O-Glycosylation modulates the stability of epidermal growth factor-like repeats and thereby regulates Notch trafficking

Journal of Biological Chemistry

Volumn 292, Issue 38, 2017, Pages 15964-15973

  Takeuchi, Hideyuki ^a,d   Yu, Hongjun ^b   Hao, Huilin ^a   Takeuchi, Megumi ^a   Ito, Atsuko ^a   Li, Huilin ^b   Haltiwanger, Robert S ^a,c  

^a UNIVERSITY OF GEORGIA   (United States)

^b VAN ANDEL RESEARCH INSTITUTE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d NAGOYA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADDITIVES; AMINO ACIDS; CELL MEMBRANES; CRYSTAL STRUCTURE; GLUCOSE; GLYCOSYLATION; POLYSACCHARIDES; PROTEINS; QUALITY ASSURANCE;

CELL SURFACE EXPRESSION; ENDOPLASMIC RETICULUM; EPIDERMAL GROWTH FACTOR-LIKE REPEAT; EPIDERMAL GROWTH FACTORS; FUCOSYLTRANSFERASES; GLUCOSYLTRANSFERASES; INTRAMOLECULAR INTERACTIONS; STABILIZING EFFECTS;

QUALITY CONTROL;

EPIDERMAL GROWTH FACTOR; FUCOSE; FUCOSYLTRANSFERASE; GLUCOSE; GLUCOSYLTRANSFERASE; NOTCH1 RECEPTOR; PROTEIN POFUT1; PROTEIN POGLUT1; UNCLASSIFIED DRUG; NOTCH RECEPTOR; OXYGEN; POGLUT1 PROTEIN, HUMAN; POLYPEPTIDE FUCOSYLTRANSFERASE;

ARTICLE; CONTROLLED STUDY; EPIDERMAL GROWTH FACTOR LIKE REPEAT; IN VITRO STUDY; MOLECULAR INTERACTION; MOUSE; NONHUMAN; NOTCH SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN MOTIF; PROTEIN STABILITY; PROTEIN UNFOLDING; AMINO ACID REPEAT; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; DEFICIENCY; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR MODEL; PROTEIN CONFORMATION; PROTEIN TRANSPORT;

AMINO ACID SEQUENCE; ANIMALS; EPIDERMAL GROWTH FACTOR; FUCOSYLTRANSFERASES; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; GLUCOSE; GLUCOSYLTRANSFERASES; GLYCOSYLATION; HEK293 CELLS; HUMANS; MICE; MODELS, MOLECULAR; OXYGEN; PROTEIN CONFORMATION; PROTEIN TRANSPORT; RECEPTOR, NOTCH1; RECEPTORS, NOTCH; REPETITIVE SEQUENCES, AMINO ACID;

EID: 85029741460     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M117.800102     Document Type: Article

References (51)

1. Braakman, I., and Hebert, D. N. (2013) Protein folding in the endoplasmic reticulum. Cold Spring Harb. Perspect. Biol. 5, a013201
2. Xu, C., and Ng, D. T. (2015) Glycosylation-directed quality control of protein folding. Nat. Rev. Mol. Cell Biol. 16, 742–752
3. Vasudevan, D., Takeuchi, H., Johar, S. S., Majerus, E., and Haltiwanger, R. S. (2015) Peters plus syndrome mutations disrupt a noncanonical ER quality-control mechanism. Curr. Biol. 25, 286 –295
4. Adams, J. C., and Tucker, R. P. (2000) The thrombospondin type 1 repeat (TSR) superfamily: diverse proteins with related roles in neuronal development. Dev. Dyn. 218, 280 –299
5. Luo, Y., Koles, K., Vorndam, W., Haltiwanger, R. S., and Panin, V. M. (2006) Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J. Biol. Chem. 281, 9393–9399
6. Luo, Y., Nita-Lazar, A., and Haltiwanger, R. S. (2006) Two distinct pathways for O-fucosylation of epidermal growth factor-like or thrombospondin type 1 repeats. J. Biol. Chem. 281, 9385–9392
7. Luo, Y., and Haltiwanger, R. S. (2005) O-Fucosylation of Notch occurs in the endoplasmic reticulum. J. Biol. Chem. 280, 11289 –11294
8. Acar, M., Jafar-Nejad, H., Takeuchi, H., Rajan, A., Ibrani, D., Rana, N. A., Pan, H., Haltiwanger, R. S., and Bellen, H. J. (2008) Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132, 247–258
9. Campbell, I. D., and Bork, P. (1993) Epidermal growth factor-like modules. Curr. Opin. Struct. Biol. 3, 385–392
10. Haltom, A. R., and Jafar-Nejad, H. (2015) The multiple roles of epidermal growth factor repeat O-glycans in animal development. Glycobiology 25, 1027–1042
11. Takeuchi, H., and Haltiwanger, R. S. (2014) Significance of glycosylation in Notch signaling. Biochem. Biophys. Res. Commun. 453, 235–242
12. Harvey, B. M., Rana, N. A., Moss, H., Leonardi, J., Jafar-Nejad, H., and Haltiwanger, R. S. (2016) Mapping sites of O-glycosylation and fringe elongation on Drosophila Notch. J. Biol. Chem. 291, 16348 –16360
13. Kakuda, S., and Haltiwanger, R. S. (2017) Deciphering the fringe-mediated Notch code: identification of activating and inhibiting sites allowing discrimination between ligands. Dev. Cell 40, 193–201
14. Rana, N. A., Nita-Lazar, A., Takeuchi, H., Kakuda, S., Luther, K. B., and Haltiwanger, R. S. (2011) O-Glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J. Biol. Chem. 286, 31623–31637
15. Shi, S., and Stanley, P. (2003) Protein O-fucosyltransferase I is an essential component of Notch signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 100, 5234 –5239
16. Fernandez-Valdivia, R., Takeuchi, H., Samarghandi, A., Lopez, M., Leonardi, J., Haltiwanger, R. S., and Jafar-Nejad, H. (2011) Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development 138, 1925–1934
17. Sawaguchi, S., Varshney, S., Ogawa, M., Sakaidani, Y., Yagi, H., Takeshita, K., Murohara, T., Kato, K., Sundaram, S., Stanley, P., and Okajima, T. (2017) O-GlcNAc on NOTCH1 EGF repeats regulates ligand-induced Notch signaling and vascular development in mammals. eLife 6, e24419
18. Li, M., Cheng, R., Liang, J., Yan, H., Zhang, H., Yang, L., Li, C., Jiao, Q., Lu, Z., He, J., Ji, J., Shen, Z., Li, C., Hao, F., Yu, H., and Yao, Z. (2013) Mutations in POFUT1, encoding protein O-fucosyltransferase 1, cause generalized Dowling-Degos disease. Am. J. Hum. Genet. 92, 895–903
19. Basmanav, F. B., Oprisoreanu, A. M., Pasternack, S. M., Thiele, H., Fritz, G., Wenzel, J., Grösser, L., Wehner, M., Wolf, S., Fagerberg, C., Bygum, A., Altmüller, J., Rütten, A., Parmentier, L., El Shabrawi-Caelen, L., et al. (2014) Mutations in POGLUT1, encoding protein O-glucosyltransferase 1, cause autosomal-dominant Dowling-Degos disease. Am. J. Hum. Genet. 94, 135–143
20. Servián-Morilla, E., Takeuchi, H., Lee, T. V., Clarimon, J., Mavillard, F., Area-Gómez, E., Rivas, E., Nieto-González, J. L., Rivero, M. C., Cabrera-Serrano, M., Gómez-Sánchez, L., Martínez-López, J. A., Estrada, B., Márquez, C., Morgado, Y., et al. (2016) A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol. Med. 8, 1289 –1309
21. Sethi, M. K., Buettner, F. F., Ashikov, A., Krylov, V. B., Takeuchi, H., Nifantiev, N. E., Haltiwanger, R. S., Gerardy-Schahn, R., and Bakker, H. (2012) Molecular cloning of a xylosyltransferase that transfers the second xylose to O-glucosylated epidermal growth factor repeats of notch. J. Biol. Chem. 287, 2739 –2748
22. Sethi, M. K., Buettner, F. F., Krylov, V. B., Takeuchi, H., Nifantiev, N. E., Haltiwanger, R. S., Gerardy-Schahn, R., and Bakker, H. (2010) Identification of glycosyltransferase 8 family members as xylosyltransferases acting on O-glucosylated notch epidermal growth factor repeats. J. Biol. Chem. 285, 1582–1586
23. Rampal, R., Li, A. S., Moloney, D. J., Georgiou, S. A., Luther, K. B., Nita-Lazar, A., and Haltiwanger, R. S. (2005) Lunatic fringe, manic fringe, and radical fringe recognize similar specificity determinants in O-fucosylated epidermal growth factor-like repeats. J. Biol. Chem. 280, 42454 – 42463
24. 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., and Vogt, T. F. (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406, 369 –375
25. Lee, T. V., Sethi, M. K., Leonardi, J., Rana, N. A., Buettner, F. F., Haltiwanger, R. S., Bakker, H., and Jafar-Nejad, H. (2013) Negative regulation of notch signaling by xylose. PLoS Genet. 9, e1003547
26. Lee, T. V., Pandey, A., and Jafar-Nejad, H. (2017) Xylosylation of the Notch receptor preserves the balance between its activation by trans- and inhibition by cis-ligands in Drosophila. PLoS Genet. 13, e1006723
27. Sakaidani, Y., Nomura, T., Matsuura, A., Ito, M., Suzuki, E., Murakami, K., Nadano, D., Matsuda, T., Furukawa, K., and Okajima, T. (2011) O-Linked N-acetylglucosamine on extracellular protein domains mediates epithelial cell–matrix interactions. Nat. Commun. 2, 583
28. Okajima, T., Xu, A., Lei, L., and Irvine, K. D. (2005) Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science 307, 1599 –1603
29. Stahl, M., Uemura, K., Ge, C., Shi, S., Tashima, Y., and Stanley, P. (2008) Roles of Pofut1 and O-fucose in mammalian Notch signaling. J. Biol. Chem. 283, 13638 –13651
30. Okamura, Y., and Saga, Y. (2008) Pofut1 is required for the proper localization of the Notch receptor during mouse development. Mech. Dev. 125, 663– 673
31. Ishio, A., Sasamura, T., Ayukawa, T., Kuroda, J., Ishikawa, H. O., Aoyama, N., Matsumoto, K., Gushiken, T., Okajima, T., Yamakawa, T., and Matsuno, K. (2015) O-Fucose monosaccharide of Drosophila Notch has a temperature-sensitive function and cooperates with O-glucose glycan in Notch transport and Notch signaling activation. J. Biol. Chem. 290, 505–519
32. Harris, R. J., and Spellman, M. W. (1993) O-Linked fucose and other post-translational modifications unique to EGF modules. Glycobiology 3, 219 –224
33. Takeuchi, H., Kantharia, J., Sethi, M. K., Bakker, H., and Haltiwanger, R. S. (2012) 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
34. Handford, P. A., Baron, M., Mayhew, M., Willis, A., Beesley, T., Brownlee, G. G., and Campbell, I. D. (1990) The first EGF-like domain from human factor IX contains a high-affinity calcium binding site. EMBO J. 9, 475– 480
35. Rao, Z., Handford, P., Mayhew, M., Knott, V., Brownlee, G. G., and Stuart, D. (1995) The structure of a Ca2+-binding epidermal growth factor-like domain: its role in protein–protein interactions. Cell 82, 131–141
36. Yu, H., Takeuchi, H., Takeuchi, M., Liu, Q., Kantharia, J., Haltiwanger, R. S., and Li, H. (2016) Structural analysis of Notch-regulating Rumi reveals basis for pathogenic mutations. Nat. Chem. Biol. 12, 735–740
37. Luca, V. C., Jude, K. M., Pierce, N. W., Nachury, M. V., Fischer, S., and Garcia, K. C. (2015) Structural biology. Structural basis for Notch1 engagement of Delta-like 4. Science 347, 847– 853
38. Luca, V. C., Kim, B. C., Ge, C., Kakuda, S., Wu, D., Roein-Peikar, M., Haltiwanger, R. S., Zhu, C., Ha, T., and Garcia, K. C. (2017) Notch-Jagged complex structure implicates a catch bond in tuning ligand sensitivity. Science 355, 1320 –1324
39. Hayakawa, S., Koide, R., Hinou, H., and Nishimura, S. (2016) Synthetic human NOTCH1 EGF modules unraveled molecular mechanisms for the structural and functional roles of calcium ions and O-glycans in the ligand-binding region. Biochemistry 55, 776 –787
40. Taylor, P., Takeuchi, H., Sheppard, D., Chillakuri, C., Lea, S. M., Haltiwanger, R. S., and Handford, P. A. (2014) Fringe-mediated extension of Olinked fucose in the ligand-binding region of Notch1 increases binding to mammalian Notch ligands. Proc. Natl. Acad. Sci. U.S.A. 111, 7290 –7295
41. Matsumoto, K., Ayukawa, T., Ishio, A., Sasamura, T., Yamakawa, T., and Matsuno, K. (2016) Dual roles of O-glucose glycans redundant with monosaccharide O-fucose on Notch in Notch trafficking. J. Biol. Chem. 291, 13743–13752
42. Gordon, W. R., Zimmerman, B., He, L., Miles, L. J., Huang, J., Tiyanont, K., McArthur, D. G., Aster, J. C., Perrimon, N., Loparo, J. J., and Blacklow, S. C. (2015) Mechanical allostery: evidence for a force requirement in the proteolytic activation of Notch. Dev. Cell 33, 729 –736
43. Berger, R. P., Sun, Y. H., Kulik, M., Lee, J. K., Nairn, A. V., Moremen, K. W., Pierce, M., and Dalton, S. (2016) ST8SIA4-dependent polysialylation is part of a developmental program required for germ layer formation from human pluripotent stem cells. Stem Cells 34, 1742–1752
44. Shao, L., Moloney, D. J., and 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, 7775–7782
45. Takeuchi, H., Fernández-Valdivia, R. C., Caswell, D. S., Nita-Lazar, A., Rana, N. A., Garner, T. P., Weldeghiorghis, T. K., Macnaughtan, M. A., Jafar-Nejad, H., and Haltiwanger, R. S. (2011) Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc. Natl. Acad. Sci. U.S.A. 108, 16600 –16605
46. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125–132
47. Battye, T. G., Kontogiannis, L., Johnson, O., Powell, H. R., and Leslie, A. G. (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr. D Biol. Crystallogr. 67, 271–281
48. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22–25
49. Pannu, N. S., Murshudov, G. N., Dodson, E. J., and Read, R. J. (1998) Incorporation of prior phase information strengthens maximum-likelihood structure refinement. Acta Crystallogr. D Biol. Crystallogr. 54, 1285–1294
50. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486 –501
51. Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G., McCoy, A., McNicholas, S. J., Murshudov, G. N., Pannu, N. S., Potterton, E. A., Powell, H. R., et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallogr. D Biol. Crystallogr. 67, 235–242