C., Gerber, S., Numao, S., Aebi, M. & Locher, K.P. X-ray structure of a bacterial oligosaccharyltransferase. Nature 474, 350-355 (2011).
15. Lazarus, M.B. et al. HCF-1 is cleaved in the active site of O-GlcNAc transferase. Science 342, 1235-1239 (2013).
16. Schimpl, M. et al. O-GlcNAc transferase invokes nucleotide sugar pyrophosphate participation in catalysis. Nat. Chem. Biol. 8, 969-974 (2012).
17. Vasudevan, D. & Haltiwanger, R.S. Novel roles for O-linked glycans in protein folding. Glycoconj. J. 31, 417-426 (2014).
18. Chen, C.I. et al. Structure of human POFUT2: insights into thrombospondin type 1 repeat fold and O-fucosylation. EMBO J. 31, 3183-3197 (2012).
19. Lira-Navarrete, E. et al. Structural insights into the mechanism of protein O-fucosylation. PLoS One 6, e25365 (2011).
20. Valero-González, J. et al. A proactive role of water molecules in acceptor recognition by protein O-fucosyltransferase 2. Nat. Chem. Biol. 12, 240-246 (2016).
21. Yu, H. et al. Notch-modifying xylosyltransferase structures support an SNi-like retaining mechanism. Nat. Chem. Biol. 11, 847-854 (2015).
22. Wouters, M.A. et al. Evolution of distinct EGF domains with specific functions. Protein Sci. 14, 1091-1103 (2005).
23. Takeuchi, H., Kantharia, J., Sethi, M.K., Bakker, H. & Haltiwanger, R.S. Site-specific O-glucosylation of the epidermal growth factor-like (EGF) repeats of notch: efficiency of glycosylation is affected by proper folding and amino acid sequence of individual EGF repeats. J. Biol. Chem. 287, 33934-33944 (2012).
24. Liu, Q. et al. Structures from anomalous diffraction of native biological macromolecules. Science 336, 1033-1037 (2012).
25. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
26. Larivière, L., Sommer, N. & Morera, S. Structural evidence of a passive base-flipping mechanism for AGT, an unusual GT-B glycosyltransferase. J. Mol. Biol. 352, 139-150 (2005).
27. Takeuchi, H. et al. Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc. Natl. Acad. Sci. USA 108, 16600-16605 (2011).
28. Xu, A., Lei, L. & Irvine, K.D. Regions of Drosophila Notch that contribute to ligand binding and the modulatory influence of Fringe. J. Biol. Chem. 280, 30158-30165 (2005).
29. Rana, N.A. et al. O-glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J. Biol. Chem. 286, 31623-31637 (2011).
30. Lairson, L.L., Henrissat, B., Davies, G.J. & Withers, S.G. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555 (2008).
31. Breton, C., Fournel-Gigleux, S. & Palcic, M.M. Recent structures, evolution and mechanisms of glycosyltransferases. Curr. Opin. Struct. Biol. 22, 540-549 (2012).
32. Larivière, L., Gueguen-Chaignon, V. & Morera, S. Crystal structures of the T4 phage beta-glucosyltransferase and the D100A mutant in complex with UDP-glucose: glucose binding and identification of the catalytic base for a direct displacement mechanism. J. Mol. Biol. 330, 1077-1086 (2003).
33. Ntziachristos, P., Lim, J.S., Sage, J. & Aifantis, I. From fly wings to targeted cancer therapies: A centennial for Notch signaling. Cancer Cell 25, 318-334 (2014).
34. Rampias, T. et al. A new tumor suppressor role for the Notch pathway in bladder cancer. Nat. Med. 20, 1199-1205 (2014).
35. Klinakis, A. et al. A novel tumour-suppressor function for the Notch pathway in myeloid leukaemia. Nature 473, 230-233 (2011).
36. Cerami, E. et al. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401-404 (2012).
37. Wang, N.J. et al. Loss-of-function mutations in Notch receptors in cutaneous and lung squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 108, 17761-17766 (2011).
38. Agrawal, N. et al. Exome sequencing of head and neck squamous cell carcinoma reveals inactivating mutations in NOTCH1. Science 333, 1154-1157 (2011).
39. Jonusiene, V. et al. Down-regulated expression of Notch signaling molecules in human endometrial cancer. Med. Oncol. 30, 438 (2013).
40. Hanneken, S. et al. [Galli-Galli disease. Clinical and histopathological investigation using a case series of 18 patients]. Hautarzt. 62, 842-851 (2011).
41. Mauerer, A., Betz, R.C., Pasternack, S.M., Landthaler, M. & Hafner, C. Generalized solar lentigines in a patient with a history of radon exposure. Dermatology 221, 206-210 (2010).
42. Andersson, E.R. & Lendahl, U. Therapeutic modulation of Notch signalling-Are we there yet? Nat. Rev. Drug Discov. 13, 357-378 (2014).
43. Rizzo, P. et al. Rational targeting of Notch signaling in cancer. Oncogene 27, 5124-5131 (2008).
44. Kabsch, W. Xds. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132 (2010).
45. Battye, T.G., Kontogiannis, L., Johnson, O., Powell, H.R. & Leslie, A.G. iMOSFLM: A new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271-281 (2011).
46. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997).
47. Winn, M.D. et al. Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235-242 (2011).
48. Schneider, T.R. & Sheldrick, G.M. Substructure solution with SHELXD. Acta Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002).
49. Adams, P.D. et al. PHENIX: A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
50. Vagin, A. & Teplyakov, A. Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25 (2010).
51. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
52. Pannu, N.S., Murshudov, G.N., Dodson, E.J. & Read, R.J. Incorporation of prior phase information strengthens maximum-likelihood structure refinement. Acta Crystallogr. D Biol. Crystallogr. 54, 1285-1294 (1998).