Multiple members of the UDP-GalNAc: Polypeptide N- acetylgalactosaminyltransferase family are essential for viability in Drosophila

Journal of Biological Chemistry

Volumn 287, Issue 8, 2012, Pages 5243-5252

  Tran, Duy T ^a   Zhang, Liping ^a   Zhang, Ying ^b   Tian, E ^a   Earl, Lesley A ^a   Ten Hagen, Kelly G ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIGESTIVE TRACT; EUKARYOTIC SPECIES; EXTRACELLULAR MATRICES; GLYCOSYL TRANSFERASE; IN-VIVO; O-GLYCOSYLATION; ORGAN SYSTEMS; POST-TRANSLATIONAL MODIFICATIONS; RNA INTERFERENCE; SPECIALIZED CELLS; TEMPORAL PATTERN; TRACHEAL SYSTEM;

CELL ADHESION; DIGESTIVE SYSTEM; ENZYMES; ESTERIFICATION; GENES; GLYCOSYLATION; HISTOLOGY; RNA;

TISSUE;

N ACETYLGALACTOSAMINYLTRANSFERASE;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DROSOPHILA; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; GENE TARGETING; MULTIGENE FAMILY; NONHUMAN; ORGANOGENESIS; PGANT GENE; PGANT4 GENE; PGANT5 GENE; PGANT7 GENE; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; RNA INTERFERENCE;

ANIMALS; CELL ADHESION; DIGESTIVE SYSTEM; DROSOPHILA MELANOGASTER; FEMALE; GLYCOSYLATION; HYDROGEN-ION CONCENTRATION; MALE; MUTATION; N-ACETYLGALACTOSAMINYLTRANSFERASES; ORGAN SPECIFICITY; OXYGEN; RNA INTERFERENCE; WING;

EID: 84863170130     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.306159     Document Type: Article

References (48)

1. Hart, G. W., and Copeland, R. J. (2010) Glycomics hits the big time. Cell 143, 672-676
2. Liu, L., Xu, Y. X., and Hirschberg, C. B. (2010) The role of nucleotide sugar transporters in development of eukaryotes. Semin. Cell Dev. Biol. 21, 600-608
3. Love, D. C., Krause, M. W., and Hanover, J. A. (2010) O-GlcNAc cycling. Emerging roles in development and epigenetics. Semin. Cell Dev. Biol. 21, 646-654
4. Nakamura, N., Lyalin, D., and Panin, V. M. (2010) Protein O-mannosylation in animal development and physiology. From human disorders to Drosophila phenotypes. Semin. Cell Dev. Biol. 21, 622-630
5. Schachter, H. (2010) Mgat1-dependent N-glycans are essential for the normal development of both vertebrate and invertebrate metazoans. Semin. Cell Dev. Biol. 21, 609-615
6. Tabak, L. A. (2010) The role of mucin-type O-glycans in eukaryotic development. Semin. Cell Dev. Biol. 21, 616-621
7. Takeuchi, H., and Haltiwanger, R. S. (2010) Role of glycosylation of Notch in development. Semin. Cell Dev. Biol. 21, 638-645
8. Kramer, K. L. (2010) Specific sides to multifaceted glycosaminoglycans are observed in embryonic development. Semin. Cell Dev. Biol. 21, 631-637
9. Kingsley, P. D., Hagen, K. G., Maltby, K. M., Zara, J., and Tabak, L. A. (2000) Diverse spatial expression patterns of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase family member mRNAs during mouse development. Glycobiology 10, 1317-1323 (Pubitemid 32124329)
10. Tian, E., and Ten Hagen, K. G. (2006) Expression of the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase family is spatially and temporally regulated during Drosophila development. Glycobiology 16, 83-95 (Pubitemid 43125965)
11. Tian, E., and Ten Hagen, K. G. (2007) O-Linked glycan expression during Drosophila development. Glycobiology 17, 820-827 (Pubitemid 47241819)
12. Tian, E., and Ten Hagen, K. G. (2009) Recent insights into the biological roles of mucin-type O-glycosylation. Glycoconj. J. 26, 325-334
13. Young, W. W., Jr., Holcomb, D. R., Ten Hagen, K. G., and Tabak, L. A. (2003) Expression of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase isoforms in murine tissues determined by real-time PCR. A new view of a large family. Glycobiology 13, 549-557 (Pubitemid 36850128)
14. Gerken, T. A., Ten Hagen, K. G., and Jamison, O. (2008) Conservation of peptide acceptor preferences between Drosophila and mammalian polypeptide-GalNAc-transferase ortholog pairs. Glycobiology 18, 861-870
15. Ten Hagen, K. G., Fritz, T. A., and Tabak, L. A. (2003) All in the family. The UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferases. Glycobiology 13, 1R-16R
16. Perrine, C. L., Ganguli, A., Wu, P., Bertozzi, C. R., Fritz, T. A., Raman, J., Tabak, L. A., and Gerken, T. A. (2009) Glycopeptide-preferring polypeptide GalNAc-transferase 10 (ppGalNAc T10), involved in mucin-type O-glycosylation, has a unique GalNAc-O-Ser/Thr-binding site in its catalytic domain not found in ppGalNAc T1 or T2. J. Biol. Chem. 284, 20387-20397
17. Ten Hagen, K. G., Tetaert, D., Hagen, F. K., Richet, C., Beres, T. M., Gagnon, J., Balys, M. M., VanWuyckhuyse, B., Bedi, G. S., Degand, P., and Tabak, L. A. (1999) Characterization of a UDP-GalNAc:polypeptide N- acetylgalactosaminyltransferase that displays glycopeptide N- acetylgalactosaminyltransferase activity. J. Biol. Chem. 274, 27867-27874
18. Ten Hagen, K. G., Tran, D. T., Gerken, T. A., Stein, D. S., and Zhang, Z. (2003) Functional characterization and expression analysis of members of the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase family from Drosophila melanogaster. J. Biol. Chem. 278, 35039-35048 (Pubitemid 37102265)
19. Ju, T., and Cummings, R. D. (2005) Protein glycosylation. Chaperone mutation in Tn syndrome. Nature 437, 1252 (Pubitemid 41568663)
20. Ichikawa, S., Guigonis, V., Imel, E. A., Courouble, M., Heissat, S., Henley, J. D., Sorenson, A. H., Petit, B., Lienhardt, A., and Econs, M. J. (2007) Novel GALNT3 mutations causing hyperostosis-hyperphosphatemia syndrome result in low intact fibroblast growth factor 23 concentrations. J. Clin. Endocrinol. Metab. 92, 1943-1947 (Pubitemid 46997214)
21. 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., and Sprecher, E. (2004) Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat. Genet. 36, 579-581 (Pubitemid 38715983)
22. 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., and Cupples, L. A. (2007) A genome-wide association study for blood lipid phenotypes in the Framingham Heart Study. BMC Med. Genet. 8, Suppl. 1, S17
23. Teslovich, T. M., Musunuru, K., Smith, A. V., Edmondson, A. C., Stylianou, I. M., Koseki, M., Pirruccello, J. P., Ripatti, S., Chasman, D. I., Willer, C. J., Johansen, C. T., Fouchier, S. W., Isaacs, A., Peloso, G. M., Barbalic, M., Ricketts, S. L., Bis, J. C., Aulchenko, Y. S., Thorleifsson, G., Feitosa, M. F., Chambers, J., Orho-Melander, M., Melander, O., Johnson, T., Li, X., Guo, X., Li, M., Shin Cho, Y., Jin Go, M., Jin Kim, Y., Lee, J. Y., Park, T., Kim, K., Sim, X., Twee-Hee Ong, R., Croteau-Chonka, D. C., Lange, L. A., Smith, J. D., Song, K., Hua Zhao, J., Yuan, X., Luan, J., Lamina, C., Ziegler, A., Zhang, W., Zee, R. Y., Wright, A. F., Witteman, J. C., Wilson, J. F., Willemsen, G., Wichmann, H. E., Whitfield, J. B., Waterworth, D. M., Wareham, N. J., Waeber, G., Vollenweider, P., Voight, B. F., Vitart, V., Uitterlinden, A. G., Uda, M., Tuomilehto, J., Thompson, J. R., Tanaka, T., Surakka, I., Stringham, H. M., Spector, T. D., Soranzo, N., Smit, J. H., Sinisalo, J., Silander, K., Sijbrands, E. J., Scuteri, A., Scott, J., Schlessinger, D., Sanna, S., Salomaa, V., Saharinen, J., Sabatti, C., Ruokonen, A., Rudan, I., Rose, L. M., Roberts, R., Rieder, M., Psaty, B. M., Pramstaller, P. P., Pichler, I., Perola, M., Penninx, B. W., Pedersen, N. L., Pattaro, C., Parker, A. N., Pare, G., Oostra, B. A., O'Donnell, C. J., Nieminen, M.S., Nickerson, D. A., Montgomery, G. W., Meitinger, T., McPherson, R., McCarthy, M. I., McArdle, W., Masson, D., Martin, N. G., Marroni, F., Mangino, M., Magnusson, P. K., Lucas, G., Luben, R., Loos, R. J., Lokki, M. L., Lettre, G., Langenberg, C., Launer, L. J., Lakatta, E. G., Laaksonen, R., Kyvik, K. O., Kronenberg, F., Konig, I. R., Khaw, K. T., Kaprio, J., Kaplan, L. M., Johansson, A., Jarvelin, M. R., Janssens, A. C., Ingelsson, E., Igl, W., Kees Hovingh, G., Hottenga, J. J., Hofman, A., Hicks, A. A., Hengstenberg, C., Heid, I. M., Hayward, C., Havulinna, A. S., Hastie, N. D., Harris, T. B., Haritunians, T., Hall, A. S., Gyllensten, U., Guiducci, C., Groop, L. C., Gonzalez, E., Gieger, C., Freimer, N. B., Ferrucci, L., Erdmann, J., Elliott, P., Ejebe, K. G., Doring, A., Dominiczak, A. F., Demissie, S., Deloukas, P., de Geus, E. J., de Faire, U., Crawford, G., Collins, F. S., Chen, Y. D., Caulfield, M. J., Campbell, H., Burtt, N. P., Bonnycastle, L. L., Boomsma, D. I., Boekholdt, S. M., Bergman, R. N., Barroso, I., Bandinelli, S., Ballantyne, C. M., Assimes, T. L., Quertermous, T., Altshuler, D., Seielstad, M., Wong, T. Y., Tai, E. S., Feranil, A. B., Kuzawa, C. W., Adair, L. S., Taylor, H. A., Jr., Borecki, I. B., Gabriel, S. B., Wilson, J. G., Holm, H., Thorsteinsdottir, U., Gudnason, V., Krauss, R. M., Mohlke, K. L., Ordovas, J. M., Munroe, P. B., Kooner, J. S., Tall, A. R., Hegele, R. A., Kastelein, J. J., Schadt, E. E., Rotter, J. I., Boerwinkle, E., Strachan, D. P., Mooser, V., Stefansson, K., Reilly, M. P., Samani, N. J., Schunkert, H., Cupples, L. A., Sandhu, M. S., Ridker, P. M., Rader, D. J., van Duijn, C. M., Peltonen, L., Abecasis, G. R., Boehnke, M., and Kathiresan, S. (2010) Biological, clinical and population relevance of 95 loci for blood lipids. Nature 466, 707-713
24. Willer, C. J., Sanna, S., Jackson, A. U., Scuteri, A., Bonnycastle, L. L., Clarke, R., Heath, S. C., Timpson, N. J., Najjar, S. S., Stringham, H. M., Strait, J., Duren, W. L., Maschio, A., Busonero, F., Mulas, A., Albai, G., Swift, A. J., Morken, M. A., Narisu, N., Bennett, D., Parish, S., Shen, H., Galan, P., Meneton, P., Hercberg, S., Zelenika, D., Chen, W. M., Li, Y., Scott, L. J., Scheet, P. A., Sundvall, J., Watanabe, R. M., Nagaraja, R., Ebrahim, S., Lawlor, D. A., Ben-Shlomo, Y., Davey-Smith, G., Shuldiner, A. R., Collins, R., Bergman, R. N., Uda, M., Tuomilehto, J., Cao, A., Collins, F. S., Lakatta, E., Lathrop, G. M., Boehnke, M., Schlessinger, D., Mohlke, K. L., and Abecasis, G. R. (2008) Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat. Genet. 40, 161-169 (Pubitemid 351171403)
25. Fakhro, K. A., Choi, M., Ware, S. M., Belmont, J. W., Towbin, J. A., Lifton, R. P., Khokha, M. K., and Brueckner, M. (2011) Rare copy number variations in congenital heart disease patients identify unique genes in left-right patterning. Proc. Natl. Acad. Sci. U.S.A. 108, 2915-2920
26. 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., and Markowitz, S. D. (2009) Inactivating germ-line and somatic mutations in polypeptide N-acetylgalactosaminyltransferase 12 in human colon cancers. Proc. Natl. Acad. Sci. U.S.A. 106, 12921-12925
27. Schwientek, T., Bennett, E. P., Flores, C., Thacker, J., Hollmann, M., Reis, C. A., Behrens, J., Mandel, U., Keck, B., Schäfer, M. A., Haselmann, K., Zubarev, R., Roepstorff, P., Burchell, J. M., Taylor-Papadimitriou, J., Hollingsworth, M. A., and Clausen, H. (2002) Functional conservation of subfamilies of putative UDP-N-acetylgalactosamine:polypeptide N-acetylgalactosaminyltransferases in Drosophila, Caenorhabditis elegans, and mammals. One subfamily composed of l(2)35Aa is essential in Drosophila. J. Biol. Chem. 277, 22623-22638 (Pubitemid 34967240)
28. Ten Hagen, K. G., and Tran, D. T. (2002) A UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase is essential for viability in Drosophila melanogaster. J. Biol. Chem. 277, 22616-22622 (Pubitemid 34967239)
29. Tian, E., and Ten Hagen, K. G. (2007) A UDP-GalNAc:polypeptide Nacetylgalactosaminyltransferase is required for epithelial tube formation. J. Biol. Chem. 282, 606-614 (Pubitemid 47076626)
30. Zhang, L., Tran, D. T., and Ten Hagen, K. G. (2010) An O-glycosyltransferase promotes cell adhesion during development by influencing secretion of an extracellular matrix integrin ligand. J. Biol. Chem. 285, 19491-19501
31. Zhang, L., Zhang, Y., and Hagen, K. G. (2008) A mucin-type O-glycosyltransferase modulates cell adhesion during Drosophila development. J. Biol. Chem. 283, 34076-34086
32. Tenno, M., Ohtsubo, K., Hagen, F. K., Ditto, D., Zarbock, A., Schaerli, P., von Andrian, U. H., Ley, K., Le, D., Tabak, L. A., and Marth, J. D. (2007) Initiation of protein O-glycosylation by the polypeptide GalNAcT-1 in vascular biology and humoral immunity. Mol. Cell. Biol. 27, 8783-8796
33. Pastor-Pareja, J. C., and Xu, T. (2011) Shaping cells and organs in Drosophila by opposing roles of fat body-secreted collagen IV and perlecan. Dev. Cell 21, 245-256
34. Neumüller, R. A., Richter, C., Fischer, A., Novatchkova, M., Neumüller, K. G., and Knoblich, J. A. (2011) Genome-wide analysis of self-renewal in Drosophila neural stem cells by transgenic RNAi. Cell Stem Cell 8, 580-593
35. Zacharogianni, M., Kondylis, V., Tang, Y., Farhan, H., Xanthakis, D., Fuchs, F., Boutros, M., and Rabouille, C. (2011) EMBO J. 30, 3684-3700
36. Shiga, Y., Tanaka-Matakatsu, M., and Hayashi, S. (1996) A nuclear GFP/β-galactosidase fusion protein as a marker for morphogenesis in living Drosophila. Dev. Growth Differ. 38, 99-106 (Pubitemid 26061341)
37. Dietzl, G., Chen, D., Schnorrer, F., Su, K. C., Barinova, Y., Fellner, M., Gasser, B., Kinsey, K., Oppel, S., Scheiblauer, S., Couto, A., Marra, V., Keleman, K., and Dickson, B. J. (2007) A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature 448, 151-156 (Pubitemid 47067374)
38. Thibault, S. T., Singer, M.A., Miyazaki, W.Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L., Ryner, L., Cheung, L. M., Chong, A., Erickson, C., Fisher, W. W., Greer, K., Hartouni, S. R., Howie, E., Jakkula, L., Joo, D., Killpack, K., Laufer, A., Mazzotta, J., Smith, R. D., Stevens, L. M., Stuber, C., Tan, L. R., Ventura, R., Woo, A., Zakrajsek, I., Zhao, L., Chen, F., Swimmer, C., Kopczynski, C., Duyk, G., Winberg, M. L., and Margolis, J. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287 (Pubitemid 38282754)
39. Lee, Y. S., and Carthew, R. W. (2003) Making a better RNAi vector for Drosophila. Use of intron spacers. Methods 30, 322-329 (Pubitemid 36793969)
40. Rubin, G. M., and Spradling, A. C. (1982) Genetic transformation of Drosophila with transposable element vectors. Science 218, 348-353 (Pubitemid 12037603)
41. Spradling, A. C., and Rubin, G. M. (1982) Transposition of cloned P elements into Drosophila germ line chromosomes. Science 218, 341-347 (Pubitemid 12037602)
42. Dubreuil, R. R. (2004) Copper cells and stomach acid secretion in the Drosophila midgut. Int. J. Biochem. Cell Biol. 36, 745-752
43. Shanbhag, S., and Tripathi, S. (2009) Epithelial ultrastructure and cellular mechanisms of acid and base transport in the Drosophila midgut. J. Exp. Biol. 212, 1731-1744
44. Ten Hagen, K. G., Bedi, G. S., Tetaert, D., Kingsley, P. D., Hagen, F. K., Balys, M. M., Beres, T. M., Degand, P., and Tabak, L. A. (2001) Cloning and characterization of a ninth member of the UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase family, ppGaNTase-T9. J. Biol. Chem. 276, 17395-17404
45. Wandall, H. H., Hassan, H., Mirgorodskaya, E., Kristensen, A. K., Roepstorff, P., Bennett, E. P., Nielsen, P. A., Hollingsworth, M. A., Burchell, J., Taylor-Papadimitriou, J., and Clausen, H. (1997) Substrate specificities of three members of the human UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase family, GalNAc-T1, -T2, and -T3. J. Biol. Chem. 272, 23503-23514 (Pubitemid 27410917)
46. Van der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A., Meijerink, J. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., and Einerhand, A. W. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131, 117-129 (Pubitemid 44015753)
47. Velcich, A., Yang, W., Heyer, J., Fragale, A., Nicholas, C., Viani, S., Kucherlapati, R., Lipkin, M., Yang, K., and Augenlicht, L. (2002) Colorectal cancer in mice genetically deficient in the mucin Muc2. Science 295, 1726-1729 (Pubitemid 34202910)
48. An, G., Wei, B., Xia, B., McDaniel, J. M., Ju, T., Cummings, R. D., Braun, J., and Xia, L. (2007) Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans. J. Exp. Med. 204, 1417-1429 (Pubitemid 46919879)