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Synthesis and biological roles of O-glycans in insects

  • Weidong Li
  • Kristof De Schutter
  • Els J. M. Van Damme
  • Guy SmaggheEmail author
Original Article

Abstract

Protein O-glycosylation is the attachment of carbohydrate structures to the oxygen atom in the hydroxyl group of Serine and Threonine residues. This post-translational modification is commonly found on the majority of proteins trafficking through the secretory pathway and is reported to influence protein characteristics such as folding, secretion, stability, solubility, oligomerization and intracellular localization. In addition, O-glycosylation is essential for cell-cell interactions, protein-protein interactions and many biological processes, such as stress response, immunization, phosphorylation, ubiquitination, cell division, metabolism and cell signaling. The availability of sequenced genomes and genetic tools to create mutants with clear phenotypes makes insects an interesting model system to study O-glycosylation. In this review, we provide an overview of the current knowledge of O-glycosylation, mainly obtained from the model organism Drosophila melanogaster, with a focus on the synthesis and biological roles of the common O-glycans in insects.

Keywords

Protein O-glycosylation O-glycans Drosophila melanogaster Function Glycoproteins 

Notes

Acknowledgements

This work is supported by the Special Research Fund from Ghent University (Belgium). W.L. is a recipient of a Chinese Scholarship Council (CSC) scholarship.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. 1.
    SPIRO, R.G., Lucas, F., Rudall, K.: Glycosylation of hydroxylysine in collagens. Nat New Biol. 231(19), 54–55 (1971).  https://doi.org/10.1038/newbio231054a0 Google Scholar
  2. 2.
    Zarschler, K., Janesch, B., Pabst, M., Altmann, F., Messner, P., Schaffer, C.: Protein tyrosine O-glycosylation-a rather unexplored prokaryotic glycosylation system. Glycobiology. 20(6), 787–798 (2010).  https://doi.org/10.1093/glycob/cwq035 Google Scholar
  3. 3.
    Kieliszewski, M.J.: The latest hype on Hyp-O-glycosylation codes. Phytochemistry. 57(3), 319–323 (2001).  https://doi.org/10.1016/S0031-9422(01)00029-2 Google Scholar
  4. 4.
    Joshi, H.J., Narimatsu, Y., Schjoldager, K.T., Tytgat, H.L.P., Aebi, M., Clausen, H., Halim, A.: SnapShot: O-Glycosylation pathways across kingdoms. Cell. 172(3), 632–632 e632 (2018).  https://doi.org/10.1016/j.cell.2018.01.016 Google Scholar
  5. 5.
    Hart, G.W., Haltiwanger, R.S., Holt, G.D., Kelly, W.G.: Glycosylation in the nucleus and cytoplasm. Annu. Rev. Biochem. 58, 841–874 (1989).  https://doi.org/10.1146/annurev.bi.58.070189.004205 Google Scholar
  6. 6.
    Fukuda, M.: Roles of mucin-type O-glycans in cell adhesion. Biochim. Biophys. Acta. 1573(3), 394–405 (2002).  https://doi.org/10.1016/S0304-4165(02)00409-9 Google Scholar
  7. 7.
    Chaffey, P.K., Guan, X., Chen, C., Ruan, Y., Wang, X., Tran, A.H., Koelsch, T.N., Cui, Q., Feng, Y., Tan, Z.: Structural insight into the stabilizing effect of O-glycosylation. Biochemistry. 56, 2897–2906 (2017).  https://doi.org/10.1021/acs.biochem.7b00195 Google Scholar
  8. 8.
    Chaffey, P.K., Guan, X., Wang, X., Ruan, Y., Biochemistry, L.-Y.: Quantitative effects of O-linked Glycans on protein folding. Biochemistry. 56, 4539–4548 (2017).  https://doi.org/10.1021/acs.biochem.7b00483 Google Scholar
  9. 9.
    Hart, G.W., Copeland, R.J.: Glycomics hits the big time. Cell. 143(5), 672–676 (2010).  https://doi.org/10.1016/j.cell.2010.11.008 Google Scholar
  10. 10.
    Goto, M.: Protein O-glycosylation in fungi: diverse structures and multiple functions. 71(6), 1415–1427 (2007).  https://doi.org/10.1271/bbb.70080
  11. 11.
    Martinez, M.R., Dias, T.B., Natov, P.S., Zachara, N.E.: Stress-induced O-GlcNAcylation: an adaptive process of injured cells. Biochem. Soc. Trans. 45(1), 237–249 (2017).  https://doi.org/10.1042/BST20160153 Google Scholar
  12. 12.
    Aoki, K., Porterfield, M., Lee, S.S., Dong, B., Nguyen, K., McGlamry, K.H., Tiemeyer, M.: The diversity of O-linked glycans expressed during Drosophila melanogaster development reflects stage-and tissue-specific requirements for cell signaling. J. Biol. Chem. 283(44), 30385–30400 (2008).  https://doi.org/10.1074/jbc.M804925200 Google Scholar
  13. 13.
    Tian, E., Hagen, K.G.: Expression of the UDP-GalNAc : polypeptide N-acetylgalactosaminyltransferase family is spatially and temporally regulated during Drosophila development. Glycobiology. 16(2), 83–95 (2006).  https://doi.org/10.1093/glycob/cwj051 Google Scholar
  14. 14.
    Tran, D.T., Ten Hagen, K.G.: Mucin-type O-glycosylation during development. J. Biol. Chem. 288(10), 6921–6929 (2013).  https://doi.org/10.1074/jbc.R112.418558 Google Scholar
  15. 15.
    Yamamoto-Hino, M., Yoshida, H., Ichimiya, T.: Phenotype-based clustering of glycosylation-related genes by RNAi-mediated gene silencing. Genes Cells. 20, 521–542 (2015).  https://doi.org/10.1111/gtc.12246 Google Scholar
  16. 16.
    Zhang, L., Zhang, Y., Ten Hagen, K.G.: A mucin-type O-glycosyltransferase modulates cell adhesion during Drosophila development. J. Biol. Chem. 283(49), 34076–34086 (2008).  https://doi.org/10.1074/jbc.M804267200 Google Scholar
  17. 17.
    Zhang, L., Tran, D.T., Ten Hagen, K.G.: An O-glycosyltransferase promotes cell adhesion during development by influencing secretion of an extracellular matrix integrin ligand. J. Biol. Chem. 285(25), 19491–19501 (2010).  https://doi.org/10.1074/jbc.M109.098145 Google Scholar
  18. 18.
    Zhang, L., Syed, Z.A., van Dijk Hard, I., Lim, J.M., Wells, L., Ten Hagen, K.G.: O-glycosylation regulates polarized secretion by modulating Tango1 stability. Proc. Natl. Acad. Sci. U.S.A. 111(20), 7296–7301 (2014).  https://doi.org/10.1073/pnas.1322264111 Google Scholar
  19. 19.
    Zhang, L., Turner, B., Ribbeck, K., Ten Hagen, K.G.: Loss of the mucosal barrier alters the progenitor cell niche via Janus kinase/signal transducer and activator of transcription (JAK/STAT) signaling. J. Biol. Chem. 292(52), 21231–21242 (2017).  https://doi.org/10.1074/jbc.M117.809848 Google Scholar
  20. 20.
    Tran, D.T., Zhang, L., Zhang, Y., Tian, E., Earl, L.A., Ten Hagen, K.G.: Multiple members of the UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase family are essential for viability in Drosophila. J. Biol. Chem. 287(8), 5243–5252 (2012).  https://doi.org/10.1074/jbc.M111.306159 Google Scholar
  21. 21.
    Ji, S., Samara, N.L., Revoredo, L., Zhang, L., Tran, D.T., Muirhead, K., Tabak, L.A., Ten Hagen, K.G.: A molecular switch orchestrates enzyme specificity and secretory granule morphology. Nat. Commun. 9(1), 3508 (2018).  https://doi.org/10.1038/s41467-018-05978-9 Google Scholar
  22. 22.
    Tian, E., Ten Hagen, K.G.: A UDP-GalNAc: polypeptide N-acetylgalactosaminyltransferase is required for epithelial tube formation. J. Biol. Chem. 282(1), 606–614 (2007).  https://doi.org/10.1074/jbc.M606268200 Google Scholar
  23. 23.
    Dönitz, J., Schmitt-Engel, C., Grossmann, D., Gerischer, L., Tech, M., Schoppmeier, M., Klingler, M., Bucher, G.: iBeetle-base: a database for RNAi phenotypes in the red flour beetle Tribolium castaneum. Nucleic Acids Res. 43(Database issue), 5–D725 (2015).  https://doi.org/10.1093/nar/gku1054 Google Scholar
  24. 24.
    Kurz, S., Aoki, K., Jin, C.S., Karlsson, N.G., Tiemeyer, M., Wilson, I.B.H., Paschinger, K.: Targeted release and fractionation reveal glucuronylated and sulphated N- and O-glycans in larvae of dipteran insects. J. Proteome. 126, 172–188 (2015).  https://doi.org/10.1016/j.jprot.2015.05.030 Google Scholar
  25. 25.
    Lin, Y.R., Reddy, B., Irvine, K.D.: Requirement for a core 1 galactosyltransferase in the Drosophila nervous system. Dev. Dyn. 237(12), 3703–3714 (2008).  https://doi.org/10.1002/dvdy.21775 Google Scholar
  26. 26.
    Müller, R., Hülsmeier, A.J., Altmann, F., Ten Hagen, K., Tiemeyer, M., Hennet, T.: Characterization of mucin-type core-1 β1-3 galactosyltransferase homologous enzymes in Drosophila melanogaster. FEBS J. 272(17), 4295–4305 (2005).  https://doi.org/10.1111/j.1742-4658.2005.04838.x Google Scholar
  27. 27.
    Yoshida, H., Fuwa, T.J., Arima, M., Hamamoto, H., Sasaki, N., Ichimiya, T., Osawa, K.-i., Ueda, R., Nishihara, S.: Identification of the Drosophila core 1 1, 3-galactosyltransferase gene that synthesizes T antigen in the embryonic central nervous system and hemocytes. Glycobiology. 18(12), 1094–1104 (2008).  https://doi.org/10.1093/glycob/cwn094 Google Scholar
  28. 28.
    Itoh, K., Akimoto, Y., Fuwa, T.J., Sato, C., Komatsu, A., Nishihara, S.: Mucin-type core 1 glycans regulate the localization of neuromuscular junctions and establishment of muscle cell architecture in Drosophila. Dev. Biol. 412(1), 114–127 (2016).  https://doi.org/10.1016/j.ydbio.2016.01.032 Google Scholar
  29. 29.
    Kim, B.T., Tsuchida, K., Lincecum, J., Kitagawa, H., Bernfield, M., Sugahara, K.: Identification and characterization of three Drosophila melanogaster glucuronyltransferases responsible for the synthesis of the conserved glycosaminoglycan-protein linkage region of proteoglycans. Two novel homologs exhibit broad specificity toward oligosaccharides from proteoglycans, glycoproteins, and glycosphingolipids. J. Biol. Chem. 278(11), 9116–9124 (2003).  https://doi.org/10.1074/jbc.M209344200 Google Scholar
  30. 30.
    Itoh, K., Akimoto, Y., Kondo, S., Ichimiya, T., Aoki, K., Tiemeyer, M., Nishihara, S.: Glucuronylated core 1 glycans are required for precise localization of neuromuscular junctions and normal formation of basement membranes on Drosophila muscles. Dev. Biol. 436(2), 108–124 (2018).  https://doi.org/10.1016/j.ydbio.2018.02.017 Google Scholar
  31. 31.
    Weiszmann, R., Hammonds, A.S., Celniker, S.E.: Determination of gene expression patterns using high-throughput RNA in situ hybridization to whole-mount Drosophila embryos. Nat. Protoc. 4(5), 605–618 (2009).  https://doi.org/10.1038/nprot.2009.55 Google Scholar
  32. 32.
    Pandey, R., Blanco, J., Udolph, G.: The glucuronyltransferase GlcAT-P is required for stretch growth of peripheral nerves in drosophila. PloS one. 6(11) (2011).  https://doi.org/10.1371/journal.pone.0028106
  33. 33.
    Gaunitz, S., Jin, C., Nilsson, A., Liu, J., Karlsson, N.G., Holgersson, J.: Mucin-type proteins produced in the Trichoplusia ni and Spodoptera frugiperda insect cell lines carry novel O-glycans with phosphocholine and sulfate substitutions. Glycobiology. 23(7), 778–796 (2013).  https://doi.org/10.1093/glycob/cwt015 Google Scholar
  34. 34.
    Schwientek, T., Mandel, U., Roth, U., Muller, S., Hanisch, F.G.: A serial lectin approach to the mucin-type O-glycoproteome of Drosophila melanogaster S2 cells. Proteomics. 7(18), 3264–3277 (2007).  https://doi.org/10.1002/pmic.200600793 Google Scholar
  35. 35.
    Walski, T., De Schutter, K., Van Damme, E.J.M., Smagghe, G.: Diversity and functions of protein glycosylation in insects. Insect Biochem. Mol. Biol. 83, 21–34 (2017).  https://doi.org/10.1016/j.ibmb.2017.02.005 Google Scholar
  36. 36.
    Bond, M.R., Hanover, J.A.: A little sugar goes a long way: the cell biology of O-GlcNAc. J. Cell Biol. 208(7), 869–880 (2015).  https://doi.org/10.1083/jcb.201501101 Google Scholar
  37. 37.
    Holt, G.D., Hart, G.W.: The subcellular distribution of terminal N-acetylglucosamine moieties. Localization of a novel protein-saccharide linkage, O-linked GlcNAc. J. Biol. Chem. 261(17), 8049–8057 (1986)Google Scholar
  38. 38.
    Ogawa, M., Sawaguchi, S., Furukawa, K., Okajima, T.: N-acetylglucosamine modification in the lumen of the endoplasmic reticulum. Biochim. Biophys. Acta. 1850(6), 1319–1324 (2015).  https://doi.org/10.1016/j.bbagen.2015.03.003 Google Scholar
  39. 39.
    Yang, X., Qian, K.: Protein O-GlcNAcylation: emerging mechanisms and functions. Nat. Rev. Mol. Cell Biol. 18(7), 452–465 (2017).  https://doi.org/10.1038/nrm.2017.22 Google Scholar
  40. 40.
    Park, S., Park, S.-H., Baek, J.Y., Jy, Y.J., Kim, K.S., Roth, J., Cho, J.W., Choe, K.-M.: Protein O-GlcNAcylation regulates Drosophila growth through the insulin signaling pathway. Cell. Mol. Life Sci. 68(20), 3377–3384 (2011).  https://doi.org/10.1007/s00018-011-0640-7 Google Scholar
  41. 41.
    Sekine, O., Love, D.C., Rubenstein, D.S., Hanover, J.A.: Blocking O-linked GlcNAc cycling in Drosophila insulin-producing cells perturbs glucose-insulin homeostasis. J. Biol. Chem. 285(49), 38684–38691 (2010).  https://doi.org/10.1074/jbc.M110.155192 Google Scholar
  42. 42.
    Pekkurnaz, G., Trinidad, J.C., Wang, X., Kong, D., Schwarz, T.L.: Glucose regulates mitochondrial motility via Milton modification by O-GlcNAc transferase. Cell. 158(1), 54–68 (2014).  https://doi.org/10.1016/j.cell.2014.06.007 Google Scholar
  43. 43.
    Hart, G.W., Slawson, C., Ramirez-Correa, G., Lagerlof, O.: Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu. Rev. Biochem. 80, 825–858 (2011).  https://doi.org/10.1146/annurev-biochem-060608-102511 Google Scholar
  44. 44.
    Sinclair, D.A., Syrzycka, M., Macauley, M.S., Rastgardani, T., Komljenovic, I., Vocadlo, D.J., Brock, H.W., Honda, B.M.: Drosophila O-GlcNAc transferase (OGT) is encoded by the Polycomb group (PcG) gene, super sex combs (sxc). Proc. Natl. Acad. Sci. U. S. A. 106(32), 13427–13432 (2009).  https://doi.org/10.1073/pnas.0904638106 Google Scholar
  45. 45.
    Lagerlöf, O., Hart, G.W., Huganir, R.L.: O-GlcNAc transferase regulates excitatory synapse maturity. Proc. Natl. Acad. Sci. U.S.A. (2017).  https://doi.org/10.1073/pnas.1621367114
  46. 46.
    Gambetta, M.C., Oktaba, K., Muller, J.: Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science. 325(5936), 93–96 (2009).  https://doi.org/10.1126/science.1169727 Google Scholar
  47. 47.
    Gambetta, M.C., Muller, J.: O-GlcNAcylation prevents aggregation of the Polycomb group repressor polyhomeotic. Dev. Cell. 31(5), 629–639 (2014).  https://doi.org/10.1016/j.devcel.2014.10.020 Google Scholar
  48. 48.
    Mariappa, D., Ferenbach, A.T., van Aalten, D.M.F.: Effects of hypo-O-GlcNAcylation on Drosophila development. J. Biol. Chem. 293(19), 7209–7221 (2018).  https://doi.org/10.1074/jbc.RA118.002580 Google Scholar
  49. 49.
    Radermacher, P.T., Myachina, F., Bosshardt, F., Pandey, R., Mariappa, D., Muller, H.A.J., Lehner, C.F.: O-GlcNAc reports ambient temperature and confers heat resistance on ectotherm development. Proc. Natl. Acad. Sci. U.S.A. 111(15), 5592–5597 (2014).  https://doi.org/10.1073/pnas.1322396111 Google Scholar
  50. 50.
    Leney, A.C., Atmioui, E.D., Wu, W.: Elucidating crosstalk mechanisms between phosphorylation and O-GlcNAcylation. Proc. Natl. Acad. Sci. U.S.A. (2017).  https://doi.org/10.1073/pnas.1620529114
  51. 51.
    Kim, E.Y., Jeong, E.H., Park, S., Jeong, H.J., Edery, I., Cho, J.W.: A role for O-GlcNAcylation in setting circadian clock speed. Genes Dev. 26(5), 490–502 (2012).  https://doi.org/10.1101/gad.182378.111 Google Scholar
  52. 52.
    Kaasik, K., Kivimae, S., Allen, J.J., Chalkley, R.J., Huang, Y., Baer, K., Kissel, H., Burlingame, A.L., Shokat, K.M., Ptacek, L.J., Fu, Y.H.: Glucose sensor O-GlcNAcylation coordinates with phosphorylation to regulate circadian clock. Cell Metab. 17(2), 291–302 (2013).  https://doi.org/10.1016/j.cmet.2012.12.017 Google Scholar
  53. 53.
    Draime, A., Bridoux, L., Belpaire, M., Pringels, T., Degand, H., Morsomme, P., Rezsohazy, R.: The O-GlcNAc transferase OGT interacts with and post-translationally modifies the transcription factor HOXA1. FEBS Lett. 592, 1185–1201 (2018).  https://doi.org/10.1002/1873-3468.13015 Google Scholar
  54. 54.
    Liu, T.W., Myschyshyn, M., Sinclair, D.A., Cecioni, S., Beja, K., Honda, B.M., Morin, R.D., Vocadlo, D.J.: Genome-wide chemical mapping of O-GlcNAcylated proteins in Drosophila melanogaster. Nat. Chem. Biol. 13(2), 161–167 (2017).  https://doi.org/10.1038/nchembio.2247 Google Scholar
  55. 55.
    Park, S., Lee, Y., Pak, J.W., Kim, H., Choi, H., Kim, J.-W., Roth, J., Cho, J.W.: O-GlcNAc modification is essential for the regulation of autophagy in Drosophila melanogaster. Cell. Mol. Life Sci. 72(16), 3173–3183 (2015).  https://doi.org/10.1007/s00018-015-1889-z Google Scholar
  56. 56.
    Sümegi, M., Hunyadi-Gulyás, É., Medzihradszky, K.F., Udvardy, A.: 26S proteasome subunits are O-linked N-acetylglucosamine-modified in Drosophila melanogaster. Biochem. Biophys. Res. Commun. 312(4), 1284–1289 (2003).  https://doi.org/10.1016/j.bbrc.2003.11.074 Google Scholar
  57. 57.
    Varshney, S., Stanley, P.: EOGT and O-GlcNAc on secreted and membrane proteins. Biochem. Soc. Trans. 45(2), 401–408 (2017).  https://doi.org/10.1042/BST20160165 Google Scholar
  58. 58.
    Alfaro, J.F., Gong, C.X., Monroe, M.E., Aldrich, J.T., Clauss, T.R., Purvine, S.O., Wang, Z., Camp 2nd, D.G., Shabanowitz, J., Stanley, P., Hart, G.W., Hunt, D.F., Yang, F., Smith, R.D.: Tandem mass spectrometry identifies many mouse brain O-GlcNAcylated proteins including EGF domain-specific O-GlcNAc transferase targets. Proc. Natl. Acad. Sci. U.S.A. 109(19), 7280–7285 (2012).  https://doi.org/10.1073/pnas.1200425109 Google Scholar
  59. 59.
    Haltom, A.R., Jafar-Nejad, H.: O-linked glycans in drosophila drosophila development: Overview. In: Glycoscience: Biology and Medicine. pp. 809–815. Springer, (2015)Google Scholar
  60. 60.
    Sakaidani, Y., Nomura, T., Matsuura, A., Ito, M., Suzuki, E., Murakami, K., Nadano, D., Matsuda, T., Furukawa, K., Okajima, T.: O-linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell-matrix interactions. Nat. Commun. 2, 583 (2011).  https://doi.org/10.1038/ncomms1591 Google Scholar
  61. 61.
    Müller, R., Jenny, A., Stanley, P.: The EGF repeat-specific O-GlcNAc-transferase Eogt interacts with notch signaling and pyrimidine metabolism pathways in Drosophila. PLoS One. 8, e62835 (2013).  https://doi.org/10.1371/journal.pone.0062835 Google Scholar
  62. 62.
    Kelly, W.G., Hart, G.W.: Glycosylation of chromosomal proteins: localization of O-linked N-acetylglucosamine in Drosophila chromatin. Cell. 57(2), 243–251 (1989).  https://doi.org/10.1016/0092-8674(89)90962-8 Google Scholar
  63. 63.
    Shaheen, R., Aglan, M., Keppler-Noreuil, K.: Mutations in EOGT confirm the genetic heterogeneity of autosomal-recessive Adams-Oliver syndrome. Am. J. Hum. Genet. 92, 598–604 (2013).  https://doi.org/10.1016/j.ajhg.2013.02.012 Google Scholar
  64. 64.
    Varshney, S., Stanley, P.: Multiple roles for O-Glycans in notch signalling. FEBS Lett. 592(23), 3819–3834 (2018).  https://doi.org/10.1002/1873-3468.13251 Google Scholar
  65. 65.
    Selvan, N., Williamson, R., Mariappa, D., Campbell, D.G., Gourlay, R., Ferenbach, A.T., Aristotelous, T., Hopkins-Navratilova, I., Trost, M., van Aalten, D.M.F.: A mutant O-GlcNAcase enriches Drosophila developmental regulators. Nat. Chem. Biol. 13(8), 882–887 (2017).  https://doi.org/10.1038/nchembio.2404 Google Scholar
  66. 66.
    Sprung, R., Nandi, A., Chen, Y., Kim, S.C., Barma, D., Falck, J.R., Zhao, Y.: Tagging-via-substrate strategy for probing O-GlcNAc modified proteins. J. Proteome Res. 4(3), 950–957 (2005).  https://doi.org/10.1021/pr050033j Google Scholar
  67. 67.
    Ishio, A., Sasamura, T., Ayukawa, T., Kuroda, J., Ishikawa, H.O., Aoyama, N., Matsumoto, K., Gushiken, T., Okajima, T., Yamakawa, T.: 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(1), 505–519 (2015).  https://doi.org/10.1074/jbc.M114.616847 Google Scholar
  68. 68.
    Okajima, T., Xu, A., Lei, L., Irvine, K.D.: Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science. 307(5715), 1599–1603 (2005).  https://doi.org/10.1126/science.1108995 Google Scholar
  69. 69.
    Luo, Y., Koles, K., Vorndam, W., Haltiwanger, R.S., Panin, V.M.: Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J. Biol. Chem. 281(14), 9393–9399 (2006).  https://doi.org/10.1074/jbc.M511975200 Google Scholar
  70. 70.
    Okajima, T., Xu, A.G., Irvine, K.D.: Modulation of notch-ligand binding by protein O-Fucosyltransferase 1 and fringe. J. Biol. Chem. 278(43), 42340–42345 (2003).  https://doi.org/10.1074/jbc.M308687200 Google Scholar
  71. 71.
    Sasamura, T., Ishikawa, H.O., Sasaki, N., Higashi, S., Kanai, M., Nakao, S., Ayukawa, T., Aigaki, T., Noda, K., Miyoshi, E.: The O-fucosyltransferase O-fut1 is an extracellular component that is essential for the constitutive endocytic trafficking of notch in Drosophila. Development. 134(7), 1347–1356 (2007).  https://doi.org/10.1242/dev.02811 Google Scholar
  72. 72.
    Okajima, T., Irvine, K.D.: Regulation of notch signaling by O-linked fucose. Cell. 111(6), 893–904 (2002).  https://doi.org/10.1016/S0092-8674(02)01114-5 Google Scholar
  73. 73.
    Glavic, A., Lopez-Varea, A., de Cells, J.F.: The balance between GMD and OFUT1 regulates notch signaling pathway activity by modulating notch stability. Biol. Res. 44(1), 25–34 (2011).  https://doi.org/10.4067/S0716-97602011000100004 Google Scholar
  74. 74.
    Moloney, D.J., Panin, V.M., Johnston, S.H., Chen, J.H., Shao, L., Wilson, R., Wang, Y., Stanley, P., Irvine, K.D., Haltiwanger, R.S., Vogt, T.F.: Fringe is a glycosyltransferase that modifies notch. Nature. 406(6794), 369–375 (2000).  https://doi.org/10.1038/35019000 Google Scholar
  75. 75.
    Munro, S., Freeman, M.: The notch signalling regulator fringe acts in the Golgi apparatus and requires the glycosyltransferase signature motif DXD. Curr. Biol. 10(14), 813–820 (2000).  https://doi.org/10.1016/S0960-9822(00)00578-9 Google Scholar
  76. 76.
    LeBon, L., Lee, T.V., Sprinzak, D., Jafar-Nejad, H., Elowitz, M.B.: Fringe proteins modulate notch-ligand cis and trans interactions to specify signaling states. eLife. 3, e02950 (2014).  https://doi.org/10.7554/eLife.02950 Google Scholar
  77. 77.
    Xu, A., Haines, N., Dlugosz, M., Rana, N.A., Takeuchi, H., Haltiwanger, R.S., Irvine, K.D.: In vitro reconstitution of the modulation of Drosophila notch-ligand binding by fringe. J. Biol. Chem. 282(48), 35153–35162 (2007).  https://doi.org/10.1074/jbc.M707040200 Google Scholar
  78. 78.
    Cho, K.O., Choi, K.W.: Fringe is essential for mirror symmetry and morphogenesis in the Drosophila eye. Nature. 396(6708), 272–276 (1998).  https://doi.org/10.1038/24394 Google Scholar
  79. 79.
    Zhao, D.B., Clyde, D., Bownes, M.: Expression of fringe is down regulated by Gurken/epidermal growth factor receptor signalling and is required for the morphogenesis of ovarian follicle cells. J. Cell Sci. 113(21), 3781–3794 (2000)Google Scholar
  80. 80.
    Irvine, K.D., Wieschaus, E.: Fringe, a boundary-specific signaling molecule, mediates interactions between dorsal and ventral cells during drosophila wing development. Cell. 79(4), 595–606 (1994).  https://doi.org/10.1016/0092-8674(94)90545-2 Google Scholar
  81. 81.
    Correia, T., Papayannopoulos, V., Panin, V., Woronoff, P., Jiang, J., Vogt, T.F., Irvine, K.D.: Molecular genetic analysis of the glycosyltransferase fringe in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 100(11), 6404–6409 (2003).  https://doi.org/10.1073/pnas.1131007100 Google Scholar
  82. 82.
    Gelbart, W., Emmert, D.: Flybase high throughput expression pattern data. FlyBase Analysis (flybaseorg/reports/FBrf0221009html 29 October 2013, date last accessed) (2013)Google Scholar
  83. 83.
    Mummery-Widmer, J.L., Yamazaki, M., Stoeger, T., Novatchkova, M., Bhalerao, S., Chen, D., Dietzl, G., Dickson, B.J., Knoblich, J.A.: Genome-wide analysis of notch signalling in Drosophila by transgenic RNAi. Nature. 458(7241), 987–992 (2009).  https://doi.org/10.1038/nature07936 Google Scholar
  84. 84.
    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(9), 6485–6498 (2001).  https://doi.org/10.1074/jbc.M008073200 Google Scholar
  85. 85.
    Tepass, U., Theres, C., Knust, E.: Crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell. 61(5), 787–799 (1990).  https://doi.org/10.1016/0092-8674(90)90189-L Google Scholar
  86. 86.
    Lyalin, D., Koles, K., Roosendaal, S.D., Repnikova, E., Van Wechel, L., Panin, V.M.: The twisted gene encodes Drosophila protein O-mannosyltransferase 2 and genetically interacts with the rotated abdomen gene encoding Drosophila protein O-mannosyltransferase 1. Genetics. 172(1), 343–353 (2006).  https://doi.org/10.1534/genetics.105.049650 Google Scholar
  87. 87.
    Ichimiya, T., Manya, H., Ohmae, Y., Yoshida, H., Takahashi, K., Ueda, R., Endo, T., Nishihara, S.: The twisted abdomen phenotype of Drosophila POMT1 and POMT2 mutants coincides with their heterophilic protein O-mannosyltransferase activity. J. Biol. Chem. 279(41), 42638–42647 (2004).  https://doi.org/10.1074/jbc.M404900200 Google Scholar
  88. 88.
    Haines, N., Seabrooke, S., Stewart, B.A.: Dystroglycan and protein O-mannosyltransferases 1 and 2 are required to maintain integrity of Drosophila larval muscles. Mol. Biol. Cell. 18(12), 4721–4730 (2007).  https://doi.org/10.1091/mbc.E07-01-0047 Google Scholar
  89. 89.
    Baker, R., Nakamura, N., Chandel, I., of …, H.-B.: Protein O-mannosyltransferases affect sensory axon wiring and dynamic chirality of body posture in the Drosophila embryo. J. Neurosci. 38(7), 1850–1865 (2017).  https://doi.org/10.1523/JNEUROSCI.0346-17.2017
  90. 90.
    Cooley, L., Kelley, R., Spradling, A.: Insertional mutagenesis of the Drosophila genome with single P-elements. Science. 239(4844), 1121–1128 (1988).  https://doi.org/10.1126/science.2830671 Google Scholar
  91. 91.
    Ueyama, M., Akimoto, Y., Ichimiya, T., Ueda, R., Kawakami, H., Aigaki, T., Nishihara, S.: Increased apoptosis of myoblasts in Drosophila model for the Walker-Warburg syndrome. PLoS One. 5(7), e11557 (2010).  https://doi.org/10.1371/journal.pone.0011557 Google Scholar
  92. 92.
    Nakamura, N., Stalnaker, S.H., Lyalin, D., Lavrova, O., Wells, L., Panin, V.M.: Drosophila Dystroglycan is a target of O-mannosyltransferase activity of two protein O-mannosyltransferases, rotated abdomen and twisted. Glycobiology. 20(3), 381–394 (2010).  https://doi.org/10.1093/glycob/cwp189 Google Scholar
  93. 93.
    Yatsenko, A.S., Gray, E.E., Shcherbata, H.R., Patterson, L.B., Sood, V.D., Kucherenko, M.M., Baker, D., Ruohola-Baker, H.: A putative Src homology 3 domain binding motif but not the C-terminal dystrophin WW domain binding motif is required for dystroglycan function in cellular polarity in Drosophila. J. Biol. Chem. 282(20), 15159–15169 (2007).  https://doi.org/10.1074/jbc.M608800200 Google Scholar
  94. 94.
    Soya, S., Şahar, U., Karaçalı, S.: Monosaccharide profiling of silkworm (Bombyx mori L.) nervous system during development and aging. Invertebr. Neurosci. 16(3), 8 (2016).  https://doi.org/10.1007/s10158-016-0191-6 Google Scholar
  95. 95.
    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(41), 33934–33944 (2012).  https://doi.org/10.1074/jbc.M112.401315 Google Scholar
  96. 96.
    Stanley, P.: Glucose: a novel regulator of notch signaling. ACS Chem. Biol. 3(4), 210–213 (2008).  https://doi.org/10.1021/cb800073x Google Scholar
  97. 97.
    Matsumoto, K., Ayukawa, T., Ishio, A., Sasamura, T., Yamakawa, T., Matsuno, K.: Dual roles of O-glucose glycans redundant with monosaccharide O-Fucose on notch in notch trafficking. J. Biol. Chem. 291(26), 13743–13752 (2016).  https://doi.org/10.1074/jbc.M115.710483 Google Scholar
  98. 98.
    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(11), e1004795 (2014).  https://doi.org/10.1371/journal.pgen.1004795 Google Scholar
  99. 99.
    Takeuchi, H., Fernandez-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(40), 16600–16605 (2011).  https://doi.org/10.1073/pnas.1109696108 Google Scholar
  100. 100.
    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(16), 3569–3578 (2011).  https://doi.org/10.1242/dev.068361 Google Scholar
  101. 101.
    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(2), 247–258 (2008).  https://doi.org/10.1016/j.cell.2007.12.016 Google Scholar
  102. 102.
    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(36), 31623–31637 (2011).  https://doi.org/10.1074/jbc.M111.268243 Google Scholar
  103. 103.
    Whitworth, G.E., Zandberg, W.F., Clark, T., Vocadlo, D.J.: Mammalian notch is modified by D-Xyl-alpha 1-3-D-Xyl-alpha 1-3-D-Glc-beta 1-O-Ser: implementation of a method to study O-glucosylation. Glycobiology. 20(3), 287–299 (2010).  https://doi.org/10.1093/glycob/cwp173 Google Scholar
  104. 104.
    Pandey, A., Li-Kroeger, D., Sethi, M.K., Lee, T.V., Buettner, F.F.R., Bakker, H., Jafar-Nejad, H.: Sensitized genetic backgrounds reveal differential roles for EGF repeat xylosyltransferases in Drosophila notch signaling. Glycobiology. 28(11), 849–859 (2018).  https://doi.org/10.1093/glycob/cwy080 Google Scholar
  105. 105.
    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(4) (2017).  https://doi.org/10.1371/journal.pgen.1006723
  106. 106.
    Lee, T.V., Sethi, M.K., Leonardi, J., Rana, N.A., Buettner, F.F.R., Haltiwanger, R.S., Bakker, H., Jafar-Nejad, H.: Negative regulation of notch signaling by xylose. PLoS Genet. 9(6), e1003547 (2013).  https://doi.org/10.1371/journal.pgen.1003547 Google Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratory of Agrozoology, Department of Plants and Crops, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium
  2. 2.Laboratory of Biochemistry and Glycobiology, Department of Biotechnology, Faculty of Bioscience EngineeringGhent UniversityGhentBelgium

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