Protein O-glucosylation: another essential role of glucose in biology

Current Opinion in Structural Biology

Volumn 56, Issue , 2019, Pages 64-71

  Yu, Hongjun ^a   Takeuchi, Hideyuki ^b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; GLUCOSE; GLYCOSYLTRANSFERASE; NOTCH RECEPTOR; PROTEIN POGLUT1; PROTEIN POGLUT2; PROTEIN POGLUT3; PROTEIN RUMI; PROTEIN XXYLT1; UNCLASSIFIED DRUG; GLYCOPROTEIN;

DROSOPHILA; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME REGULATION; ENZYME STABILITY; ENZYME STRUCTURE; GLYCOSYLATION; HUMAN; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; NONHUMAN; NOTCH SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN O GLUCOSYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; CHEMISTRY; METABOLISM; SIGNAL TRANSDUCTION;

GLUCOSE; GLYCOPROTEINS; GLYCOSYLATION; HUMANS; SIGNAL TRANSDUCTION;

EID: 85060182630     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2018.12.001     Document Type: Review

References (40)

1. Takeuchi, H., Haltiwanger, R.S., Significance of glycosylation in Notch signaling. Biochem Biophys Res Commun 453 (2014), 235–242.
2. Acar, M., Jafar-Nejad, H., Takeuchi, H., Rajan, A., Ibrani, D., Rana, N.A., Pan, H., Haltiwanger, R.S., Bellen, H.J., Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132 (2008), 247–258 This study identified a long-sought proteinO-glucosyltransferase, POGLUT1/Rumi, that modifies Notch as an essential component for Notch signaling.
3. Fernandez-Valdivia, R., Takeuchi, H., Samarghandi, A., Lopez, M., Leonardi, J., Haltiwanger, R.S., Jafar-Nejad, H., Regulation of mammalian Notch signaling and embryonic development by the protein O-glucosyltransferase Rumi. Development 138 (2011), 1925–1934.
4. Ramkumar, N., Harvey, B.M., Lee, J.D., Alcorn, H.L., Silva-Gagliardi, N.F., McGlade, C.J., Bestor, T.H., Wijnholds, J., Haltiwanger, R.S., Anderson, K.V., Protein O-glucosyltransferase 1 (POGLUT1) promotes mouse gastrulation through modification of the apical polarity protein CRUMBS2. PLoS Genet, 11, 2015, e1005551.
5. Basmanav, F.B., Oprisoreanu, A.M., Pasternack, S.M., Thiele, H., Fritz, G., Wenzel, J., Größer, L., Wehner, M., Wolf, S., Fagerberg, C., et al. Mutations in POGLUT1, encoding protein O-glucosyltransferase 1, cause autosomal-dominant Dowling-Degos disease. Am J Hum Genet 94 (2014), 135–143.
6. Zhang, J., Li, M., Yao, Z., Updated review of genetic reticulate pigmentary disorders. Br J Dermatol 177 (2017), 945–959.
7. Shi, S., Stanley, P., Protein O-fucosyltransferase 1 is an essential component of Notch signaling pathways. Proc Natl Acad Sci U S A 100 (2003), 5234–5239.
8. 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., et al. A POGLUT1 mutation causes a muscular dystrophy with reduced Notch signaling and satellite cell loss. EMBO Mol Med 8 (2016), 1289–1309.
9. Wang, Y., Chang, N., Zhang, T., Liu, H., Ma, W., Chu, Q., Lai, Q., Liu, L., Wang, W., Overexpression of human CAP10-like protein 46 KD in T-acute lymphoblastic leukemia and acute myelogenous leukemia. Genet Test Mol Biomark 14 (2010), 127–133.
10. Fang, H., Chu, Q., Zhang, J., Wang, H., Yu, X., Ge, S., Song, M., Wu, L., Lang, M., Chang, N., et al. Human CAP10-like protein 46 kDa gene promotes malignancy in colorectal cancer. OMICS 21 (2017), 266–274.
11. Chammaa, M., Malysa, A., Redondo, C., Jang, H., Chen, W., Bepler, G., Fernandez-Valdivia, R., RUMI is a novel negative prognostic marker and therapeutic target in non-small-cell lung cancer. J Cell Physiol 233 (2018), 9548–9562.
12. Sethi, M.K., Buettner, F.F., Krylov, V.B., Takeuchi, H., Nifantiev, N.E., Haltiwanger, R.S., Gerardy-Schahn, R., Bakker, H., Identification of glycosyltransferase 8 family members as xylosyltransferases acting on O-glucosylated notch epidermal growth factor repeats. J Biol Chem 285 (2010), 1582–1586.
13. Sethi, M.K., Buettner, F.F., Ashikov, A., Krylov, V.B., Takeuchi, H., Nifantiev, N.E., Haltiwanger, R.S., Gerardy-Schahn, R., Bakker, H., Molecular cloning of a xylosyltransferase that transfers the second xylose to O-glucosylated epidermal growth factor repeats of notch. J Biol Chem 287 (2012), 2739–2748.
14. Lee, T.V., Sethi, M.K., Leonardi, J., Rana, N.A., Buettner, F.F., Haltiwanger, R.S., Bakker, H., Jafar-Nejad, H., Negative regulation of notch signaling by xylose. PLoS Genet, 9, 2013, e1003547.
15. Lee, T.V., Pandey, A., Jafar-Nejad, H., Xylosylation of the Notch receptor preserves the balance between its activation by trans-Delta and inhibition by cis-ligands in Drosophila. PLoS Genet, 13, 2017, e1006723.
16. Yu, H., Takeuchi, M., LeBarron, J., Kantharia, J., London, E., Bakker, H., Haltiwanger, R.S., Li, H., Takeuchi, H., Notch-modifying xylosyltransferase structures support an SNi-like retaining mechanism. Nat Chem Biol 11 (2015), 847–854 Structural characterization of XXYLT1 and its related reveals the molecular mechanism of its modification of Notch EGF repeats. This study describes the unexpected conformational change of EGF repeat when recognized by XXYLT1 also describes a competent Michaelis complex to illuminate the elusive mechanism for retaining glycosyltransferases.
17. Aster, J.C., Pear, W.S., Blacklow, S.C., The varied roles of Notch in cancer. Annu Rev Pathol 12 (2017), 245–275.
18. 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 (2011), 3569–3578.
19. Haltom, A.R., Lee, T.V., Harvey, B.M., Leonardi, J., Chen, Y.J., Hong, Y., Haltiwanger, R.S., Jafar-Nejad, H., The protein O-glucosyltransferase Rumi modifies eyes shut to promote rhabdomere separation in Drosophila. PLoS Genet, 10, 2014, e1004795.
20. Thakurdas, S.M., Lopez, M.F., Kakuda, S., Fernandez-Valdivia, R., Zarrin-Khameh, N., Haltiwanger, R.S., Jafar-Nejad, H., Jagged1 heterozygosity in mice results in a congenital cholangiopathy which is reversed by concomitant deletion of one copy of Poglut1 (Rumi). Hepatology 63 (2016), 550–565.
21. 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 (2012), 33934–33944.
22. Yu, H., Takeuchi, H., Takeuchi, M., Liu, Q., Kantharia, J., Haltiwanger, R.S., Li, H., Structural analysis of Notch-regulating Rumi reveals basis for pathogenic mutations. Nat Chem Biol 12 (2016), 735–740 This study together with Ref. 23• reveals the molecular basis of POGLUT1’s modification of Notch EGF repeats, including its specificity towards folded EGF repeats and catalytic mechanism.
23. Li, Z., Fischer, M., Satkunarajah, M., Zhou, D., Withers, S.G., Rini, J.M., Structural basis of Notch O-glucosylation and O-xylosylation by mammalian protein-O-glucosyltransferase 1 (POGLUT1). Nat Commun, 8, 2017, 185 This study reports human POGLUT1 in complex with three different EGF repeats and also describes a Michaelis ternary complex with EGF repeat and a glucose analogue, deepening our understanding of the molecular basis of POGLUT1.
24. Rana, N.A., Nita-Lazar, A., Takeuchi, H., Kakuda, S., Luther, K.B., Haltiwanger, R.S., O-Glucose trisaccharide is present at high but variable stoichiometry at multiple sites on mouse Notch1. J Biol Chem 286 (2011), 31623–31637.
25. 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., Haltiwanger, R.S., Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proc Natl Acad Sci U S A 108 (2011), 16600–16605 This study revealed, for the first time, the uncommon dual donor specificity of POGLUT1.
26. Luca, V.C., Jude, K.M., Pierce, N.W., Nachury, M.V., Fischer, S., Garcia, K.C., Structural biology. Structural basis for Notch1 engagement of Delta-like 4. Science 347 (2015), 847–853 This study for the first time reported the co-crystallized structure of the Notch1-DLL4 ligand complex which revealed significant roles ofO-glycans on EGF repeats in the Notch-ligand interaction.
27. Takeuchi, H., Schneider, M., Williamson, D.B., Ito, A., Takeuchi, M., Handford, P.A., Haltiwanger, R.S., Two novel protein O-glucosyltransferases that modify sites distinct from POGLUT1 and affect Notch trafficking and signaling. Proc Natl Acad Sci U S A 115 (2018), E8395–E8402.
28. Lairson, L.L., Henrissat, B., Davies, G.J., Withers, S.G., Glycosyltransferases: structures, functions, and mechanisms. Annu Rev Biochem 77 (2008), 521–555.
29. Takeuchi, H., Yu, H., Hao, H., Takeuchi, M., Ito, A., Li, H., Haltiwanger, R.S., O-Glycosylation modulates the stability of epidermal growth factor-like repeats and thereby regulates Notch trafficking. J Biol Chem 292 (2017), 15964–15973 This study revealed cooperative stabilizing effects ofO-Glc and O-Fuc glycans on EGF repeats that are required for proper trafficking of NOTCH1 in mammalian cells.
30. Luca, V.C., Kim, B.C., Ge, C., Kakuda, S., Wu, D., Roein-Peikar, M., Haltiwanger, R.S., Zhu, C., Ha, T., Garcia, K.C., Notch-Jagged complex structure implicates a catch bond in tuning ligand sensitivity. Science 355 (2017), 1320–1324 This study demonstrated a catch bond mechanism which regulates ligand-mediated Notch activation.
31. 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 and expression of a novel GDP-fucose protein O-fucosyltransferase. J Biol Chem 276 (2001), 40338–40345.
32. Luo, Y., Haltiwanger, R.S., O-Fucosylation of notch occurs in the endoplasmic reticulum. J Biol Chem 280 (2005), 11289–11294.
33. Taylor, P., Takeuchi, H., Sheppard, D., Chillakuri, C., Lea, S.M., Haltiwanger, R.S., Handford, P.A., Fringe-mediated extension of O-linked fucose in the ligand-binding region of Notch1 increases binding to mammalian Notch ligands. Proc Natl Acad Sci U S A 111 (2014), 7290–7295.
34. 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.
35. Vasudevan, D., Takeuchi, H., Johar, S.S., Majerus, E., Haltiwanger, R.S., Peters plus syndrome mutations disrupt a noncanonical ER quality-control mechanism. Curr Biol 25 (2015), 286–295.
36. Rao, Z., Handford, P.A., Knott, V., Mayhew, M., Brownlee, G.G., Stuart, D., Crystallization of a calcium-binding EGF-like domain. Acta Crystallogr D Biol Crystallogr 51 (1995), 402–403.
37. Kopan, R., Ilagan, M.X., The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137 (2009), 216–233.
38. Braakman, I., Hebert, D.N., Protein folding in the endoplasmic reticulum. Cold Spring Harb Perspect Biol, 5, 2013, a013201.
39. Xu, C., Ng, D.T., Glycosylation-directed quality control of protein folding. Nat Rev Mol Cell Biol 16 (2015), 742–752.
40. Takeuchi, H., Biochemical significance of regulation of protein stability by O-glucose glycans. Seikagaku 90 (2018), 519–523.