Germinal Center Marker GL7 Probes Activation-Dependent Repression of N-Glycolylneuraminic Acid, a Sialic Acid Species Involved in the Negative Modulation of B-Cell Activation

REFERENCES

• Alizadeh, A. A., M. B. Eisen, R. E. Davis, C. Ma, I. S. Lossos, A. Rosenwald, J. C. Boldrick, H. Sabet, T. Tran, X. Yu, J. I. Powell, L. Yang, G. E. Marti, T. Moore, J. Hudson, Jr., L. Lu, D. B. Lewis, R. Tibshirani, G. Sherlock, W. C. Chan, T. C. Greiner, D. D. Weisenburger, J. O. Armitage, R. Warnke, R. Levy, W. Wilson, M. R. Grever, J. C. Byrd, D. Botstein, P. O. Brown, and L. M. Staudt. 2000. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature 403:503–511.
   PubMed Web of Science ®Google Scholar
• Baum, L. G., K. Derbin, N. L. Perillo, T. Wu, M. Pang, and C. Uittenbogaart. 1996. Characterization of terminal sialic acid linkages on human thymocytes. Correlation between lectin-binding phenotype and sialyltransferase expression. J. Biol. Chem. 271:10793–10799.
   PubMedGoogle Scholar
• Blixt, O., B. E. Collins, I. M. Van Den Nieuwenhof, P. R. Crocker, and J. C. Paulson. 2003. Sialoside specificity of the Siglec family assessed using novel multivalent probes: identification of potent inhibitors of myelin associated glycoproteins. J. Biol. Chem. 278:31007–31019.
   PubMed Web of Science ®Google Scholar
• Buhl, A. M., and J. C. Cambier. 1997. Co-receptor and accessory regulation of B-cell antigen receptor signal transduction. Immunol. Rev. 160:127–138.
   PubMed Web of Science ®Google Scholar
• Cervenak, L., A. Magyar, R. Boja, and G. Laszlo. 2001. Differential expression of GL7 activation antigen on bone marrow B cell subpopulations and peripheral B cells. Immunol. Lett. 78:89–96.
   PubMedGoogle Scholar
• Chou, H. H., H. Takematsu, S. Diaz, J. Iber, E. Nickerson, K. L. Wright, E. A. Muchmore, D. L. Nelson, S. T. Warren, and A. Varki. 1998. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl. Acad. Sci. USA 95:11751–11756.
   PubMed Web of Science ®Google Scholar
• Clark, E. A. 1993. CD22, a B cell-specific receptor, mediates adhesion and signal transduction. J. Immunol. 150:4715–4718.
   PubMed Web of Science ®Google Scholar
• Coico, R. F., B. S. Bhogal, and G. J. Thorbecke. 1983. Relationship of germinal centers in lymphoid tissue to immunologic memory. VI. Transfer of B cell memory with lymph node cells fractionated according to their receptors for peanut agglutinin. J. Immunol. 131:2254–2257.
   PubMed Web of Science ®Google Scholar
• Crocker, P. R. 2002. Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling. Curr. Opin. Struct. Biol. 12:609–615.
   PubMed Web of Science ®Google Scholar
• Crocker, P. R., S. Kelm, C. Dubois, B. Martin, A. S. McWilliam, D. M. Shotton, J. C. Paulson, and S. Gordon. 1991. Purification and properties of sialoadhesin, a sialic acid-binding receptor of murine tissue macrophages. EMBO J. 10:1661–1669.
   PubMed Web of Science ®Google Scholar
• Crocker, P. R., and A. Varki. 2001. Siglecs in the immune system. Immunology 103:137–145.
   PubMed Web of Science ®Google Scholar
• Crocker, P. R., and A. Varki. 2001. Siglecs, sialic acids and innate immunity. Trends Immunol. 22:337–342.
   PubMed Web of Science ®Google Scholar
• Cyster, J. G., and C. C. Goodnow. 1997. Tuning antigen receptor signaling by CD22: Integrating cues from antigens and the microenvironment. Immunity 6:509–517.
   PubMed Web of Science ®Google Scholar
• Ellies, L. G., D. Ditto, G. G. Levy, M. Wahrenbrock, D. Ginsburg, A. Varki, D. T. Le, and J. D. Marth. 2002. Sialyltransferase ST3Gal-IV operates as a dominant modifier of hemostasis by concealing asialoglycoprotein receptor ligands. Proc. Natl. Acad. Sci. USA 99:10042–10047.
   PubMedGoogle Scholar
• Gagneux, P., and A. Varki. 1999. Evolutionary considerations in relating oligosaccharide diversity to biological function. Glycobiology 9:747–755.
   PubMed Web of Science ®Google Scholar
• Han, H., D. J. Bearss, L. W. Browne, R. Calaluce, R. B. Nagle, and D. D. Von Hoff. 2002. Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res. 62:2890–2896.
   PubMed Web of Science ®Google Scholar
• Han, S., S. R. Dillon, B. Zheng, M. Shimoda, M. S. Schlissel, and G. Kelsoe. 1997. V(D)J recombinase activity in a subset of germinal center B lymphocytes. Science 278:301–305.
   PubMed Web of Science ®Google Scholar
• Han, S., B. Zheng, D. G. Schatz, E. Spanopoulou, and G. Kelsoe. 1996. Neoteny in lymphocytes: Rag1 and Rag2 expression in germinal center B cells. Science 274:2094–2097.
   PubMed Web of Science ®Google Scholar
• Hathcock, K. S., C. E. Pucillo, G. Laszlo, L. Lai, and R. J. Hodes. 1995. Analysis of thymic subpopulations expressing the activation antigen GL7: expression, genetics, and function. J. Immunol. 155:4575–4581.
   PubMedGoogle Scholar
• Hennet, T., D. Chui, J. C. Paulson, and J. D. Marth. 1998. Immune regulation by the ST6Gal sialyltransferase. Proc. Natl. Acad. Sci. USA 95:4504–4509.
   PubMedGoogle Scholar
• Hokazono, Y., T. Adachi, M. Wabl, N. Tada, T. Amagasa, and T. Tsubata. 2003. Inhibitory coreceptors activated by antigens but not by anti-Ig heavy chain antibodies install requirement of costimulation through CD40 for survival and proliferation of B cells. J. Immunol. 171:1835–1843.
   PubMed Web of Science ®Google Scholar
• Irie, A., S. Koyama, Y. Kozutsumi, T. Kawasaki, and A. Suzuki. 1998. The molecular basis for the absence of N-glycolylneuraminic acid in humans. J. Biol. Chem. 273:15866–15871.
   PubMed Web of Science ®Google Scholar
• Itohara, S., P. Mombaerts, J. Lafaille, J. Iacomini, A. Nelson, A. R. Clarke, M. L. Hooper, A. Farr, and S. Tonegawa. 1993. T cell receptor delta gene mutant mice: independent generation of alpha beta T cells and programmed rearrangements of gamma delta TCR genes. Cell 72:337–348.
   PubMed Web of Science ®Google Scholar
• Kawano, T., S. Koyama, H. Takematsu, Y. Kozutsumi, H. Kawasaki, S. Kawashima, T. Kawasaki, and A. Suzuki. 1995. Molecular cloning of cytidine monophospho-N-acetylneuraminic acid hydroxylase. Regulation of species- and tissue-specific expression of N-glycolylneuraminic acid. J. Biol. Chem. 270:16458–16463.
   PubMedGoogle Scholar
• Kawano, T., Y. Kozutsumi, T. Kawasaki, and A. Suzuki. 1994. Biosynthesis of N-glycolylneuraminic acid-containing glycoconjugates. Purification and characterization of the key enzyme of the cytidine monophospho-N-acetylneuraminic acid hydroxylation system. J. Biol. Chem. 269:9024–9029.
   PubMedGoogle Scholar
• Kelm, S., A. Pelz, R. Schauer, M. T. Filbin, S. Tang, M. E. de Bellard, R. L. Schnaar, J. A. Mahoney, A. Hartnell, P. Bradfield, et al. 1994. Sialoadhesin, myelin-associated glycoprotein and CD22 define a new family of sialic acid-dependent adhesion molecules of the immunoglobulin superfamily. Curr. Biol 4:965–972.
   PubMed Web of Science ®Google Scholar
• Koyama, S., T. Yamaji, H. Takematsu, T. Kawano, Y. Kozutsumi, A. Suzuki, and T. Kawasaki. 1996. A naturally occurring 46-amino-acid deletion of cytidine monophospho-N-acetylneuraminic acid hydroxylase leads to a change in the intracellular distribution of the protein. Glycoconj. J. 13:353–358.
   PubMedGoogle Scholar
• Laszlo, G., K. S. Hathcock, H. B. Dickler, and R. J. Hodes. 1993. Characterization of a novel cell-surface molecule expressed on subpopulations of activated T and B cells. J. Immunol. 150:5252–5262.
   PubMedGoogle Scholar
• Lossos, I. S., A. A. Alizadeh, M. B. Eisen, W. C. Chan, P. O. Brown, D. Botstein, L. M. Staudt, and R. Levy. 2000. Ongoing immunoglobulin somatic mutation in germinal center B cell-like but not in activated B cell-like diffuse large cell lymphomas. Proc. Natl. Acad. Sci. USA 97:10209–10213.
   PubMed Web of Science ®Google Scholar
• MacLennan, I. C. 1994. Germinal centers. Annu. Rev. Immunol. 12:117–139.
   PubMed Web of Science ®Google Scholar
• Martin, M. J., A. Muotri, F. Gage, and A. Varki. 2005. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat. Med. 11:228–232.
   PubMed Web of Science ®Google Scholar
• McHeyzer-Williams, L. J., M. Cool, and M. G. McHeyzer-Williams. 2000. Antigen-specific B cell memory: expression and replenishment of a novel B220− memory B cell compartment. J. Exp. Med. 191:1149–1166.
   PubMedGoogle Scholar
• McHeyzer-Williams, L. J., D. J. Driver, and M. G. McHeyzer-Williams. 2001. Germinal center reaction. Curr. Opin. Hematol. 8:52–59.
   PubMedGoogle Scholar
• Mills, D. M., J. C. Stolpa, and J. C. Cambier. 2004. Cognate B cell signaling via MHC class II: differential regulation of B cell antigen receptor and MHC class II/Ig-αβ signaling by CD22. J. Immunol. 172:195–201.
   PubMedGoogle Scholar
• Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7:1063–1066.
   PubMed Web of Science ®Google Scholar
• Muchmore, E. A., M. Milewski, A. Varki, and S. Diaz. 1989. Biosynthesis of N-glycolylneuraminic acid. The primary site of hydroxylation of N-acetylneuraminic acid is the cytosolic sugar nucleotide pool. J. Biol. Chem. 264:20216–20223.
   PubMed Web of Science ®Google Scholar
• Muramatsu, M., V. S. Sankaranand, S. Anant, M. Sugai, K. Kinoshita, N. O. Davidson, and T. Honjo. 1999. Specific expression of activation-induced cytidine deaminase (AID), a novel member of the RNA-editing deaminase family in germinal center B cells. J. Biol. Chem. 274:18470–18476.
   PubMed Web of Science ®Google Scholar
• Murasawa, M., S. Okada, S. Obata, M. Hatano, H. Moriya, and T. Tokuhisa. 2002. GL7 defines the cycling stage of pre-B cells in murine bone marrow. Eur. J. Immunol. 32:291–298.
   PubMedGoogle Scholar
• Nitschke, L. 2005. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr. Opin. Immunol. 17:290–297.
   PubMed Web of Science ®Google Scholar
• Novoradovskaya, N., M. L. Whitfield, L. S. Basehore, A. Novoradovsky, R. Pesich, J. Usary, M. Karaca, W. K. Wong, O. Aprelikova, M. Fero, C. M. Perou, D. Botstein, and J. Braman. 2004. Universal reference RNA as a standard for microarray experiments. BMC Genomics 5:20.
   PubMed Web of Science ®Google Scholar
• Pasare, C., and R. Medzhitov. 2005. Control of B-cell responses by Toll-like receptors. Nature 438:364–368.
   PubMed Web of Science ®Google Scholar
• Paulson, J. C., J. Weinstein, and A. Schauer. 1989. Tissue-specific expression of sialyltransferases. J. Biol. Chem. 264:10931–10934.
   PubMed Web of Science ®Google Scholar
• Poe, J. C., Y. Fujimoto, M. Hasegawa, K. M. Haas, A. S. Miller, I. G. Sanford, C. B. Bock, M. Fujimoto, and T. F. Tedder. 2004. CD22 regulates B lymphocyte function in vivo through both ligand-dependent and ligand-independent mechanisms. Nat. Immunol. 5:1078–1087.
   PubMed Web of Science ®Google Scholar
• Powell, L. D., and A. Varki. 1994. The oligosaccharide binding specificities of CD22 beta, a sialic acid-specific lectin of B cells. J. Biol. Chem. 269:10628–10636.
   PubMed Web of Science ®Google Scholar
• Razi, N., and A. Varki. 1998. Masking and unmasking of the sialic acid-binding lectin activity of CD22 (Siglec-2) on B lymphocytes. Proc. Natl. Acad. Sci. USA 95:7469–7474.
   PubMed Web of Science ®Google Scholar
• Reichert, R. A., W. M. Gallatin, I. L. Weissman, and E. C. Butcher. 1983. Germinal center B cells lack homing receptors necessary for normal lymphocyte recirculation. J. Exp. Med. 157:813–827.
   PubMed Web of Science ®Google Scholar
• Schauer, R. 1982. Sialic acids: chemistry, metabolism and function. Cell biology monographs, vol. 10. Springer-Verlag, New York, NY.
   Google Scholar
• Schulte, R. J., M. A. Campbell, W. H. Fischer, and B. M. Sefton. 1992. Tyrosine phosphorylation of CD22 during B cell activation. Science 258:1001–1004.
   PubMedGoogle Scholar
• Schwarzkopf, M., K. P. Knobeloch, E. Rohde, S. Hinderlich, N. Wiechens, L. Lucka, I. Horak, W. Reutter, and R. Horstkorte. 2002. Sialylation is essential for early development in mice. Proc. Natl. Acad. Sci. USA 99:5267–5270.
   PubMed Web of Science ®Google Scholar
• Sgroi, D., A. Varki, S. Braesch-Andersen, and I. Stamenkovic. 1993. CD22, a B cell-specific immunoglobulin superfamily member, is a sialic acid-binding lectin. J. Biol. Chem. 268:7011–7018.
   PubMedGoogle Scholar
• Shaffer, A. L., A. Rosenwald, E. M. Hurt, J. M. Giltnane, L. T. Lam, O. K. Pickeral, and L. M. Staudt. 2001. Signatures of the immune response. Immunity 15:375–385.
   PubMed Web of Science ®Google Scholar
• Shapiro-Shelef, M., K. I. Lin, L. J. McHeyzer-Williams, J. Liao, M. G. McHeyzer-Williams, and K. Calame. 2003. Blimp-1 is required for the formation of immunoglobulin secreting plasma cells and pre-plasma memory B cells. Immunity 19:607–620.
   PubMed Web of Science ®Google Scholar
• Shaw, L., and R. Schauer. 1988. The biosynthesis of N-glycolylneuraminic acid occurs by hydroxylation of the CMP-glycoside of N-acetylneuraminic acid. Biol. Chem. Hoppe-Seyler 369:477–486.
   PubMed Web of Science ®Google Scholar
• Shaw, L., and R. Schauer. 1989. Detection of CMP-N-acetylneuraminic acid hydroxylase activity in fractionated mouse liver. Biochem. J. 263:355–363.
   PubMedGoogle Scholar
• Shih, T. A., E. Meffre, M. Roederer, and M. C. Nussenzweig. 2002. Role of BCR affinity in T cell dependent antibody responses in vivo. Nat. Immunol. 3:570–575.
   PubMed Web of Science ®Google Scholar
• Sjoberg, E. R., L. D. Powell, A. Klein, and A. Varki. 1994. Natural ligands of the B cell adhesion molecule CD22 beta can be masked by 9-O-acetylation of sialic acids. J. Cell Biol. 126:549–562.
   PubMedGoogle Scholar
• Takematsu, H., S. Diaz, A. Stoddart, Y. Zhang, and A. Varki. 1999. Lysosomal and cytosolic sialic acid 9-O-acetylesterase activities can be encoded by one gene via differential usage of a signal peptide-encoding exon at the N terminus. J. Biol. Chem. 274:25623–25631.
   PubMedGoogle Scholar
• Tedder, T. F., J. Tuscano, S. Sato, and J. H. Kehrl. 1997. CD22, a B lymphocyte-specific adhesion molecule that regulates antigen receptor signaling. Annu. Rev. Immunol. 15:481–504.
   PubMed Web of Science ®Google Scholar
• Tsuji, S. 1996. Molecular cloning and functional analysis of sialyltransferases. J. Biochem. (Tokyo) 120:1–13.
   PubMed Web of Science ®Google Scholar
• Varki, A. 1992. Diversity in the sialic acids Glycobiology 2:25–40. (Erratum, 2:168.)
   PubMed Web of Science ®Google Scholar
• Varki, A. 1997. Sialic acids as ligands in recognition phenomena. FASEB J. 11:248–255.
   PubMed Web of Science ®Google Scholar
• Varki, A., and T. Angata. 2006 Siglecs—the major subfamily of I-type lectins. Glycobiology 16:1R–27R.
   PubMed Web of Science ®Google Scholar
• Wakabayashi, C., T. Adachi, J. Wienands, and T. Tsubata. 2002. A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science 298:2392–2395.
   PubMed Web of Science ®Google Scholar
• Wuensch, S. A., R. Y. Huang, J. Ewing, X. Liang, and J. T. Lau. 2000. Murine B cell differentiation is accompanied by programmed expression of multiple novel β-galactoside α2, 6-sialyltransferase mRNA forms. Glycobiology 10:67–75.
   PubMedGoogle Scholar
• Yamaji, T., T. Teranishi, M. S. Alphey, P. R. Crocker, and Y. Hashimoto. 2002. A small region of the natural killer cell receptor, Siglec-7, is responsible for its preferred binding to α2,8-disialyl and branched α2,6-sialyl residues. A comparison with Siglec-9. J. Biol. Chem. 277:6324–6332.
   PubMed Web of Science ®Google Scholar
• Zhang, J., I. C. MacLennan, Y. J. Liu, and P. J. Lane. 1988. Is rapid proliferation in B centroblasts linked to somatic mutation in memory B cell clones? Immunol. Lett. 18:297–299.
   PubMedGoogle Scholar