The EGF Repeat-Specific O-GlcNAc-Transferase Eogt Interacts with Notch Signaling and Pyrimidine Metabolism Pathways in Drosophila

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Müller, Reto ^a   Jenny, Andreas ^a   Stanley, Pamela ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; NOTCH RECEPTOR; PROTEIN DUMPY; PROTEIN EOGT; PROTEIN OGT; PYRIMIDINE; TRANSFERASE; UNCLASSIFIED DRUG; URACIL;

AMINO ACID SYNTHESIS; ANIMAL CELL; ARTHROPOD LARVA; ARTICLE; BLISTER; CATABOLISM; CELL METABOLISM; CONTROLLED STUDY; CYTOSOL; DROSOPHILA MELANOGASTER; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; GENE INTERACTION; GENE MUTATION; GENE SILENCING; HETEROZYGOSITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PYRIMIDINE METABOLISM; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; BLOTTING, WESTERN; CELL LINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE KNOCKDOWN TECHNIQUES; GENETIC COMPLEMENTATION TEST; HEK293 CELLS; HUMANS; LARVA; MOLECULAR SEQUENCE DATA; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROTEIN BINDING; PYRIMIDINES; RECEPTORS, NOTCH; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; URACIL; WING;

EID: 84877343228     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0062835     Document Type: Article

References (69)

1. Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P, et al. (2009) Essentials of Glycobiology; Varki A, Cummings RD, Esko JD, Freeze HH, Stanley P et al., editors. New York: Cold Spring Harbor laboratory Press.
2. Moloney DJ, Panin VM, Johnston SH, Chen J, Shao L, et al. (2000) Fringe is a glycosyltransferase that modifies Notch. Nature 406: 369-375.
3. Bruckner K, Perez L, Clausen H, Cohen S, (2000) Glycosyltransferase activity of Fringe modulates Notch-Delta interactions. Nature 406: 411-415.
4. Irvine KD, (1999) Fringe, Notch, and making developmental boundaries. Curr Opin Genet Dev 9: 434-441.
5. Stanley P, Okajima T, (2010) Roles of glycosylation in Notch signaling. Curr Top Dev Biol 92: 131-164.
6. Butkinaree C, Park K, Hart GW, (2010) O-linked beta-N-acetylglucosamine (O-GlcNAc): Extensive crosstalk with phosphorylation to regulate signaling and transcription in response to nutrients and stress. Biochim Biophys Acta 1800: 96-106.
7. Hanover JA, Krause MW, Love DC, (2012) Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nat Rev Mol Cell Biol 13: 312-321.
8. Hart GW, Housley MP, Slawson C, (2007) Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins. Nature 446: 1017-1022.
9. Gambetta MC, Oktaba K, Muller J, (2009) Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science 325: 93-96.
10. Matsuura A, Ito M, Sakaidani Y, Kondo T, Murakami K, et al. (2008) O-linked N-acetylglucosamine is present on the extracellular domain of notch receptors. J Biol Chem 283: 35486-35495.
11. Sakaidani Y, Nomura T, Matsuura A, Ito M, Suzuki E, et al. (2011) O-linked-N-acetylglucosamine on extracellular protein domains mediates epithelial cell-matrix interactions. Nat Commun 2: 583.
12. Alfaro JF, Gong CX, Monroe ME, Aldrich JT, Clauss TR, et al. (2012) 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: 7280-7285.
13. Wilkin MB, Becker MN, Mulvey D, Phan I, Chao A, et al. (2000) Drosophila dumpy is a gigantic extracellular protein required to maintain tension at epidermal-cuticle attachment sites. Curr Biol 10: 559-567.
14. Carmon A, Guertin MJ, Grushko O, Marshall B, MacIntyre R, (2010) A molecular analysis of mutations at the complex dumpy locus in Drosophila melanogaster. PLoS One 5: e12319.
15. Carmon A, Topbas F, Baron M, MacIntyre RJ, (2010) dumpy interacts with a large number of genes in the developing wing of Drosophila melanogaster. Fly (Austin) 4: 117-127.
16. Bokel C, Prokop A, Brown NH, (2005) Papillote and Piopio: Drosophila ZP-domain proteins required for cell adhesion to the apical extracellular matrix and microtubule organization. J Cell Sci 118: 633-642.
17. Kjer T, (1987) The physiological effects of dumpy mutations on de-novo pyrimidine synthesis in Drosophila melanogaster. Hereditas 107: 213-217.
18. Blass DH, Hunt DM, (1980) Pyrimidine biosynthesis in the dumpy mutants of Drosophila melanogaster. Mol Gen Genet 178: 437-442.
19. Stroman P, (1974) Pyrimidine-sensitive drosophila wing mutants: withered (whd), tilt (tt) and dumpy (dp). Hereditas 78: 157-168.
20. Muller R, Jenny A, Stanley P, (2009) An ancient,putative glycosyltransferase is essential for viability of Drosophila melanogaster. Glycobiology 19: 1337.
21. Sakaidani Y, Ichiyanagi N, Saito C, Nomura T, Ito M, et al. (2012) O-linked-N-acetylglucosamine modification of mammalian Notch receptors by an atypical O-GlcNAc transferase Eogt1. Biochem Biophys Res Commun 419: 14-19.
22. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
23. Comer FI, Vosseller K, Wells L, Accavitti MA, Hart GW, (2001) Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine. Anal Biochem 293: 169-177.
24. Ramakrishnan B, Boeggeman E, Ramasamy V, Qasba PK, (2004) Structure and catalytic cycle of beta-1,4-galactosyltransferase. Curr Opin Struct Biol 14: 593-600.
25. Breton C, Bettler E, Joziasse DH, Geremia RA, Imberty A, (1998) Sequence-function relationships of prokaryotic and eukaryotic galactosyltransferases. J Biochem 123: 1000-1009.
26. Prout M, Damania Z, Soong J, Fristrom D, Fristrom JW, (1997) Autosomal mutations affecting adhesion between wing surfaces in Drosophila melanogaster. Genetics 146: 275-285.
27. Hutterer A, Knoblich JA, (2005) Numb and alpha-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep 6: 836-842.
28. Walsh EP, Brown NH, (1998) A screen to identify Drosophila genes required for integrin-mediated adhesion. Genetics 150: 791-805.
29. Reed BH, Wilk R, Schock F, Lipshitz HD, (2004) Integrin-dependent apposition of Drosophila extraembryonic membranes promotes morphogenesis and prevents anoikis. Curr Biol 14: 372-380.
30. Martin D, Zusman S, Li X, Williams EL, Khare N, et al. (1999) wing blister, a new Drosophila laminin alpha chain required for cell adhesion and migration during embryonic and imaginal development. J Cell Biol 145: 191-201.
31. Ise H, Kobayashi S, Goto M, Sato T, Kawakubo M, et al. (2010) Vimentin and desmin possess GlcNAc-binding lectin-like properties on cell surfaces. Glycobiology 20: 843-864.
32. Wodarz A, Hinz U, Engelbert M, Knust E, (1995) Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 82: 67-76.
33. Herranz H, Stamataki E, Feiguin F, Milan M, (2006) Self-refinement of Notch activity through the transmembrane protein Crumbs: modulation of gamma-secretase activity. EMBO Rep 7: 297-302.
34. Mahoney MB, Parks AL, Ruddy DA, Tiong SY, Esengil H, et al. (2006) Presenilin-based genetic screens in Drosophila melanogaster identify novel notch pathway modifiers. Genetics 172: 2309-2324.
35. Okajima T, Irvine KD, (2002) Regulation of notch signaling by o-linked fucose. Cell 111: 893-904.
36. Acar M, Jafar-Nejad H, Takeuchi H, Rajan A, Ibrani D, et al. (2008) Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell 132: 247-258.
37. Hartley DA, Xu TA, Artavanis-Tsakonas S, (1987) The embryonic expression of the Notch locus of Drosophila melanogaster and the implications of point mutations in the extracellular EGF-like domain of the predicted protein. EMBO J 6: 3407-3417.
38. Kelley MR, Kidd S, Deutsch WA, Young MW, (1987) Mutations altering the structure of epidermal growth factor-like coding sequences at the Drosophila Notch locus. Cell 51: 539-548.
39. Li Y, Lei L, Irvine KD, Baker NE, (2003) Notch activity in neural cells triggered by a mutant allele with altered glycosylation. Development 130: 2829-2840.
40. de Celis JF, Garcia-Bellido A, (1994) Modifications of the notch function by Abruptex mutations in Drosophila melanogaster. Genetics 136: 183-194.
41. Groth AC, Fish M, Nusse R, Calos MP, (2004) Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166: 1775-1782.
42. Kopan R, (1999) All good things must come to an end: how is Notch signaling turned off? Sci STKE 1999: PE1.
43. Rizki RM, Rizki TM, (1965) Morphogenetic effects of 6-azauracil and 6-azauridine. Science 150: 222-223.
44. Simmons AJ, Rawls JM, Piskur J, Davidson JN, (1999) A mutation that uncouples allosteric regulation of carbamyl phosphate synthetase in Drosophila. J Mol Biol 287: 277-285.
45. Piskur J, Kolbak D, Sondergaard L, Pedersen MB, (1993) The dominant mutation Suppressor of black indicates that de novo pyrimidine biosynthesis is involved in the Drosophila tan pigmentation pathway. Mol Gen Genet 241: 335-340.
46. Wojcik E, Murphy AM, Fares H, Dang-Vu K, Tsubota SI, (1994) Enhancer of rudimentaryp1, e(r)p1, a highly conserved enhancer of the rudimentary gene. Genetics 138: 1163-1170.
47. Clynes MM, Duke EJ, (1976) Developmental effects of inhibitors of nucleotide metabolism in Drosophila. J Insect Physiol 22: 1709-1715.
48. Rawls JM Jr, (2006) Analysis of pyrimidine catabolism in Drosophila melanogaster using epistatic interactions with mutations of pyrimidine biosynthesis and beta-alanine metabolism. Genetics 172: 1665-1674.
49. Meyer V, Oliver B, Pauli D, (1998) Multiple developmental requirements of noisette, the Drosophila homolog of the U2 snRNP-associated polypeptide SP3a60. Mol Cell Biol 18: 1835-1843.
50. Morris DH, Dubnau J, Park JH, Rawls JM Jr, (2012) Divergent functions through alternative splicing: the Drosophila CRMP gene in pyrimidine metabolism, brain, and behavior. Genetics 191: 1227-1238.
51. Borycz J, Borycz JA, Edwards TN, Boulianne GL, Meinertzhagen IA, (2012) The metabolism of histamine in the Drosophila optic lobe involves an ommatidial pathway: beta-alanine recycles through the retina. J Exp Biol 215: 1399-1411.
52. Phillips AM, Smart R, Strauss R, Brembs B, Kelly LE, (2005) The Drosophila black enigma: the molecular and behavioural characterization of the black1 mutant allele. Gene 351: 131-142.
53. Thierry-Mieg D, Thierry-Mieg J (2006) AceView: a comprehensive cDNA-supported gene and transcripts annotation. Genome Biol 7 Suppl 1: S12 11-14.
54. Tepass U, Theres C, Knust E, (1990) crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61: 787-799.
55. Stroman P, Bahn E, Norby S, Sick K, (1973) 6-Azauracil induced phenocopies of rudimentary wing mutants and their suppression by a suppressor mutant of rudimentary in Drosophila melanogaster. Hereditas 73: 239-246.
56. Waddington CH, (1941) The Genetic Control of Wing Development in Drosophila. J Genet 41: 75-139.
57. Fausto-Sterling A, (1977) Studies on the female sterile mutant rudimentary of Drosophila melanogaster. II. An analysis of aspartate transcarbamylase and dihydroorotase activities in wild-type and rudimentary strains. Biochem Genet 15: 803-815.
58. Carey FG, Wyatt GR, (1960) Uridine diphosphate derivatives in the tissues and hemolymph of insects. Biochim Biophys Acta 41: 178-179.
59. Shaheen R, Aglan M, Keppler-Noreuil K, Faqeih E, Ansari S, et al. (2013) Mutations in EOGT Confirm the Genetic Heterogeneity of Autosomal-Recessive Adams-Oliver Syndrome. Am J Hum Genet in press.
60. Hassed SJ, Wiley GB, Wang S, Lee JY, Li S, et al. (2012) RBPJ mutations identified in two families affected by Adams-Oliver syndrome. Am J Hum Genet 91: 391-395.
61. Tsubota SI, Vogel AC, Phillips AC, Ibach SM, Weber NK, et al. (2011) Interactions between enhancer of rudimentary and Notch and deltex reveal a regulatory function of enhancer of rudimentary in the Notch signaling pathway in Drosophila melanogaster. Fly (Austin) 5.
62. Smyk A, Szuminska M, Uniewicz KA, Graves LM, Kozlowski P, (2006) Human enhancer of rudimentary is a molecular partner of PDIP46/SKAR, a protein interacting with DNA polymerase delta and S6K1 and regulating cell growth. FEBS J 273: 4728-4741.
63. Thorig GE, Heinstra PW, de Ruiter BL, Scharloo W, (1987) The effects of recessive lethal Notch mutations of Drosophila melanogaster on flavoprotein enzyme activities whose inhibitions cause Notch-like phenocopies. Biochem Genet 25: 7-25.
64. Cavener DR, (1987) Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15: 1353-1361.
65. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
66. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
67. Ho SN, Hunt HD, Horton RM, Pullen JK, Pease LR, (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77: 51-59.
68. Halfon MS, Gisselbrecht S, Lu J, Estrada B, Keshishian H, et al. (2002) New fluorescent protein reporters for use with the Drosophila Gal4 expression system and for vital detection of balancer chromosomes. Genesis 34: 135-138.
69. Leonardi J, Fernandez-Valdivia R, Li YD, Simcox AA, Jafar-Nejad H, (2011) Multiple O-glucosylation sites on Notch function as a buffer against temperature-dependent loss of signaling. Development 138: 3569-3578.