Activities and expression pattern of the carbohydrate sulfotransferase GlcNAc6ST-3 (I-GlcNAc6ST): Functional implications

Glycobiology

Volumn 13, Issue 4, 2003, Pages 245-254

  Lee, Jin Kyu ^a,b   Bistrup, Annette ^a   van Zante, Annemieke ^a   Rosen, Steven D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF GEORGIA   (United States)

Author keywords

GlcNAc 6 O sulfotransferase; Homing; L selectin; Mucin; Sulfation

Indexed keywords

COMPLEMENTARY DNA; GLYCOPROTEIN; L SELECTIN; MESSENGER RNA; MUCIN; SULFOTRANSFERASE;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STRUCTURE; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LYMPH NODE; LYMPHOCYTE HOMING; MOLECULAR CLONING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FUNCTION; SULFATION; VENULE;

ANIMALS; CERCOPITHECUS AETHIOPS; CHO CELLS; COS CELLS; CRICETINAE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FEMALE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; ISOENZYMES; L-SELECTIN; LIGANDS; LYMPHATIC SYSTEM; MALE; OLIGOSACCHARIDES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUBSTRATE SPECIFICITY; SULFATES; SULFOTRANSFERASES;

EID: 0038325741     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/cwg018     Document Type: Article

References (57)

1. Akama, T.O., Nishida, K., Nakayama, J., Watanabe, H., Ozaki, K., Nakamura, T., Dota, A., Kawasaki, S., Inoue, Y., Maeda, N., and others. (2000) Macular corneal dystrophy type I and type II are caused by distinct mutations in a new sulphotransferase gene. Nat. Genet., 26, 237-241.
2. Akama, T.O., Nakayama, J., Nishida, K., Hiraoka, N., Suzuki, M., McAuliffe, J., Hindsgaul, O., Fukuda, M., and Fukuda, M.N. (2001) Human corneal GlcNac 6-O-sulfotransferase and mouse intestinal GlcNac6-O-sulfotransferase both produce keratan sulfate. J. Biol. Chem., 276, 16271-16278.
3. Andre, P., Spertini, O., Guia, S., Rihet, P., Dignat-George, F., Brailly, H., Sampol, J., Anderson, P.J., and Vivier, E. (2000) Modification of P-selectin glycoprotein ligand-1 with a natural killer cell-restricted sulfated lactosamine creates an alternate ligand for L-selectin. Proc. Natl Acad. Sci. USA, 97, 3400-3405.
4. Bazan, J.F., Bacon, K.B., Harsiman, G., Wang, W., Soo, K., Rossi, D., Greaves, D.R., Zlotnik, A., and Schall, T.J. (1997) A new class of membrane-bound chemokine with a CX3C motif. Nature, 385, 640-644.
5. Berg, E.L., Robinson, M.K., Warnock, R.A., and Butcher, E.C. (1991) The human peripheral lymph node vascular addressin is a ligand for LECAM-1, the peripheral lymph node homing receptor. J. Cell Biol., 114, 343-349.
6. Bhakta, S., Bartes, A., Bowman, K.G., Kao, W.M., Polsky, I., Lee, J.K., Cook, B.N., Bruehl, R.E., Rosen, S.D., Bertozzi, C.R., and Hemmerich, S. (2000) Sulfation of N-acetylglucosamine by chondroitin 6-sulfotransferase 2 (GST-5). J. Biol. Chem., 275, 40226-40234.
7. Bierhuizen, M.F. and Fukuda, M. (1992) 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. USA, 89, 9326-9330.
8. Bistrup, A., Bhakta, S., Lee, J.K., Belov, Y.C., Gunn, M.D., Zuo, F-R., Huang, C.-C., Kannagi, R., Rosen, S.D., and Hemmerich, S. (1999) Sulfotransferases of two specificities function in the reconstitution of high-endothelial-cell ligands for L-selectin. J. Cell Biol., 145, 899-910.
9. Bowman, K.G. and Bertozzi, C.R. (1999) Carbohydrate sulfotransferases: mediators of extracellular communication. Chem. Biol., 6, R9-R22.
10. Bowman, K.G., Hemmerich, S., Bakhta, S., Singer, M.S., Bistrup, A., Rosen, S.D., and Bertozzi, C.R. (1998) Identification of an N-acetylglucamine-6-O-sulfotransferase activity specific to lymphoid tissue: an enzyme with a possible role in lymphocyte homing. Chem. Biol., 5, 447-460.
11. Bowman, K.G., Cook, B.N., de Graffenried, C.L., and Bertozzi, C.R. (2001) Biosynthesis of L-selectin ligands: sulfation of sialyl Lewis x-related oligosaccharides by a family of GlcNAc-6-sulfotransferases. Biochemistry, 40, 5382-5391.
12. Brown, K.L., Maiti, A., and Johnson, P. (2001) Role of sulfation in CD44-mediated hyaluronan binding induced by inflammatory mediators in human CD14(+) peripheral blood monocytes. J. Immunol., 167, 5367-5374.
13. Capon, C., Wieruszeski, J.M., Lemoine, J., Byrd, J.C., Leffler, H., and Kim, Y.S. (1997) Sulfated lewis x determinants as a major structural motif in glycans from LS174T-HM7 human colon carcinoma mucin. J. Biol. Chem., 272, 31957-31968.
14. Carter, S.R., Slomiany, A., Gwozdzinski, K., Liau, Y.H., and Slomiany, B.L. (1988) Enzymatic sulfation of mucus glycoprotein in gastric mucosa. Effect of ethanol. J. Biol. Chem., 263, 11977-11984.
15. Delmotte, P., Degroote, S., Lafitte, J.J., Lamblin, G., Perini, J.M., and Roussel, P. (2001) TNF{a} increases the expression of glycosyltransferases and sulfotransferases responsible for the biosynthesis of sialylated and/or sulfated Lewis x epitopes in the human bronchial mucosa. J. Biol. Chem., 277, 424-431.
16. Fan, Q.W., Uchimura, K., Yuzawa, Y., Matsuo, S., Mitsuoka, C., Kannagi, R., Muramatsu, H., Kadomatsu, K., and Muramatsu, T. (1999) Spatially and temporally regulated expression of N-acetylglucosamine-6-O-sulfotransferase during mouse embryogenesis. Glycobiology, 9, 947-955.
17. Fukuda, M., Hiraoka, N., Akama, T.O., and Fukuda, M.N. (2001) Carbohydrate-modifying sulfotransferases: structure, function, and pathophysiology. J. Biol. Chem., 276, 47747-47750.
18. Fukuta, M., Inazawa, J., Torii, T., Tsuzuki, K., Shimada, E., and Habuchi, O. (1997) Molecular cloning and characterization of human keratan sulfate Gal-6-sulfotransferase. J. Biol. Chem., 272, 32321-32328.
19. Giordanengo, V., Limouse, M., Peyron, J.F., and Lefebvre, J.C. (1995) Lymphocytic CD43 and CD45 bear sulfate residues potentially implicated in cell to cell interactions. Eur. J. Immunol., 25, 274-278.
20. Girard, J.-P. and Springer, T.A. (1995) Cloning from purified high endothelial venule cells of hevin, a close relative of the antiadhesive extracellular matrix protein SPARC. Immunity, 2, 113-123.
21. Goso, Y. and Hotta, K. (1993) Regional differences in sulfated oligosaccharides of rat gastrointestinal mucin as detected by two-dimensional chromatography. Arch. Biochem. Biophys., 302, 212-217.
22. Habuchi, O. (2000) Diversity and functions of glycosaminoglycan sulfotransferases. Biochim. Biophys. Acta., 1474, 115-127.
23. Hasegawa, N., Torii, T., Kato, T., Miyajima, H., Furuhata, A., Nakayasu, K., Kanai, A., and Habuchi, O. (2000) Decreased GlcNAc 6-O-sulfotransferase activity in the cornea with macular corneal dystrophy. Invest. Ophthalmol. Vis. Sci., 41, 3670-3677.
24. Hemmerich, S. and Rosen, S.D. (2000) Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology, 10, 849-856.
25. Hemmerich, S., Butcher, E.C., and Rosen, S.D. (1994) Sulfation-dependent recognition of HEV-ligands by L-selectin and MECA 79, an adhesion-blocking mAb. J. Exp. Med., 180, 2219-2226.
26. Hemmerich, S., Leffler, H., and Rosen, S.D. (1995) Structure of the O-glycans in GlyCAM-1, an endothelial-derived ligand for L-selectin. J. Biol. Chem., 270, 12035-12047.
27. Hemmerich, S., Bistrup, A., Singer, M.S., Zante, A.v., Lee, J.K., Tsay, D., Peters, M., Carminati, J.L., Brennan, T.J., Carver-Moore, K., and others. (2001a) Sulfation of L-selectin ligands by an HEV-restricted sulfotransferase regulates lymphocyte homing to lymph nodes. Immunity, 15, 237-247.
28. Hemmerich, S., Lee, J.K., Bhakta, S., Bistrup., A., Ruddle, N., and Rosen, S.D. (2001b) Chromosomal localization and genomic organization for the galactose/N-acetylgalactosamine/N-acetylglucosamine 6-O-sulfotransferase gene family. Glycobiology, 11, 75-87.
29. Hiraoka, N., Petryniak, B., Nakayama, J., Tsuboi, S., Suzuki, M., Yeh, J.-C., Izawa, D., Tanaka, T., Miyasaka, M., Lowe, J.B., and Fukuda, M. (1999) A novel, high endothelial venule-specific sulfotransferase expresses 6-sulfo sialyl lewis x, an L-selectin ligand displayed by CD34. Immunity, 11, 79-89.
30. Hooper, L.V., Manzella, S.M., and Baenziger, J.U. (1996) From legumes to leukocytes: biological roles for sulfated carbohydrates. FASEB J., 10, 1137-1146.
31. Kanamori, A., Kojima, N., Uchimura, K., Muramatsu, T., Tamatani, T., Berndt, M.C., Kansas, G.S., and Kannagi, R. (2002) Distinct sulfation requirements of selectins disclosed using cells which support rolling mediated by all three selectins under shear flow. J. Biol. Chem., 277, 32578-32586.
32. Kannagi, R. and Kanamori, A. (1999) Glycobiology of sialyl 6-sulfo lewis x, a new carbohydrate ligand for selectins. Trends Glycosci. Glycotechnol., 11, 329-344.
33. Kim, Y.S. and Gum, J.R. Jr. (1995) Diversity of mucin genes, structure, function, and expression. Gastroenterology, 109, 999-1001.
34. Kimura, N., Mitsuoka, C., Kanamori, A., Hiraiwa, N., Uchimura, K., Muramatsu, T., Tamatani, T., Kansas, G.S., and Kannagi, R. (1999) Reconstitution of functional L-selectin ligands on a cultured human endothelial cell line by cotransfection of alpha1→-3 fucosyltransferase VII and newly cloned GlcNAcbeta:6-sulfotransferase cDNA. Proc. Natl Acad Sci. USA, 96, 4530-4535.
35. Kitagawa, H., Fujita, M., Ito, N., and Suphara, K. (2000) Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem., 275, 21075-21080.
36. Lee, J.K., Bhakta, S., Rosen, S.D., and Hemmerich, S. (1999) Cloning and characterization of a mammalian N-acetylglucosamine-6-sulfotransferase that is highly restricted to intestinal tissue. Biochem. Biophys. Res. Commun., 263, 543-549.
37. Li, X. and Tedder, T.F. (1999) CHST1 and CHST2 sulfotransferases expressed by human vascular endothelial cells: cDNA cloning, expression, and chromosomal localization. Genomics, 55, 345-347.
38. Lo-Guidice, J.M., Wieruszeski, J.M., Lemoine, J., Verbert, A., Roussel, P., and Lamblin, G. (1994) Sialylation and sulfation of the carbohydrate chains in respiratory mucins from a patient with cystic fibrosis. J. Biol. Chem., 269, 18794-18813.
39. Maiti, A., Maki, G., and Johnson, P. (1998) TNF-alpha induction of CD44-mediated leukocyte adhesion by sulfation. Science, 282, 941-943.
40. McEver, R.P. and Cummings, R.D. (1997) Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest., 100, S97-S103.
41. Mitsuoka, C., Sawada-Kasugai, M., Ando-Furui, K., Izawa, M., Nakanishi, H., Nakamura, S., Ishida, H., Kiso, M., and Kannagi, R. (1998) Identification of a major carbohydrate capping group of the L-selectin ligand on high endothelial venules in human lymph nodes as 6-sulfo sialyl Lewis X. J. Biol. Chem., 273, 11225-11233.
42. Nakazawa, K., Takahashi, I., and Yamamoto, Y. (1998) Glycosyltransferase and sulfotransferase activities in chick corneal stromal cells before and after in vitro culture. Arch. Biochem. Biophys., 359, 269-282.
43. Ohmori, K., Kanda, K., Mitsuoka, C., Kanamori, A., Kurata-Miura, K., Sasaki, K., Nishi, T., Tamatani, T., and Kannagi, R. (2000) P- and E-selectins recognize sialyl 6-sulfo lewis X, the recently identified L-selectin ligand. Biochem. Biophys. Res. Commun., 278, 90-96.
44. Puri, K.D., Finger, E.B., Gaudernack, G., and Springer, T.A. (1995) Sialomucin CD34 is the major L-selectin ligand in human tonsil high endothelial venules. J. Cell Biol., 131, 261-270.
45. Rosen, S.D. (1999) Endothelial ligands for L-selectin: from lymphocyte recirculation to allograft rejection. Am. J. Pathol., 155, 1013-1020.
46. Sassetti, C., Van Zante, M., and Rosen, S.D. (2000) Identification of endoglycan, a member of the CD34/podocalyxin family of sialomucins. J. Biol. Chem., 275, 9001-9010.
47. Seko, A., Sumiya, J., Yonezawa, S., Nagata, K., and Yamashita, K. (2000) Biochemical differences between two types of N-acetylglucosamine→6sulfotransferases in human colonic adenocarcinomas and the adjacent normal mucosa: specific expression of a GlcNAc→6sulfotransferase in mucinous adenocarcinoma. Glycobiology, 10, 919-929.
48. Simmons, D.L. (1993) Cloning cell surface molecules by transient expression in mammalian cells. In D.A. Hartley (ed.), Cellular interactions in development. A practical approach. IRL Press, Oxford, pp. 93-127.
49. Spiro, R.G., Yasumoto, Y., and Bhoyroo, V. (1996) Characterization of a rat liver Golgi sulphotransferase responsible for the 6-O-sulphation of N-acetylglucosamine residues in beta-linkage to mannose: role in assembly of sialyl-galactosyl-N-acetylglucosamine 6-sulphate sequence of N-linked oligosaccharides. Biochem. J., 319, 209-216.
50. Tangemann, K., Bistrup, A., Hemmerich, S., and Rosen, S.D. (1999) Sulfation of an HEV-expressed ligand for L-selectin: effects on tethering and rolling of lymphocytes. J. Exp. Med., 190, 935-941.
51. Uchimura, K., Muramatsu, H., Kadomatsu, K., Fan, Q.W., Kurosawa, N., Mitsuoka, C., Kannagi, R., Habuchi, O., and Muramatsu, T. (1998a) Molecular cloning and characterization of an N-acetylglucosamine-6-O-sulfotransferase. J. Biol. Chem., 273, 22577-22583.
52. Uchimura, K., Muramatsu, H., Kaname, T., Ogawa, H., Yamakawa, T., Fan, Q.W., Mitsuoka, C., Kannagi, R., Habuchi, O., Yokoyama, I., and others. (1998b) Human N-acetylglucosamine-6-O-sulfotransferase involved in the biosynthesis of 6-sulfo sialyl Lewis X: molecular cloning, chromosomal mapping, and expression in various organs and tumor cells. J. Biochem. (Tokyo), 124, 670-678.
53. Uchimura, K., Fasakhany, F., Kadomatsu, K., Matsukawa, T., Yamakawa, T., Kurosawa, N., and Muramatsu, T. (2000) Diversity of N-acetylglucosamine-6-O-sulfotransferases: molecular cloning of a novel enzyme with different distribution and specificities. Biochem. Biophys. Res. Commun., 274, 291-296.
54. Uchimura, K., El-Fasakhany, F.M., Hori, M., Hemmerich, S., Blink, S.E., Kansas, G.S., Kanamori, A., Kumamoto, K., Kannagi, R., and Muramatsu, T. (2002) Specificities of N-acetylglucosamine-6-O-sulfotransferases in relation to L-selectin ligand synthesis and tumor-associated enzyme expression. J. Biol. Chem., 277, 3979-3984.
55. 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.
56. Watson, S.R., Imai, Y., Fennie, C., Geoffroy, J.S., Rosen, S.D., and Lasky, L.A. (1990) A homing receptor-IgG chimera as a probe for adhesive ligands of lymph node high endothelial venules. J. Cell Biol., 110, 2221-2229.
57. Yeh, J.C., Hiraoka, N., Petryniak, B., Nakayama, J., Ellies, L.G., Rabuka, D., Hindsgaul, O., Marth, J.D., Lowe, J.B., and Fukuda, M. (2001) Novel sulfated lymphocyte homing receptors and their control by a Core 1 extension beta 1,3-N-acetylglucosaminyltransferase. Cell, 105, 957-969.