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Linked Glycans N of Lymphocytes Leads to Dramatic Remodeling T+ and CD8 + Activation of Murine Activation of Murine CD4+ and CD8+ T Lymphocytes Leads to Dramatic Remodeling of N-Linked Glycans This information is current as Elena M. Comelli, Mark Sutton-Smith, Qi Yan, Margarida of September 29, 2021. Amado, Maria Panico, Tim Gilmartin, Thomas Whisenant, Caroline M. Lanigan, Steven R. Head, David Goldberg, Howard R. Morris, Anne Dell and James C. Paulson J Immunol 2006; 177:2431-2440; ; doi: 10.4049/jimmunol.177.4.2431 Downloaded from http://www.jimmunol.org/content/177/4/2431 Supplementary http://www.jimmunol.org/content/suppl/2006/08/08/177.4.2431.DC1 Material http://www.jimmunol.org/ References This article cites 68 articles, 28 of which you can access for free at: http://www.jimmunol.org/content/177/4/2431.full#ref-list-1 Why The JI? Submit online. • Rapid Reviews! 30 days* from submission to initial decision by guest on September 29, 2021 • No Triage! Every submission reviewed by practicing scientists • Fast Publication! 4 weeks from acceptance to publication *average Subscription Information about subscribing to The Journal of Immunology is online at: http://jimmunol.org/subscription Permissions Submit copyright permission requests at: http://www.aai.org/About/Publications/JI/copyright.html Email Alerts Receive free email-alerts when new articles cite this article. Sign up at: http://jimmunol.org/alerts The Journal of Immunology is published twice each month by The American Association of Immunologists, Inc., 1451 Rockville Pike, Suite 650, Rockville, MD 20852 Copyright © 2006 by The American Association of Immunologists All rights reserved. Print ISSN: 0022-1767 Online ISSN: 1550-6606. The Journal of Immunology Activation of Murine CD4؉ and CD8؉ T Lymphocytes Leads to Dramatic Remodeling of N-Linked Glycans1 Elena M. Comelli,2* Mark Sutton-Smith,‡ Qi Yan,* Margarida Amado,* Maria Panico,‡ Tim Gilmartin,† Thomas Whisenant,† Caroline M. Lanigan,† Steven R. Head,† David Goldberg,§ Howard R. Morris,3‡ Anne Dell,‡ and James C. Paulson4* Differentiation and activation of lymphocytes are documented to result in changes in glycosylation associated with biologically important consequences. In this report, we have systematically examined global changes in N-linked glycosylation following activation of murine CD4 T cells, CD8 T cells, and B cells by MALDI-TOF mass spectrometry profiling, and investigated the molecular basis for those changes by assessing alterations in the expression of glycan transferase genes. Surprisingly, the major change observed in activated CD4 and CD8 T cells was a dramatic reduction of sialylated biantennary N-glycans carrying the terminal NeuGc␣2-6Gal sequence, and a corresponding increase in glycans carrying the Gal␣1-3Gal sequence. This change was Downloaded from accounted for by a decrease in the expression of the sialyltransferase ST6Gal I, and an increase in the expression of the galac- tosyltransferase, ␣1-3GalT. Conversely, in B cells no change in terminal sialylation of N-linked glycans was evident, and the expression of the same two glycosyltransferases was increased and decreased, respectively. The results have implications for differential recognition of activated and unactivated T cells by dendritic cells and B cells expressing glycan-binding proteins that recognize terminal sequences of N-linked glycans. The Journal of Immunology, 2006, 177: 2431–2440. http://www.jimmunol.org/ ifferentiation and activation of lymphocytes are accom- ST3Gal Inull mice that are constitutively PNAhigh undergo rapid panied by programmed remodeling of cell surface gly- apoptosis in the periphery, reducing the CD8 population to 10% of D cans of glycoproteins with biologically important con- wild type (2). Yet, conversion from PNAlow to PNAhigh is a natural sequences. Notably, the conversion of the peanut agglutinin consequence of activation of wild-type CD8 cells resulting from (PNA)5 high (PNAhigh) phenotype of immature CD4/CD8 medul- down-regulation of ST3Gal I (2, 8, 9). In contrast, ST3Gal I is lary thymocytes to the PNAlow phenotype of the mature single- differentially regulated in activated and polarized Th1 and Th2 positive CD8 and CD4 thymocytes results from conversion of the CD4 cells leading to the PNAhigh and PNAlow phenotype, respec- ␤ ␣ PNA ligand, the O-linked glycan Gal 1-3GalNAc Thr/Ser, to its tively (10). The additional increased expression of fucosyl- and by guest on September 29, 2021 sialylated form, NeuAc␣2–3Gal␤1-3GalNAc␣Thr/Ser, that is no sialyltransferases in Th1 cells promotes synthesis of the selectin longer recognized by PNA due to increased expression of a sia- ligand sialyl-Lewis X (NeuAc␣2-3Gal␤1-4[Fuca1-3]GlcNAc), lyltransferase, ST3Gal I (1–4). In CD8 T cells, this glycosylation while Th2 helper cells lack sialyl-Lewis X sequences because a change reduces the affinity of CD8 for MHC class I, suggesting key fucosyltransferase, Fuc-T VII, is not expressed. Such differ- that sialylation of CD8 O-glycans modulates CD8 function during ential glycosylation accounts for the selectin-mediated recruitment selection and maturation of CD8 T cells (5–7). Naive CD8 cells of of CD4 Th1 cells to sites of inflammation (11–17). Insights into the importance of N-linked glycan structures in *Departments of Molecular Biology and Molecular and Experimental Medicine and lymphocyte biology have also been obtained by ablation or over- †DNA Microarray Core Facility, The Scripps Research Institute, La Jolla, CA 92037; expression of key glycosyltransferases. For example, ablation of ‡ Division of Molecular Biosciences, Imperial College, London, United Kingdom; and the GlcNAc transferase Mgat5 leads to increased TCR signaling §Scripps-Palo Alto Research Center Institute for Advanced Biomedical Sciences, Palo Alto, CA 94304 and autoimmune disease, and promotes Th2 over Th1 responses, a ␤ Received for publication February 17, 2006. Accepted for publication April 26, 2006. result of the loss of N-linked glycans with a GlcNAc 1-6Man The costs of publication of this article were defrayed in part by the payment of page branch that interacts with galectins and reduces TCR signaling by charges. This article must therefore be hereby marked advertisement in accordance restricting TCR clustering (18). A sialyltransferase that elaborates with 18 U.S.C. Section 1734 solely to indicate this fact. the terminal sequence NeuAc␣2-6Gal␤1-4GlcNAc on N-linked 1 This work was supported by National Institutes of Health Grants AI50143 (to J.C.P.) and O-linked glycans has been shown to block the binding of ga- and GM074128 (to D.G.) and by research grants from the Biotechnology and Bio- logical Sciences Research Council and the Wellcome Trust (to H.R.M. and A.D.). lectin-1 that induces T cell death by clustering of CD45 and re- Microarray analysis was performed by the Microarray Core of the Consortium for duction of its phosphatase activity (19). The same sequence has Functional Glycomics (GM62116). A.D. is a Biotechnology and Biological Sciences been documented to be the glycan ligand for CD22 (Siglec-2), a Research Council Professorial Fellow. regulator of B cell signaling, that has been proposed to mediate 2 Current address: Nestle´Research Centre, Lausanne, Switzerland. adhesion of B cells to T cells (20–25). The expression of the en- 3 Current address: M-SCAN Mass Spectrometry Research and Training Centre, Sil- wood Park, Ascot SL5 7PZ, U.K. zyme responsible for the synthesis of the sequence, ST6Gal I, was 4 Address correspondence and reprint requests to Dr. James C. Paulson, Department noted to be down-regulated in a microarray analysis of Ag-acti- of Molecular Biology and Molecular and Experimental Medicine, The Scripps Re- vated CD8 cells, but the consequences on the structures of CD8 search Institute, 10550 North Torrey Pines Road, MEM-L71, La Jolla, CA 92037. cell glycans were not investigated (26). E-mail address: [email protected] Despite the importance of glycosylation in lymphocyte function, 5 Abbreviations used in this paper: PNA, peanut agglutinin; MS, mass spectrometry; SNA, Sambucus nigra agglutinin; GS, Griffonia simplicifolia; RMA, robust multiar- changes in glycosylation are largely studied through indirect ray analysis. means such as probing for the presence or absence of specific Copyright © 2006 by The American Association of Immunologists, Inc. 0022-1767/06/$02.00 2432 GLYCOSYLATION CHANGES IN ACTIVATED LYMPHOCYTES glycan sequences with plant or animal lectins or carbohydrate- Briefly, cells were resuspended in PBS containing 5 mg/ml BSA and 2 specific Abs. Although this approach has provided biologically mM EDTA and incubated with anti-CD4, anti-CD8, or anti-CD19 mi- important information, it is limited to examining aspects of struc- crobeads for 15 min at 4°C for purification of CD4, CD8 T cells, or B cells, respectively. After washing, cells were resuspended in the same ture relevant to the specificity of the probes used, and does not buffer and applied to the column. Purity of cell preparations was always address the extent to which changes occur. Indeed, there have been Ն90%, as judged by flow cytometry. Purified cells were either washed few investigations of glycosylation changes in lymphocytes in with PBS twice and immediately frozen and stored at Ϫ80°C until use which direct analysis of glycan structure has been conducted. An or immediately used for flow cytometry analysis. exception is a rigorous analysis conducted nearly 20 years ago Flow cytometry investigating the O-linked glycans of human leukosialin before ϫ and after activation of human T cells (27). This study revealed that Purified CD4, CD8 T cells and B cells were incubated in aliquots of 5 105 cells in 100 ␮l of PBS containing 10 mg/ml BSA with or without the predominant disialylated “core 1” glycans of naive T cells GS-I-B4-FITC lectin from Griffonia simplicifolia (GS; EY Laboratories) at (NeuAc␣2-3Gal␤1-3(NeuAc␣2-6)GalNAc␣Thr/Ser) were re- a concentration of 20 ␮g/ml or Sambucus nigra agglutinin (SNA) lectin placed by larger branched “core 2” structures (NeuAc␣2-3Gal␤1- (Vector Laboratories) at a concentration of 40 ␮g/ml, for 30 min on ice.
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