Department of Respiratory Diseases, Roche Bioscience, Palo Alto, CA 94304, USA, 2Department of Anatomy and Program in Immunology, University of California, San Francisco, CA 941430452, USA, and 3Department of Epidemiology and Public Health, Yale University School of Medicine, New Haven, CT 065208034, USA
Received on July 7, 2000; revised on September 5, 2000; accepted on September 6, 2000.
![]() |
Abstract |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: sulfotransferase/chromosomal localization/genomic organization/glucosaminoglycan biosynthesis/lymphocyte homing
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Hexose units in glycoconjugates can be sulfated either at a 2-amino-group or at the 3, 4, or 6 hydroxyl groups. These regioselective sulfation modifications are facilitated in the Golgi by a class of enzymes known as carbohydrate sulfotransferases. Based on sequence similarities, some of those have been grouped into families including the heparin-sulfate sulfotransferases (Shworak et al., 1999) and the galactose/N-acetylgalactosamine/N-acetylglucosamine 6-O-sulfotransferases (GSTs). A number of other carbohydrate sulfotransferases such as the HNK-1 sulfotransferase or the galactocerebroside sulfotransferase display sequence similarities to certain glycosyltransferases or possess unique amino acid sequences (Rosen et al., 2000). The GST-family (Hemmerich and Rosen, 2000
) is a recently discovered family of carbohydrate sulfotransferases that facilitates 6-O-sulfation on the 6-hydroxyl of galactose, GalNAc or GlcNAc. To date six members of this family (GST-0 through 5) are known in human and mouse (Table I). These enzymes have been implicated in proteoglycan biosynthesis (Fukuta et al., 1995
, 1997; Uchimura et al., 1998b
; Kitagawa et al., 2000
) as well as lymphocyte homing (Hemmerich and Rosen, 2000
). Thus, a particular member of this enzyme family, GST-3, also known as high endothelial cell N-acetylglucosamine 6-sulfotransferase (HEC-GlcNAc6ST) or L-selectin ligand sulfotransferase (LSST), is highly restricted in its expression to lymph-node high endothelial venules (HEV) and has been implicated in L-selectin ligand biosynthesis (Bistrup et al., 1999
; Hiraoka et al., 1999
). It is tempting to speculate that the highly related intestinal N-acetylglucosmine 6-O-sulfotransferase GST-4 may have similar functions (Lee et al., 1999
). Other members of these family such as GST-0, -1, and -2 can sulfate GalNAc, galactose, or GlcNAc (respectively) in chondroitin sulfate or keratan sulfate biosynthesis (Fukuta et al., 1995
, 1997; Uchimura et al., 1998b
). However, at least in vitro GST-1 can also contribute to L-selectin ligand formation (Bistrup et al., 1999
). In order to facilitate further functional comparison within this family and enable gene-deletion strategies, we have determined the chromosomal localizations and genomic organizations of the genes encoding these GST enzymes in human and mouse. The human and murine genes encoding GSTs implicated in proteoglycan biosynthesis are located at loci on different chromosomes that are usually syntenic between mouse and human. The genes encoding GST-3 and GST-4 are located within the same band on chromosome 16 in human and the syntenic region on chromosome 8 in mouse.
|
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
|
|
|
Mouse homologues of human GST-1 and GST-5
A full length cDNA encoding mouse GST-1 was identified by screening GenBanks mouse EST database with a probe derived from the human GST1 ORF. The matching EST (accession number AA821661) was retrieved, and plasmid DNA sequenced in full length. This clone was found to be a full-length cDNA (2164 bp) containing a complete long ORF of 1236 bp followed by a polyadenylated 3'UTR (submitted to GenBank under accession no. AF280087). The predicted 411 aa mouse enzyme encoded by the long ORF is a typical type II transmembrane glycoprotein with 95.6% similarity and 94.2% identity to human GST-1 on the amino acid level. The mouse GST1 cDNA sequence together with translation of the ORF and a comparison to human GST-1 are shown in Figure 6. Mouse GST-5 (the murine analogue of human chondroitin 6-O-sulfotransferase-2; Kitagawa et al., 2000) has been cloned by homology screening of a mouse BAC library with a human GST-5 derived probe (GenBank accession no. AF280089; Bhakta et al., 2000
).
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Using data generated by the public human genome sequencing project, we have assembled partial or complete genomic sequences corresponding to the GST loci. Only for the GST4 locus (H4) were we able to assemble a complete 160 kDa contig (Figure 4); however, the information obtained from the other partial contigs suggest, that in human all six GST genes are organized along similar lines. Thus, except for GST0, the coding sequences (ORF) in all GST genes are contained within single exons (Figure 3). In most cases the 3'UTR is fused to the ORF within the same exon; however, the 5'UTR of the GST mRNAs are usually contained within several short exons upstream of the ORF. This overall genomic organization resembles that of the topologically and functionally related 3-galactosyltransferases and
(1,3)fucosyltransferases (Gersten et al., 1995
; Smith et al., 1996
; Amado et al., 1998
), but is very different from the genomic organization of the human heparan sulfate N-deacetylase/N-sulfotransferase genes, whose protein coding sequences are distributed over 13 or 14 exons (Gladwin et al., 1996
; Humphries et al., 1998
).
For the GST3 gene we have shown that its mRNA expressed in human tonsillar HEC utilizes a 5'UTR that is different form the 5'UTR utilized in GST3 mRNA from human gall bladder. The presence of two different 5'UTRs associated with the two cDNAs corresponding to GST3 implies that different mature mRNAs are derived by differential splicing. Features of the 5'UTR contribute significantly to the specificity and overall efficiency of translation initiation (Gary and Wickens, 1998). This is controlled at the level of secondary structure, which affects general accessibility, and also at the level of specific sequences, which interact with specific mRNA binding proteins. It is also possible that features of the 5'UTR affect the stability of the transcript, thereby conferring another level of control of expression. Thus, the expression of different 5'UTRs for GST3 possibly represents one mechanism for exerting tissue specific control of enzymatic activity.
Our analysis has revealed that the human GST4 locus (H4) contains a tandem repeat of two genes predicting highly similar isozymes GST-4 and GST-4
(Figure 3). GST-4
has been shown to encode a novel N-acetylglucosamine 6-O-sulfotransferse that is expressed predominantly in intestinal tissue. The existence of these tandem GST4 genes in the human genome is further evidenced by our Southern analysis (Figure 2). Thus, the BglII or HindIII restriction sites flanking the GST4
ORF are two BglII sites located in H4 at positions 45752 and 50139 (5' and 3' of GST4
ORF, respectively). The pertinent sites flanking the GST4
ORF are again two BglII sites located at positions 95503 and 101014 (5' and 3' of GST4
ORF, respectively). The pattern of labeled bands predicted from this arrangement (4387 bp and 5511 bp) indeed agrees with our experimental data. Of the three other enzymes used in our analysis, the closest flanking sites for the GST4
or GST4
ORF are in both cases EcoRI sites located in H4 at positions 39727, 55239, 98108, and 108392. This confirmed our observation that the banding pattern with EcoRI was unchanged by either of the other two enzymes (XbaI or ClaI) used in combination with EcoRI (Figure 2). Of the predicted band pattern (15512 bp and 10284 bp), only the 15 kb band is seen in the Figure 2. The second
4 kb band in the EcoRI digests requires the existence of an additional EcoRI site in H4 more proximal to either the GST4
or GST4
ORF. The absence of such a site could be due either to a sequencing error or to a polymorphism at an appropriate location within H4.
The existence of ESTs mapping to either GST4 (Lee et al., 1999
) or GST4
suggests that both isozymes are indeed expressed. Three overlapping human ESTs mapping to GST4
were found in a lung tumor derived library (EST AI824100) or brain libraries (Incyte ESTs). A full-length GST4
cDNA sequence (Figure 5) was constructed from these ESTs and compared to our GST4
cDNA (Lee et al., 1999
). The amino acid sequences predicted by the GST4
and GST4
ORFs are highly similar (85.6% identity). Therefore, probes derived from either ORF are unlikely to differentiate between both genes, as exemplified by our 152 bp probe from the center of the GST4
ORF, that hybridized to both genes on our Southern blot. The same probe was used previously for Northern analysis. It hybridized to a relatively abundant
2.6 kb transcript as well as at least three less abundant longer transcript at
3.5,
4.0 and
4.5 kb present only in intestinal tissue-derived mRNA (Lee et al., 1999
). Based solely on size comparison, the 2.6 kb transcript may correspond to our GST4
cDNA (2.2 kb), while the larger transcripts may correspond to the GST4
cDNA (3.8 kb). Splicing variants of both transcripts may occur. Thus, both GST4
and GST4
appear to be expressed predominantly in the intestine. Analysis of differential expression of both genes requires probes specific for one or the other gene. As discussed above, comparison of the GST4
and GST4
cDNA across their coding sequences reveals high similarity on the nucleotide and protein level. However, both cDNAs diverge rapidly about 270 bp downstream of their respective ORF stop-codons as well as 70 bp upstream of their ORF start-codons. Sequences derived from these regions are expected to be useful in design of specific probes for GST4
or GST4
gene expression.
The close proximity of both GST4 genes (<50 kb) suggests, that they may be regulated by common promoters and/or enhancers. In this context, a conspicuous triplet of binding sites for the zinc-dependent Sp1 transcription factor (Kadonaga et al., 1987) is found upstream of the GST4
gene. Though there are a few matches to human ESTs found in the region between the Sp1 triplet and the first exon of GST4
5'UTR (4a_5U4), none of these matches appears to encode a long ORF. Thus this repeat of Sp1 binding sites may be pertinent to regulation of GST4 gene expression. Sp1 binding sites are found in the 5' regulatory sequences of many genes for carbohydrate modifying enzymes, such as the genes encoding sialyltransferases ST6GalNAc III and IV (Takashima et al., 2000
), the polysialyltransferase ST8SiaIV (Eckhardt and Gerardy-Schahn, 1998
), and fucosyltransferase VII (R.Kannagi, Aichi Cancer Center, Nagoya, personal communication, 25 August 1999; GenBank accession no. AB012668). The duplication of the GST4 gene appears to have occurred recently in evolution, after the divergence of rodents and primates. Thus the mouse GST4 gene is phylogenetically more remote from human GST4
and GST4
than the two latter are from each other (Figure 7). Furthermore, the fact that all five matching mouse ESTs present in GenBanks mouse EST database map to the same mouse GST4 ORF (GenBank accession no. AF176840; Lee et al., 1999
) further supports the notion, that only one GST4 gene is present in the mouse genome.
To date, six human and four murine sulfotransferases of the GST family have been described at the molecular level. Since we have now identified mouse homologues of human GST1 (Figure 6) and human GST5 (Bhakta et al., 2000; GenBank accession no. AF280089) as well as a gene encoding a novel human GST-4 isozyme (GST4
, Figure 5), the family now includes seven human and six mouse genes. Figure 7 depicts the evolutionary relationship between these genes. Thus, the family is apparently composed of two subfamilies, one group coding for enzymes that sulfate GlcNAc and the other for those that sulfate galactose. One member of each subfamily, GST-0 and GST-5, is reported to catalyze 6-O-sulfation of GalNAc in chondroitin (Fukuta et al., 1998
; Kitagawa et al., 2000
). Each human enzyme has a mouse homologue except for the two human GST-4 isozymes that together appear to have only one mouse homologue. While similarities between family members range from 35 to 60%, cross species homologies range from 75% to nearly 100%. All members of the GST family contain three highly conserved regions as reviewed elsewhere (Hemmerich and Rosen, 2000
). Their relatively high sequence homologies and similar genomic organization suggests that these genes may have arisen through evolution by several gene duplication events from a primordial GST gene. The intriguing role that some of these enzymes may play in leukocyte migration may render them attractive targets for pharmaceutical intervention.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Chromosomal localization of GST genes by fluorescent in situ hybridization (FISH)
BAC DNA containing a given GST gene was labeled with digoxigenin dUTP by nick translation. Labeled probe was combined with sheared human DNA and hybridized to normal metaphase chromosomes derived from PHA stimulated peripheral blood lymphocytes in a solution containing 50% formamide, 10% dextran sulfate, and 2x SSC. Specific hybridization signals were detected by incubating the slides with fluoresceinated anti-digoxigenin antibodies followed by counterstaining with DAPI for one color experiments (hybridization to mouse chromosomes). Probe detection for two color experiments (all hybridizations to human chromosomes) was accomplished by incubating the slides in fluoresceinated antidigoxigenin antibodies and Texas red avidin followed by counterstaining with DAPI. The initial experiment always resulted in specific labeling of a particular chromosome whose identity was assigned on the basis of size, morphology, and banding pattern. A second experiment was conducted in which a biotin labeled probe that was specific for the heterochromatic region of the previously assigned particular chromosome was cohybridized with the pertinent GST BAC DNA. This second experiment resulted in the specific labeling of the heterochromatin (> in Figure 1) and the specific locus of the pertinent GST gene ( in Figure 1).
Southern analysis of human GST4 genomic BAC DNA
DNA generated from the BAC containing the human GST4 gene was digested with restriction enzymes EcoRI and ClaI, EcoRI and XbaI, or HindIII and BglII. These enzyme combinations were chosen because the absence of respective restriction sites within the GST4
ORF. Digests were fractionated by horizontal agarose gel electrophoresis followed by transfer of the DNA fragments to a nitrocellulose membrane. The membrane was then probed with a 32P-labeled DNA probe from the center of the GST4
ORF (AF176838, nt 620772; Lee et al., 1999
).
Cloning of a human GST4 cDNA
EST clones AI824100, 5968031,and 6869651 were retrieved from Research Genetics or Incyte Genomics, expanded in E.coli, and plasmid DNA isolated. All three plasmids were sequenced over their entire inserts on both strands. Thus, AI824100 was found to contain a 5' portion of the novel GST4 ORF as well as 5'UTR capped by a 5' EcoRI cloning site and ending in a 3' NotI cloning site that represents the internal NotI site at nt 796 in the GST4
cDNA depicted in Figure 5. EST 6869651 was found to contain the residual 3' portion of the GST4
ORF starting at the same NotI site as 5' cloning site followed by 300 bp of 3'UTR capped by a 3'EcoRI cloning site. These inserts were excised and ligated into the EcoRI site of a pCDNA3.1 expression vector (Invitrogen). Recombinant plasmids (pCDNA3.1-GST4
) were screened for correct orientation by PCR across the 5' EcoRI junction and the internal Not I junction. The sequence of this partial cDNA (AF280086 nt 11694) that contained the entire GST4
ORF was confirmed by sequencing of both strands. Incyte EST 5968031 was found to contain 2106 bp of GST4
3'UTR (AF280086 nt 1681-end). The GST4
complete cDNA sequence depicted in Figure 5 was compiled from pCDNA3.1-GST4
and EST 5968031.
![]() |
Acknowledgments |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Abbreviations |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Sequence data from this article have been deposited with the GenBank data library under accession nos. AF280086 (human GST4 cDNA), AF280087 (mouse GST1 cDNA), AF280088 (human GST3 cDNA from tonsillar high endothelial cells), and AF280089 (mouse GST5 intronless genomic coding sequence).
![]() |
Footnotes |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bhakta, S., Bartes, A., Bowman, K.G., Polsky, I., Lee, J.K., Kao, W.-M., Cook, B.N., Bruehl, R.E., Bertozzi, C.R., Rosen, S.D., and Hemmerich, S. (2000) Sulfation of N-Acetylglucosamine by chondroitin 6-O-sulfotransferase-2. J. Biol. Chem., forthcoming.
Bistrup, A., Bhakta, S., Lee, J.K., Belov, Y.Y., 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. and Bertozzi, C.R. (1999) Carbohydrate sulfotransferases: mediators of extracellular communication. Chem. Biol., 6, R9R22.
Blake, J.A., Eppig, J.T., Richardson, J.E., and Davisson, M.T. (2000) The Mouse Genome Database (MGD): expanding genetic and genomic resources for the laboratory mouse. The Mouse Genome Database Group. Nucleic Acids Res., 28, 108111.
Callen, D.F., Eyre, H., Lane, S., Shen, Y., Hansmann, I., Spinner, N., Zackai, E., McDonald-McGinn, D., Schuffenhauer, S., Wauters, J., Van Thienen, M.-N., Van Roy, B., Sutherland, G.R., and Haan, E.A. (1993) High resolution mapping of interstitial long arm deletions of chromosome 16: relationship to phenotype. J. Med. Genet., 30, 828832.[Abstract]
Eckhardt, M. and Gerardy-Schahn, R. (1998) Genomic organization of the murine polysialyltransferase gene ST8SiaIV (PST-1). Glycobiology, 8, 11651172.
Fukuta, M., Inazawa, J., Torii, T., Tsuzuki, K., Shimada, E., and Habuchi, O. (1997) Molecular cloning and characterization of human keratan sulfate Gal 6-O-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]
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.
Gary, N.K. and Wickens, M. (1998) Control of translation initiation in animals. Annu. Rev. Cell. Dev. Biol., 14, 399459.[ISI][Medline]
Gersten, K.M., Natsuka, S., Trinchera, M., Petryniak, B., Kelly, R.J., Hiraiwa, N., Jenkins, N.A., Gilbert, D.J., Copeland, N.G., and Lowe, J.B. (1995) Molecular cloning, expression, chromosomal assignment and tissue- specific expression of a murine a (1, 3)-fucosyltransferase locus corresponding to the human ELAM-1 ligand fucosyl transferase. J. Biol. Chem., 270, 2504725056.
Gladwin, A.J., Dixon, J., Loftus, S.K., Wasmuth, J.J., and Dixon, M.J. (1996) Genomic organization of the human heparan sulfate-N-deacetylase/N-sulfotransferase gene: exclusion from a causative role in the pathogenesis of Treacher Collins syndrome. Genomics, 32, 471473.[ISI][Medline]
Habuchi, O. (2000) Diversity and functions of glycosaminoglycan sulfotransferases. Biochim. Biophys. Acta, 1474, 115127.[ISI][Medline]
Hemmerich, S. and Rosen, S.D. (2000) Carbohydrate sulfotransferases in lymphocyte homing. Glycobiology, 10, 844856.
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., Manzella, S.M., and Baenziger, J.U. (1996) From legumes to leukocytes: biological roles for sulfated carbohydrates. FASEB J., 10, 11371146.
Humphries, D.E., Lanciotti, J., and Karlinsky, J.B. (1998) cDNA cloning, genomic organization and chromosomal localization of human heparan glucosaminyl N-deacetylase/N-sulphotransferase-2. Biochem. J., 332, 303307.[ISI][Medline]
Kadonaga, J.T., Carner, K.R., Masiarz, F.R., and Tjian, R. (1987) Isolation of cDNA encoding transcription factor Sp1 and functional analysis of the DNA binding domain. Cell, 51, 107990.[ISI][Medline]
Kitagawa, H., Fujita, M., Ito, N., and Sugahara, K. (2000) Molecular cloning and expression of a novel chondroitin 6-O-sulfotransferase. J. Biol. Chem., 275, 2170521080.
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]
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]
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]
Nelson, R.M., Venot, A., Bevilacqua, M.P., Linhardt, R.J., and Stamenkovic, I. (1995) Carbohydrateprotein interactions in vascular biology. Annu. Rev. Cell. Dev. Biol., 11, 601631.
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, vol. 2, pp. 245260.
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, 51705184.
Smith, P.L., Gersten, K.M., Petryniak, B., Kelly, R.J., Rogers, C., Natsuka, Y., Alford, J.A., Scheidegger, E.P., Natsuka, S., and Lowe, J.B. (1996) Expression of the (1, 3)fucosyltransferase Fuc-TVII in lymphoid aggregate high endothelial venules correlates with expression of L-selectin ligands. J. Biol. Chem., 271, 82508259.
Takashima, S., Kurosawa, N., Tachida, Y., Inoue, M., and Tsuji, S. (2000) Comparative analysis of the genomic structures and promoter activities of mouse Sia (2, 3)Gal
(1, 3)GalNAc GalNAc
(2, 6)-sialyltransferase genes (ST6GalNAc III and IV): characterization of their Sp1 binding sites. J. Biochem. (Tokyo), 127, 399409.[Abstract]
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, 467380.[Abstract]
Tsutsumi, K., Shimakawa, H., Kitagawa, H., and Sugahara, K. (1998) Functional expression and genomic structure of human chondroitin 6-O-sulfotransferase. FEBS Lett., 441, 235241.[ISI][Medline]
Uchimura, K., Kadomatsu, K., Fan, Q.W., Muramatsu, H., Kurosawa, N., Kaname, T., Yamamura, K., Fukuta, M., Habuchi, O., and Muramatsu, T. (1998a) Mouse chondroitin 6-sulfotransferase: molecular cloning, characterization and chromosomal mapping. Glycobiology, 8, 48996.
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, 2257783.
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. (Tokyo), 124, 670678.[Abstract]
Werner, W., Kraft S., Callen D.F., Bartsch, O., and Hinkel, G.K. (1997) A small deletion of 16q23.116q24.2 [del (16) (q23.1q24.2).ish del (l6) (q23.1q24.2) (D16S395+, D16S348-, P5432+)] in a boy with iris coloboma and minor anomalies. Am. J. Med. Genet., 70, 371376.[ISI][Medline]