The lectin domain of the polypeptide GalNAc transferase family of glycosyltransferases (ppGalNAc Ts) acts as a switch directing glycopeptide substrate glycosylation in an N- or C-terminal direction, further controlling mucin type O-Glycosylation

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19900-19914

  Gerken, Thomas A ^a,b   Revoredo, Leslie ^b   Thome, Joseph J C ^a,g   Tabak, Lawrence A ^c   Vester Christensen, Malene Bech ^d   Clausen, Henrik ^d   Gahlay, Gagandeep K ^e   Jarvis, Donald L ^e   Johnson, Roy W ^f   Moniz, Heather A ^f   Moremen, Kelley ^f  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

^e UNIVERSITY OF WYOMING   (United States)

^f UNIVERSITY OF GEORGIA   (United States)

^g Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOHYDRATE BINDING; CATALYTIC DOMAINS; FLEXIBLE LINKERS; GLOBULAR DOMAINS; GLYCOSYLTRANSFERASES; HUMAN ISOFORMS; O-GLYCOSYLATION; SUBSTRATE UTILIZATION;

ENZYMES; ESTERIFICATION; GLYCOSYLATION; SUBSTRATES;

PEPTIDES;

GLYCOPEPTIDE; ISOENZYME; LECTIN; LECTIN GLYCOPEPTIDE SUBSTRATE; MUCIN; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINYLTRANSFERASE; POLYPEPTIDE N ACETYLGALACTOSAMINYLTRANSFERASE; THREONINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING KINETICS; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SUBSTRATE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN GLYCOSYLATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REGULATORY MECHANISM;

CONTROL OF GLYCOSYLATION; CONVERTASES; EDMAN SEQUENCING; GLYCOBIOLOGY; GLYCOPROTEIN BIOSYNTHESIS; GLYCOSYLTRANSFERASES; LECTIN; MUCINS; O-GLYCOSYLATION; RANDOM GLYCOPEPTIDE;

CATALYSIS; GLYCOPEPTIDES; GLYCOSYLATION; HUMANS; ISOENZYMES; LECTINS; N-ACETYLGALACTOSAMINYLTRANSFERASES; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84880063633     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.477877     Document Type: Article

References (76)

1. Bennett, E. P., Mandel, U., Clausen, H., Gerken, T. A., Fritz, T. A., and Tabak, L. A. (2012) Control of mucin-type O-glycosylation. A classification of the polypeptide GalNAc-transferase gene family. Glycobiology 22, 736-756
2. Hollingsworth, M. A., and Swanson, B. J. (2004) Mucins in cancer. Protection and control of the cell surface. Nat. Rev. Cancer 4, 45-60
3. Brockhausen, I. (2006) Mucin-type O-glycans in human colon and breast cancer. Glycodynamics and functions. Endocrinology 7, 599-604
4. Gill, D. J., Clausen, H., and Bard, F. (2011) Location, location, location. New insights into O-GalNAc protein glycosylation. Trends Cell Biol. 21, 149-158
5. Wopereis, S., Lefeber, D. J., Morava, E., and Wevers, R. A. (2006) Mechanisms in protein O-glycan biosynthesis and clinical and molecular aspects of protein O-glycan biosynthesis defects. A Review. Clin. Chem. 52, 574-600
6. Tian, E., and Ten Hagen, K. (2009) Recent insights into the biological roles of mucin-type O-glycosylation. Glycoconj. J. 26, 325-334
7. Lang, T., Hansson, G. C., and Samuelsson, T. (2007) Gel-forming mucins appeared early in metazoan evolution. Proc. Natl. Acad. Sci. U.S.A. 104, 16209-16214
8. Carmon, A., Wilkin, M., Hassan, J., Baron, M., and MacIntyre, R. (2007) Concerted evolution within the Drosophila dumpy gene. Genetics 176, 309-325
9. Alfalah, M., Jacob, R., Preuss, U., Zimmer, K. P., Naim, H., and Naim, H. Y. (1999) O-Linked glycans mediate apical sorting of human intestinal sucrase-isomaltase through association with lipid rafts. Curr. Biol. 9, 593-596
10. Tani, M., Iida, H., and Ito, M. (2003) O-Glycosylation of mucin-like domain retains the neutral ceramidase on the plasma membranes as a type II integral membrane protein. J. Biol. Chem. 278, 10523-10530
11. Li, F., Wilkins, P. P., Crawley, S., Weinstein, J., Cummings, R. D., and McEver, R. P. (1996) Post-translational modifications of recombinant Pselectin glycoprotein ligand-1 required for binding to P-and E-selectin. J. Biol. Chem. 271, 3255-3264
12. Lee, S. H., Yu, S. Y., Nakayama, J., Khoo, K. H., Stone, E. L., Fukuda, M. N., Marth, J. D., and Fukuda, M. (2010) Core2 O-glycan structure is essential for the cell surface expression of sucrase isomaltase and dipeptidyl peptidase-IV during intestinal cell differentiation. J. Biol. Chem. 285, 37683-37692
13. Potter, B. A., Hughey, R. P., and Weisz, O. A. (2006) Role of N-and Oglycans in polarized biosynthetic sorting. Am. J. Physiol. Cell Physiol. 290, C1-C10
14. Kinlough, C. L., Poland, P. A., Gendler, S. J., Mattila, P. E., Mo, D., Weisz, O. A., and Hughey, R. P. (2011) Core-glycosylated mucin-like repeats from MUC1 are an apical targeting signal. J. Biol. Chem. 286, 39072-39081
15. Nakayama, Y., Nakamura, N., Oki, S., Wakabayashi, M., Ishihama, Y., Miyake, A., Itoh, N., and Kurosaka, A. (2012) A putative polypeptide Nacetylgalactosaminyltransferase/Williams-Beuren syndrome chromosome region 17 (WBSCR17) regulates lamellipodium formation and macropinocytosis. J. Biol. Chem. 287, 32222-32235
16. Steentoft, C., Vakhrushev, S. Y., Joshi, H. J., Kong, Y., Vester-Christensen, M. B., Schjoldager, K. T. B., Lavrsen, K., Dabelsteen, S., Pedersen, N. B., Marcos-Silva, L., Gupta, R., Paul Bennett, E., Mandel, U., Brunak, S., Wandall, H. H., Levery, S. B., and Clausen, H. (2013) Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. EMBO J. 32, 1478-1488
17. Schjoldager, K. T., Vakhrushev, S. Y., Kong, Y., Steentoft, C., Nudelman, A. S., Pedersen, N. B., Wandall, H. H., Mandel, U., Bennett, E. P., Levery, S. B., and Clausen, H. (2012) Probing isoform-specific functions of polypeptide GalNAc-transferases using zinc finger nuclease glycoengineered SimpleCells, Proc. Natl. Acad. Sci. U.S.A. 109, 9893-9898
18. Vakhrushev, S. Y., Steentoft, C., Vester-Christensen, M. B., Bennett, E. P., Clausen, H., and Levery, S. B. (2013) Enhanced mass spectrometric mapping of the human GalNAc-typeO-glycoproteome with SimpleCells. Mol. Cell. Proteomics, in press
19. Schjoldager, K. T., and Clausen, H. (2012) Site-specific protein O-glycosylation modulates proprotein processing. Deciphering specific functions of the large polypeptide GalNAc-transferase gene family. Biochim. Biophys. Acta 1820, 2079-2094
20. Schjoldager, K. T., Vester-Christensen, M. B., Goth, C. K., Petersen, T. N., Brunak, S., Bennett, E. P., Levery, S. B., and Clausen, H. (2011) A systematic study of site-specific GalNAc-type O-glycosylation modulating proprotein convertase processing. J. Biol. Chem. 286, 40122-40132
21. Kato, K., Jeanneau, C., Tarp, M. A., Benet-Pages, A., Lorenz-Depiereux, B., Bennett, E. P., Mandel, U., Strom, T. M., and Clausen, H. (2006) Polypeptide GaINAc-transferase T3 and familial tumoral calcinosis. Secretion of FGF23 requires O-glycosylation. J. Biol. Chem. 281, 18370-18377
22. Schjoldager, K. T., Vester-Christensen, M. B., Bennett, E. P., Levery, S. B., Schwientek, T., Yin, W., Blixt, O., and Clausen, H. (2010) O-Glycosylation modulates proprotein convertase activation of angiopoietin-like protein 3. J. Biol. Chem. 285, 36293-36303
23. Herr, P., Korniychuk, G., Yamamoto, Y., Grubisic, K., and Oelgeschläger, M. (2008) Regulation of TGF-β signalling by N-acetylgalactosaminyltransferase-like 1, Development 135, 1813-1822
24. Wagner, K. W., Punnoose, E. A., Januario, T., Lawrence, D. A., Pitti, R. M., Lancaster, K., Lee, D., von Goetz, M., Yee, S. F., Totpal, K., Huw, L., Katta, V., Cavet, G., Hymowitz, S. G., Amler, L., and Ashkenazi, A. (2007) Deathreceptor O-glycosylation controls tumor-cell sensitivity to the proapoptotic ligand Apo2L/TRAIL. Nat. Med. 13, 1070-1077
25. Ichikawa, S., Sorenson, A. H., Austin, A. M., Mackenzie, D. S., Fritz, T. A., Moh, A., Hui, S. L., and Econs, M. J. (2009) Ablation of the Galnt3 gene leads to low-circulating intact fibroblast growth factor 23 (Fgf23) concentrations and hyperphosphatemia despite increased Fgf23 expression. Endocrinology 150, 2543-2550
26. Simmons, A. D., Musy, M. M., Lopes, C. S., Hwang, L. Y., Yang, Y. P., and Lovett, M. (1999) A direct interaction between EXT proteins and glycosyltransferases is defective in hereditary multiple exostoses. Hum. Mol. Genet. 8, 2155-2164
27. Holleboom, A. G., Karlsson, H., Lin, R. S., Beres, T. M., Sierts, J. A., Herman, D. S., Stroes, E. S., Aerts, J. M., Kastelein, J. J., Motazacker, M. M., Dallinga-Thie, G. M., Levels, J. H., Zwinderman, A. H., Seidman, J. G., Seidman, C. E., Ljunggren, S., Lefeber, D. J., Morava, E., Wevers, R. A., Fritz, T. A., Tabak, L. A., Lindahl, M., Hovingh, G. K., and Kuivenhoven, J. A. (2011) Heterozygosity for a loss-of-function mutation in GALNT2 improves plasma triglyceride clearance in man. Cell Metab. 14, 811-818
28. 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. G., 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. J. H., Pedersen, N. L., Pattaro, C., Parker, A. N., Pare, G., Oostra, B. A., 'Donnell, C. J., Nieminen, M. S., Nickerson, D. A., Montgomery, G. W., Meitinger, T., McPherson, R., Mc-Carthy, M. I., McArdle, W., Masson, D., Martin, N. G., Marroni, F., Mangino, M., Magnusson, P. K. E., Lucas, G., Luben, R., Loos, R. J. F., 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., Cecile, J. W. J., 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. C., 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 Jr., H. A., 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. P., 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
29. 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
30. Gaziel-Sovran, A., Segura, M. F., Di Micco, R., Collins, M. K., Hanniford, D., Vega-Saenz de Miera, E., Rakus, J. F., Dankert, J. F., Shang, S., Kerbel, R. S., Bhardwaj, N., Shao, Y., Darvishian, F., Zavadil, J., Erlebacher, A., Mahal, L. K., Osman, I., and Hernando, E. (2011) miR-30b/30d Regulation of GalNAc Transferases Enhances Invasion and Immunosuppression during Metastasis, Cancer Cell 20, 104-118
31. Park, J. H., Katagiri, T., Chung, S., Kijima, K., and Nakamura, Y. (2011) Polypeptide N-acetylgalactosaminyltransferase 6 disrupts mammary acinar morphogenesis through O-glycosylation of fibronectin. Neoplasia 13, 320-326
32. Taniuchi, K., Cerny, R. L., Tanouchi, A., Kohno, K., Kotani, N., Honke, K., Saibara, T., and Hollingsworth, M. A. (2011) Overexpression of GalNActransferase GalNAc-T3 promotes pancreatic cancer cell growth. Oncogene 30, 4843-4854
33. Berois, N., Mazal, D., Ubillos, L., Trajtenberg, F., Nicolas, A., Sastre-Garau, X., Magdelenat, H., and Osinaga, E. (2006) UDP-N-acetyl-D- galactosamine. Polypeptide N-acetylgalactosaminyltransferase-6 as a new immunohistochemical breast cancer marker. J. Histochem. Cytochem. 54, 317-328
34. Berois, N., Gattolliat, C. H., Barrios, E., Capandeguy, L., Douc-Rasy, S., Valteau-Couanet, D., Bénard, J., and Osinaga, E. (2013) GALNT9 gene expression is a prognostic marker in neuroblastoma patients. Clin. Chem. 59, 225-233
35. Xia, L., Ju, T., Westmuckett, A., An, G., Ivanciu, L., McDaniel, J. M., Lupu, F., Cummings, R. D., and McEver, R. P. (2004) Defective angiogenesis and fatal embryonic hemorrhage in mice lacking core 1-derived O-glycans. J. Cell Biol. 164, 451-459
36. ten Hagen, K. G., Zhang, L., Tian, E., and Zhang, Y. (2009) Glycobiology on the fly. Developmental and mechanistic insights from Drosophila. Glycobiology 19, 102-111
37. Tabak, L. A. (2010) The role of mucin-type O-glycans in eukaryotic development. Semin. Cell Dev. Biol. 21, 616-621
38. Tran, D. T., Zhang, L., Zhang, Y., Tian, E., Earl, L. A., and Ten Hagen, K. G. (2012) Multiple members of the UDP-GalNAc. Polypeptide N-acetylgalactosaminyltransferase family are essential for viability in Drosophila. J. Biol. Chem. 287, 5243-5252
39. Tran, D. T., and Ten Hagen, K. G. (2013) Mucin-type O-glycosylation during development. J. Biol. Chem. 288, 6921-6929
40. Tian, E., Hoffman, M. P., and Ten Hagen, K. G. (2012) O-Glycosylation modulates integrin and FGF signalling by influencing the secretion of basement membrane components. Nat. Commun. 3, 869
41. Raman, J., Guan, Y., Perrine, C. L., Gerken, T. A., and Tabak, L. A. (2012) UDP-N-acetyl-α-D-galactosamine: polypeptide N- acetylgalactosaminyltransferases. Completion of the family tree. Glycobiology 22, 768-777
42. Fritz, T. A., Raman, J., and Tabak, L. A. (2006) Dynamic association between the catalytic and lectin domains of human UDP-GalNAc: polypeptide α-N-acetylgalactosaminyltransferase-2. J. Biol. Chem. 281, 8613-8619
43. Gerken, T. A., Jamison, O., Perrine, C. L., Collette, J. C., Moinova, H., Ravi, L., Markowitz, S. D., Shen, W., Patel, H., and Tabak, L. A. (2011) Emerging paradigms for the initiation of mucin type protein O-glycosylation by the polypeptide GalNAc transferase (ppGalNAc T) family of glycosyltransferases. J. Biol. Chem. 286, 14493-14507
44. Gerken, T. A., Raman, J., Fritz, T. A., and Jamison, O. (2006) Identification of common and unique peptide substrate preferences for the UDPGalNAc. Polypeptide α-N-acetylgalactosaminyltransferases T1 and T2 (ppGalNAc T1 and T2) derived from oriented random peptide substrates. J. Biol. Chem. 281, 32403-32416
45. Perrine, C. L., Ganguli, A., Wu, P., Bertozzi, C. R., Fritz, T. A., Raman, J., Tabak, L. A., and Gerken, T. A. (2009) The 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
46. Gerken, T. A., Gilmore, M., and Zhang, J. (2002) Determination of the site-specific oligosaccharide distribution of the O-glycans attached to the porcine submaxillary mucin tandem repeat. Further evidence for the modulation of O-glycan side chain structures by peptide sequence. J. Biol. Chem. 277, 7736-7751
47. Gerken, T. A., Tep, C., and Rarick, J. (2004) Role of peptide sequence and neighboring residue glycosylation on the substrate specificity of the uridine 5'-diphosphate-α-N-acetylgalactosamine: polypeptide N-acetylgalactosaminyl transferases T1 and T2. Kinetic modeling of the porcine and canine submaxillary gland mucin tandem repeats. Biochemistry 43, 9888-9900
48. Hassan, H., Reis, C. A., Bennett, E. P., Mirgorodskaya, E., Roepstorff, P., Hollingsworth, M. A., Burchell, J., Taylor-Papadimitriou, J., and Clausen, H. (2000) The lectin domain of UDP-N-acetyl-D-galactosamine. Polypeptide N-acetylgalactosaminyltransferase-T4 directs its glycopeptide specificities, J. Biol. Chem. 275, 38197-38205
49. Hanisch, F. G., Reis, C. A., Clausen, H., and Paulsen, H. (2001) Evidence for glycosylation-dependent activities of polypeptide N- acetylgalactosaminyltransferases rGalNAc-T2 and -T4 on mucin glycopeptides, Glycobiology 11, 731-740
50. Wandall, H. H., Irazoqui, F., Tarp, M. A., Bennett, E. P., Mandel, U., Takeuchi, H., Kato, K., Irimura, T., Suryanarayanan, G., Hollingsworth, M. A., and Clausen, H. (2007) The lectin domains of polypeptide GalNActransferases exhibit carbohydrate-binding specificity for GalNAc. Lectin binding to GalNAc-glycopeptide substrates is required for high density GalNAc-O- glycosylation. Glycobiology 17, 374-387
51. Raman, J., Fritz, T. A., Gerken, T. A., Jamison, O., Live, D., Liu, M., and Tabak, L. A. (2008) The catalytic and lectin domains of UDP-GalNAc: polypeptide α-N-acetylgalactosaminyltransferase function in concert to direct glycosylation site selection. J. Biol. Chem. 283, 22942-22951
52. Bennett, E. P., Hassan, H., Hollingsworth, M. A., and Clausen, H. (1999) A novel human UDP-N-acetyl-D-galactosamine: polypeptide N- acetylgalactosaminyltransferase, GalNAc-T7, with specificity for partial GalNAcglycosylated acceptor substrates. FEBS Lett. 460, 226-230
53. Cheng, L., Tachibana, K., Zhang, Y., Guo, J., Kahori Tachibana, K., Kameyama, A., Wang, H., Hiruma, T., Iwasaki, H., Togayachi, A., Kudo, T., and Narimatsu, H. (2002) Characterization of a novel human UDPGalNAc transferase, pp-GalNAc-T10. FEBS Lett. 531, 115-121
54. Pedersen, J. W., Bennett, E. P., Schjoldager, K. T., Meldal, M., Holmér, A. P., Blixt, O., Cló, E., Levery, S. B., Clausen, H., and Wandall, H. H. (2011) Lectin domains of polypeptide GalNAc-transferases exhibit glycopeptide binding specificity. J. Biol. Chem. 286, 32684-32696
55. Yoshimura, Y., Nudelman, A. S., Levery, S. B., Wandall, H. H., Bennett, E. P., Hindsgaul, O., Clausen, H., and Nishimura, S. (2012) Elucidation of the sugar recognition ability of the lectin domain of UDP-GalNAc: polypeptideN-acetylgalactosaminyltransferase 3 by using unnatural glycopeptide substrates. Glycobiology 22, 429-438
56. Gerken, T. A., Ten Hagen, K. G., and Jamison, O. (2008) Conservation of peptide acceptor preferences between Drosophila and mammalian polypeptide-GalNAc transferase orthologue pairs. Glycobiology 18, 861-870
57. Barb, A. W., Meng, L., Gao, Z., Johnson, R. W., Moremen, K. W., and Prestegard, J. H. (2012) NMR characterization of immunoglobulin G Fc glycan motion on enzymatic sialylation. Biochemistry 51, 4618-4626
58. Vester-Christensen, M. B., Bennett, E. P., Clausen, H., and Mandel, U. (2013) in Glycosyltransferases: Methods and Protocols (Brockhausen, I., ed), Methods in Molecular Biology, Humana Press, in press
59. Gerken, T. A., Zhang, J., Levine, J., and Elhammer, A. (2002) Mucin core O-glycosylation is modulated by neighboring residue glycosylation status. Kinetic modeling of the site-specific glycosylation of the apo-porcine sumbaxillary mucin tandem repeat by UDP-GalNAc: polypeptide Nacetylgalactosaminyltransferases T1 and T2, J. Biol. Chem. 277, 49850-49862
60. Fritz, T. A., Hurley, J. H., Trinh, L. B., Shiloach, J., and Tabak, L. A. (2004) The beginnings of mucin biosynthesis. The crystal structure of UDPGalNAc: polypeptideα-N-acetylgalactosaminyltransferase-T1. Proc. Natl. Acad. Sci. U.S.A. 101, 15307-15312
61. Kubota, T., Shiba, T., Sugioka, S., Furukawa, S., Sawaki, H., Kato, R., Wakatsuki, S., and Narimatsu, H. (2006) Structural basis of carbohydrate transfer activity by human UDP-GalNAc. Polypeptide α-N- acetylgalactosaminyltransferase (pp-GalNAc-T10). J. Mol. Biol. 359, 708-727
62. Wakinaka, T., Kiyohara, M., Kurihara, S., Hirata, A., Chaiwangsri, T., Ohnuma, T., Fukamizo, T., Katayama, T., Ashida, H., and Yamamoto, K. (2013) Bifidobacterial α-galactosidase with unique carbohydrate-binding module specifically acts on blood group B antigen. Glycobiology 23, 232-240
63. Cuskin, F., Flint, J. E., Gloster, T. M., Morland, C., Baslé, A., Henrissat, B., Coutinho, P. M., Strazzulli, A., Solovyova, A. S., Davies, G. J., and Gilbert, H. J. (2012)Hownature can exploit nonspecific catalytic and carbohydrate binding modules to create enzymatic specificity. Proc. Natl. Acad. Sci. U.S.A. 109, 20889-20894
64. Boraston, A. B., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2004) Carbohydrate-binding modules. Fine-tuning polysaccharide recognition. Biochem. J. 382, 769-781
65. Hervé, C., Rogowski, A., Blake, A. W., Marcus, S. E., Gilbert, H. J., and Knox, J. P. (2010) Carbohydrate-binding modules promote the enzymatic deconstruction of intact plant cell walls by targeting and proximity effects. Proc. Natl. Acad. Sci. U.S.A. 107, 15293-15298
66. Fujimoto, Z., Kuno, A., Kaneko, S., Yoshida, S., Kobayashi, H., Kusakabe, I., and Mizuno, H. (2000) Crystal structure of Streptomyces olivaceoviridis E-86 β-xylanase containing xylan-binding domain. J. Mol. Biol. 300, 575-585
67. Imberty, A., Piller, V., Piller, F., and Breton, C. (1997) Fold recognition and molecular modeling of a lectin-like domain in UDP-GalNac: polypeptide N-acetylgalactosaminyltransferases. Protein Eng. 10, 1353-1356
68. Hazes, B. (1996) The (QxW)3 domain. A flexible lectin scaffold. Protein Sci. 5, 1490-1501
69. Maveyraud, L., Niwa, H., Guillet, V., Svergun, D. I., Konarev, P. V., Palmer, R. A., Peumans, W. J., Rougé, P., Van Damme, E. J., Reynolds, C. D., and Mourey, L. (2009) Structural basis for sugar recognition, including the Tn carcinoma antigen, by the lectin SNA-II from Sambucus nigra. Proteins 75, 89-103
70. Raju, T. S., and Davidson, E. A. (1994) Role of sialic acid on the viscosity of canine tracheal mucin glycoprotein. Biochem. Biophys. Res. Commun. 205, 402-409
71. Tenno, M., Saeki, A., Kézdy, F. J., Elhammer, A. P., and Kurosaka, A. (2002) The lectin domain of UDP-GalNAc: polypeptide N- acetylgalactosaminyltransferase 1 is involved in O-glycosylation of a polypeptide with multiple acceptor sites. J. Biol. Chem. 277, 47088-47096
72. Tenno, M., Kézdy, F. J., Elhammer, A. P., and Kurosaka, A. (2002) Function of the lectin domain of polypeptide N-acetylgalactosaminyltransferase 1. Biochem. Biophys. Res. Commun. 298, 755-759
73. Zhang, Y., Iwasaki, H., Wang, H., Kudo, T., Kalka, T. B., Hennet, T., Kubota, T., Cheng, L., Inaba, N., Gotoh, M., Togayachi, A., Guo, J., Hisatomi, H., Nakajima, K., Nishihara, S., Nakamura, M., Marth, J. D., and Narimatsu, H. (2003) Cloning and characterization of a new human UDPN-acetyl-α-D- galactosamine: polypeptide N-acetylgalactosaminyltransferase, designated pp-GalNAc-T13, that is specifically expressed in neurons and synthesizes Tn antigen. J. Biol. Chem. 278, 573-584
74. Garringer, H. J., Fisher, C., Larsson, T. E., Davis, S. I., Koller, D. L., Cullen, M. J., Draman, M. S., Conlon, N., Jain, A., Fedarko, N. S., Dasgupta, B., and White, K. E. (2006) The role of mutant UDP-N-acetyl-α-D- galactosaminepolypeptide N-acetylgalactosaminyltransferase 3 in regulating serum intact fibroblast growth factor 23 and matrix extracellular phosphoglycoprotein in heritable tumoral calcinosis. J. Clin. Endocrinol. Metab. 91, 4037-4042
75. 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
76. Bennett, E. P., Hassan, H., Mandel, U., Hollingsworth, M. A., Akisawa, N., Ikematsu, Y., Merkx, G., van Kessel, A. G., Olofsson, S., and Clausen, H. (1999) Cloning and characterization of a close homologue of human UDPN-acetyl- α-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase-T3, designated GalNAc-T6. Evidence for genetic but not functional redundancy. J. Biol. Chem. 274, 25362-25370