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

Nature Communications

Volumn 8, Issue 1, 2017, Pages

  Li, Zhijie ^a   Fischer, Michael ^b   Satkunarajah, Malathy ^a   Zhou, Dongxia ^a   Withers, Stephen G ^b   Rini, James M ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; GLUCOSE; GLUCOSYLTRANSFERASE; NOTCH RECEPTOR; NOTCH1 RECEPTOR; URIDINE DIPHOSPHATE GLUCOSE; URIDINE DIPHOSPHATE XYLOSE; XYLOSE; POGLUT1 PROTEIN, HUMAN;

ENZYME; ENZYME ACTIVITY; GLUCOSE; GROWTH; PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CATALYSIS; COMPLEX FORMATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; FUCOSYLATION; HEK293 CELL LINE; HYDROGEN BOND; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; SIGNAL TRANSDUCTION; SURFACE AREA; THERMOSTABILITY; ENZYME ACTIVE SITE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; PHYSIOLOGY;

MAMMALIA;

CATALYTIC DOMAIN; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSYLTRANSFERASES; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; PROTEIN CONFORMATION; RECEPTORS, NOTCH;

EID: 85026726254     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/s41467-017-00255-7     Document Type: Article

References (51)

1. Teng, Y. et al. Cloning, expression and characterization of a novel human CAP10-like gene hCLP46 from CD34(+) stem/progenitor cells. Gene 371, 7-15 (2006).
2. Acar, M. et al. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132, 247-258 (2008).
3. Moloney, D. J. et al. Mammalian Notch1 is modified with two unusual forms of O-linked glycosylation found on epidermal growth factor-like modules. J. Biol. Chem. 275, 9604-9611 (2000).
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. Haltom, A. R. et al. The protein O-glucosyltransferase Rumi modifies eyes shut to promote rhabdomere separation in Drosophila. PLoS Genet. 10, e1004795 (2014).
6. 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).
7. 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).
8. Servian-Morilla, E. et al. A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol. Med. 8, 1289-1309 (2016).
9. Wang, Y. & Spellman, M. W. Purification and characterization of a GDPfucose: polypeptide fucosyltransferase from Chinese hamster ovary cells. J. Biol. Chem. 273, 8112-8118 (1998).
10. Takeuchi, H., Kantharia, J., Sethi, M. K., Bakker, H. & Haltiwanger, R. S. Sitespecific 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).
11. Vasudevan, D. & Haltiwanger, R. S. Novel roles for O-linked glycans in protein folding. Glycoconj. J. 31, 417-426 (2014).
12. Haltom, A. R. & Jafar-Nejad, H. The multiple roles of epidermal growth factor repeat O-glycans in animal development. Glycobiology 25, 1027-1042 (2015).
13. 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).
14. 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).
15. Shao, L., Luo, Y., Moloney, D. J. & Haltiwanger, R. O-glycosylation of EGF repeats: identification and initial characterization of a UDP-glucose: protein O-glucosyltransferase. Glycobiology 12, 763-770 (2002).
16. Yu, H. et al. Structural analysis of Notch-regulating Rumi reveals basis for pathogenic mutations. Nat. Chem. Biol. 12, 735-740 (2016).
17. Li, Z. et al. Recognition of EGF-like domains by the Notch-modifying O-fucosyltransferase POFUT1. Nat. Chem. Biol. 13, 757-763 (2017).
18. Coutinho, P. M., Deleury, E., Davies, G. J. & Henrissat, B. An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307-317 (2003).
19. Lawrence, M. C. & Colman, P. M. Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234, 946-950 (1993).
20. Wouters, M. A. et al. Evolution of distinct EGF domains with specific functions. Protein Sci. 14, 1091-1103 (2005).
21. Morgan, J. L. et al. Observing cellulose biosynthesis and membrane translocation in crystallo. Nature 531, 329-334 (2016).
22. Gibson, R. P., Tarling, C. A., Roberts, S., Withers, S. G. & Davies, G. J. The donor subsite of trehalose-6-phosphate synthase: binary complexes with UDPglucose and UDP-2-deoxy-2-fluoro-glucose at 2 A resolution. J. Biol. Chem. 279, 1950-1955 (2004).
23. Grosdidier, A., Zoete, V. & Michielin, O. SwissDock, a protein-small molecule docking web service based on EADock DSS. Nucleic Acids Res. 39, W270-W277 (2011).
24. Morris, G. M. et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785-2791 (2009).
25. Trott, O. & Olson, A. J. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 31, 455-461 (2010).
26. Lemmon, G. & Meiler, J. Rosetta ligand docking with flexible XML protocols. Methods Mol. Biol. 819, 143-155 (2012).
27. 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).
28. Lairson, L. L., Henrissat, B., Davies, G. J. & Withers, S. G. Glycosyltransferases: structures, functions, and mechanisms. Annu. Rev. Biochem. 77, 521-555 (2008).
29. Dunbrack, R. L. Jr. & Karplus, M. Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J. Mol. Biol. 230, 543-574 (1993).
30. Shapovalov, M. V. & Dunbrack, R. L. Jr. A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions. Structure 19, 844-858 (2011).
31. Bennett, E. P. et al. Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22, 736-756 (2012).
32. Qasba, P. K., Ramakrishnan, B. & Boeggeman, E. Substrate-induced conformational changes in glycosyltransferases. Trends Biochem. Sci. 30, 53-62 (2005).
33. Breton, C., Snajdrova, L., Jeanneau, C., Koca, J. & Imberty, A. Structures and mechanisms of glycosyltransferases. Glycobiology 16, 29R-37R (2006).
34. Lee, T. V. et al. Negative regulation of notch signaling by xylose. PLoS Genet. 9, e1003547 (2013).
35. Matsumoto, K. et al. Dual roles of O-glucose glycans redundant with Monosaccharide O-fucose on Notch in Notch trafficking. J. Biol. Chem. 291, 13743-13752 (2016).
36. Bakker, H. et al. Functional UDP-xylose transport across the endoplasmic reticulum/Golgi membrane in a Chinese hamster ovary cell mutant defective in UDP-xylose Synthase. J. Biol. Chem. 284, 2576-2583 (2009).
37. Nakajima, K. et al. Simultaneous determination of nucleotide sugars with ionpair reversed-phase HPLC. Glycobiology 20, 865-871 (2010).
38. Li, Z., Michael, I. P., Zhou, D., Nagy, A. & Rini, J. M. Simple piggyBac transposon-based mammalian cell expression system for inducible protein production. Proc. Natl Acad. Sci. USA 110, 5004-5009 (2013).
39. Barash, S., Wang, W. & Shi, Y. Human secretory signal peptide description by hidden Markov model and generation of a strong artificial signal peptide for secreted protein expression. Biochem. Biophys. Res. Commun. 294, 835-842 (2002).
40. Reeves, P. J., Callewaert, N., Contreras, R. & Khorana, H. G. Structure and function in rhodopsin: high-level expression of rhodopsin with restricted and homogeneous N-glycosylation by a tetracycline-inducible Nacetylglucosaminyltransferase I-negative HEK293S stable mammalian cell line. Proc. Natl Acad. Sci. USA 99, 13419-13424 (2002).
41. Robbins, P. W. et al. Primary structure of the Streptomyces enzyme endo-beta-N-acetylglucosaminidase H. J. Biol. Chem. 259, 7577-7583 (1984).
42. Sheldrick, G. M. A short history of SHELX. Acta Crystallogr. A 64, 112-122 (2008).
43. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
44. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997).
45. Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
46. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010).
47. Grosdidier, A., Zoete, V. & Michielin, O. Fast docking using the CHARMM force field with EADock DSS. J. Comput. Chem. 32, 2149-2159 (2011).
48. Gosselin, S., Alhussaini, M., Streiff, M. B., Takabayashi, K. & Palcic, M. M. A continuous spectrophotometric assay for glycosyltransferases. Anal. Biochem. 220, 92-97 (1994).
49. Duggleby, R. G. Analysis of enzyme progress curves by nonlinear regression. Methods Enzymol. 249, 61-90 (1995).
50. Kuzmic, P. Program DYNAFIT for the analysis of enzyme kinetic data: application to HIV proteinase. Anal. Biochem. 237, 260-273 (1996).
51. Strohalm, M., Kavan, D., Novak, P., Volny, M. & Havlicek, V. mMass 3: a cross-platform software environment for precise analysis of mass spectrometric data. Anal. Chem. 82, 4648-4651 (2010).