Acceptor specificities and selective inhibition of recombinant human Gal- and GlcNAc-transferases that synthesize core structures 1, 2, 3 and 4 of O-glycans

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 8, 2013, Pages 4274-4281

  Gao, Yin ^a   Aryal, Rajindra P ^b   Ju, Tongzhong ^b   Cummings, Richard D ^b   Gahlay, Gagandeep ^c   Jarvis, Donald L ^c   Matta, Khushi L ^d   Vlahakis, Jason Z ^a   Szarek, Walter A ^a   Brockhausen, Inka ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WYOMING   (United States)

^d TumorEnd LLC   (United States)

Author keywords

C1GalT; C2GnT; C3GnT; Inhibitors; O Glycans; Specificity

Indexed keywords

AGLYCONE; BENZYL 2 BUTANAMIDO 2 ALPHA GALACTOSIDE; CARBOHYDRATE DERIVATIVE; GLYCAN; IMIDAZOLE; N ACETYLGALACTOSAMINE TRANSFERASE; N ACETYLGLUCOSAMINE TRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CARBOHYDRATE ANALYSIS; CHEMICAL MODIFICATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GLYCOSYLATION; HYDROPHOBICITY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN INTERACTION;

GALACTOSYLTRANSFERASES; GLYCOSYLATION; HUMANS; N-ACETYLGLUCOSAMINYLTRANSFERASES; POLYSACCHARIDES; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84878131172     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.04.001     Document Type: Article

References (55)

1. M.A. Hollingsworth, and B.J. Swansson Mucins in cancer: protection and control of the cell surface Nat. Rev. Cancer 4 2004 45 60 (Pubitemid 38082153)
2. H. Läubli, and L. Borsig Selectins promote tumor metastasis Semin. Cancer Biol. 20 2010 169 177
3. M.J. Schultz, A.F. Swindall, and S.L. Bellis Regulation of the metastatic cell phenotype by sialylated glycans Cancer Metastasis Rev. 31 2012 501 518
4. G. Patsos, V. Hebbe-Viton, C. Robbe-Masselot, D. Masselot, R. San Martin, R. Greenwood, C. Paraskeva, A. Klein, M. Graessmann, J.C. Michalski, T. Gallagher, and A. Corfield O-glycan inhibitors generate aryl-glycans, induce apoptosis and lead to growth inhibition in colorectal cancer cell lines Glycobiology 19 2009 382 398
5. E.P. Bennett, U. Mandel, H. Clausen, T.A. Gerken, T.A. Fritz, and L.A. Tabak Control of mucin-type O-glycosylation: a classification of the polypeptide GalNAc-transferase gene family Glycobiology 22 2012 736 756
6. I. Brockhausen Biosynthesis of complex mucin-type O-glycans, comprehensive natural products II chemistry and biology L. Mander, H.-W. Lui, P.G. Wang, Carbohydrates, nucleosides and nucleic acids vol. 6 2010 Elsevier Oxford 315 350 (Chapter 11)
7. T. Ju, V.I. Otto, and R.D. Cummings The Tn antigen-structural simplicity and biological complexity Angew. Chem. Int. Ed Engl. 50 2011 1770 1791
8. I. Brockhausen Glycosyltransferases involved in the synthesis of mucin type O-glycans in human cancer cells EMBO Rep. 7 2006 599 604
9. P.R. Desai Immunoreactive T and Tn antigens in malignancy: role in carcinoma diagnosis, prognosis, and immunotherapy Transfus. Med. Rev. 14 2000 312 325
10. R. Mi, L. Song, Y. Wang, X. Ding, J. Zeng, S. Lehoux, R.P. Aryal, J. Wang, V.K. Crew, I. van Die, A.B. Chapman, R.D. Cummings, and T. Ju Epigenetic silencing of the chaperone Cosmc in human leukocytes expressing tn antigen J. Biol. Chem. 287 2012 41523 41533
11. T. Ju, and R.D. Cummings A unique molecular chaperone Cosmc required for activity of the mammalian core 1 beta 3-galactosyltransferase Proc. Natl. Acad. Sci. U. S. A. 99 2002 16613 16618 (Pubitemid 36034021)
12. Y. Wang, T. Ju, X. Ding, B. Xia, W. Wang, L. Xia, M. He, and R.D. Cummings Cosmc is an essential chaperone for correct protein O-glycosylation Proc. Natl. Acad. Sci. U. S. A. 107 2010 9228 9233
13. L. Xia, T. Ju, A. Westmuckett, G. An, L. Ivanciu, J.M. McDaniel, F. Lupu, R.D. Cummings, and R.P. McEver Defective angiogenesis and fatal embryonic hemorrhage in mice lacking core 1-derived O-glycans J. Cell Biol. 164 2004 451 459 (Pubitemid 38174772)
14. T. Ju, R.D. Cummings, and W.M. Canfield Purification, characterization, and subunit structure of rat core 1 beta1,3-galactosyltransferase J. Biol. Chem. 277 2002 169 177 (Pubitemid 34952042)
15. I. Brockhausen, K.L. Matta, J. Orr, and H. Schachter Mucin synthesis. UDP-GlcNAc:GalNAc-R beta 3-N-acetylglucosaminyltransferase and UDP-GlcNAc:GlcNAc beta 1-3GalNAc-R (GlcNAc to GalNAc) beta 6-N-acetylglucosaminyltransferase from pig and rat colon mucosa Biochemistry 24 1985 1866 1874 (Pubitemid 15019779)
16. T. Iwai, N. Inaba, A. Naundorf, Y. Zhang, M. Gotoh, H. Iwasaki, T. Kudo, A. Togayachi, Y. Ishizuka, H. Nakanishi, and H. Narimatsu Molecular cloning and characterization of a novel UDP-GlcNAc:GalNAc-peptide beta1,3-N- acetylglucosaminyltransferase (beta 3Gn-T6), an enzyme synthesizing the core 3 structure of O-glycans J. Biol. Chem. 277 2002 12802 12809 (Pubitemid 34952643)
17. T. Iwai Core 3 synthase is down-regulated in colon carcinoma and suppresses the cancer metastasis Seikagaku 78 2006 429 433
18. F. Vavasseur, J.M. Yang, K. Dole, H. Paulsen, and I. Brockhausen Synthesis of O-glycan core 3: characterization of UDP-GlcNAc: GalNAc-R beta 3-N-acetyl-glucosaminyltransferase activity from colonic mucosal tissues and lack of the activity in human cancer cell lines Glycobiology 5 1995 351 357
19. T. Iwai, T. Kudo, R. Kawamoto, T. Kubota, A. Togayachi, T. Hiruma, T. Okada, T. Kawamoto, K. Morozumi, and H. Narimatsu Core 3 synthase is down-regulated in colon carcinoma and profoundly suppresses the metastatic potential of carcinoma cells Proc. Natl. Acad. Sci. U. S. A. 102 2005 4572 4577 (Pubitemid 40397153)
20. S.H. Lee, S. Hatakeyama, S.Y. Yu, X. Bao, C. Ohyama, K.H. Khoo, M.N. Fukuda, and M. Fukuda Core3 O-glycan synthase suppresses tumor formation and metastasis of prostate carcinoma PC3 and LNCaP cells through down-regulation of alpha2beta1 integrin complex J. Biol. Chem. 284 2009 17157 17169
21. G. An, B. Wei, B. Xia, J.M. McDaniel, T. Ju, R.D. Cummings, J. Braun, and L. Xia Increased susceptibility to colitis and colorectal tumors in mice lacking core 3-derived O-glycans J. Exp. Med. 204 2007 1417 1429 (Pubitemid 46919879)
22. I. Brockhausen, G. Möller, A. Pollex-Krüger, V. Rutz, H. Paulsen, and K.L. Matta Control of O-glycan synthesis: specificity and inhibition of O-glycan core 1 UDP-galactose:N-acetylgalactosamine-alpha-R beta 3-galactosyltransferase from rat Liver Biochem. Cell Biol. 70 1992 99 108
23. I. Brockhausen, G. Möller, G. Merz, K. Adermann, and H. Paulsen Control of mucin synthesis: the peptide portion of synthetic O-glycopeptide substrates influences the activity of O-glycan core 1 UDP-galactose: N-acetyl-alpha-galactosaminyl-R β3-galactosyl-transferase Biochemistry 29 1990 10206 10212 (Pubitemid 20384525)
24. M. Granovsky, T. Bielfeldt, S. Peters, H. Paulsen, M. Meldal, J. Brockhausen, and I. Brockhausen UDP-galactose: glycoprotein-N-acetyl-d- galactosamine 3-β-d-galactosyltransferase activity synthesizing O-glycan core 1 is controlled by the amino acid sequence and glycosylation of glycopeptide substrates Eur. J. Biochem. 221 1994 1039 1046
25. M.F. Bierhuizen, and M. Fukuda Expression cloning of a cDNA encoding UDP-GlcNAc:Gal beta 1-3-GalNAc-R (GlcNAc to GalNAc) beta 1-6GlcNAc transferase by gene transfer into CHO cells expressing polyoma large tumor antigen Proc. Natl. Acad. Sci. U. S. A. 89 1992 9326 9330
26. W. Kuhns, V. Rutz, H. Paulsen, K.L. Matta, M.A. Baker, M. Barner, M. Granovsky, and I. Brockhausen Processing O-glycan core 1, Gal beta 1-3GalNAc alpha-R. Specificities of core 2, UDP-GlcNAc: Gal beta 1-3 GalNAc-R(GlcNAc to GalNAc) beta 6-N-acetylglucosaminyltransferase and CMP-sialic acid: Gal beta 1-3GalNAc-R alpha 3-sialyltransferase Glycoconj. J. 10 1993 381 394 (Pubitemid 23314657)
27. I. Brockhausen, T. Dowler, and H. Paulsen Site directed processing: role of amino acid sequences and glycosylation of acceptor glycopeptides in the assembly of extended mucin type O-glycan core 2 Biochim. Biophys. Acta 1790 2009 1244 1257
28. T. Schwientek, M. Nomoto, S.B. Levery, G. Merkx, A.G. van Kessel, E.P. Bennett, M.A. Hollingsworth, and H. Clausen Control of O-glycan branch formation. Molecular cloning of human cDNA encoding a novel beta1,6-N- acetylglucosaminyltransferase forming core 2 and core 4 J. Biol. Chem. 274 1999 4504 4512
29. J.C. Yeh, E. Ong, and M. Fukuda Molecular cloning and expression of a novel beta-1, 6-N-acetylglucosaminyltransferase that forms core 2, core 4, and I branches J. Biol. Chem. 274 1999 3215 3221 (Pubitemid 29075411)
30. C.A. St Hill, D. Baharo-Hassan, and M. Farooqui C2-O-sLeX glycoproteins are E-selectin ligands that regulate invasion of human colon and hepatic carcinoma cells PLoS One 6 2011 e16281
31. C.A. St Hill, M. Farooqui, G. Mitcheltree, H.E. Gulbahce, J. Jessurun, Q. Cao, and B. Walcheck The high affinity selectin glycan ligand C2-O-sLex and mRNA transcripts of the core 2 beta-1,6-N-acetylglucosaminyltransferase (C2GnT1) gene are highly expressed in human colorectal adenocarcinomas BMC Cancer 9 2009 79
32. Y. Suzuki, M. Sutoh, S. Hatakeyama, K. Mori, H. Yamamoto, T. Koie, H. Saitoh, K. Yamaya, T. Funyu, T. Habuchi, Y. Arai, M. Fukuda, C. Ohyama, and S. Tsuboi MUC1 carrying core 2 O-glycans functions as a molecular shield against NK cell attack, promoting bladder tumor metastasis Int. J. Oncol. 40 2012 1831 1838
33. M.C. Huang, H.Y. Chen, H.C. Huang, J. Huang, J.T. Liang, T.L. Shen, N.Y. Lin, C.C. Ho, I.M. Cho, and S.M. Hsu C2GnT-M is downregulated in colorectal cancer and its re-expression causes growth inhibition of colon cancer cells Oncogene 25 2006 3267 3276 (Pubitemid 43846311)
34. D. Toki, M.A. Granovsky, F. Reck, W. Kuhns, M.A. Baker, K.L. Matta, and I. Brockhausen Inhibition of UDP-GlcNAc:Gal beta 1-3GalNAc-R (GlcNAc to GalNAc) beta 6-N-acetylglucosaminyltransferase from acute myeloid leukaemia cells by photoreactive nitrophenyl substrate derivatives Biochem. Biophys. Res. Commun. 198 1994 417 423
35. Y. Gao, J.Z. Vlahakis, W.A. Szarek, and I. Brockhausen Selective inhibition of glycosyltransferases by bivalent imidazolium salts Bioorg. Med. Chem. 21 2013 1305 1311
36. J.Z. Vlahakis, C. Lazar, I.E. Crandall, and W.A. Szarek Anti-Plasmodium activity of imidazolium and triazolium salts Bioorg. Med. Chem. 18 2010 6184 6196
37. Y. Gao, C. Lazar, W.A. Szarek, and I. Brockhausen Specificity of β1,4-galactosyltransferase inhibition by 2-naphthyl 2-butanamido-2-deoxy-1- thio-β-d-glucopyranoside Glycoconj. J. 27 2010 673 684
38. I. Brockhausen, M. Benn, S. Bhat, S. Marone, J.G. Riley, P. Montoya-Peleaz, J.Z. Vlahakis, H. Paulsen, J.S. Schutzbach, and W.A. Szarek UDP-Gal: GlcNAc-R β1,4-galactosyltransferase - a target enzyme for drug design. Acceptor specificity and inhibition of the enzyme Glycoconj. J. 23 2006 523 539
39. J. Xia, J. Xue, R.D. Locke, E.V. Chandrasekaran, T. Srikrishnan, and K.L. Matta Synthesis of fluorinated mucin core 2 branched oligosaccharides with the potential of novel substrates and enzyme inhibitors for glycosyltransferases and sulfotransferases J. Org. Chem. 71 2006 3696 3706
40. E.V. Chandrasekaran, J. Xue, C. Piskorz, R.D. Locke, K. Tóth, H.K. Slocum, and K.L. Matta Potential tumor markers for human gastric cancer: an elevation of glycan:sulfotransferases and a concomitant loss of alpha1,2-fucosyltransferase activities J. Cancer Res. Clin. Oncol. 133 2007 599 611 (Pubitemid 47077051)
41. N. Mathieux, H. Paulsen, M. Meldal, and K. Bock Synthesis of glycopeptide sequences of repeating units of the mucins MUC 2 and MUC 3 containing oligosaccharide side-chains with core 1, core 2, core 3, core 4 and core 6 structure J. Chem. Soc. Perkin Trans. 1 1997 2359 2368 (Pubitemid 127784464)
42. D. Toki, M. Sarkar, B. Yip, F. Reck, D. Joziasse, M. Fukuda, H. Schachter, and I. Brockhausen Expression of stable human O-glycan core 2 β1,6-N-acetylglucosaminyltransferase in Sf9 insect cells Biochem. J. 325 1997 63 69
43. D.L. Jarvis Baculovirus-insect cell expression systems Methods Enzymol. 463 2009 191 222
44. Y. Gao, V.B. Chachadi, P.W. Cheng, and I. Brockhausen Glycosylation potential of human prostate cancer cell lines Glycoconj. J. 29 2012 525 537
45. J.E. Pak, P. Arnoux, S. Zhou, P. Sivarajah, M. Satkunarajah, X. Xing, and J.M. Rini X-ray crystal structure of leukocyte type core 2 beta1,6-N- acetylglucosaminyltransferase. Evidence for a convergence of metal ion-independent glycosyltransferase mechanism J. Biol. Chem. 281 2006 26693 26701 (Pubitemid 44401878)
46. J.E. Pak, M. Satkunarajah, J. Seetharaman, and J.M. Rini Structural and mechanistic characterization of leukocyte-type core 2 β1,6-N- acetylglucosaminyltransferase: a metal-ion-independent GT-A glycosyltransferase J. Mol. Biol. 414 2011 798 811
47. C. Robbe, C. Capon, B. Coddeville, and J.C. Michalski Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract Biochem. J. 384 2004 307 316 (Pubitemid 39656243)
48. S.K. Krakun, E. Clo, H. Clausen, S.B. Levery, K.J. Jensen, and O. Blixt Random glycopeptide bead libraries for seromic biomarker discovery J. Proteome Res. 9 2010 6705 67614
49. T. Kubota, T. Shiba, S. Sugioka, S. Furukawa, H. Sawaki, R. Kato, S. Wakatsuki, and H. Narimatsu Structural basis of carbohydrate transfer activity by human UDP-GalNAc: polypeptide alpha-N-acetylgalactosaminyltransferase (pp-GalNAc-T10) J. Mol. Biol. 359 2006 708 727 (Pubitemid 43767270)
50. T.A. Fritz, J. Raman, and L.A. Tabak Dynamic association between the catalytic and lectin domains of human UDP-GalNAc:polypeptide alpha-N-acetylgalactosaminyltransferase-2 J. Biol. Chem. 281 2006 8613 8619 (Pubitemid 43847965)
51. T.A. Fritz, J.H. Hurley, L.B. Trinh, J. Shiloach, and T.A. Tabak The beginnings of mucin biosynthesis: the crystal structure of UDP-GalNAc: polypeptide alpha-N-acetylgalactosaminyltransferase-T1 Proc. Natl. Acad. Sci. U. S. A. 101 2004 15307 15312 (Pubitemid 39441537)
52. C. Breton, S. Fournel-Gigleux, and M.M. Palcic Recent structures, evolution and mechanisms of glycosyltransferases Curr. Opin. Struct. Biol. 22 2012 540 549
53. S. Mukhopadhyay, C. Bachert, D.R. Smith, and A.D. Linstedt Manganese-induced trafficking and turnover of the cis-Golgi glycoprotein GPP130 Mol. Biol. Cell 21 2010 1282 1292
54. T. Schwientek, J.C. Yeh, S.B. Levery, B. Keck, G. Merkx, A.G. van Kessel, M. Fukuda, and H. Clausen Control of O-glycan branch formation. Molecular cloning and characterization of a novel thymus-associated core 2 beta1, 6-n-acetylglucosaminyltransferase J. Biol. Chem. 275 2000 11106 11113 (Pubitemid 30212753)
55. M. Hashimoto, S. Tan, N. Mori, H. Cheng, and P.W. Cheng Mucin biosynthesis: Molecular cloning and expression of mouse mucus-type core 2 beta1,6 N-acetylglucosaminyltransferase Glycobiology 17 2007 994 100 (Pubitemid 47423889)