Insight into the Regulation of Glycan Synthesis in Drosophila Chaoptin Based on Mass Spectrometry

PLoS ONE

Volumn 4, Issue 5, 2009, Pages

  Kanie, Yoshimi ^a   Yamamoto Hino, Miki ^a   Karino, Yayoi ^b   Yokozawa, Hiroki ^b   Nishihara, Shoko ^c   Ueda, Ryu ^d   Goto, Satoshi ^a   Kanie, Osamu ^a  

^a MITSUBISHI KAGAKU INSTITUTE OF LIFE SCIENCES   (Japan)

^b MITSUBISHI CHEMICAL CORPORATION   (Japan)

^c SOKA UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF GENETICS   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

POLYSACCHARIDE;

ANIMAL; ARTICLE; BIOSYNTHESIS; CHEMISTRY; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GLYCOSYLATION; MASS SPECTROMETRY; METABOLISM; METHODOLOGY; PROTEIN CONFORMATION;

ANIMALS; DROSOPHILA MELANOGASTER; GENE EXPRESSION REGULATION; GLYCOSYLATION; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; POLYSACCHARIDES; PROTEIN CONFORMATION;

EID: 67649808100     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005434     Document Type: Article

References (51)

1. Reinke R, Krantz DE, Yen D, Zipursky SL, (1988) Chaoptin, a cell surface glycoprotein required for Drosophila photoreceptor cell morphogenesis, contains a repeat motif found in yeast and human. Cell 52: 291-301.
2. Krantz DE, Zipursky SL, (1990) Drosophila chaoptin, a member of the leucine-rich repeat family, is a photoreceptor cell-specific adhesion molecule. EMBO 9: 1969-1977.
3. Pollock JA, Ellisman MH, Benzer S, (1990) Subcellular localization of transcripts in Drosophila photoreceptor neurons: chaoptic mutants have an aberrant distribution. Genes Dev 4: 806-821.
4. Zelhof AC, Hardy RW, Ann B, Zuker CS, (2006) Transforming the architecture of compound eyes. Nature 443: 696-699.
5. Van Vactor DJ, Krantz DE, Reinke R, Zipursky SL, (1998) Analysis of mutants in chaoptin, a photoreceptor cell-specific glycoprotein in Drosophila, reveals its role in cellular morphogenesis. Cell 52: 281-290.
6. Yamawaki-Takaoka Y, Tamaoki T, Choe HR, Tanaka H, Takaoka T, (1989) Adenylate cyclases in yeast: A comparison of the genes from Schizosaccharomyces pombe and Saccharomyces cerevisiae. Proc Natl Acad Sci USA 86: 5693-5697.
7. Krantz DD, Zidovetzki R, Kagan BL, Zipursky SL, (1991) Amphipathic β structure of a leucine-rich repeat peptide. J Biol Chem 266: 16801-16807.
8. Kajava AV, Vassart G, Wodak SJ, (1995) Modeling of the three-dimensional structure of proteins with the typical leucine-rich repeats. Structure 3: 867-877.
9. Kobe B, Kajava AV, (2001) The leucine-rich repeat as a protein recognition motif. Curr Opin Struct Biol 11: 725-732.
10. Gay NJ, Packman LC, Weldon MA, Barna JC, (1991) A leucine-rich repeat peptide derived from the Drosophila Toll receptor forms extended filaments with a β-sheet structure. FEBS 291: 87-91.
11. Hirai-Fujita Y, Yamamoto-Hino M, Kanie O, Goto S, (2008) N-Glycosylation of Drosophila neural protein, chaoptin, is essential for its stability, cell surface transport and adhesive activity. FEBS Lett 582: 2572-2576.
12. Cumming DA, (1991) Glycosylation of recombinant protein therapeutics: control and functional implications. Glycobiology 1: 115-130.
13. Lis H, Sharon N, (1993) Protein glycosylation. Structural and functional aspects. Eur J Biochem 218: 1-27.
14. Cointe D, Beliard R, Jorieux S, Leroy Y, Glacet A, et al.(2000) Unusual N-glycosylation of a recombinant human erythropoietin expressed in a human lymphoblastoid cell line does not alter its biological properties. Glycobiology 10: 511-519.
15. Branza-Nichita N, Negroiu G, Petrescu AJ, Garman EF, Platt FM, et al.(2000) Mutations at critical N-glycosylation sites reduce tyrosinase activity by altering folding and quality control. J Biol Chem 275: 8169-8175.
16. Walsh G, Jefferis R, (2006) Post-translational modifications in the context of therapeutic proteins. Nat Biotech 24: 1241-1252.
17. Wuher M, Catalina MI, Deelder AM, Hokke CH, (2007) Glycoproteomics based on tandem mass spectrometry of glycopeptides. J Chromatogr B 849: 115-128.
18. Dell A, Morris HR, (2001) Glycoprotein structure determination by mass spectrometry. Science 291: 2351-2356.
19. Wuher M, Hokke CH, Deelder AM, (2004) Glycopeptide analysis by matrix-assisted laser desorption/ionization tandem time-of-flight mass spectrometry reveals novel features of horseradish peroxidase glycosylation. Rapid Commun Mass Spectrom 18: 1741-1748.
20. Harazono A, Kawasaki N, Kawanishi T, Hayakawa T, (2005) Site-specific glycosylation analysis of human apolipoprotein B100 using LC/ESI MS/MS. Glycobiology 15: 447-462.
21. Bykova NV, Rampitsch C, Krokhin O, Standing KG, Ens W, (2006) Determination and characterization of site-specific N-glycosylation using MALDI-Qq-TOF tandem mass spectrometry: case study with a plant protease. Anal Chem 78: 1093-1103.
22. Lowe JB, Freeze H, (1999) Naturally occurring genetic disorders of glycosylation. In: Varki A, editors. Essentials of Glycobiology New York Cold Spring Harbor Laboratory Press pp. 486-487.
23. Wada Y, Tajiri M, Yoshida S, (2004) Hydrophilic affinity isolation and MALDI multiple-stage tandem mass spectrometry of glycopeptides for glycoproteomics. Anal Chem 76: 6560-6565.
24. Tanner S, Payne SH, Dasari S, Shen Z, Wilmarth PA, et al.(2008) Accurate annotation of peptide modifications through unrestrictive database search. J Proteome Res 7: 170-180.
25. Tarentino AL, Plummer TH, (1994) Enzymatic degradation of asparagine-linked glycans: purification, properties, and specificity of oligosaccharide-cleaving enzymes from Flavobacterium meningosepticum. Methods Enzymol 230: 44-57.
26. Rendić D, Linder A, Paschinger K, Borth N, Wilson IBH, et al.(2006) Modulation of neural carbohydrate epitope expression in Drosophila melanogaster cells. J Biol Chem 281: 3343-3353.
27. Wilson IBH, Harthill JE, Mullin NP, Ashford DA, Altmann F, (1998) Core α1,3-fucose is a key part of the epitope recognized by antibodies reacting against plant N-linked oligosaccharides and is present in a wide variety of plant extracts. Glycobiology 8: 651-661.
28. Yano H, Goto S, (2008) Spatial and temporal regulation of glycosylation during Drosophila eye development. Cell Tissue Res DOI 10.1007/s00441-009-0753-6.
29. Fabini G, Freilinger A, Altmann F, Wilson IBH, (2001) Identification of core α1,3-fucosylated glycans and cloning of the requisite fucosyltransferase cDNA from Drosophila melanogaster. J Biol Chem 276: 28058-28067.
30. Aoki K, Perlman M, Lim JM, Cantu R, Wells L, et al.(2007) Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J Biol Chem 282: 9127-9142.
31. Altmann F, Kornfeld G, Dalik T, Staudacher E, Glossl J, (1993) Processing of asparagine-linked oligosaccharides in insect cells. N-Acetylglucosaminyltransferase I and II activities in cultured lepidopteran cells. Glycobiology 3: 619-625.
32. Staudacher E, Marz L, (1998) Strict order of (Fuc to Asn-linked GlcNAc) fucosyltransferases forming core-difucosylated structure. Glycoconjugate J 15: 355-360.
33. Paschinger K, Staudacher E, Stemmer U, Fabini G, Wilson IBH, (2005) Fucosyltransferase substrate specificity and the order of fucosylation in invertebrates. Glycobiology 15: 463-474.
34. Choe J, Kelker MS, Wilson IA, (2005) Crystal structure of human Toll-like receptor 3 (TLR3) ectodomain. Science 309: 581-585.
35. Kolarich D, Altmann F, Sunderasan E, (2006) Structural analysis of the glycoprotein allergen Hev b 4 from natural rubber latex by mass spectrometry. Biochim Biophys Acta 1760: 715-720.
36. Wada Y, Azadi P, Costello CE, Dell A, Dwek RA, et al.(2007) Comparison of the methods for profiling glycoprotein glycans-HUPO human disease glycomics/proteome initiative multi-institutional study. Glycobiology 17: 411-422.
37. Nishihara S, Ueda R, Goto S, Toyoda H, Ishida H, et al.(2004) Approach for functional analysis of glycan using RNA interference. Glycoconjugate J 21: 63-68.
38. Hale JE, Butler JP, Knierman MD, Becker GW, (2000) Increased sensitivity of tryptic peptide detection by MALDI-TOF mass spectrometry is achieved by conversion of lysine to homoarginine. Anal Biochem 287: 110-117.
39. Tulsiani DRP, Hubbard SC, Robbins PW, Touster O, (1982) α-d-Mannosidases of rat liver Golgi membranes. J Biol Chem 257: 3660-3668.
40. Sarkar M, Leventis PA, Silvescu CI, Reinhold VN, Shachter H, et al.(2006) Null mutations in Drosophila N-acetylglucosaminyltransferase I produce defects in locomotion and a reduced life span. J Biol Chem 281: 12776-12785.
41. Chui D, Oh-Eda M, Liao Y, Panneerselvam K, Lai A, et al.(1997) Alpha-mannosidase-II deficiency results in dyserythropoiesis and unveils an alternate pathway in oligosaccharide biosynthesis. Cell 90: 157-167.
42. Helenius A, Aebi M, (2001) Intracellular functions of N-linked glycans. Science 291: 2364-2369.
43. Kleizen B, Braakman I, (2004) Protein folding and quality control in the endoplasmic reticulum. Curr Opin Cell Biol 16: 343-349.
44. Rosenbaum EE, Hardie RC, Colley NJ, (2005) Calnexin is essential for rhodopsin maturation. Ca2+ regulation and photoreceptor cell survival. Neuron 49: 229-241.
45. Ito Y, Hagihara S, Matsuo I, Totani K, (2005) Structural approaches to the study of oligosaccharides in glycoprotein quality control. Curr Opin Struct Biol 15: 481-489.
46. Fujita SC, Zipursky SL, Benzer S, Ferrus A, Shotwell SL, (1982) Monoclonal antibodies against the Drosophila nervous system. Proc Natl Acad Sci USA 79: 7929-7933.
47. Zipursky SL, Venkatesh TR, Teplow DB, Benzer S, (1984) Neuronal development in the Drosophila retina: monoclonal antibodies as molecular probes. Cell 36: 15-26.
48. Zipursky SL, Venkatesh TR, Benzer S, (1985) From monoclonal antibody to gene for a neuron specific glycoprotein in Drosophila. Proc Natl Acad Sci USA 82: 1855-1859.
49. Brancia FL, Oliver SG, Gaskell SJ, (2000) Improved matrix-assisted laser desorption/ionization mass spectrometric analysis of tryptic hydrolysates of proteins following guanidination of lysine-containing peptides. Rapid Commun Mass Spectrum 14: 2070-2073.
50. Hase S, Ikenaka T, Matsushima Y, (1978) Structure analysis of oligosaccharides by tagging of the reducing end sugars with a fluorescent compound. Biochem Biophys Res Commun 85: 257-263.
51. Hase S, Ikenaka T, (1990) Estimation of elution times on reversed-phase high-performance liquid chromatography of pyridylamino derivatives of sugar chains from glycoproteins. Anal Biochem 184: 135-138.