The N's and O's of Drosophila glycoprotein glycobiology

Glycoconjugate Journal

Volumn 30, Issue 1, 2013, Pages 57-66

  Katoh, Toshihiko ^a   Tiemeyer, Michael ^a,b  

^a UNIVERSITY OF GEORGIA   (United States)

^b University of Georgia   (United States)

Author keywords

Drosophila; Glycosylation; N linked; O linked

Indexed keywords

FUCOSYLTRANSFERASE; GALACTOSYLTRANSFERASE; GLUCOSYLTRANSFERASE; GLYCAN; GLYCOPROTEIN; N ACETYL BETA GLUCOSAMINIDASE; NOTCH RECEPTOR;

ARTICLE; CARBOHYDRATE ANALYSIS; DROSOPHILA; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; FERTILITY; FUCOSYLATION; GENE MUTATION; GLYCOBIOLOGY; GOLGI COMPLEX; INSECT GENOME; MORPHOGENESIS; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

ANIMALS; DROSOPHILA MELANOGASTER; GLYCOMICS; GLYCOPROTEINS; GLYCOSYLATION; MUTATION; POLYSACCHARIDES; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 84872712215     PISSN: 02820080     EISSN: 15734986     Source Type: Journal    
DOI: 10.1007/s10719-012-9442-x     Document Type: Article

References (105)

1. Lin, X.: Functions of heparan sulfate proteoglycans in cell signaling during development. Development 131(24), 6009-6021 (2004). doi: 10.1242/dev.01522
2. Selleck, S.B.: Genetic dissection of proteoglycan function in Drosophila and C. elegans. Semin. Cell Dev. Biol. 12(2), 127-134 (2001). doi: 10.1006/scdb.2000.0242
3. Chen, Y.W., Pedersen, J.W., Wandall, H.H., Levery, S.B., Pizette, S., Clausen, H., Cohen, S.M.: Glycosphingolipids with extended sugar chain have specialized functions in development and behavior of Drosophila. Dev. Biol. 306(2), 736-749 (2007). doi: 10.1016/j.ydbio.2007.04.013
4. Dahlgaard, K., Jung, A., Qvortrup, K., Clausen, H., Kjaerulff, O., Wandall, H.H.: Neurofibromatosis-like phenotype in Drosophila caused by lack of glucosylceramide extension. Proc. Natl. Acad. Sci. U. S. A. (2012). doi: 10.1073/pnas.1115453109
5. Muller, R., Altmann, F., Zhou, D., Hennet, T.: The Drosophila melanogaster brainiac protein is a glycolipid-specific beta 1,3 N-Acetylglucosaminyltransferase. J. Biol. Chem. 277(36), 32417-32420 (2002). doi: 10.1074/jbc.C200381200
6. Pizette, S., Rabouille, C., Cohen, S.M., Therond, P.: Glycosphingolipids control the extracellular gradient of the Drosophila EGFR ligand Gurken. Development 136(4), 551-561 (2009). doi: 10.1242/dev.031104
7. Schwientek, T., Keck, B., Levery, S.B., Jensen, M.A., Pedersen, J.W., Wandall, H.H., Stroud, M., Cohen, S.M., Amado, M., Clausen, H.: The Drosophila gene brainiac encodes a glycosyltransferase putatively involved in glycosphingolipid synthesis. J. Biol. Chem. 277(36), 32421-32429 (2002). doi: 10.1074/jbc.M206213200
8. Seppo, A., Moreland, M., Schweingruber, H., Tiemeyer, M.: Zwitterionic and acidic glycosphingolipids of the Drosophila melanogaster embryo. Eur. J. Biochem. FEBS 267(12), 3549-3558 (2000)
9. Seppo, A., Tiemeyer, M.: Function and structure of Drosophila glycans. Glycobiology 10(8), 751-760 (2000)
10. Stolz, A., Haines, N., Pich, A., Irvine, K.D., Hokke, C.H., Deelder, A.M., Gerardy-Schahn, R., Wuhrer, M., Bakker, H.: Distinct contributions of beta 4GalNAcTA and beta 4GalNAcTB to Drosophila glycosphingolipid biosynthesis. Glycoconj. J. 25(2), 167-175 (2008). doi: 10.1007/s10719-007-9069-5
11. Wandall, H.H., Pedersen, J.W., Park, C., Levery, S.B., Pizette, S., Cohen, S.M., Schwientek, T., Clausen, H.: Drosophila egghead encodes a beta 1,4-mannosyltransferase predicted to form the immediate precursor glycosphingolipid substrate for brainiac. J. Biol. Chem. 278(3), 1411-1414 (2003). doi: 10.1074/jbc.C200619200
12. Wandall, H.H., Pizette, S., Pedersen, J.W., Eichert, H., Levery, S.B., Mandel, U., Cohen, S.M., Clausen, H.: Egghead and brainiac are essential for glycosphingolipid biosynthesis in vivo. J. Biol. Chem. 280(6), 4858-4863 (2005). doi: 10.1074/jbc.C400571200
13. 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. CMLS 68(20), 3377-3384 (2011). doi: 10.1007/s00018-011-0640-7
14. 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). doi: 10.1074/jbc.M110.155192
15. Aoki, K., Perlman, M., Lim, J.M., Cantu, R., Wells, L., Tiemeyer, M.: Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J. Biol. Chem. 282(12), 9127-9142 (2007). doi: 10.1074/jbc.M606711200
16. Aoki, K., Tiemeyer, M.: The glycomics of glycan glucuronylation in Drosophila melanogaster. Methods Enzymol. 480, 297-321 (2010). doi: 10.1016/S0076-6879(10)80014-X
17. North, S.J., Koles, K., Hembd, C., Morris, H.R., Dell, A., Panin, V.M., Haslam, S.M.: Glycomic studies of Drosophila melanogaster embryos. Glycoconj. J. 23(5-6), 345-354 (2006). doi: 10.1007/s10719-006-6693-4
18. ten Hagen, K.G., Zhang, L., Tian, E., Zhang, Y.: Glycobiology on the fly: developmental and mechanistic insights from Drosophila. Glycobiology 19(2), 102-111 (2009). doi: 10.1093/glycob/cwn096
19. Helenius, A., Aebi, M.: Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049 (2004). doi: 10.1146/annurev. biochem.73.011303.073752
20. Helenius, A., Aebi, M.: Intracellular functions of N-linked glycans. Science 291(5512), 2364-2369 (2001)
21. Hargrave, P.A.: The amino-terminal tryptic peptide of bovine rhodopsin. A glycopeptide containing two sites of oligosaccharide attachment. Biochim. Biophys. Acta. 492(1), 83-94 (1977)
22. Murray, A.R., Fliesler, S.J., Al-Ubaidi, M.R.: Rhodopsin: the functional significance of asn-linked glycosylation and other post-translational modifications. Ophthalmic Genet 30(3), 109-120 (2009). doi: 10.1080/ 13816810902962405
23. Dryja, T.P., Li, T.: Molecular genetics of retinitis pigmentosa. Hum. Mol. Genet 4, 1739-1743 (1995)
24. Webel, R., Menon, I., O'Tousa, J.E., Colley, N.J.: Role of asparagine-linked oligosaccharides in rhodopsin maturation and association with its molecular chaperone, NinaA. J. Biol. Chem. 275(32), 24752-24759 (2000). doi: 10.1074/jbc.M002668200
25. Katanosaka, K., Tokunaga, F., Kawamura, S., Ozaki, K.: N-linked glycosylation of Drosophila rhodopsin occurs exclusively in the amino-teminal domain and function in rhodopsin maturation. FEBS Lett. 424, 149-154 (1998)
26. Satoh, A., Tokunaga, F., Kawamura, S., Ozaki, K.: In situ inhibition of vesicle transport and protein processing in the dominant negative Rab1 mutant of Drosophila. J. Cell Sci. 110(Pt 23), 2943-2953 (1997)
27. Cao, J., Li, Y., Xia, W., Reddig, K., Hu, W., Xie, W., Li, H.S., Han, J.: A Drosophila metallophosphoesterase mediates deglycosylation of rhodopsin. EMBO J. 30(18), 3701-3713 (2011). doi: 10.1038/emboj.2011.254
28. Suzuki, T., Park, H., Hollingsworth, N.M., Sternglanz, R., Lennarz, W.J.: PNG1, a yeast gene encoding a highly conserved peptide:N-glycanase. J. Cell Biol. 149(5), 1039-1052 (2000)
29. Suzuki, T.: Cytoplasmic peptide:N-glycanase and catabolic pathway for free N-glycans in the cytosol. Semin Cell Dev. Biol. 18(6), 762-769 (2007). doi: 10.1016/j.semcdb.2007.09.010
30. Spiro, R.G.: Role of N-linked polymannose oligosaccharides in targeting glycoproteins for endoplasmic reticulum-Associated degradation. Cell Mol Life Sci, CMLS 61(9), 1025-1041 (2004). doi: 10.1007/s00018-004-4037-8
31. Altrich-VanLith, M.L., Ostankovitch, M., Polefrone, J.M., Mosse, C.A., Shabanowitz, J., Hunt, D.F., Engelhard, V.H.: Processing of a class I-restricted epitope from tyrosinase requieres peptide N-glycanase and the cooperative action of endoplasmic reticulum aminopeptidase 1 and cytosolic protease. J. Immunol. (2006).
32. Kario, E., Tirosh, B., Ploegh, H.L., Navon, A.: N-linked glycosylation does not impair proteasomal degradation but affects class I major histocompatibility complex presentation. J. Biol. Chem. 283(1), 244-254 (2008). doi: 10.1074/jbc.M706237200
33. Funakoshi, Y., Negishi, Y., Gengen, J.P., Seino, J., Ishii, K., Lennarz, W.J., Matsuo, I., Ito, Y., Taniguchi, N., Suzuki, T.: Evidence for an Essential Deglycosylation-Independent Activity of PNGase in Drosophila melanogaster. PLoS One 5(5), e10545 (2010). doi: 10.1371/journal.pone.0010545.g001
34. Leonard, R., Rendic, D., Rabouille, C., Wilson, I.B., Preat, T., Altmann, F.: The Drosophila fused lobes gene encodes an N-Acetylglucosaminidase involved in N-glycan processing. J. Biol. Chem. 281(8), 4867-4875 (2006). doi: 10.1074/jbc.M511023200
35. Geisler, C., Aumiller, J.J., Jarvis, D.L.: A fused lobes gene encodes the processing beta-N-Acetylglucosaminidase in Sf9 cells. J. Biol. Chem. 283(17), 11330-11339 (2008). doi: 10.1074/jbc.M710279200
36. Boquet, I., Hitier, R., Dumas, M., Chaminade, M., Preat, T.: Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. J. Neurobiol. 42(1), 33-48 (2000)
37. Sarkar, M., Leventis, P.A., Silvescu, C.I., Reinhold, V.N., Schachter, H., Boulianne, G.L.: Null mutations in Drosophila N- Acetylglucosaminyltransferase I produce defects in locomotion and a reduced life span. J. Biol. Chem. 281(18), 12776-12785 (2006). doi: 10.1074/jbc.M512769200
38. Sarkar, M., Iliadi, K.G., Leventis, P.A., Schachter, H., Boulianne, G.L.: Neuronal expression of Mgat1 rescues the shortened life span of Drosophila Mgat11 null mutants and increases life span. Proc. Natl. Acad. Sci. U. S. A. 107(21), 9677-9682 (2010). doi: 10.1073/pnas.1004431107
39. Fredieu, J.R., Mahowald, A.P.: Glycoconjugate expression during Drosophila embryogenesis. Acta anatomica 149(2), 89-99 (1994)
40. Williams, P.J., Wormald, M.R., Dwek, R.A., Rademacher, T.W., Parker, G.F., Roberts, D.R.: Characterisation of oligosaccharides from Drosophila melanogaster glycoproteins. Biochim. Biophys. Acta 1075(2), 146-153 (1991)
41. Nakamura, Y., Haines, N., Chen, J., Okajima, T., Furukawa, K., Urano, T., Stanley, P., Irvine, K.D., Furukawa, K.: Identification of a Drosophila gene encoding xylosylprotein beta4-galactosyltransferase that is essential for the synthesis of glycosaminoglycans and for morphogenesis. J. Biol. Chem. 277(48), 46280-46288 (2002). doi: 10.1074/jbc.M203873200
42. Takemae, H., Ueda, R., Okubo, R., Nakato, H., Izumi, S., Saigo, K., Nishihara, S.: Proteoglycan UDP-galactose:beta-xylose beta 1,4- galactosyltransferase I is essential for viability in Drosophila melanogaster. J. Biol. Chem. 278(18), 15571-15578 (2003). doi: 10.1074/jbc.M301123200
43. Vadaie, N., Hulinsky, R.S., Jarvis, D.L.: Identification and characterization of a Drosophila melanogaster ortholog of human beta1,4-galactosyltransferase VII. Glycobiology 12(10), 589-597 (2002)
44. Haines, N., Irvine, K.D.: Functional analysis of Drosophila beta1,4-N-Acetlygalactosaminyltransferases. Glycobiology 15(4), 335-346 (2005). doi: 10.1093/glycob/cwi017
45. Sasaki, N., Yoshida, H., Fuwa, T.J., Kinoshita-Toyoda, A., Toyoda, H., Hirabayashi, Y., Ishida, H., Ueda, R., Nishihara, S.: Drosophila beta 1,4-N-Acetylgalactosaminyltransferase-A synthesizes the LacdiNAc structures on several glycoproteins and glycosphingolipids. Biochem. Biophys. Res. Commun. 354(2), 522-527 (2007). doi: 10.1016/j.bbrc.2007.01.015
46. Ramakrishnan, B., Qasba, P.K.: Role of a single amino acid in the evolution of glycans of invertebrates and vertebrates. J. Mol. Biol. 365(3), 570-576 (2007). doi: 10.1016/j.jmb.2006.10.034
47. Johswich, A., Kraft, B., Wuhrer, M., Berger, M., Deelder, A.M., Hokke, C.H., Gerardy-Schahn, R., Bakker, H.: Golgi targeting of Drosophila melanogaster beta4GalNAcTB requires a DHHC protein family-related protein as a pilot. J Cell Biol 184(1), 173-183 (2009). doi: 10.1083/jcb.200801071
48. Koles, K., Irvine, K.D., Panin, V.M.: Functional characterization of Drosophila sialyltransferase. J. Biol. Chem. 279(6), 4346-4357 (2004). doi: 10.1074/jbc.M309912200
49. Repnikova, E., Koles, K., Nakamura, M., Pitts, J., Li, H., Ambavane, A., Zoran, M.J., Panin, V.M.: Sialyltransferase regulates nervous system function in Drosophila. J. Neurosci. 30(18), 6466-6476 (2010). doi: 10.1523/JNEUROSCI.5253- 09.2010
50. Ripoche, J., Link, B., Yucel, J.K., Tokuyasu, K., Malhotra, V.: Location of Golgi membranes with reference to dividing nuclei in syncytial Drosophila embryos. Proc. Natl. Acad. Sci. U. S. A. 91(5), 1878-1882 (1994)
51. Yamamoto-Hino, M., Abe, M., Shibano, T., Setoguchi, Y., Awano, W., Ueda, R., Okano, H., Goto, S.: Cisterna-specific Localization of Glycosylation-related Proteins to the Golgi Apparatus. Cell. Struct. Funct. 37(1), 55-63 (2012)
52. Yano, H., Yamamoto-Hino, M., Abe, M., Kuwahara, R., Haraguchi, S., Kusaka, I., Awano, W., Kinoshita-Toyoda, A., Toyoda, H., Goto, S.: Distinct functional units of the Golgi complex in Drosophila cells. Proc. Natl. Acad. Sci. U. S. A. 102(38), 13467-13472 (2005). doi: 10.1073/pnas.0506681102
53. Yamamoto-Hino, M., Kanie, Y., Awano, W., Aoki-Kinoshita, K.F., Yano, H., Nishihara, S., Okano, H., Ueda, R., Kanie, O., Goto, S.: Identification of genes required for neural-specific glycosylation using functional genomics. PLoS Genet 6(12), e1001254 (2010). doi: 10.1371/journal.pgen.1001254
54. Baas, S., Sharrow, M., Kotu, V., Middleton, M., Nguyen, K., Flanagan-Steet, H., Aoki, K., Tiemeyer, M.: Sugar-free frosting, a homolog of SAD kinase, drives neural-specific glycan expression in the Drosophila embryo. Development 138(3), 553-563 (2011). doi: 10.1242/dev.055376
55. Farhan, H., Wendeler, M.W., Mitrovic, S., Fava, E., Silberberg, Y., Sharan, R., Zerial, M., Hauri, H.P.: MAPK signaling to the early secretory pathway revealed by kinase/phosphatase functional screening. J. Cell Biol. 189(6), 997-1011 (2010). doi: 10.1083/jcb.200912082
56. Lowe, M., Rabouille, C., Nakamura, N., Watson, R., Jackman, M., Jamsa, E., Rahman, D., Pappin, D.J., Warren, G.: Cdc2 kinase directly phosphorylates the cis-Golgi matrix protein GM130 and is required for Golgi fragmentation in mitosis. Cell 94(6), 783-793 (1998)
57. Snow, P.M., Patel, N.H., Harrelson, A.L., Goodman, C.S.: Neural-specific carbohydrate moiety shared by many surface glycoproteins in Drosophila and grasshopper embryos. J. Neurosci. 7(12), 4137-4144 (1987)
58. Kramerov, A.A., Arbatsky, N.P., Rozovsky, Y.M., Mikhaleva, E.A., Polesskaya, O.O., Gvozdev, V.A., Shibaev, V.N.: Mucin-type glycoprotein from Drosophila melanogaster embryonic cells: characterization of carbohydrate component. FEBS Lett. 378(3), 213-218 (1996)
59. Kramerov, A.A., Mikhaleva, E.A., Rozovsky Ya, M., Pochechueva, T.V., Baikova, N.A., Arsenjeva, E.L., Gvozdev, V.A.: Insect mucin-type glycoprotein: immunodetection of the O-glycosylated epitope in Drosophila melanogaster cells and tissues. Insect Biochem. Mol. Biol. 27(6), 513-521 (1997)
60. Haines, N., Irvine, K.D.: Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4(10), 786-797 (2003). doi: 10.1038/nrm1228
61. Theopold, U., Dorian, C., Schmidt, O.: Changes in glycosylation during Drosophila development. The influence of ecdysone on hemomucin isoforms. Insect Biochem. Mol. Biol. 31(2), 189-197 (2001)
62. Tian, E., Ten 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). doi: 10.1093/glycob/cwj051
63. Tian, E., Ten Hagen, K.G.: O-linked glycan expression during Drosophila development. Glycobiology 17(8), 820-827 (2007). doi: 10.1093/glycob/cwm056
64. Okajima, T., Xu, A., Irvine, K.D.: Modulation of notch-ligand binding by protein O-fucosyltransferase 1 and fringe. J. Biol. Chem. 278(43), 42340-42345 (2003). doi: 10.1074/jbc.M308687200
65. Haltiwanger, R.S., Stanley, P.: Modulation of receptor signaling by glycosylation: fringe is an O-fucose-beta1,3-N-Acetylglucosaminyltransferase. Biochim. Biophys. Acta 1573(3), 328-335 (2002)
66. 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., Vogt, T.F.: Fringe is a glycosyltransferase that modifies Notch. Nature 406(6794), 369-375 (2000). doi: 10.1038/35019000
67. 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). doi: 10.1074/jbc.M606268200
68. 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). doi: 10.1074/jbc.M111. 306159
69. Zhang, L., Zhang, Y., Hagen, K.G.: A mucin-type O-glycosyltransferase modulates cell adhesion during Drosophila development. J. Biol. Chem. 283(49), 34076-34086 (2008). doi: 10.1074/jbc.M804267200
70. Fakhro, K.A., Choi, M., Ware, S.M., Belmont, J.W., Towbin, J.A., Lifton, R.P., Khokha, M.K., Brueckner, M.: Rare copy number variations in congenital heart disease patients identify unique genes in left-right patterning. Proc. Natl. Acad. Sci. U. S. A. 108(7), 2915-2920 (2011). doi: 10.1073/pnas.1019645108
71. Guda, K., Moinova, H., He, J., Jamison, O., Ravi, L., Natale, L., Lutterbaugh, J., Lawrence, E., Lewis, S., Willson, J.K., Lowe, J.B., Wiesner, G.L., Parmigiani, G., Barnholtz-Sloan, J., Dawson, D.W., Velculescu, V.E., Kinzler, K.W., Papadopoulos, N., Vogelstein, B., Willis, J., Gerken, T.A., Markowitz, S.D.: Inactivating germ-line and somatic mutations in polypeptide N-Acetylgalactosaminyltransferase 12 in human colon cancers. Proc. Natl. Acad. Sci. U. S. A. 106(31), 12921-12925 (2009). doi: 10.1073/pnas.0901454106
72. Ichikawa, S., Guigonis, V., Imel, E.A., Courouble, M., Heissat, S., Henley, J.D., Sorenson, A.H., Petit, B., Lienhardt, A., Econs, M.J.: Novel GALNT3 mutations causing hyperostosis-hyperphosphatemia syndrome result in low intact fibroblast growth factor 23 concentrations. J. Clin. Endocrinol. Metab. 92(5), 1943-1947 (2007). doi: 10.1210/jc.2006-1825
73. Ju, T., Cummings, R.D.: Protein glycosylation: chaperone mutation in Tn syndrome. Nature 437(7063), 1252 (2005). doi: 10.1038/4371252a
74. Kathiresan, S., Manning, A.K., Demissie, S., D'Agostino, R.B., Surti, A., Guiducci, C., Gianniny, L., Burtt, N.P., Melander, O., Orho-Melander, M., Arnett, D.K., Peloso, G.M., Ordovas, J.M., Cupples, L.A.: A genome-wide association study for blood lipid phenotypes in the Framingham Heart Study. BMC Med. Genet. 8(Suppl 1), S17 (2007). doi: 10.1186/1471-2350-8-S1-S17
75. Topaz, O., Shurman, D.L., Bergman, R., Indelman, M., Ratajczak, P., Mizrachi, M., Khamaysi, Z., Behar, D., Petronius, D., Friedman, V., Zelikovic, I., Raimer, S., Metzker, A., Richard, G., Sprecher, E.: Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat. Genet. 36(6), 579-581 (2004). doi: 10.1038/ng1358
76. Okajima, T., Reddy, B., Matsuda, T., Irvine, K.D.: Contributions of chaperone and glycosyltransferase activities of O-fucosyltransferase 1 to Notch signaling. BMC Biol. 6, 1 (2008). doi: 10.1186/1741-7007-6-1
77. Sasamura, T., Ishikawa, H.O., Sasaki, N., Higashi, S., Kanai, M., Nakao, S., Ayukawa, T., Aigaki, T., Noda, K., Miyoshi, E., Taniguchi, N., Matsuno, K.: 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). doi: 10.1242/dev.02811
78. 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). doi: 10.1074/jbc.M804925200
79. Ishikawa, H.O., Ayukawa, T., Nakayama, M., Higashi, S., Kamiyama, S., Nishihara, S., Aoki, K., Ishida, N., Sanai, Y., Matsuno, K.: Two pathways for importing GDP-fucose into the endoplasmic reticulum lumen function redundantly in the O-fucosylation of Notch in Drosophila. J. Biol. Chem. 285(6), 4122-4129 (2010). doi: 10.1074/jbc.M109.016964
80. Ishikawa, H.O., Higashi, S., Ayukawa, T., Sasamura, T., Kitagawa, M., Harigaya, K., Aoki, K., Ishida, N., Sanai, Y., Matsuno, K.: Notch deficiency implicated in the pathogenesis of congenital disorder of glycosylation IIc. Proc. Natl. Acad. Sci. U. S. A. 102(51), 18532-18537 (2005). doi: 10.1073/pnas.0504115102
81. Yamakawa, T., Ayukawa, T., Matsuno, K.: Metabolism and transportation pathways of GDP-fucose that are required for the O-fucosylation of Notch. Adv. Exp. Med. Biol. 727, 37-46 (2012). doi: 10.1007/978-1-4614-0899-4-3
82. Lubke, T., Marquardt, T., Etzioni, A., Hartmann, E., von Figura, K., Korner, C.: Complementation cloning identifies CDG-IIc, a new type of congenital disorders of glycosylation, as a GDP-fucose transporter deficiency. Nat. Genet. 28(1), 73-76 (2001). doi: 10.1038/88299
83. Luhn, K., Wild, M.K., Eckhardt, M., Gerardy-Schahn, R., Vestweber, D.: The gene defective in leukocyte adhesion deficiency II encodes a putative GDP-fucose transporter. Nat. Genet. 28(1), 69-72 (2001). doi: 10.1038/88289
84. Stanley, P., Okajima, T.: Roles of glycosylation in Notch signaling. Curr. Top. Dev. Biol. 92, 131-164 (2010). doi: 10.1016/S0070-2153(10)92004-8
85. 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). doi: 10.1016/j.cell.2007.12.016
86. 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(5), 583-589 (2011). doi: 10.1016/j.sbi.2011.08.008
87. Takeuchi, h., Fernandez-Valdivia, R.C., Caswell, D.S., Nita-Lazar, A., Rana, N.A., Garner, T.P., Weldeghioeghis, T.K., Macnaughtan, M.A., Jafar-Nejad, H., Haltiwanger, R.S.: Rumi functions as both a protein O-glucosyltransferase and a protein O-xylosyltransferase. Proceedings of the National Academy of Sciences of the United States of America (2011). doi: 10.1073/pnas.1109696108/-/ DCSupplemental
88. 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(10), 1925-1934 (2011). doi: 10.1242/dev.060020
89. 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(3), 1582-1586 (2010). doi: 10.1074/jbc.C109.065409
90. 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(4), 2739-2748 (2012). doi: 10.1074/jbc.M111.302406
91. Matsuura, A., Ito, M., Sakaidani, Y., Kondo, T., Murakami, K., Furukawa, K., Nadano, D., Matsuda, T., Okajima, T.: O-linked N-Acetylglucosamine is present on the extracellular domain of notch receptors. J. Biol. Chem. 283(51), 35486-35495 (2008). doi: 10.1074/jbc.M806202200
92. Sakaidani, Y., Ichiyanagi, N., Saito, C., Nomura, T., Ito, M., Nishio, Y., Nadano, D., Matsuda, T., Furukawa, K., Okajima, T.: O-linked-N- Acetylglucosamine modification of mammalian Notch receptors by an atypical O-GlcNAc transferase Eogt1. Biochem. Biophys. Res. Commun. 419(1), 14-19 (2012). doi: 10.1016/j.bbrc.2012.01.098
93. 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). doi: 10.1146/annurev-biochem-060608-102511
94. Kreppel, L.K., Blomberg, M.A., Hart, G.W.: Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 272(14), 9308-9315 (1997)
95. 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. Comm. 2, 583 (2011). doi: 10.1038/ncomms1591
96. 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). doi: 10.1091/mbc.E07-01-0047
97. 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). doi: 10.1534/genetics.105.049650
98. 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). doi: 10.1093/glycob/cwp189
99. Barresi, R., Campbell, K.P.: Dystroglycan: from biosynthesis to pathogenesis of human disease. J. Cell Sci. 119(Pt 2), 199-207 (2006). doi: 10.1242/jcs.02814
100. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S.H., Davis, S., Kunz, S., Madson, M., Oldstone, M.B., Schachter, H., Wells, L., Campbell, K.P.: O-mannosyl phosphorylation of alpha-dystroglycan is required for laminin binding. Science 327(5961), 88-92 (2010). doi: 10.1126/science.1180512
101. Dino, M.R., Harroch, S., Hockfield, S., Matthews, R.T.: Monoclonal antibody Cat-315 detects a glycoform of receptor protein tyrosine phosphatase beta/phosphacan early in CNS development that localizes to extrasynaptic sites prior to synapse formation. Neuroscience 142(4), 1055-1069 (2006). doi: 10.1016/j.neuroscience.2006.07.054
102. Stalnaker, S.H., Aoki, K., Lim, J.M., Porterfield, M., Liu, M., Satz, J.S., Buskirk, S., Xiong, Y., Zhang, P., Campbell, K.P., Hu, H., Live, D., Tiemeyer, M., Wells, L.: Glycomic analyses of mouse models of congenital muscular dystrophy. J. Biol. Chem. 286(24), 21180-21190 (2011). doi: 10.1074/jbc.M110.203281
103. Kozma, K., Keusch, J.J., Hegemann, B., Luther, K.B., Klein, D., Hess, D., Haltiwanger, R.S., Hofsteenge, J.: Identification and characterization of abeta1,3-glucosyltransferase that synthesizes the Glc-beta1,3-Fuc disaccharide on thrombospondin type 1 repeats. J. Biol. Chem. 281(48), 36742-36751 (2006). doi: 10.1074/jbc.M605912200
104. 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). doi: 10.1074/jbc.M511975200
105. Hess, D., Keusch, J.J., Oberstein, S.A., Hennekam, R.C., Hofsteenge, J.: Peters Plus syndrome is a new congenital disorder of glycosylation and involves defective Omicron-glycosylation of thrombospondin type 1 repeats. J. Biol. Chem. 283(12), 7354-7360 (2008). doi: 10.1074/jbc.M710251200