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J. Biol. Chem., Vol. 279, Issue 4, 2337-2340, January 23, 2004

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ACCELERATED PUBLICATIONS

N-Acetylglucosaminyltransferase IX Acts on the GlcNAc1,2-Man1-Ser/Thr Moiety, Forming a 2,6-Branched Structure in Brain O-Mannosyl Glycan^*

Kei-ichiro Inamori, Takeshi Endo, Jianguo Gu, Ichiro Matsuo, Yukishige Ito, Shigeru Fujii¶, Hiroko Iwasaki||, Hisashi Narimatsu||, Eiji Miyoshi, Koichi Honke**, and Naoyuki Taniguchi

From the Department of Biochemistry, Osaka University Medical School, 2-2 Yamadaoka, Suita, Osaka 565-0871, Japan, the RIKEN (The Institute of Physical and Chemical Research), 2-1 Hirosawa, Wako-shi, Saitama 351-0198, Japan, the ^¶Laboratory of Chemistry, Kansai Medical University, 18-89 Uyama-Higashi, Hirakata, Osaka 573-1136, Japan, the ^||Glycogene Function Team, Research Center for Glycoscience, National Institute of Advanced Industrial Science and Technology, Open Space Laboratory C-2, 1-1-1 Umezono, Tsukuba, Ibaraki 305-8568, Japan, and the ^**Department of Molecular Genetics, Kochi Medical School, Kohasu, Oko-cho, Nankoku, Kochi 783-8505, Japan

Received for publication, October 31, 2003 , and in revised form, November 13, 2003.

	ABSTRACT

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS AND DISCUSSION REFERENCES

 
Mammals contain O-linked mannose residues with 2-mono- and 2,6-di-substitutions by GlcNAc in brain glycoproteins. It has been demonstrated that the transfer of GlcNAc to the 2-OH position of the mannose residue is catalyzed by the enzyme, protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1), but the enzymatic basis of the transfer to the 6-OH position is unknown. We recently reported on a brain-specific 1,6-N-acetylglucosaminyltransferase, GnT-IX, that catalyzes the transfer of GlcNAc to the 6-OH position of the mannose residue of GlcNAc1,2-Man on both the 1,3- and 1,6-linked mannose arms in the core structure of N-glycan (Inamori, K., Endo, T., Ide, Y., Fujii, S., Gu, J., Honke, K., and Taniguchi, N. (2003) J. Biol. Chem. 278, 43102–43109). Here we examined the issue of whether GnT-IX is able to act on the same sequence of the GlcNAc1,2-Man in O-mannosyl glycan. Using three synthetic Ser-linked mannose-containing saccharides, Man1-Ser, GlcNAc1,2-Man1-Ser, and Gal1,4-GlcNAc1,2-Man1-Ser as acceptor substrates, the findings show that ¹⁴C-labeled GlcNAc was incorporated only into GlcNAc1,2-Man1-Ser after separation by thin layer chromatography. To simplify the assay, high performance liquid chromatography was employed, using a fluorescence-labeled acceptor substrate GlcNAc1,2-Man1-Ser-pyridylaminoethylsuccinamyl (PAES). Consistent with the above data, GnT-IX generated a new product which was identified as GlcNAc1,2-(GlcNAc1,6-)Man1-Ser-PAES by mass spectrometry and ¹H NMR. Furthermore, incorporation of an additional GlcNAc residue into a synthetic mannosyl peptide Ac-Ala-Ala-Pro-Thr(Man)-Pro-Val-Ala-Ala-Pro-NH₂ by GnT-IX was only observed in the presence of POMGnT1. Collectively, these results strongly suggest that GnT-IX may be a novel 1,6-N-acetylglucosaminyltransferase that is responsible for the formation of the 2,6-branched structure in the brain O-mannosyl glycan.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS AND DISCUSSION REFERENCES

 
Nearly all secreted and cell surface proteins in mammalian cells are glycosylated, and two major groups on glycoproteins are N- and O-glycans. In O-glycans, the mucin-type O-GalNAc linkage and O-xylose linkage in proteoglycans are well known. In addition to these O-glycans, several other unique linkages such as O-linked fucose (1–3), O-linked glucose (2, 4), O-linked GlcNAc (5, 6), and O-linked mannose (7) have also been reported. O-Mannosylation is one of the rare types of O-glycosylation in mammals, existing in a limited number of glycoproteins of brain, nerve, and skeletal muscle (7). One of the obvious functional roles of O-mannosylation has been shown to involve a sialyl O-mannosyl glycan, Sia2,3-Gal1,4-GlcNAc1,2-Man, is the laminin binding ligand of -dystroglycan (8). Recently, protein O-mannose 1,2-N-acetylglucosaminyltransferase (POMGnT1),¹ which catalyzes the transfer of GlcNAc to O-linked mannose of glycoproteins, was identified and the POMGnT1 gene was demonstrated to be responsible for muscle-eye-brain disease (MEB) (9, 10). MEB is congenital muscular dystrophy caused by a defect in the binding activity of dystroglycan to its ligands, including laminin, neurexin, and agrin due to the hypoglycosylation of -dystroglycan (11).

Interestingly, O-mannosyl glycan is one of major O-glycans in the brain (its ratio to the O-linked GalNAc is about 1:3), which contains GlcNAc1,2-Man and GlcNAc1,2-(GlcNAc1,6-)Man structures (12). In addition, the brain contains the HNK-1 epitope (sulfoglucuronyl lactosamine) carried on O-mannosyl glycans that contain 2-mono- and 2,6-di-substituted mannose (13). To date, it has been demonstrated that the GlcNAc1,2-Man linkage is formed by the action of POMGnT1, but the enzymatic basis of the formation of the GlcNAc1,6-Man linkage in O-mannosyl glycan remains unclear.

We recently identified a new 1,6-N-acetylglucosaminyltransferase, GnT-IX, as a homolog of N-acetylglucosaminyltransferase V (GnT-V), which is specifically expressed in the brain (14). GnT-IX was found to catalyze the transfer of GlcNAc to the 6-OH position of the mannose in the sequence of GlcNAc1,2-Man, present in both the 1,3- and 1,6-linked mannose arms in the core structure of N-glycan. In the present study, we provide evidence to show that GnT-IX also catalyzes the transfer of GlcNAc in 1,6-linkage to O-mannosyl glycan, indicating that GnT-IX is responsible for the formation of the 2,6-branched structure of O-mannosyl glycans in the brain.

	EXPERIMENTAL PROCEDURES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS AND DISCUSSION REFERENCES

 
Materials—Ser-linked mannose-containing saccharides, Man1-O-Ser, GlcNAc1,2-Man1-O-Ser, and Gal1,4-GlcNAc1,2-Man1-O-Ser were synthesized as reported previously (15). GlcNAc1,2-Man1-O-Ser was fluorescence-labeled with N-[2-(2-pyridylamino)ethyl]succinamic acid 5-norbornene-2,3-dicarboxyimide ester (Wako, Osaka, Japan) and the labeled substrate (GnM-S-PAES) was purified by TSKgel Amide-80 column (21.5 x 300 mm; Tosoh) and TSKgel ODS-80TM column (7.8 x 300 mm; Tosoh) using a Shimadzu LC-VP HPLC system. The labeled substrate was eluted with a linear gradient of acetonitrile in 0.1% trifluoroacetic acid from an amide column and with 20 mM ammonium acetate (pH 4.0) from an ODS column and monitored with a fluorescence spectrophotometer (excitation, 320 nm; emission, 400 nm). The synthetic mannosyl peptide (Ac-Ala-Ala-Pro-Thr(Man)-Pro-Val-Ala-Ala-Pro-NH₂) was kindly provided by Dr. Toshiyuki Inazu (Department of Applied Chemistry, School of Engineering, Tokai University). Recombinant soluble GnT-IX was prepared as described previously (14).

Activity Assay for GnT-IX—The activity assay using the synthetic Ser-linked mannose-containing saccharides as acceptor substrates was performed in a mixture of 0.1 M MOPS (pH 7.5), 10 mM EDTA, 21.9 µM UDP-[¹⁴C]GlcNAc (71.2 Ci/mol), 0.5 mM substrate and recombinant soluble GnT-IX in a volume of 20 µl. After incubation for 12 h at 37 °C, the reaction mixture was boiled for 3 min, diluted with 80 µl of water, and then passed through an AG-X8 column (Bio-Rad, acetate form, 0.1 ml). The flow-through was evaporated and redissolved in 10 µl of water and then applied to a Silica gel 60 HPTLC plate (Merck). The plate was developed with methanol:n-butyl alcohol:acetic acid:water (2:2:1:1 by volume), and the incorporation of the radioactivity was visualized by a phosphorimager (BAS-2500, Fuji Film, Tokyo). The reaction using a synthetic mannosyl peptide, Ac-Ala-Ala-Pro-Thr(Man)-Pro-Val-Ala-Ala-Pro-NH₂, was performed in a mixture of 0.1 M MOPS (pH 7.5), 10 mM MnCl₂,40mM UDP-GlcNAc, 200 mM GlcNAc, 0.5% Triton X-100, 40 µM mannosyl peptide, with or without recombinant soluble GnT-IX and partially purified recombinant POMGnT1. The enzymatic product was separated by HPLC.

MALDI-TOF MS Analysis—MALDI-TOF MS was performed with a Perseptive Biosystems Voyager RP-DE instrument. The mass spectra were acquired in the reflectron mode under a 20 kV accelerating voltage with positive detection. 2,5-Dihydroxybenzoic acid (10 mg/ml) was used as the matrix.

NMR Analysis—For preparation of the NMR sample, a large scale reaction was carried out in a mixture of 0.1 M MOPS (pH 7.5), 10 mM EDTA, 40 mM UDP-GlcNAc, 100 mM GlcNAc, 0.5 M glycine, 0.5 mM GnM-S-PAES, and recombinant soluble GnT-IX. After 36 h of incubation at 37 °C, the reaction product was isolated using a TSKgel ODS-80TM column (7.8 x 300 mm, Tosoh) as described previously (14). The separated sugar chains were lyophilized, dissolved in 99.9% D₂O, and then lyophilized from D₂O twice and dissolved in this solvent. Proton NMR measurements were carried out on a Varian Unity-400 spectrometer at 400 MHz at 30 °C. Chemical shifts are expressed as parts per million (ppm) relative to an external standard of 3-(trimethylsilyl)propionic acid-d₄.

	RESULTS AND DISCUSSION

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS AND DISCUSSION REFERENCES

 
The reports of GlcNAc substitution at the 6-OH position of mannose in the brain O-mannosyl glycans (12, 13) prompted us to investigate whether GnT-IX was able to act, not only on the 1,3- and 1,6-linked mannose arms of the core of N-glycan, but on the GlcNAc1,2-Man in the O-mannosyl glycan as well. Three synthetic Ser-linked mannose-containing saccharides, Man1-O-Ser, GlcNAc1,2-Man1-O-Ser, and Gal1,4-GlcNAc1,2-Man1-O-Ser, were separately incubated with recombinant soluble GnT-IX and UDP-[¹⁴C]GlcNAc. After incubation, unreacted UDP-[¹⁴C]GlcNAc was removed by anion-exchange column chromatography and the reaction product was separated on HPTLC. Interestingly, radioactivity was incorporated only when GlcNAc1,2-Man1-O-Ser was used as an acceptor (Fig. 1A). When POMGnT1 and GnT-IX were simultaneously incubated with a synthetic mannosyl peptide, Ac-Ala-Ala-Pro-Thr(Man)-Pro-Val-Ala-Ala-Pro-NH₂, two GlcNAc residues were incorporated into the substrate (m/z values for (M + Na)⁺ of 1425.6 and (M + K)⁺ of 1441.5), but no transfer was detected by GnT-IX in the absence of POMGnT1 (data not shown), as confirmed by HPLC and MS analysis (Fig. 2C) of the enzymatic product. It supports the view that GnT-IX acts on the GlcNAc1,2-Man structure in O-mannosyl glycans of glycoproteins as a substrate, and the action is dependent on prior action of POMGnT1. This substrate specificity is similar to that of the homolog, GnT-V, which is not able to catalyze the transfer of GlcNAc to the galactosylated biantennary sugar chains, as reported previously (16).

View larger version (51K): [in this window] [in a new window]   FIG. 1. N-Acetylglucosaminyltransferase assay using Ser-linked mannose-containing saccharides and the elution profile of the reaction mixture on HPLC. A, synthetic Ser-linked mannose-containing saccharides were used as acceptor substrates in the presence or absence of GnT-IX. The reaction mixtures were separated by HPTLC. M-S, Man1-Ser; GnM-S, GlcNAc1,2-Man1-Ser; GGnM-S, Gal1,4-GlcNAc1,2-Man1-Ser. B, a reaction mixture using a fluorescence-labeled acceptor substrate GnM-S-PAES was analyzed by HPLC as described under "Experimental Procedures." S, substrate; P, enzymatic product.

View larger version (17K): [in this window] [in a new window]   FIG. 2. MALDI-TOF MS and proton NMR analyses of the substrate and enzymatic product. MS spectra (A) and proton NMR spectra (B) of the substrate GnM-S-PAES (S) and the enzymatic product (P) by GnT-IX. Ac indicates a signal due to ammonium acetate used as elution buffer for HPLC. C, MS spectra of the synthetic mannosyl peptide and the enzymatic products by POMGnT1 alone and by POMGnT1 and GnT-IX. Man-p, mannosyl peptide.

NMR analyses were carried out to further confirm the structure of the enzymatic product. Proton NMR spectra of the substrate and the product are shown in Fig. 2B. In the spectrum of the substrate, anomeric proton signals of Man and GlcNAc were observed at 4.838 and 4.546 ppm, respectively, and a methyl proton signal corresponding to the acetyl group of GlcNAc was detected at 2.057 ppm. The anomeric proton signal of GlcNAc appeared as a doublet with a coupling constant of 8.2 Hz. In the spectrum of the product, a methyl proton signal of an additional GlcNAc appeared at 2.038 ppm. The chemical shift value was similar to that of the methyl proton signal of GlcNAc, which was linked to the 6-OH position of Man 4 in the tetra'-antennary sugar chain (14). A new anomeric proton signal consistent with the GlcNAc was found at 4.594 ppm as a doublet with a coupling constant of 8.0 Hz. The coupling constant value indicates that the linkage of the GlcNAc is . The anomeric proton signal of Man was observed at 4.797 ppm and showed a shift to higher field by 0.041 ppm relative to that of the substrate (spectra of S and P in Fig. 2B). A similar up-field shift of the Man anomeric proton signal was observed when GlcNAc was attached to 6-OH position of Man (14). These results indicate that the additional GlcNAc of the product is linked to the 6-OH position of Man and that the anomeric configuration is .

To determine whether GnT-V also catalyzes the same reaction, recombinant GnT-V, possessing equivalent enzymatic activity toward the GnGn-bi-PA substrate with GnT-IX, was incubated with GnM-S-PAES, but no activity was detected (data not shown). As a result, we conclude that GnT-IX, but not GnT-V, acts on the GlcNAc1,2-Man structure in the O-mannosyl glycan, as a 1,6-N-acetylglucosaminyltransferase.

Fig. 3 shows a proposed biosynthetic pathway for the brain O-mannosyl glycan mediated by POMGnT1 and GnT-IX. It has been suggested that a putative O-mannosyltransferase, POMT1, catalyzes the addition of mannose to OH groups of Ser and Thr residues of polypeptides (17). The POMT1 gene is responsible for Walker-Warburg syndrome (18), an autosomal recessive developmental disorder that has similar clinical features to and is more severe than two other genetically distinct diseases, MEB (9) and Fukuyama congenital muscular dystrophy (19). However, POMT1 has not yet been characterized. POMGnT1 catalyzes the next step, in which the GlcNAc1–2Man structure is formed (10), while GnT-IX acts on the POMGnT1 product to form the GlcNAc1–6Man linkage. After this step, one or more 4GalTs (20) are able to form the Gal1,4-GlcNAc structure in O-mannosyl glycans. Subsequently, one or more ST3Gals (21) catalyze the formation of the Sia2,3-Gal structure in the -dystroglycan-type sialyl O-mannosyl glycan, or GlcATs (22–24) and HNK-1ST (25, 26) catalyze the formation of the HNK-1 epitope. It has also been reported that the Lewis X epitope is present in the brain O-mannosyl glycan (12, 27), however, the issue of whether the Lewis X epitope-carrying O-mannosyl glycans contains the GlcNAc1–6Man structure is currently unknown. In addition to these genes, fukutin (28), fukutin-related protein (FKRP) (29), and Large (30) have been also identified to be responsible for congenital muscular dystrophies and thought to be involved in O-glycan synthesis; however, GnT-IX has no similarity to these genes.

View larger version (15K): [in this window] [in a new window]   FIG. 3. Proposed synthetic pathway of the brain O-mannosyl glycan mediated by POMGnT1 and GnT-IX. It has been suggested that a putative O-mannosyltransferase POMT1 catalyzes the transfer of mannose in the first step in O-mannosyl glycan synthesis. POMGnT1 catalyzes the next step forming the GlcNAc1,2-Man structure. GnT-IX acts on the POMGnT1 product before the action of 4GalTs. After the addition of Gal residues, ST3Gals forms the -dystroglycan (DG)-type O-mannosyl glycan or GlcATs and HNK-1ST form the HNK-1 epitope. Fuc-TIX is the enzyme most responsible for the synthesis of the Lewis X epitope in the brain (31, 32), but whether the Lewis X epitope-carrying O-mannosyl glycan contains a GlcNAc1–6Man linkage is unknown. GlcAT, glucuronyltransferase; HNK-1ST, HNK-1 sulfotransferase.

	FOOTNOTES

 
^* This work was supported by the New Energy and Industrial Technology Development Organization (NEDO) as a part of Biotechnology Foundation Research Program for Health Maintenance and Improvement and by a Grant-in-aid for Scientific Research (S) No. 13854010 from the Japan Society for the promotion of Science and by the 21st Century COE Program by the Ministry of Education, Science, Culture, Sports and Technology in Japan. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence may be addressed. Tel.: 81-88-880-2313; Fax: 81-88-880-2314; E-mail: khonke{at}med.kochi-ms.ac.jp. To whom correspondence may be addressed. Tel.: 81-6-6879-3420; Fax: 81-6-6879-3429; E-mail: proftani{at}biochem.med.osaka-u.ac.jp.

¹ The abbreviations used are: POMGnT1, protein O-mannose 1,2-N-acetylglucosaminyltransferase; GnT-IX, N-acetylglucosaminyltransferase IX; GnT-V, 1,6-N-acetylglucosaminyltransferase V; GlcNAc, N-acetylglucosamine; MEB, muscle-eye-brain disease; GnM-S, GlcNAc1,2-Man1-Ser; Man, mannose; PAES, pyridylaminoethylsuccinamyl; MOPS, 3-morpholinopropanesulfonic acid; HPLC, high performance liquid chromatography; HPTLC, high performance thin layer chromatography; MALDI-TOF, matrix-assisted laser desorption ionization time of flight; MS, mass spectrometry.

	ACKNOWLEDGMENTS

 
We are grateful to Dr. Toshiyuki Inazu (Department of Applied Chemistry, School of Engineering, Tokai University) for providing a synthetic mannosyl peptide.

	REFERENCES

TOP ABSTRACT INTRODUCTION EXPERIMENTAL PROCEDURES RESULTS AND DISCUSSION REFERENCES

 

1. Nishimura, H., Takao, T., Hase, S., Shimonishi, Y., and Iwanaga, S. (1992) J. Biol. Chem. 267, 17520–17525[Abstract/Free Full Text]
2. Harris, R. J., and Spellman, M. W. (1993) Glycobiology 3, 219–224[Abstract/Free Full Text]
3. Shao, L., and Haltiwanger, R. S. (2003) Cell Mol. Life Sci. 60, 241–250[CrossRef][Medline] [Order article via Infotrieve]
4. Hase, S., Kawabata, S., Nishimura, H., Takeya, H., Sueyoshi, T., Miyata, T., Iwanaga, S., Takao, T., Shimonishi, Y., and Ikenaka, T. (1988) J. Biochem. (Tokyo) 104, 867–868[Abstract/Free Full Text]
5. Holt, G. D., and Hart, G. W. (1986) J. Biol. Chem. 261, 8049–8057[Abstract/Free Full Text]
6. Wells, L., Whalen, S. A., and Hart, G. W. (2003) Biochem. Biophys. Res. Commun. 302, 435–441[CrossRef][Medline] [Order article via Infotrieve]
7. Endo, T. (1999) Biochim. Biophys. Acta 6, 237–246
8. Chiba, A., Matsumura, K., Yamada, H., Inazu, T., Shimizu, T., Kusunoki, S., Kanazawa, I., Kobata, A., and Endo, T. (1997) J. Biol. Chem. 272, 2156–2162[Abstract/Free Full Text]
9. Santavuori, P., Somer, H., Sainio, K., Rapola, J., Kruus, S., Nikitin, T., Ketonen, L., and Leisti, J. (1989) Brain Dev. 11, 147–153[Medline] [Order article via Infotrieve]
10. Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., Inazu, T., Mitsuhashi, H., Takahashi, S., Takeuchi, M., Herrmann, R., Straub, V., Talim, B., Voit, T., Topaloglu, H., Toda, T., and Endo, T. (2001) Dev. Cell 1, 717–724[CrossRef][Medline] [Order article via Infotrieve]
11. Michele, D. E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R. D., Satz, J. S., Dollar, J., Nishino, I., Kelley, R. I., Somer, H., Straub, V., Mathews, K. D., Moore, S. A., and Campbell, K. P. (2002) Nature 418, 417–422[CrossRef][Medline] [Order article via Infotrieve]
12. Chai, W., Yuen, C. T., Kogelberg, H., Carruthers, R. A., Margolis, R. U., Feizi, T., and Lawson, A. M. (1999) Eur. J. Biochem. 263, 879–888[Medline] [Order article via Infotrieve]
13. Yuen, C. T., Chai, W., Loveless, R. W., Lawson, A. M., Margolis, R. U., and Feizi, T. (1997) J. Biol. Chem. 272, 8924–8931[Abstract/Free Full Text]
14. Inamori, K., Endo, T., Ide, Y., Fujii, S., Gu, J., Honke, K., and Taniguchi, N. (2003) J. Biol. Chem. 278, 43102–43109[Abstract/Free Full Text]
15. Seifert, J., Ogawa, T., Kurono, S., and Ito, Y. (2000) Glycoconj. J. 17, 407–423[CrossRef][Medline] [Order article via Infotrieve]
16. Gu, J., Nishikawa, A., Tsuruoka, N., Ohno, M., Yamaguchi, N., Kangawa, K., and Taniguchi, N. (1993) J. Biochem. (Tokyo) 113, 614–619[Abstract/Free Full Text]
17. Beltran-Valero de Bernabe, D., Currier, S., Steinbrecher, A., Celli, J., van Beusekom, E., van der Zwaag, B., Kayserili, H., Merlini, L., Chitayat, D., Dobyns, W. B., Cormand, B., Lehesjoki, A. E., Cruces, J., Voit, T., Walsh, C. A., van Bokhoven, H., and Brunner, H. G. (2002) Am. J. Hum. Genet. 71, 1033–1043[CrossRef][Medline] [Order article via Infotrieve]
18. Dobyns, W. B., Pagon, R. A., Armstrong, D., Curry, C. J., Greenberg, F., Grix, A., Holmes, L. B., Laxova, R., Michels, V. V., Robinow, M., and Zimmerman, R. L. (1989) Am. J. Med. Genet. 32, 195–210[CrossRef][Medline] [Order article via Infotrieve]
19. Fukuyama, Y., Osawa, M., and Suzuki, H. (1981) Brain Dev. 3, 1–29[Medline] [Order article via Infotrieve]
20. Amado, M., Almeida, R., Schwientek, T., and Clausen, H. (1999) Biochim. Biophys. Acta 6, 35–53
21. Tsuji, S. (1996) J. Biochem. (Tokyo) 120, 1–13[Abstract/Free Full Text]
22. Terayama, K., Oka, S., Seiki, T., Miki, Y., Nakamura, A., Kozutsumi, Y., Takio, K., and Kawasaki, T. (1997) Proc. Natl. Acad. Sci. U. S. A. 94, 6093–6098[Abstract/Free Full Text]
23. Shimoda, Y., Tajima, Y., Nagase, T., Harii, K., Osumi, N., and Sanai, Y. (1999) J. Biol. Chem. 274, 17115–17122[Abstract/Free Full Text]
24. Seiki, T., Oka, S., Terayama, K., Imiya, K., and Kawasaki, T. (1999) Biochem. Biophys. Res. Commun. 255, 182–187[CrossRef][Medline] [Order article via Infotrieve]
25. Bakker, H., Friedmann, I., Oka, S., Kawasaki, T., Nifant'ev, N., Schachner, M., and Mantei, N. (1997) J. Biol. Chem. 272, 29942–29946[Abstract/Free Full Text]
26. Ong, E., Yeh, J. C., Ding, Y., Hindsgaul, O., and Fukuda, M. (1998) J. Biol. Chem. 273, 5190–5195[Abstract/Free Full Text]
27. Smalheiser, N. R., Haslam, S. M., Sutton-Smith, M., Morris, H. R., and Dell, A. (1998) J. Biol. Chem. 273, 23698–23703[Abstract/Free Full Text]
28. Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura, K., Kondo-Iida, E., Nomura, Y., Segawa, M., Yoshioka, M., Saito, K., Osawa, M., Hamano, K., Sakakihara, Y., Nonaka, I., Nakagome, Y., Kanazawa, I., Nakamura, Y., Tokunaga, K., and Toda, T. (1998) Nature 394, 388–392[CrossRef][Medline] [Order article via Infotrieve]
29. Brockington, M., Blake, D. J., Prandini, P., Brown, S. C., Torelli, S., Benson, M. A., Ponting, C. P., Estournet, B., Romero, N. B., Mercuri, E., Voit, T., Sewry, C. A., Guicheney, P., and Muntoni, F. (2001) Am. J. Hum. Genet. 69, 1198–1209[CrossRef][Medline] [Order article via Infotrieve]
30. Peyrard, M., Seroussi, E., Sandberg-Nordqvist, A. C., Xie, Y. G., Han, F. Y., Fransson, I., Collins, J., Dunham, I., Kost-Alimova, M., Imreh, S., and Dumanski, J. P. (1999) Proc. Natl. Acad. Sci. U. S. A. 96, 598–603[Abstract/Free Full Text]
31. Kudo, T., Ikehara, Y., Togayachi, A., Kaneko, M., Hiraga, T., Sasaki, K., and Narimatsu, H. (1998) J. Biol. Chem. 273, 26729–26738[Abstract/Free Full Text]
32. Nishihara, S., Iwasaki, H., Nakajima, K., Togayachi, A., Ikehara, Y., Kudo, T., Kushi, Y., Furuya, A., Shitara, K., and Narimatsu, H. (2003) Glycobiology 13, 445–455[Abstract/Free Full Text]

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