Department of Respiratory Diseases, Roche Bioscience, 3401 Hillview Ave., Palo Alto, CA 94304-1397, USA and 2Department of Anatomy, Program in Immunology and Cardiovascular Research Institute, University of California, San Francisco, CA 94143-0452, USA
Accepted on May 10, 2000;
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Two general classes of sulfotransferases exist: cytosolic sulfotransferases, which act on small molecule substrates, including steroids, neurotransmitters, and various metabolic end products (Falany, 1997); and the Golgi-localized, usually membrane-bound sulfotransferases which transfer sulfate onto protein tyrosine residues or carbohydrates on glycoproteins, proteoglycans, and glycolipids (Bowman and Bertozzi, 1999
). Sulfation of metabolites by cytosolic sulfotransferases commonly leads to their inactivation or elimination by increasing water solubility and decreasing biological activity (Falany, 1997
). By contrast, the spectrum of biological activities conferred onto their respective acceptors by the Golgi-resident sulfotransferases is much more diverse. Thus, these sulfation reactions frequently generate specific epitopes that can be recognized by extracellular matrix proteins, cell surface receptors, and viruses (Bowman and Bertozzi, 1999
; Hooper et al., 1996
; Rosen et al., 1999
). In this context, sulfation has been shown to be a critical structural requirement of the ligand determinants recognized by the cell adhesion molecules P-selectin and L-selectin. While tyrosine-sulfation is of critical importance in a determinant recognized by P-selectin (Sako et al., 1995
; De Luca et al., 1995
; Wilkins et al., 1995
), regioselective sulfation of carbohydrates in mucin-type glycoproteins is required for the determinants recognized by L-selectin (Rosen and Bertozzi, 1996
; Fukuda et al., 1999
). This review will focus on the sulfotransferases involved in the elaboration of L-selectin ligands.
![]() |
L-selectin ligands |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Early studies demonstrated that L-selectin recognizes a carbohydrate-based determinant in lymph HEV (Stoolman and Rosen, 1983; Stoolman et al., 1984
) with an essential sialic acid moiety (Imai et al., 1991
, 1992; Rosen et al., 1985
, 1989). Furthermore, the requirement for
(1,3)-linked fucose in HEV-ligands for L-selectin has now been shown through the marked reduction of ligand activity in fucosyltransferase-VII deficient mice (Maly et al., 1996
). Both the sialylation and fucosylation requirements are shared by the other two selectins, E- and P-selectin (Larsen et al., 1992
; Lowe, 1994
; Varki, 1994
). L- and P-selectin also require sulfation for optimal recognition of their ligands. In PSGL-1, which is the best characterized P-selectin ligand (McEver and Cummings, 1997
), this sulfation occurs on tyrosine, and the sulfated tyrosine is presented to P-selectin in close vicinity to a core-2 linked sialyl Lewis x moiety (De Luca et al., 1995
; Pouyani and Seed, 1995
; Sako et al., 1995
; Leppanen et al., 1999
; Wilkins et al., 1995
). The sulfate dependence for L-selectin binding of the HEV-ligand GlyCAM-1 was first established in pharmacological experiments with metabolic inhibitors of sulfation, i.e., chlorate and brefeldin A (Imai et al., 1993
; Crommie and Rosen, 1995
). Since there are no tyrosines in GlyCAM-1, it was evident early on that the requisite sulfation in GlyCAM-1 occurs on its O-linked glycans. In fact, this carbohydrate-bound sulfate may substitute for tyrosine sulfate in P-selectin binding, since native GlyCAM-1, but not undersulfated GlyCAM-1 (generated in the presence of chlorate), is capable of binding to P-selectin (Hemmerich and Rosen, unpublished observations). Subsequent experiments demonstrated the sulfation requirement for the other L-selectin ligands in extracts of metabolically labeled lymph nodes (Hemmerich et al., 1994b
; Shailubhai et al., 1997
). Furthermore, the recognition of these ligands by MECA-79 was also shown to be sulfate-dependent (Hemmerich et al., 1994b
; Shailubhai et al., 1997
). In contrast to L-selectin, recognition of these components by MECA-79 did not require the
(1,3)-linked terminal fucose (Hemmerich et al., 1994b
; Maly et al., 1996
), providing the first indication that the MECA 79 epitope is a subregion of the L-selectin determinant.
Since sulfation of O-linked glycans is crucial for recognition of HEV-ligands by L-selectin, definition of the structural context around the critical sulfated residue(s) became of great interest. To address this problem, metabolically radio-labeled GlyCAM-1 (Hemmerich et al., 1994a) and CD34 (Hemmerich and Rosen, unpublished observations) were subjected to controlled acid hydrolysis; the singly sulfated mono- and disaccharides were analyzed. 50% of the sulfate was found on C-6 of galactose and 50% on C-6 of N-acetylglucosamine. In order to understand these sulfation modifications in the context of the fucosylation and sialylation requirements, the structures of the simplest, mono-sulfated O-linked chains in GlyCAM-1 were then determined. These studies employed metabolic radio-labeling, exoglycosidase digestions, and binding of specific lectins, in conjunction with high pH anion chromatography (Hemmerich et al., 1995
; Hemmerich and Rosen, 1994
). The simplest chains in GlyCAM-1 were found to consist of seven sugar units containing sialyl Lewis x (sLex) linked to a core 2 structure (Figure 1). The sLex tetrasaccharide is known to bind weakly to all three selectins (Varki, 1994
). 50% of these chains were sulfated at C-6 of galactose, while the other 50% were sulfated at the C-6 of N-acetylglucosamine within the sLex capping group. The monosulfated hepta-saccharides accounted for less than 25% of the O-linked chains, with the rest consisting of more complex chains, many of which were multiply sulfated (Hemmerich et al., 1995
). These structures are compatible with the hydrolysis data reviewed above, in which equal amounts of galactose-6-sulfate and N-acetylglucosamine-6-sulfate were obtained from GlyCAM-1 and CD34.
|
An independent approach to elucidating the contribution of sulfation to L-selectin ligands has utilized antibodies. Kannagi and coworkers generated monoclonal antibodies against synthetic versions of the sulfated isoforms of sLex (Mitsuoka et al., 1998). Two of the mAbs-G72 and G152-were specific for the 6-sulfo sLex epitope; these stained HEV in human lymph node and inhibited L-selectin mediated binding. In contrast, antibodies directed against 6'-sulfo sLex or 6,6'-disulfo sLex failed to stain HEV.
![]() |
Molecular cloning of relevant sulfotransferases |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
The enzymatic activity and substrate specificity for these enzymes were determined using glucosaminoglycans or synthetic oligosacharides as acceptors (Fukuta et al., 1997; Uchimura et al., 1998b
; Kitagawa et al., 2000
; Cook et al., submitted; Bhakta et al., manuscript in preparation) and/or cotransfected ligand glycoproteins (Bistrup et al., 1999
; Hiraoka et al., 1999
; Lee et al., 1999
). While C6ST was found to add sulfate to the 6-position of N-acetylgalactosamine or galactose (Fukuta et al., 1995
; Habuchi et al., 1996
), GST-1 was specific for the 6-position of galactose (Bistrup et al., 1999
; Fukuta et al., 1997
). In contrast, the other three enzymes, GST-2, -3, and -4, added sulfate to the 6-position of GlcNAc (Bistrup et al., 1999
; Hiraoka et al., 1999
; Lee et al., 1999
; Uchimura et al., 1998b
; cf. Table I). GST-5 has been reported to add sulfate to the 6-hydroxyl of GalNAc in chondroitin (Kitagawa et al., 2000
). In our hands, the same enzyme is able to sulfate at the 6-hydroxyl of GlcNAc in synthetic oligosaccharide acceptors and/or recombinant GlyCAM-1, albeit less efficiently than GST-3 (Bhakta et al., manuscript in preparation). These newly cloned sulfotransferases are probably responsible for the enzymatic activities found in tissue extracts (Spiro et al., 1996
; Spiro and Bhoyroo, 1998
; Degroote et al., 1997
, 1999). GST-3, in particular, very likely corresponds to the GlcNAc-6-O-sulfotransferase activity that is enriched in high endothelial cells of porcine lymph nodes (Bowman et al., 1998
).
![]() |
Reconstitution of L-selectin ligands |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Tangemann et al. (1999) extended these studies to an analysis of ligand function under conditions of physiological flow. In this study, recombinant GlyCAM-1/IgG was generated in COS-7 cells cotransfected with cDNAs encoding C2GnT and FucT-7, as well as a cDNA for GST-1, -2, or -3. Each recombinant fusion protein was isolated and tested for its ability to support rolling of L-selectin bearing Jurkat cells in a parallel plate rolling chamber. The GlyCAM-1/IgG modified by FucT-7 produced a measurable but low number of rolling cells. This number increased markedly when GlyCAM-1/IgG was sulfated. Sulfation at C-6 of galactose (by GST-1) was most effective, while sulfation at C-6 of N-acetylglucosamine (by either GST-2 or 3) imparted a lesser increase in the number of rolling cells. Sulfation of GlyCAM-1/IgG also enhanced tethering efficiency. Again, sulfation at C-6 of galactose was superior to sulfation at C-6 of N-acetylglucosamine. GlyCAM-1/Ig sulfated by either class of sulfotransferases also supported slower rolling of lymphocytes, indicative of stronger interactions between L-selectin and the sulfated GlyCAM-1/IgG. Interestingly, in this study, synergy between Gal 6-sulfation and GlcNAc 6-sulfation did not occur, in contrast to the results with membrane-bound CD34 in CHOsLex cells (Bistrup et al., 1999
). This discrepancy may be due to relatively short O-linked glycans in the GlyCAM-1/IgG fusion protein, which may not support multiple sulfation modifications.
The data reviewed above strongly suggest that enzymes of the novel Gal/GalNAc/GlcNAc 6-sulfotransferase (GST) gene family are involved in generation of HEV-associated L-selectin ligands. It appears that both sulfation at C-6 of galactose and sulfation at C-6 of GlcNAc (very likely in the context of 6-sulfo sLex) contribute to increased affinity of HEV-ligands to L-selectin. The two modifications may synergize to confer optimal L-selectin ligand activity. The GlcNAc-6-sulfation appears to a be prerequisite for MECA-79 binding; however, since this epitope was detected only in a subset of epithelial cells expressing 6-sulfo sLex (Kimura et al., 1999) and not in CHO cells expressing the same epitope (Bistrup, Hemmerich, and Rosen, unpublished observation), additional structural elements or a high density threshold may be required. In line with previous evidence (Michie et al., 1993
; Hemmerich et al., 1994b
; Maly et al., 1996
), it can be concluded that the epitopes recognized by L-selectin and MECA-79 do not completely overlap but share a common feature (i.e., GlcNAc-6-sulfate).
GST-3, with its remarkable restriction to HEV and high expression levels in these cells, is the most likely candidate for the dominant enzyme in the synthesis of 6-sulfo sLex in HEV. This role is further supported by its apparent specificity for core-2 linked O-glycans over N-linked glycans (Hiraoka et al., 1999), since all of the biochemically defined ligands for L-selectin are mucin-like. With respect to the 6'-sulfo sLex determinant, the regio-specificity and expression pattern of GST-1 are consistent with a possible role for this enzyme in the generation of this structure and other Gal-6-SO4 modified structures within HEV. However, this enzyme is broadly distributed. Therefore, in analogy with the HEC-restricted N-acetylglucosamine 6-sulfotransferase (GST-3), one might predict the existence of a yet undiscovered HEV-specific or more highly restricted galactose 6-sulfotransferase that sulfates L-selectin ligands in vivo. With respect to the intestinal GlcNAc 6-sulfotransferase, GST-4, its cellular expression pattern is unknown at present; however, its remarkable restriction to intestinal tissue and its high homology to GST-3 prompt the speculation that it may be involved in biosynthesis of L-selectin ligands in the HEV of mucosal lymphoid organs (Wagner et al., 1996
). As was the case in deciphering the role of the different
(1,3)fucosyltransferases in selectin ligand biosynthesis, a final definition of which of the GSTs contribute to lymphocyte homing awaits the targeted deletion of these genes in mice.
The sequence of biosynthetic steps in the elaboration of the proposed sulfated capping groups (Figure 1) is another area for further study. Since the HEC-GlcNAc-6-sulfotransferase GST-3 requires terminal GlcNAc for enzymatic activity (Cook et al., submitted), it is predicted to act early in the biosynthetic process, immediately after the addition of the core-2 GlcNAc by a core-2 branching enzyme such as C2GnT (Bierhuizen and Fukuda, 1992) and/or at a terminal GlcNAc in a core-2 linked polylactosamine chain. Following the addition of the GlcNAc 6-sulfate, a ß(1,4)-galactosyltransferase that is permissive of 6-sulfation on the acceptor GlcNAc (Seko et al., 1998
) would add the galactose, followed by
(2,3)-sialylation at this galactose by an
(2,3)sialyltransferase. Since FucT-7 requires
(2,3)-sialylated lactosamine as its acceptor, but is not permissive for 6-sulfation at galactose (Maly et al., 1996
),
(1,3) fucosylation at GlcNAc must occur as the next step. Therefore, 6-sulfation at galactose is expected to be the final step in biosynthesis of either 6'-sulfo sLex or 6',6-disulfo sLex. Obviously, many steps in this proposed scheme are speculative and have to be confirmed experimentally. In this context, Habuchi and colleagues (Torii et al., 2000
) have recently shown that GST-1 effectively sulfates the 6-position of galactose in
(2,3)-sialyllactosamine, but not in sLex, mitigating against a role of this enzyme in the synthesis of 6'-sulfo sLex or the 6',6-disulfo sLex structure. It is conceivable that the increase in L-selectin ligand activity conferred by this enzyme in the binding and rolling studies reviewed above (Bistrup et al., 1999
; Tangemann et al., 1999
) was due to the presentation of 6'-sulfo sialyllactosamine capping groups (or internal galactose 6-sulfate modifications) in conjunction with sLex-capped chains. This latter possibility is reminiscent of the model of "clustered saccharide patches" proposed by Varki (1994)
.
![]() |
Conclusions |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
While HEV-expressed L-selectin ligands normally function in the process of leukocyte homing to peripheral lymphoid organs, L-selectin is also implicated in lymphocyte recruitment to sites of chronic inflammation, where MECA 79 positive HEV-like vessels can be induced (reviewed in Rosen, 1999; Girard and Springer, 1995
). To date, there is one report of the induction of GST-3 transcripts in HEV-like vessels in a murine model of thymic hyperplasia (Hiraoka et al., 1999
). Induction of this enzyme and the other members of the GST family in further examples of inflammation, particularly in human diseases, is an area of further great interest. New targets for anti-inflammatory therapeutics may emerge from such studies.
![]() |
Acknowledgments |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Baeuerle,P.A. and Huttner,W.B. (1986) Chloratea potent inhibitor of protein sulfation in intact cells. Biochem. Biophys. Res. Commun., 141, 870877.[ISI][Medline]
Baumhueter,S., Singer,M.S., Henzel,W., Hemmerich,S., Renz,M., Rosen,S.D. and Lasky,L.A. (1993) Binding of L-Selectin to the Vascular Sialomucin, CD34. Science, 262, 436438.[ISI][Medline]
Baumhueter,S., Dubal,N., Kyle,C. and Lasky,L.A. (1994) Global vascular expression of CD34, a sialomucin-like ligand for L-selectin. Blood, 84, 25542565.
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, 343349.[Abstract]
Bertozzi,C.R., Fukuda,S. and Rosen,S.D. (1995) Sulfated dissaccharide inhibitors of L-selectin; deriving structural leads from a physiological selectin ligand. Biochemistry, 34, 1427114278.[ISI][Medline]
Bierhuizen,M.F. and Fukuda,M. (1992) Expression cloning of a cDNA encoding UDP-GlcNAc:Gal ß (1,3)GalNAc-R (GlcNAc to GalNAc) ß (1,6)GlcNAc transferase by gene transfer into CHO cells expressing polyoma large tumor antigen. Proc. Natl Acad. Sci. USA, 89, 93269330.[Abstract]
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, 899910.
Bowman,K.G., Hemmerich,S., Bhakta,S., Singer,M.S., Bistrup,A., Rosen,S.D. and Bertozzi,C.R. (1998) Identification of an N-acetylglucosamine-60-sulfotransferase activity specific to lymphoid tissue: an enzyme with a possible role in lymphocyte homing. Chem. Biol., 5, 447460.[ISI][Medline]
Bowman,K.G. and Bertozzi,C.R. (1999) Carbohydrate sulfotransferases: mediators of extracellular communication. Chem. Biol., 6, R9R22.[ISI][Medline]
Butcher,E.C. and Picker,L.J. (1996) Lymphocyte homing and homeostasis. Science, 272, 6066.[Abstract]
Clark,R.A., Fuhlbrigge,R.C. and Springer,T.A. (1998) L-Selectin ligands that are O-glycoprotease resistant and distinct from MECA-79 antigen are sufficient for tethering and rolling of lymphocytes on human high endothelial venules. J. Cell Biol., 140, 721731.
Crommie,D. and Rosen,S.D. (1995) Biosynthesis of GlyCAM-1, a mucin-like ligand for L-selectin. J. Biol. Chem., 270, 2261422624.
De Luca,M., Dunlop,L.C. Andrews,R.K., Flannery,J.V.,Jr., Ettling,R., Cumming,D.A., Veldman,M. and Berndt,M.C. (1995) A novel cobra venom metalloproteinase, mocarhagin, cleaves a 10-amino acid peptide from the mature N terminus of P-selectin glycoprotein ligand receptor, PSGL-1 and abolishes P-selectin binding. J. Biol.Chem., 270, 2673426737.
Degroote,S., Lo-Guidice,J.M., Strecker,G., Ducourouble,M.P., Roussel,P. and Lamblin,G. (1997) Characterization of an N-acetylglucosamine-6-O-sulfotransferase from human respiratory mucosa active on mucin carbohydrate chains. J. Biol. Chem., 272, 2949329501.
Degroote,S., Ducourouble,M.P., Roussel,P. and Lamblin,G. (1999) Sequential biosynthesis of sulfated and/or sialylated Lewis x determinants by transferases of the human bronchial mucosa. Glycobiology, 9, 11991211.
Dowbenko,D., Kikuta,A., Fennie,C., Gillett,N. and Lasky,L.A. (1993) Glycosylation-dependent cell adhesion molecule 1 (GlyCAM-1) mucin is expressed by lactating mammary gland epithelial cells and is present in milk. J. Clin. Invest., 92, 952960.[ISI][Medline]
Falany,C.N. (1997) Enzymology of human cytosolic sulfotransferases. FASEB J., 11, 206216.
Feizi,T. and Galustian,C. (1999) Novel oligosaccharide ligands and ligand-processing pathways for the selectins. Trends Biochem.. Sci., 24, 369372.[ISI][Medline]
Fuhlbrigge,R.C., Alon,R., Puri,K.D., Lowe,J.B. and Springer,T.A. (1996) Sialylated, fucosylated ligands for L-selectin expressed on leukocytes mediate tethering and rolling adhesions in physiologic flow conditions. J. Cell Biol., 135, 837848.[Abstract]
Fukuda,M., Hiraoka,N. and Yeh,J.-C. (1999) C-type lectins and sialyl Lewis x oligosaccharides: versatile roles in cell-cell interaction. J. Cell Biol., 147, 467470.
Fukuta,M., Uchimura,K., Nakashima,K., Kato,M., Kimata,K., Shinomura,T. and Habuchi,O. (1995) Molecular cloning and expression of chick chondrocyte chondroitin 6-sulfotransferase. J.Biol.Chem., 270, 1857518580.
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, 3232132328.
Fukuta,M., Kobayashi,Y., Uchimura,K., Kimata,K. and Habuchi,O. (1998). Molecular cloning and expression of human chondroitin 6-sulfotransferase. Biochim. Biophys. Acta, 1399, 5761.[ISI][Medline]
Galustian,C., Lawson,A.M., Komba,S., Ishida,H., Kiso,M. and Feizi,T. (1997) Sialyl-Lewis x sequence 6-O-sulfated at N-acetylglucosamine rather than at galactose is the preferred ligand for L-selectin and de-N-acetylation of the sialic acid enhances its binding strength. Biochem. Biophys. Res. Commun., 240, 748751.[ISI]
Girard,J.-P. and Springer,T.A. (1995) High endothelial venules: specialized endothelium for lymphocyte migration. Immunology Today, 16, 449457.[ISI][Medline]
Girard,J.-P., Baekkevold,E.S. and Amalric,F. (1998) Sulfation in high endothelial venules: cloning and expression of the human PAPS synthetase. FASEB J., 12, 603612.
Girard,J.-P., Baekkevold,E.S., Feliu,J. and Amalric,F. (1999) Molecular cloning and functional analysis of SUT-1, a sulfate transporter from human high endothelial venules. Proc. Natl Acad. Sci. USA, 96, 1277212777.
Habuchi,O., Hirahara,Y., Uchimura,K. and Fukuta,M. (1996) Enzymatic sulfation of galactose residue of keratan sulfate by chondroitin 6-sulfotransferase. Glycobiology, 6, 5157.[Abstract]
Habuchi,O., Suzuki,Y. and Fukuta,M. (1997) Sulfation of sialyl lactosamine oligosaccharides by chondroitin 6-sulfotransferase. Glycobiology, 7, 405412.[Abstract]
Hemmerich,S. and Rosen,S.D. (1994) 6'-sulfated, sialyl Lewis x is a major capping group of GlyCAM-1. Biochemistry, 33, 48304835.[ISI][Medline]
Hemmerich,S., Bertozzi,C.R., Leffler,H. and Rosen,S.D. (1994a) Identification of the sulfated monosaccharides of GlyCAM-1, an endothelial derived ligand for L-selectin. Biochemistry, 33, 48204829.[ISI][Medline]
Hemmerich,S., Butcher,E.C. and Rosen,S.D. (1994b) Sulfation-dependent recognition of HEV-ligands by L-selectin and MECA 79, an adhesion-blocking mAb. J. Exp. Med., 180, 22192226.[Abstract]
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, 1203512047.
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, 7989.[ISI][Medline]
Hooper,L.V., Monsella,S.M. and Baenziger,J.U. (1996) From legumes to leukocytes: biological roles for sulfated carbohydrates. FASEB J., 10, 11371146.
Imai,Y., Lasky,L.A. and Rosen,S.D. (1992) Further characterization of the interaction between L-selectin and its endothelial ligands. Glycobiology, 2, 373381.[Abstract]
Imai,Y., Lasky,L.A. and Rosen,S.D. (1993) Sulphation requirement for GlyCAM-1, an endothelial ligand for L-selectin. Nature, 361, 555557.[ISI][Medline]
Imai,Y., Singer,M.S., Fennie,C., Lasky,L.A. and Rosen,S.D. (1991) Identification of a carbohydrate-based endothelial ligand for a lymphocyte homing receptor. J. Cell Biol., 113, 12131221.[Abstract]
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 (1,3)fucosyltransferase VII and newly cloned GlcNAcß:6-sulfotransferase cDNA. Proc. Natl Acad. Sci. USA, 96, 45304535.
Kitagawa,H., Fujita,M., Ito,N. and Sugahara,K. (2000) Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem., (in press: manuscript posted on the World Wide Web at http://www.jbc.org/cgi/reprint/M002101200v1.pdf).
Klaassen,C.D. and Boles,J.W. (1997) Sulfation and sulfotransferases. 5: the importance of 3'- phosphoadenosine 5'-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J., 11, 404418.
Koenig,A., Jain,R., Vig,R., Norgard-Sumnicht,K.E., Matta,K.L. and Varki,A. (1997) Selectin inhibition: Synthesis and evaluation of novel sialylated, sulfated and fucosylated oligosaccharides, including the major capping group of GlyCAM-1. Glycobiology, 7, 7993.[Abstract]
Larsen,G.R., Sako,D., Ahern,T.J., Shaffer,M., Erban,J., Sajer,S.A., Gibson,R.M., Wagner,D.D., Furie,B.C. and Furie,B. (1992) P-selectin and E-selectin. Distinct but overlapping leukocyte ligand specificities. J. Biol. Chem., 267, 1110411110.
Lasky,L.A., Singer,M.S., Dowbenko,D., Imai,Y., Henzel,E.J., Fennie,C., Gillett,N., Watson,S.R. and Rosen,S.D. (1992) An endothelial ligand for L-selectin is a novel mucin-like molecule. Cell, 69, 927938.[ISI][Medline]
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, 543549.[ISI][Medline]
Lee,M.S. and Sarvetnick,N. (1994) Induction of vascular addressins and adhesion molecules in the pancreas of IFN-gamma transgenic mice. J. Immunol., 152, 45974603.
Leppanen,A., Mehta,P., Ouyang,Y.B., Ju,T., Helin,J., Moore,K.L., van Die,I., Canfield,W.M., McEver,R.P. and Cummings,R.D. (1999) A novel glycosulfopeptide binds to P-selectin and inhibits leukocyte adhesion to P-selectin. J. Biol. Chem., 274, 2483824848.
Li,H., Deyrup,A., Mensch,J.R. Jr., Domowicz,M., Konstantinidis,A.K. and Schwartz,N.B. (1995) The isolation and characterization of cDNA encoding the mouse bifunctional ATP sulfurylase-adenosine 5'-phosphosulfate kinase. J. Biol. Chem., 270, 2945329459.
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, 345347.[ISI][Medline]
Lowe,J.B. (1994) Carbohydrate recognition in cell-cell interaction. In Fukuda,M. and Hindsgaul,O. (eds.), Molecular Glycobiology. IRL Press, New York, 163205.
Maly,P., Thall,A.D., Petryniak,B., Rogers,C.E., Mith,P.L., Marks,R.M., Kelly,R.J., Gersten,K.M., Cheng,G., Saunders,T.L., Camper,S.A., Camphausen,R.T., Sullivan,F.X., Isogai,Y., Hindsgaul,O., von Andrian,U.H. and Lowe,J.B. (1996) The Fuc-TVII alpha (1,3)fucosyltransferase controls lymphocyte homing and blood leukocyte emigration through an essential role in L-,E- and P-selectin ligand biosynthesis. Cell, 86, 643653.[ISI][Medline]
Mazany,K.D., Peng,T., Watson,C.E., Tabas,I. and Williams,K.J. (1998) Human chondroitin 6-sulfotransferase: cloning, gene structure and chromosomal localization. Biochim. Biophys. Acta, 1407, 9297.[ISI][Medline]
McEver,R.P. and Cummings,R.D. (1997) Role of PSGL-1 binding to selectins in leukocyte recruitment. J. Clin. Invest., 100, 97103.
Michie,S.A., Streeter,P.R., Bolt,P.A., Butcher,E.C. and Picker,L.J. (1993) The human peripheral lymph node vascular addressin. Am. J. Pathol., 143, 16881698.[Abstract]
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, 1122511233.
Onrust,S.V., Hartl,P.M., Rosen,S.D. and Hanahan,D. (1996) Modulation of L-selectin ligand expression during an immune response accompanying tumorigenesis in transgenic mice. J. Clin. Invest., 97, 5464.
Pouyani,T. and Seed,B. (1995) PSGL-1 recognition of P-selectin is controlled by a tyrosine sulfation consensus at the PSGL-1 amino terminus. Cell, 83, 333343.[ISI][Medline]
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, 261270.[Abstract]
Rosen,S.D. (1999) Endothelial ligands for L-selectin: from lymphocyte recirculation to allograft rejection. Am. J. Pathol., 155, 10131020.
Rosen,S.D. and Bertozzi,C.B. (1996) Leukocyte adhesion: two selectins converge on sulphate. Curr. Biol., 6, 261264.[ISI][Medline]
Rosen,S.D., Singer,M.S., Yednock,T.A. and Stoolman,L.M. (1985) Involvement of sialic acid on endothelial cells in organ-specific lymphocyte recirculation. Science, 228, 10051007.[ISI][Medline]
Rosen,S.D., Chi,S.-I., True,D.D., Singer,M.S. and Yednock,T.A. (1989) Intravenously injected sialidase inactivates attachment sites for lymphocytes on high endothelial venules. J. Immunol., 142, 18951902.
Rosen,S.D., Bistrup,A. and Hemmerich,S. (1999) Carbohydrate Sulfotransferases. In Ernst,B., Sinaÿ,P. and Hart,G. (eds.), Oligosaccharides in Chemistry and Biology. Wiley-VCH, Weinheim, in press.
Sako,D., Comess,K.M., Barone,K.M., Camphausen,R.T., Cumming,D.A. and Shaw,G.D. (1995) A sulfated peptide segment at the amino terminus of PSGL-1 is critical for P-selectin binding. Cell, 83, 323331.[ISI][Medline]
Sassetti,C., Tangemann,K., Singer,M.S., Kershaw,D.B. and Rosen,S.D. (1998) Identification of podocalyxin as an HEV ligand for L-selectin: parallels to CD34. J. Exp. Med., 187, 19651975.
Saunders,W.J., Katsumoto,T.R., Bertozzi,C.R., Rosen,S.D. and Kiessling,L.L. (1996) Selectin-carbohydrate interactions: an investigation into the relevant modifications of the Lewis x trisaccharides. Biochemistry, 35, 1486214867.[ISI][Medline]
Saunders,W.J., Gordon,E.J., Dwir,O., Beck,P.J., Alon,R. and Kiessling,L.L. (1999) Inhibition of L-selectin mediated leukocyte rolling by synthetic glycoprotein mimics. J. Biol. Chem., 274, 52715278.
Scudder,P.R., Shailubhai,K., Duffin,K.L., Streeter,P.R. and Jacob,G.S. (1994) Enzymatic synthesis of a 6-sulfated sialyl-Lewis x which is an inhibitor of L-selectin binding to peripheral addressin. Glycobiology, 4, 929933.[Abstract]
Shailubhai,K., Streeter,P., Smith,C.E. and Jacob,G.S. (1997) Sulfation and sialylation requirements for a glycoform of CD34, a major endothelial ligand for L-selectin in porcine peripheral lymph nodes. Glycobiology, 7, 305314.[Abstract]
Seko,A., Hara-Kuge,S., Yonezawa,S., Nagata,K. and Yamashita,K. (1998) Identification and characterization of N-acetylglucosamine-6-O-sulfate specific ß1,4-galactosyltransferase in human colorectal mucosa. FEBS Lett., 440, 307310.[ISI][Medline]
Shworak,N.W., Liu,J., Petros,L.M., Zhang,L., Kobayashi,M., Copeland,N.G., Jenkins,N.A. and Rosenberg,R.D. (1999) Multiple isoforms of heparan sulfate D-glucosaminyl 3-O- sulfotransferase. Isolation, characterization and expression of human cDNAs and identification of distinct genomic loci. J. Biol. Chem., 274, 517084.
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, 209216.[ISI][Medline]
Spiro,R.G. and Bhoyroo,V. (1998) Characterization of a spleen sulphotransferase responsible for the 6-O- sulphation of the galactose residue in sialyl-N-acetyl-lactosamine sequences. Biochem. J., 331, 265271.[ISI][Medline]
Stoolman,L.M. and Rosen,S.D. (1983) Possible role for cell-surface carbohydrate-binding molecules in lymphocyte recirculation. J. Cell Biol., 96, 722729.[Abstract]
Stoolman,L.M., Tenforde,T.S. and Rosen,S.D. (1984) Phosphomannosyl receptors may participate in the adhesive interaction between lymphocytes and high endothelial venules. J. Cell Biol., 99, 15351540.[Abstract]
Streeter,P.R., Rouse,B.T.N. and Butcher,E.C. (1988) Immunohistologic and functional characterization of a vascular addressin involved in lymphocyte homing into peripheral lymph nodes. J. Cell Biol., 107, 18531862.[Abstract]
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, 935941.
Thompson,J.D., Higgins,D.G. and Gibson,T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence-weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res., 22, 46734680.[Abstract]
Torii,T., Fukuta,M. and Habuchi,O. (2000) Sulfation of sialyl N-acetyllactosamine oligosaccharides and fetuin oligosaccharides by keratan sulfate Gal-6-sulfotransferase. Glycobiology, 10, 203211.
Tsuboi,S., Isogai,Y., Hada,N., King,J.K., Hindsgaul,O. and Fukuda,M. (1996) 6'-Sulfo sialyl Lex but not 6-sulfo sialyl Lex expressed on the cell surface supports L-selectin-mediated adhesion. J. Biol. Chem., 271, 2721327216.
Uchimura,K., Kadomatsu,K., Fan,Q.W., Muramatsu,H., Kurosawa,N., Kaname,T., Yamamura,K., Fukuta,M., Habuchi,O. and Muramatsu,H. (1998a) Mouse chondroitin 6-sulfotransferase: molecular cloning, characterization and chromosomal mapping. Glycobiology, 8, 489496.
Uchimura,K., Muramatsu,H., Kadomatsu,K., Fan,Q.W., Kurosawa,N., Mitsuoka,C., Kannagi,R., Habuchi,O. and Muramatsu,T. (1998b) Molecular cloning and characterization of an N-acetylglucosamine-6-O-sulfotransferase. J. Biol. Chem., 273, 2257722583.
Uchimura,K., Muramatsu,H., Kaname,T., Ogawa,H., Yamakawa,T., Fan,Q.W., Mitsuoka,C., Kannagi,R., Habuchi,O., Yokoyama,I., Yamamura,K., Ozaki,T., Nakagawara,A., Kadomatsu,K. and Muramatsu,T. (1998c) 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., 124, 670678.[Abstract]
Varki,A. (1994) Selectin ligands. Proc. Natl Acad. Sci. USA, 91, 73907397.[Abstract]
Vestweber,D. and Blanks,J.E. (1999) Mechanisms that regulate the function of the selectins and their ligands. Physiol. Rev., 79, 181213.
Wagner,N., Löhler,J., Kunkel,E.J.,Ley,K., Leung,E., Krissansen,G., Rajewsky,K. and Müller,W. (1996) Critical role for ß7 integrins in formation of the gut-associated lymphoid tissue. Nature, 382, 366370.[ISI][Medline]
Wilkins,P.P., Moore,K.L., McEver,R.P. and Cummings,R.D. (1995) Tyrosine sulfation of P-selectin glycoprotein ligand-1 is required for high affinity binding to P-selectin. J.Biol.Chem., 270, 2267722680.
Yoshino,K., Ohmoto,H., Kondo,N., Tsujishita,H., Hiramatsu,Y., Inoue,Y. and Kondo,H. (1997) Studies on selectin blockers.4. Structure-function relationships of sulfated sialyl Lewis x hexasaccharide ceramides toward E-, P- and L-selectin binding. J. Med. Chem., 40, 455462.[ISI][Medline]