Mucin-type o-glycosylation is controlled by short- And long-range glycopeptide substrate recognition that varies among members of the polypeptide GalNAc transferase family

Glycobiology

Volumn 26, Issue 4, 2016, Pages 360-376

  Revoredo, Leslie ^a   Wang, Shengjun ^b   Bennett, Eric Paul ^b   Clausen, Henrik ^b   Moremen, Kelley W ^c   Jarvis, Donald L ^d   Ten Hagen, Kelly G ^e   Tabak, Lawrence A ^f   Gerken, Thomas A ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF GEORGIA   (United States)

^d UNIVERSITY OF WYOMING   (United States)

^e Developmental Glycobiology Section   (United Kingdom)

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

Author keywords

Glycoprotein biosynthesis; Glycosyltransferase; Lectin; Mucin

Indexed keywords

GLYCOPEPTIDE; LECTIN; MUCIN; N ACETYLGALACTOSAMINE; N ACETYLGALACTOSAMINE TRANSFERASE; POLYPEPTIDE; TRANSFERASE; UNCLASSIFIED DRUG; CARBOHYDRATE; FUCOSE; N-ACETYLFUCOSAMINE; PROTEIN BINDING; SIALYLTRANSFERASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN GLYCOSYLATION; AMINO ACID SEQUENCE; ANALOGS AND DERIVATIVES; BINDING SITE; BIOSYNTHESIS; CHEMISTRY; ENZYME SPECIFICITY; GENETICS; GLYCOSYLATION; HUMAN; PHYLOGENY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; BINDING SITES; CARBOHYDRATES; CATALYTIC DOMAIN; FUCOSE; GLYCOPEPTIDES; GLYCOSYLATION; HUMANS; LECTINS; MUCINS; PHYLOGENY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; SIALYLTRANSFERASES; SUBSTRATE SPECIFICITY;

EID: 84964824978     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwv108     Document Type: Article

References (61)

1. Barb AW, Meng L, Gao Z, Johnson RW, Moremen KW, Prestegard JH. 2012. NMR characterization of immunoglobulin G Fc glycan motion on enzymatic siaylation. Biochemistry. 51:4618-4626.
2. Bennett EP, Hassan H, Hollingsworth MA, Clausen H. 1999. A novel human UDP-N-acetyl-D-galactosamine:polypeptide N-acetylgalactosaminyltransferase, GalNAc-T7, with specificity for partial GalNAc-glycosylated acceptor substrates. FEBS Lett. 460:226-230.
3. Bennett EP, Hassan H, Mandel U, Mirgorodskaya E, Roepstorff P, Burchell J, Taylor-Papadimitriou J, Hollingsworth MA, Merkx G, van Kessel AG., et al. 1998. Cloning of a human UDP-N-acetyl-alpha-D-galactosamine: polypeptide N-acetylgalactosaminyltransferase that complements other GalNAc-transferases in complete O-glycosylation of the MUC1 tandem repeat. J Biol Chem. 273:30472-30481.
4. Bennett EP, Mandel U, Clausen H, Gerken TA, Fritz TA, Tabak LA. 2012. Control of mucin-type O-glycosylation: A classification of the polypeptide GalNAc-transferase gene family. Glycobiology. 22:736-756.
5. Berois N, Mazal D, Ubillos L, Trajtenberg F, Nicolas A, Sastre-Garau X, Magdelenat H, 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.
6. Brockhausen I. 2006. Mucin-typeO-glycans in human colon and breast cancer: Glycodynamics and functions. Endocrinology. 7:599-604.
7. Chen Y-Z, Tang Y-R, Sheng Z-Y, Zhang Z. 2008. Prediction of mucin-type O-glycosylation sites in mammalian proteins using the composition of k-spaced amino acid pairs. BMC Bioinformatics. 9:101.
8. Elhammer AP, Poorman RA, Brown E, Maggiora LL, Hoogerheide JG, Kezdy FJ. 1993. The specificity of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase as inferred from a database of in vivo substrates and from the in vitro glycosylation of proteins and peptides. J Biol Chem. 268:10029-10038.
9. Fritz TA, Hurley JH, Trinh LB, Shiloach J, Tabak LA. 2004. The beginnings of mucin biosynthesis: The crystal structure of UDP-GalNAc:polypeptide {alpha}-N-acetylgalactosaminyltransferase-T1. Proc Natl Acad Sci USA. 101:15307-15312.
10. Fritz TA, Raman J, Tabak LA. 2006. Dynamic association between the catalytic and lectin domains of the human UDP-GalNAc:polypepide α-N-acetylgalactosamilyltransferase-2. J Biol Chem. 281:8613-8619.
11. Fujimoto Z, Kuno A, Kaneko S, Yoshida S, Kobayashi H, Kusakabe I, Mizuno H. 2000. Crystal structure of Streptomyces olivaceoviridis E-86 β-xylanase containing xylan-binding domain. J Mol Biol. 300:575-585.
12. Gerken TA. 2004. Kinetic modeling confirms the biosynthesis of mucin Core 1 (b-Gal(1-3) a-GalNAc-O-Ser/Thr) O-glycan structures are modulated by neighboring glycosylation effects. Biochemistry. 43:4137-4142.
13. Gerken TA, Jamison O, Perrine CL, Collete J, Moinova H, Ravi L, Markowitz SD, Schen W, Patel H, Tabak L. 2011. Emerging paradigms for the initiation of mucin type protein O-glycosylation by the polypeptide GalNAc transferases (ppGalNAc T) family of glycosyltransferases. J Biol Chem. 286:14493-14507.
14. Gerken TA, Raman J, Fritz TA, Jamison O. 2006. Identification of common and unique peptide substrate preferences for the UDP-GalNAc: Polypeptide alpha -N-acetylgalactosaminyltransferases T1 & T2 (ppGalNAc T1 & T2) derived from oriented random peptide substrates. J Biol Chem. 281:32403-32416.
15. Gerken TA, Revoredo L, Thome JJC, Tabak LA, Vester-Chrisensen MB, Gahlay GK, Jarvis DL, Johnson RW, Moniz HA, Moremen K. 2013. The lectin domain of the polypeptide GalNAc transferase family of glycosyltransferases (ppGalNAcTs) acts as a switch directing glycoyslation in an N- or C-terminal direction, further controlling mucin type O-glycosylation. J Biol Chem. 288:19900-19914.
16. Gerken TA, Zhang J, Levine J, 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 N-acetylgalactosaminyltransferases T1 and T2. J Biol Chem. 277:49850-49862.
17. Hansen JE, Lund O, Tolstrup N, Gooley AA, Williams KL, Brunak S. 1998. NetOglyc: Prediction of mucin type O-glycosylation sites based on sequence context and surface accessibility. Glycoconjugate J. 15:115-130.
18. Hassan H, Reis CA, Bennett EP, Mirgorodskaya E, Roepstorff P, Hollingsworth MA, Burchell J, Taylor-Papadimitriou J, 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.
19. Hazes B. 1996. The (QxW)3 domain: A flexible lectin scaffold. Protein Sci. 5:1490-1501.
20. Holleboom AG, Karlsson H, Lin R-S, Beres TM, Sierts JA, Herman DS, Stroes ESG, Aerts JM, Kastelein JJP, Motazacker MM, et al. 2011. Heterozygosity for a loss-of-function mutation in GALNT2 improves plasma triglyceride clearance in man. Cell Metabolism. 14:811-818.
21. Homa FL, Hollander T, Lehman DJ, Thomsen DR, Elhammer AP. 1993. Isolation and expression of a cDNA clone encoding a bovine UDPGalNAc: polypeptide N-acetylgalactosaminyltransferase. J Biol Chem. 268:12609-12616.
22. Iida S, Takeuchi H, Kato K, Yamamoto K, Irimura T. 2000. Order and maximum incorporation of N-acetyl-D-galactosamine into threonine residues of MUC2 core peptide with microsome fraction of human-colon-carcinoma LS174T cells. Biochem J. 347:535-542.
23. Imberty A, Piller V, Piller F, Breton C. 1997. Fold recognition and molecular modeling of a lectin-like domain in UDP-GalNac:polypeptide N-acetylgalactosaminyltransferases. Protein Eng. 10:1353-1356.
24. Kathiresan S, Melander O, Guiducci C, Surti A, Burtt NP, Rieder MJ, Cooper GM, Roos C, Voight BF, Havulinna AS, et al. 2008. Six new loci associated with blood low-density lipoprotein cholesterol, highdensity lipoprotein cholesterol or triglycerides in humans. NatGenet. 40:189-197.
25. Kato K, Jeanneau C, Tarp MA, Benet-Pages A, Lorenz-Depiereux B, Bennett EP, Mandel U, Strom TM, Clausen H. 2006. Polypeptide GaINAc-transferase T3 and familial tumoral calcinosis: Secretion of FGF23 requires O-glycosylation. J Biol Chem. 281:18370-18377.
26. Kato K, Takeuchi H, Kanoh A, Mandel U, Hassan H, Clausen H, Irimura T. 2001. N-acetylgalactosamine incorporation into a peptide containing consecutive threonine residues by UDP-N-acetyl-D-galactosaminide:polypeptide N-acetylgalactosaminyltransferases. Glycobiology. 11:821-829.
27. Kohsaki T, Nishimori I, Nakayama H, Miyazaki E, Enzan H, Nomoto M, Hollingsworth MA, Onishi S. 2000. Expression of UDP-GalNAc: Polypeptide N-acetylgalactosaminyltransferase isozymes T1 and T2 in human colorectal cancer. J Gastroenterol. 35:840-848.
28. Kubota T, Shiba T, Sugioka S, Furukawa S, Sawaki H, Kato R, Wakatsuki S, Narimatsu H. 2006. Structural basis of carbohydrate transfer activity by human UDP-GalNAc: Polypeptide a-N-acetylgalactosaminyltransferase (pp-GalNAc-T10). J Mol Biol. 359:708-727.
29. Li X, Wang J, Li W, Xu Y, Shao D, Xie Y, Xie W, Kubota T, Marimatsu H, Zhang Y. 2012. Characterization of ppGalNAc-T18, a member of the vertebrate-specific subfamily of UDP-N-acetyl-α-D-galactosamine:polypeptide N-acetylgalactosaminytransferases. Glycobiology. 22:602-615.
30. Libisch MG, Casas M, Chiribao M, Moreno P, Cayota A, Osinaga E, Oppezzo P, Robello C. 2014. GALNT11 as a new molecular marker in chronic lymphocytic leukemia. Gene. 533:270-279.
31. Lira-Navarrete E, de Las Rivas M, Companon I, Pallares MC, Kong Y, Iglesias-Fernandez J, Bernardes GJL, Peregrina JM, Rovira C, Bernado P, et al. 2015. Dynamic interplay between catalytic and lectin domains of GalNAc-transferases modulates protein O-glycosylation. Nat Commun. 6:article number 6937.
32. Maveyraud L, Niwa H, Guillet V, Svergun DI, Konarev PV, Palmer RA, PeumansWJ, Rouge P, Van Damme EJM, Reynolds CD, et al. 2009. Structural basis for sugar recognition, including the Tn carcinoma antigen, by the lectin SNA-II from Sambucus nigra. Proteins: Stuct Funct Bioinf. 75:89-103.
33. Miyazaki T, Mori M, Yoshida CA, Ito C, Yamatoya K, Moriishi T, Kawai Y, Komori H, Kawane T, Izumi S-I, et al. 2013. Galnt3 deficiency disrupts acrosome formation and leads to oligoasthenoteraozoospermia. Histochem Cell Biol. 139:339-354.
34. Nakayama Y, Nakamura N, Oki S, Wakabayashi M, Ishihama Y, Miyake A, Itoh N, Kurosaka A. 2012. A putative polypeptide N-acteylgalactosaminyltransferase/Williams-Beuren syndrome chromosome region 17 (WBSCR17) regulates lamellipodium formation and macropinocytosis. J Biol Chem. 287:32222-32235.
35. Nordén R, Halim A, Nyström K, Bennett EP, Mandel U, Olofsson S, Nilsson J, Larson G. 2015. O-Linked glycosylation of the mucin domain of the herpes simplex virus type 1-specific glycoprotein gC-1 is temporally regulated in a seed-and-spread manner. J Biol Chem. 290:5078-5091.
36. Pedersen NB, Wang S, Narmiatsu Y, Yang Z, Halim A, Ter-Borch Gram Schjoldager K, Daugbjerg Madsen T, Seidah NG, Bennet EP, Levery SB, et al. 2014. Low-density lipoprotein receptor class A repeats are O-glycosylated in linker regions. J Biol Chem. 289:17312-17324.
37. Pederson JW, Bennett EP, Schjodager KTB, Clausen H, Wandall HH. 2011. Lectin domains of polypeptide GalNAc transferases exhibit glycopeptide binding specificity. J Biol Chem. 286:32684-32696.
38. Perrine CL, Ganguli A, Wu P, Bertozzi CR, Fritz TA, Raman J, Tabak LA, Gerken TA. 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 ppGal- NAc T1 or T2. J Biol Chem. 284:20387-20397.
39. Pratt MR, Hang HC, Ten Hagen KG, Rarick J, Gerken TA, Tabak LA, Bertozzi CR. 2004. Deconvoluting the functions of polypeptide N-a-acetylgalactosaminyltransferase family members by glycopeptide substrate profiling. Chem Biol. 11:1009-1016.
40. Raman J, Fritz TA, Gerken TA, Jamison O, Live D, Liu M, Tabak LA. 2008. The catalytic and lectin domains of UDP-GalNAc:polypeptide alpha -N-acetylgalactosaminyltransferase function in concert to direct glycosylation site selection. J Biol Chem. 283:22942-22951.
41. Raman J, Guan Y, Perrine CL, Gerken TA, Tabak LA. 2012. UDP-Nacteyl- Alpha-D-galactosamine:polypeptide N-acetylgalactosaminyltransferases: Completion of the family tree. Glycobiology. 22:768-777.
42. Schjoldager KT-BG, Vester-Chrisensen MB, Bennet EP, Levery SB, Schwientek T, Yin W, Blixt O, Clausen H. 2010. O-Glycosylation modulated proprotein convertase activation of angiopoietin-like protein 3. J Biol Chem. 285:36293-36303.
43. Semenov AG, Postnikov AB, Tamm NN, Seferian KR, Karpova NS, Bloshchitsyna MN, Koshkina EV, Krasnoselsky MI, Serebryanaya DV, Katruka AG. 2009. Processing of pro-brain natriuretic peptide is supressed by O-glycosylation in the region close to the cleavage site. Clin Chem. 55:489-498.
44. Simmons AD, Musy MM, Lopes CS, Hwang LY, Yang YP, Lovett M. 1999. A direct interaction between EXT proteins and glycosyltransferases is defective in hereditary multiple exostoses. Human Mol Genet. 8:2155-2164.
45. Steentoft C, Vakhrushev SY, Joshi HJ, Kong Y, Vester-Chrisensen MB, Schjodager KTB, Lavrsen K, Dabelsteen S, Pedersend NB, Marcos-Silva L, et al. 2013. Precsion mapping of the human O-GalNAc glycoproteome through simple cell technology. EMBO J. 32:1478-1488.
46. Takasaki N, Tachibana K, Ogasawara S, Matsuzaki H, Hagiuda J, Ishikawa H, Mochida K, Inoue K, Ogonuki N, Ogura A, et al. 2014. A heterozyguos mutation of GALNTL5 affects male infertility with impairment of sperm motility. Proc Natl Acad Sci USA. 111:1120-1125.
47. Ten Hagen KG, Tran DT. 2002. A UDP-GalNAc: Polypeptide N-acetylgalactosaminyltransferase is essential for viability in Drosophila melanogaster. J Biol Chem. 277:22616-22622.
48. Ten Hagen KG, Tran DT, Gerken TA, Stein DS, 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.
49. Tenno M, Kézdy FJ, Elhammer AP, Kurosaka A. 2002. Function of the lectin domain of polypeptide N-acetylgalactosaminyltransferase 1. Biochem Biophys Res Commun. 298:755-759.
50. Tian E, Hoffman MP, Ten Hagen KG. 2012. O-Glycosylation modulates integrin and FGF signaling by influencing the secretion of basement membrane components. Nat Commun. 3:article number 869.
51. Tian E, Stevens SR, Guan Y, Springer DA, Anderson SA, Starost MF, Patel V, Ten Hagen KG, Tabak LA. 2015. Galnt1 is required for normal heart valve development and cardiac function. PLoS ONE. 10:e0115861.
52. Topaz O, Shurman DL, Bergman R, Indelman M, Ratajczak P, Mizrachi M, Khamaysi Z, Behar D, Petronius D, Friedman V, et al. 2004. Mutations in GALNT3, encoding a protein involved in O-linked glycosylation, cause familial tumoral calcinosis. Nat Genet. 36:579-581.
53. Toth AM, Kuo C-W, Koo K-H, Jarvis DL. 2014. A new insect cell line glycoengineering approach provides baculovirus-inducible glycogene expression and increases human type glycosylation effiency. J Biotechnol. 182-183:19-29.
54. Tran DT, Ten Hagen KG. 2013. Mucin-type O-glycosylation during development. J. Biol. Chem. 288:6921-6929.
55. Vester-Christensen M, Bennett E, Clausen H, Mandel U. 2013. Generation of monoclonal antibodies to native active human glycosyltransferases. Methods Mol. Biol. 1022:403-420.
56. Wandall HH, Irazoqui F, Tarp MA, Bennett EP, Mandel U, Takeuchi H, Kato K, Irimura T, Suryanarayanan G, Hollingsworth MA, et al. 2007. The lectin domains of polypeptide GalNAc-transferases exhibit carbohydratebinding specificity for GalNAc: Lectin binding to GalNAc-glycopeptide substrates is required for high density GalNAc-O-glycosylation. Glycobiology. 17:374-387.
57. Willer CJ, Sanna S, Jackson AU, Scuteri A, Bonnycastle LL, Clarke R, Health SC, Timpson NJ, Najjar SS, Stringham HM, et al. 2008. Newly identified loci that influence lipid concentrations and risk of coronary artery disease. Nat. Genet. 40:161-169.
58. Wood LD, Parsons DW, Jones S, Lin J, Sjoblom T, Leary RJ, Shen D, Boca SM, Barber T, Ptak J, et al. 2007. The genomic landscapes of human breast and colorectal cancers. Science. 318:1108-1113.
59. Yoshimura Y, Nudelman AS, Levery SB, Wandall HH, Bennett EP, Hindsgaul O, Clausen H, Nishimura S-I. 2012. Elucidation of the sugar recognition ability of the lectin domain of UDP-GalNAc:polypeptide N-acetylgalactosaminyltransferase 3 by using unnatural glycopeptide substrates. Glycobiology. 22:429-438.
60. Young WW Jr, Holcomb DR, Ten Hagen KG, Tabak LA. 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.
61. Zhang L, Syed ZA, van Dijk Hard I, Lim J-M, Wells L, Ten Hagen KG. 2014. O-Glycosylation regulates polarized secretion by modulating Tango1 stability. PNAS. 111:7296-7301.