L-selectin, a lectin-like receptor, mediates rolling of lymphocytes on high endothelial venules (HEVs) in secondary lymphoid organs by interacting with HEV ligands. These ligands consist of a complex of sialomucins, candidates for which are glycosylation- dependent cell adhesion molecule 1 (GlyCAM-1), CD34, and podocalyxin. The ligands must be sialylated, fucosylated, and sulfated for optimal recognition by L-selectin. Our previous structural characterization of GlyCAM-1 has demonstrated two sulfation modifications, Gal-6-sulfate and GlcNAc-6-sulfate in the context of sialyl Lewis x. We now report the cloning of a Gal-6-sulfotransferase and a GlcNAc-6-sulfotransferase, which can modify GlyCAM-1 and CD34. The Gal-6-sulfotransferase shows a wide tissue distribution. In contrast, the GlcNAc-6-sulfotransferase is highly restricted to HEVs, as revealed by Northern analysis and in situ hybridization. Expression of either enzyme in Chinese hamster ovary cells, along with CD34 and fucosyltransferase VII, results in ligand activity, as detected by binding of an L-selectin/IgM chimera. When coexpressed, the two sulfotransferases synergize to produce strongly enhanced chimera binding.
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17 May 1999
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May 17 1999
Sulfotransferases of Two Specificities Function in the Reconstitution of High Endothelial Cell Ligands for L-selectin
Annette Bistrup,
Annette Bistrup
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Sunil Bhakta,
Sunil Bhakta
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Jin Kyu Lee,
Jin Kyu Lee
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Yevgeniy Y. Belov,
Yevgeniy Y. Belov
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Michael Dee Gunn,
Michael Dee Gunn
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Feng-Rong Zuo,
Feng-Rong Zuo
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Chiao-Chain Huang,
Chiao-Chain Huang
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Reiji Kannagi,
Reiji Kannagi
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Steven D. Rosen,
Steven D. Rosen
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Stefan Hemmerich
Stefan Hemmerich
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
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Annette Bistrup
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Sunil Bhakta
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Jin Kyu Lee
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Yevgeniy Y. Belov
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Michael Dee Gunn
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Feng-Rong Zuo
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Chiao-Chain Huang
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Reiji Kannagi
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Steven D. Rosen
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Stefan Hemmerich
*Department of Anatomy and Program in Immunology, and ‡Cardiovascular Research Institute, University of California, San Francisco, California 94143; §Program in Experimental Pathology, Aichi Cancer Center, Nagoya, Japan; ‖Clontech Laboratories, Inc., Palo Alto, California 94303; and ¶Department of Respiratory Diseases, Roche Bioscience, Palo Alto, California 94304-1397
Address correspondence to Steven D. Rosen, University of California, Lung Biology Center, Box 0854, San Francisco, CA 94143-0854. Tel.: (415) 476-1579. Fax: (415) 206-4123. E-mail: [email protected] or Stefan Hemmerich, Department of Respiratory Diseases, Roche Bioscience, Palo Alto, CA 94304-1397. Tel.: (650) 354-7169. Fax: (650) 354-7554. E-mail: [email protected]
The Lifeseq EST database (Incyte Pharmaceuticals, Inc., Palo Alto) was accessed through a licensing agreement with Roche Bioscience. We thank Carmen Tam for assistance in the in situ hybridization experiments. We are grateful for the help of Ms. Katy Hoiles of Incyte Pharmaceuticals in recovering plasmids containing the LifeSeq ESTs used in this study. We are further indebted to Ms. Deborah McCarley for help in the experiments, to Mr. Steve Stoufer, Ms. Sophie Chow, and Dr. Chinh Bach for sequencing plasmids, and to Dr. Kurt Jarnagin for his support and advice during the course of the study. We thank Drs. Geoffrey Kansas for providing us with the CHO/FTVII/C2GnT cells, Minoru Fukuda for the C2GnT cDNA, John Lowe for the L-selectin/IgM and FTVII cDNAs, and David Simmons for the pIG1 plasmid. We thank Mark Singer for purifying the HECs, and Chris Sassetti for isolating the RNA from the HECs and preparing the cDNA. We are also grateful to Kirsten Tangemann, Carolyn Bertozzi, Chris Sassetti, and Kendra Bowman for many useful discussions.
The research was supported by grants to S.D. Rosen from the National Institutes of Health (R37 GM23547 and GM57411) and from Roche Bioscience. J.K. Lee is supported by a postdoctoral fellowship from the Arthritis Foundation.
Received:
December 16 1998
Revision Received:
March 03 1999
Online ISSN: 1540-8140
Print ISSN: 0021-9525
1999
J Cell Biol (1999) 145 (4): 899–910.
Article history
Received:
December 16 1998
Revision Received:
March 03 1999
Citation
Annette Bistrup, Sunil Bhakta, Jin Kyu Lee, Yevgeniy Y. Belov, Michael Dee Gunn, Feng-Rong Zuo, Chiao-Chain Huang, Reiji Kannagi, Steven D. Rosen, Stefan Hemmerich; Sulfotransferases of Two Specificities Function in the Reconstitution of High Endothelial Cell Ligands for L-selectin . J Cell Biol 17 May 1999; 145 (4): 899–910. doi: https://doi.org/10.1083/jcb.145.4.899
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