Glycosyltransferase and sulfotransferase gene expression profiles in human monocytes, dendritic cells and macrophages

Arnold, J.N., Wormald, M.R., Sim, R.B., Rudd, P.M., Dwek, R.A.: The impact of glycosylation on the biological function and structure of human immunoglobulins. Annu. Rev. Immunol. 25, 21–50 (2007). doi:10.1146/annurev.immunol.25.022106.141702 Collins, B.E., Paulson, J.C.: Cell surface biology mediated by low affinity multivalent protein-glycan interactions. Curr. Opin. Chem. Biol. 8, 617–625 (2004). doi:10.1016/j.cbpa.2004.10.004 Daniels, M.A., Hogquist, K.A., Jameson, S.C.: Sweet ’n’ sour: the impact of differential glycosylation on T cell responses. Nat. Immunol. 3, 903–910 (2002). doi:10.1038/ni1002-903 Marth, J.D., Grewal, P.K.: Mammalian glycosylation in immunity. Nat. Rev. Immunol. 8, 874–887 (2008). doi:10.1038/nri2417 Rudd, P.M., Elliott, T., Cresswell, P., Wilson, I.A., Dwek, R.A.: Glycosylation and the immune system. Science 291, 2370–2376 (2001). doi:10.1126/science.291.5512.2370 Spiro, R.G.: Protein glycosylation: nature, distribution, enzymatic formation, and disease implications of glycopeptide bonds. Glycobiology 12, 43R–56R (2002). doi:10.1093/glycob/12.4.43R Crocker, P.R.: Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling. Curr. Opin. Struct. Biol. 12, 609–615 (2002). doi:10.1016/S0959-440X(02)00375-5 Esko, J.D., Selleck, S.B.: Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 71, 435–471 (2002). doi:10.1146/annurev.biochem.71.110601.135458 Lau, K.S., Partridge, E.A., Grigorian, A., Silvescu, C.I., Reinhold, V.N., Demetriou, M., Dennis, J.W.: Complex N-glycan number and degree of branching cooperate to regulate cell proliferation and differentiation. Cell 129, 123–134 (2007). doi:10.1016/j.cell.2007.01.049 Lowe, J.B.: Glycosyltransferases and glycan structures contributing to the adhesive activities of L-, E- and P-selectin counter-receptors. Biochem. Soc. Symp. 69, 33–45 (2002) Moody, A.M., Chui, D., Reche, P.A., Priatel, J.J., Marth, J.D., Reinherz, E.L.: Developmentally regulated glycosylation of the CD8alphabeta coreceptor stalk modulates ligand binding. Cell 107, 501–512 (2001). doi:10.1016/S0092-8674(01)00577-3 Rabinovich, G.A., Baum, L.G., Tinari, N., Paganelli, R., Natoli, C., Liu, F.T., Iacobelli, S.: Galectins and their ligands: amplifiers, silencers or tuners of the inflammatory response? Trends Immunol. 23, 313–320 (2002). doi:10.1016/S1471-4906(02)02232-9 Toscano, M.A., Bianco, G.A., Ilarregui, J.M., Croci, D.O., Correale, J., Hernandez, J.D., Zwirner, N.W., Poirier, F., Riley, E.M., Baum, L.G., Rabinovich, G.A.: Differential glycosylation of TH1, TH2 and TH-17 effector cells selectively regulates susceptibility to cell death. Nat. Immunol. 8, 825–834 (2007). doi:10.1038/ni1482 Blander, J.M., Visintin, I., Janeway Jr., C.A., Medzhitov, R.: Alpha(1, 3)-fucosyltransferase VII and alpha(2, 3)-sialyltransferase IV are up-regulated in activated CD4 T cells and maintained after their differentiation into Th1 and migration into inflammatory sites. J. Immunol. 163, 3746–3752 (1999) Collins, B.E., Blixt, O., Han, S., Duong, B., Li, H., Nathan, J.K., Bovin, N., Paulson, J.C.: High-affinity ligand probes of CD22 overcome the threshold set by cis ligands to allow for binding, endocytosis, and killing of B cells. J. Immunol. 177, 2994–3003 (2006) Feizi, T.: Carbohydrate-mediated recognition systems in innate immunity. Immunol. Rev. 173, 79–88 (2000). doi:10.1034/j.1600-065X.2000.917310.x Moody, A.M., North, S.J., Reinhold, B., Van Dyken, S.J., Rogers, M.E., Panico, M., Dell, A., Morris, H.R., Marth, J.D., Reinherz, E.L.: Sialic acid capping of CD8beta core 1-O-glycans controls thymocyte-major histocompatibility complex class I interaction. J. Biol. Chem. 278, 7240–7246 (2003). doi:10.1074/jbc.M210468200 Morgan, R., Gao, G., Pawling, J., Dennis, J.W., Demetriou, M., Li, B.: N-acetylglucosaminyltransferase V (Mgat5)-mediated N-glycosylation negatively regulates Th1 cytokine production by T cells. J. Immunol. 173, 7200–7208 (2004) Pappu, B.P., Shrikant, P.A.: Alteration of cell surface sialylation regulates antigen-induced naive CD8+ T cell responses. J. Immunol. 173, 275–284 (2004) van Kooyk, Y., Rabinovich, G.A.: Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9, 593–601 (2008). doi:10.1038/ni.f.203 Demetriou, M., Granovsky, M., Quaggin, S., Dennis, J.W.: Negative regulation of T-cell activation and autoimmunity by Mgat5 N-glycosylation. Nature 409, 733–739 (2001). doi:10.1038/35055582 Moretta, L., Bottino, C., Pende, D., Castriconi, R., Mingari, M.C., Moretta, A.: Surface NK receptors and their ligands on tumor cells. Semin. Immunol. 18, 151–158 (2006). doi:10.1016/j.smim.2006.03.002 Bendelac, A., Savage, P.B., Teyton, L.: The biology of NKT cells. Annu. Rev. Immunol. 25, 297–336 (2007). doi:10.1146/annurev.immunol.25.022106.141711 Godfrey, D.I., Kronenberg, M.: Going both ways: immune regulation via CD1d-dependent NKT cells. J. Clin. Invest. 114, 1379–1388 (2004) Bax, M., Garcia-Vallejo, J.J., Jang-Lee, J., North, S.J., Gilmartin, T.J., Hernandez, G., Crocker, P.R., Leffler, H., Head, S.R., Haslam, S.M., Dell, A., van Kooyk, Y.: Dendritic cell maturation results in pronounced changes in glycan expression affecting recognition by siglecs and galectins. J. Immunol. 179, 8216–8224 (2007) Julien, S., Grimshaw, M.J., Sutton-Smith, M., Coleman, J., Morris, H.R., Dell, A., Taylor-Papadimitriou, J., Burchell, J.M.: Sialyl-Lewis(x) on P-selectin glycoprotein ligand-1 is regulated during differentiation and maturation of dendritic cells: a mechanism involving the glycosyltransferases C2GnT1 and ST3Gal I. J. Immunol. 179, 5701–5710 (2007) Gordon, S., Taylor, P.R.: Monocyte and macrophage heterogeneity. Nat. Rev. Immunol. 5, 953–964 (2005). doi:10.1038/nri1733 Hume, D.A., Ross, I.L., Himes, S.R., Sasmono, R.T., Wells, C.A., Ravasi, T.: The mononuclear phagocyte system revisited. J. Leukoc. Biol. 72, 621–627 (2002) Randolph, G.J., Beaulieu, S., Lebecque, S., Steinman, R.M., Muller, W.A.: Differentiation of monocytes into dendritic cells in a model of transendothelial trafficking. Science 282, 480–483 (1998). doi:10.1126/science.282.5388.480 Randolph, G.J., Inaba, K., Robbiani, D.F., Steinman, R.M., Muller, W.A.: Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11, 753–761 (1999). doi:10.1016/S1074-7613(00)80149-1 Banchereau, J., Steinman, R.M.: Dendritic cells and the control of immunity. Nature 392, 245–252 (1998). doi:10.1038/32588 Kapsenberg, M.L.: Dendritic-cell control of pathogen-driven T-cell polarization. Nat. Rev. Immunol. 3, 984–993 (2003). doi:10.1038/nri1246 Reis e Sousa, C.: Dendritic cells in a mature age. Nat. Rev. Immunol. 6, 476–483 (2006). doi:10.1038/nri1845 Rossi, M., Young, J.W.: Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 175, 1373–1381 (2005) Iwasaki, A., Medzhitov, R.: Toll-like receptor control of the adaptive immune responses. Nat. Immunol. 5, 987–995 (2004). doi:10.1038/ni1112 Takeda, K., Akira, S.: Toll-like receptors in innate immunity. Int. Immunol. 17, 1–14 (2005). doi:10.1093/intimm/dxh186 Gosset, P., Bureau, F., Angeli, V., Pichavant, M., Faveeuw, C., Tonnel, A.B., Trottein, F.: Prostaglandin D2 affects the maturation of human monocyte-derived dendritic cells: consequence on the polarization of naive Th cells. J. Immunol. 170, 4943–4952 (2003) Sallusto, F., Lanzavecchia, A.: Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179, 1109–1118 (1994). doi:10.1084/jem.179.4.1109 Young, D.A., Lowe, L.D., Clark, S.C.: Comparison of the effects of IL-3, granulocyte-macrophage colony-stimulating factor, and macrophage colony-stimulating factor in supporting monocyte differentiation in culture. Analysis of macrophage antibody-dependent cellular cytotoxicity. J. Immunol. 145, 607–615 (1990) Turville, S.G., Cameron, P.U., Handley, A., Lin, G., Pohlmann, S., Doms, R.W., Cunningham, A.L.: Diversity of receptors binding HIV on dendritic cell subsets. Nat. Immunol. 3, 975–983 (2002). doi:10.1038/ni841 van Kooyk, Y., Geijtenbeek, T.B.: DC-SIGN: escape mechanism for pathogens. Nat. Rev. Immunol. 3, 697–709 (2003). doi:10.1038/nri1182 Fleetwood, A.J., Lawrence, T., Hamilton, J.A., Cook, A.D.: Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 178, 5245–5252 (2007) Verreck, F.A., de Boer, T., Langenberg, D.M., Hoeve, M.A., Kramer, M., Vaisberg, E., Kastelein, R., Kolk, A., de Waal-Malefyt, R., Ottenhoff, T.H.: Human IL-23-producing type 1 macrophages promote but IL-10-producing type 2 macrophages subvert immunity to (myco) bacteria. Proc. Natl. Acad. Sci. USA 101, 4560–4565 (2004). doi:10.1073/pnas.0400983101 Lockhart, D.J., Dong, H., Byrne, M.C., Follettie, M.T., Gallo, M.V., Chee, M.S., Mittmann, M., Wang, C., Kobayashi, M., Horton, H., Brown, E.L.: Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14, 1675–1680 (1996). doi:10.1038/nbt1296-1675 Hess, A., Iyer, H.: Fisher’s combined p-value for detecting differentially expressed genes using Affymetrix expression arrays. BMC Genomics 8, 96 (2007). doi:10.1186/1471-2164-8-96 Bolstad, B.M., Irizarry, R.A., Astrand, M., Speed, T.P.: A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19, 185–193 (2003). doi:10.1093/bioinformatics/19.2.185 Irizarry, R.A., Bolstad, B.M., Collin, F., Cope, L.M., Hobbs, B., Speed, T.P.: Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15 (2003). doi:10.1093/nar/gng015 Elbim, C., Hakim, J., Gougerot-Pocidalo, M.A.: Heterogeneity in Lewis-X and sialyl-Lewis-X antigen expression on monocytes in whole blood: relation to stimulus-induced oxidative burst. Am. J. Pathol. 152, 1081–1090 (1998) Skacel, P.O., Edwards, A.J., Harrison, C.T., Watkins, W.M.: Enzymic control of the expression of the X determinant (CD15) in human myeloid cells during maturation: the regulatory role of 6-sialytransferase. Blood 78, 1452–1460 (1991) Becker, S., Warren, M.K., Haskill, S.: Colony-stimulating factor-induced monocyte survival and differentiation into macrophages in serum-free cultures. J. Immunol. 139, 3703–3709 (1987) Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., Steinman, R.M.: Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176, 1693–1702 (1992). doi:10.1084/jem.176.6.1693 Sasaki, K., Kurata-Miura, K., Ujita, M., Angata, K., Nakagawa, S., Sekine, S., Nishi, T., Fukuda, M.: Expression cloning of cDNA encoding a human beta-1, 3-N-acetylglucosaminyltransferase that is essential for poly-N-acetyllactosamine synthesis. Proc. Natl. Acad. Sci. USA 94, 14294–14299 (1997). doi:10.1073/pnas.94.26.14294 Weinhold, B., Seidenfaden, R., Rockle, I., Muhlenhoff, M., Schertzinger, F., Conzelmann, S., Marth, J.D., Gerardy-Schahn, R., Hildebrandt, H.: Genetic ablation of polysialic acid causes severe neurodevelopmental defects rescued by deletion of the neural cell adhesion molecule. J. Biol. Chem. 280, 42971–42977 (2005). doi:10.1074/jbc.M511097200 Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D., Stamatos, N.M.: Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. J. Biol. Chem. 282, 30346–30356 (2007). doi:10.1074/jbc.M702965200 Kitagawa, H., Shimakawa, H., Sugahara, K.: The tumor suppressor EXT-like gene EXTL2 encodes an alpha1, 4-N-acetylhexosaminyltransferase that transfers N-acetylgalactosamine and N-acetylglucosamine to the common glycosaminoglycan-protein linkage region. The key enzyme for the chain initiation of heparan sulfate. J. Biol. Chem. 274, 13933–13937 (1999). doi:10.1074/jbc.274.20.13933 Wegrowski, Y., Milard, A.L., Kotlarz, G., Toulmonde, E., Maquart, F.X., Bernard, J.: Cell surface proteoglycan expression during maturation of human monocytes-derived dendritic cells and macrophages. Clin. Exp. Immunol. 144, 485–493 (2006). doi:10.1111/j.1365-2249.2006.03059.x Jenner, J., Kerst, G., Handgretinger, R., Muller, I.: Increased alpha2, 6-sialylation of surface proteins on tolerogenic, immature dendritic cells and regulatory T cells. Exp. Hematol. 34, 1212–1218 (2006). doi:10.1016/j.exphem.2006.04.016 Martinez, F.O., Gordon, S., Locati, M., Mantovani, A.: Transcriptional profiling of the human monocyte-to-macrophage differentiation and polarization: new molecules and patterns of gene expression. J. Immunol. 177, 7303–7311 (2006) Suzuki, A., Yamakawa, M., Tsukamoto, M.: The adhesion molecules, l-selectin and sialyl lewis x, relate to the formation of the follicular dendritic cell-lymphocyte cluster in the mantle zone. Immunol. Lett. 79, 181–187 (2001). doi:10.1016/S0165-2478(01)00282-6 Crocker, P.R.: Siglecs in innate immunity. Curr. Opin. Pharmacol. 5, 431–437 (2005). doi:10.1016/j.coph.2005.03.003 Campbell, B.J., Yu, L.G., Rhodes, J.M.: Altered glycosylation in inflammatory bowel disease: a possible role in cancer development. Glycoconj. J. 18, 851–858 (2001). doi:10.1023/A:1022240107040 Coulouarn, C., Lefebvre, G., Derambure, C., Lequerre, T., Scotte, M., Francois, A., Cellier, D., Daveau, M., Salier, J.P.: Altered gene expression in acute systemic inflammation detected by complete coverage of the human liver transcriptome. Hepatology 39, 353–364 (2004). doi:10.1002/hep.20052 Van Dijk, W., Brinkman-Van der Linden, E.C., Havenaar, E.C.: Occurrence and possible function of inflammation-induced expression of sialyl Lewis-x on acute-phase proteins. Adv. Exp. Med. Biol 435, 145–150 (1998) Kim, B.T., Kitagawa, H., Tanaka, J., Tamura, J., Sugahara, K.: In vitro heparan sulfate polymerization: crucial roles of core protein moieties of primer substrates in addition to the EXT1-EXT2 interaction. J. Biol. Chem. 278, 41618–41623 (2003). doi:10.1074/jbc.M304831200 Brigl, M., Bry, L., Kent, S.C., Gumperz, J.E., Brenner, M.B.: Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat. Immunol. 4, 1230–1237 (2003). doi:10.1038/ni1002 De Libero, G., Moran, A.P., Gober, H.J., Rossy, E., Shamshiev, A., Chelnokova, O., Mazorra, Z., Vendetti, S., Sacchi, A., Prendergast, M.M., Sansano, S., Tonevitsky, A., Landmann, R., Mori, L.: Bacterial infections promote T cell recognition of self-glycolipids. Immunity 22, 763–772 (2005). doi:10.1016/j.immuni.2005.04.013 Mattner, J., Debord, K.L., Ismail, N., Goff, R.D., Cantu 3rd, C., Zhou, D., Saint-Mezard, P., Wang, V., Gao, Y., Yin, N., Hoebe, K., Schneewind, O., Walker, D., Beutler, B., Teyton, L., Savage, P.B., Bendelac, A.: Exogenous and endogenous glycolipid antigens activate NKT cells during microbial infections. Nature 434, 525–529 (2005). doi:10.1038/nature03408 Paget, C., Mallevaey, T., Speak, A.O., Torres, D., Fontaine, J., Sheehan, K.C., Capron, M., Ryffel, B., Faveeuw, C., Leite de Moraes, M., Platt, F., Platt, F., Trottein, F., Trottein, F.: Activation of invariant NKT cells by toll-like receptor 9-stimulated dendritic cells requires type I interferon and charged glycosphingolipids. Immunity 27, 597–609 (2007). doi:10.1016/j.immuni.2007.08.017 Salio, M., Speak, A.O., Shepherd, D., Polzella, P., Illarionov, P.A., Veerapen, N., Besra, G.S., Platt, F.M., Cerundolo, V.: Modulation of human natural killer T cell ligands on TLR-mediated antigen-presenting cell activation. Proc. Natl. Acad. Sci. USA 104, 20490–20495 (2007). doi:10.1073/pnas.0710145104 Tupin, E., Kinjo, Y., Kronenberg, M.: The unique role of natural killer T cells in the response to microorganisms. Nat. Rev. Microbiol. 5, 405–417 (2007). doi:10.1038/nrmicro1657 Garcia-Vallejo, J.J., Gringhuis, S.I., van Dijk, W., van Die, I.: Gene expression analysis of glycosylation-related genes by real-time polymerase chain reaction. Methods Mol. Biol. 347, 187–209 (2006) Groux-Degroote, S., Krzewinski-Recchi, M.A., Cazet, A., Vincent, A., Lehoux, S., Lafitte, J.J., Van Seuningen, I., Delannoy, P.: IL-6 and IL-8 increase the expression of glycosyltransferases and sulfotransferases involved in the biosynthesis of sialylated and/or sulfated Lewisx epitopes in the human bronchial mucosa. Biochem. J. 410, 213–223 (2008). doi:10.1042/BJ20070958