Differentiating between Memory and Effector CD8 T Cells by Altered Expression of Cell Surface O-Glycans

doi:10.1084/jem.191.7.1241

Published online 3 April 2000.

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© The Rockefeller University Press, 0022-1007/2000/4/1241/ $5.00
The Journal of Experimental Medicine, Volume 191, Number 7, April 3, 2000 1241-1246

Brief Definitive Report

Differentiating between Memory and Effector CD8 T Cells by Altered Expression of Cell Surface O-Glycans

Laurie E. Harrington^a, Marisa Galvan^b, Linda G. Baum^b, John D. Altman^a, and Rafi Ahmed^a
^a Emory Vaccine Center and Department of Microbiology and Immunology, Emory University School of Medicine, Atlanta, Georgia 30322
^b Department of Pathology and Laboratory Medicine, University of California Los Angeles School of Medicine, Los Angeles, California 90095

Correspondence to: Rafi Ahmed, Emory Vaccine Center and Dept. of Microbiology and Immunology, Emory University School of Medicine, G211 Rollins Research Bldg., 1510 Clifton Rd., Atlanta, GA 30322. Tel:404-727-3571 Fax:404-727-3722 E-mail:ra{at}microbio.emory.edu.

Currently there are few reliable cell surface markers that canclearly discriminate effector from memory T cells. To determineif there are changes in O-glycosylation between these two celltypes, we analyzed virus-specific CD8 T cells at various timepoints after lymphocytic choriomeningitis virus infection ofmice. Antigen-specific CD8 T cells were identified using majorhistocompatibility complex class I tetramers, and glycosylationchanges were monitored with a monoclonal antibody (1B11) thatrecognizes O-glycans on mucin-type glycoproteins. We observeda striking upregulation of a specific cell surface O-glycanepitope on virus-specific CD8 T cells during the effector phaseof the primary cytotoxic T lymphocyte (CTL) response. This upregulationshowed a strong correlation with the acquisition of effectorfunction and was downregulated on memory CD8 T cells. Upon reinfection,there was again increased expression of this specific O-glycanepitope on secondary CTL effectors, followed once more by decreasedexpression on memory cells. Thus, this study identifies a newcell surface marker to distinguish between effector and memoryCD8 T cells. This marker can be used to isolate pure populationsof effector CTLs and also to determine the proportion of memoryCD8 T cells that are recruited into the secondary response uponreencounter with antigen. This latter information will be ofvalue in optimizing immunization strategies for boosting CD8T cell responses.

Key Words: memory T cells, effector T cells, cytotoxic T lymphocytes, viralimmunity, O-glycosylation

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Fuller, M. J., Zajac, A. J. (2003). Ablation of CD8 and CD4 T Cell Responses by High Viral Loads. J. Immunol. 170: 477-486 [Abstract] [Full Text]
Zenewicz, L. A., Foulds, K. E., Jiang, J., Fan, X., Shen, H. (2002). Nonsecreted Bacterial Proteins Induce Recall CD8 T Cell Responses But Do Not Serve as Protective Antigens. J. Immunol. 169: 5805-5812 [Abstract] [Full Text]
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Hernandez, J. D., Baum, L. G. (2002). Ah, sweet mystery of death! Galectins and control of cell fate. Glycobiology 12: 127R-136R [Abstract] [Full Text]
Schepers, K., Toebes, M., Sotthewes, G., Vyth-Dreese, F. A., Dellemijn, T. A. M., Melief, C. J. M., Ossendorp, F., Schumacher, T. N. M. (2002). Differential Kinetics of Antigen-Specific CD4+ and CD8+ T Cell Responses in the Regression of Retrovirus-Induced Sarcomas. J. Immunol. 169: 3191-3199 [Abstract] [Full Text]
Miller, J. D., Peters, M., Oran, A. E., Beresford, G. W., Harrington, L., Boss, J. M., Altman, J. D. (2002). CD94/NKG2 Expression Does Not Inhibit Cytotoxic Function of Lymphocytic Choriomeningitis Virus-Specific CD8+ T Cells. J. Immunol. 169: 693-701 [Abstract] [Full Text]
Sedegah, M., Brice, G. T., Rogers, W. O., Doolan, D. L., Charoenvit, Y., Jones, T. R., Majam, V. F., Belmonte, A., Lu, M., Belmonte, M., Carucci, D. J., Hoffman, S. L. (2002). Persistence of Protective Immunity to Malaria Induced by DNA Priming and Poxvirus Boosting: Characterization of Effector and Memory CD8+-T-Cell Populations. Infect. Immun. 70: 3493-3499 [Abstract] [Full Text]
Becker, T. C., Wherry, E. J., Boone, D., Murali-Krishna, K., Antia, R., Ma, A., Ahmed, R. (2002). Interleukin 15 Is Required for Proliferative Renewal of Virus-specific Memory CD8 T Cells. JEM 195: 1541-1548 [Abstract] [Full Text]
Onami, T. M., Harrington, L. E., Williams, M. A., Galvan, M., Larsen, C. P., Pearson, T. C., Manjunath, N., Baum, L. G., Pearce, B. D., Ahmed, R. (2002). Dynamic Regulation of T Cell Immunity by CD43. J. Immunol. 168: 6022-6031 [Abstract] [Full Text]
Priatel, J. J., Utting, O., Teh, H.-S. (2001). TCR/Self-Antigen Interactions Drive Double-Negative T Cell Peripheral Expansion and Differentiation into Suppressor Cells. J. Immunol. 167: 6188-6194 [Abstract] [Full Text]
Nguyen, J. T., Evans, D. P., Galvan, M., Pace, K. E., Leitenberg, D., Bui, T. N., Baum, L. G. (2001). CD45 Modulates Galectin-1-Induced T Cell Death: Regulation by Expression of Core 2 O-Glycans. J. Immunol. 167: 5697-5707 [Abstract] [Full Text]
Voehringer, D., Blaser, C., Brawand, P., Raulet, D. H., Hanke, T., Pircher, H. (2001). Viral Infections Induce Abundant Numbers of Senescent CD8 T Cells. J. Immunol. 167: 4838-4843 [Abstract] [Full Text]
Chang, J., Srikiatkhachorn, A., Braciale, T. J. (2001). Visualization and Characterization of Respiratory Syncytial Virus F-Specific CD8+ T Cells During Experimental Virus Infection. J. Immunol. 167: 4254-4260 [Abstract] [Full Text]
Weninger, W., Crowley, M. A., Manjunath, N., von Andrian, U. H. (2001). Migratory Properties of Naive, Effector, and Memory CD8+ T Cells. JEM 194: 953-966 [Abstract] [Full Text]
Bai, X.-F., Bender, J., Liu, J., Zhang, H., Wang, Y., Li, O., Du, P., Zheng, P., Liu, Y. (2001). Local Costimulation Reinvigorates Tumor-Specific Cytolytic T Lymphocytes for Experimental Therapy in Mice with Large Tumor Burdens. J. Immunol. 167: 3936-3943 [Abstract] [Full Text]
Bergmann, C. C., Ramakrishna, C., Kornacki, M., Stohlman, S. A. (2001). Impaired T Cell Immunity in B Cell-Deficient Mice Following Viral Central Nervous System Infection. J. Immunol. 167: 1575-1583 [Abstract] [Full Text]
Moser, J. M., Altman, J. D., Lukacher, A. E. (2001). Antiviral CD8+ T Cell Responses in Neonatal Mice: Susceptibility to Polyoma Virus-induced Tumors Is Associated with Lack of Cytotoxic Function by Viral Antigen-specific T Cells. JEM 193: 595-606 [Abstract] [Full Text]
Hogan, R. J., Usherwood, E. J., Zhong, W., Roberts, A. D., Dutton, R. W., Harmsen, A. G., Woodland, D. L. (2001). Activated Antigen-Specific CD8+ T Cells Persist in the Lungs Following Recovery from Respiratory Virus Infections. J. Immunol. 166: 1813-1822 [Abstract] [Full Text]
Grayson, J. M., Murali-Krishna, K., Altman, J. D., Ahmed, R. (2001). Gene Expression in Antigen-Specific CD8+ T Cells During Viral Infection. J. Immunol. 166: 795-799 [Abstract] [Full Text]
Ahmadzadeh, M., Hussain, S. F., Farber, D. L. (2001). Heterogeneity of the Memory CD4 T Cell Response: Persisting Effectors and Resting Memory T Cells. J. Immunol. 166: 926-935 [Abstract] [Full Text]
Holtappels, R., Pahl-Seibert, M.-F., Thomas, D., Reddehase, M. J. (2000). Enrichment of Immediate-Early 1 (m123/pp89) Peptide-Specific CD8 T Cells in a Pulmonary CD62Llo Memory-Effector Cell Pool during Latent Murine Cytomegalovirus Infection of the Lungs. J. Virol. 74: 11495-11503 [Abstract] [Full Text]
Fukuoka, M., Fukudome, K., Yamashita, Y., Tokushima, M., Miyake, K., Kimoto, M. (2000). Antiadhesive function of 130-kd glycoform of CD43 expressed in CD4 T-lymphocyte clones and transfectant cell lines. Blood 96: 4267-4275 [Abstract] [Full Text]
Galvan, M., Tsuboi, S., Fukuda, M., Baum, L. G. (2000). Expression of a Specific Glycosyltransferase Enzyme Regulates T Cell Death Mediated by Galectin-1. J. Biol. Chem. 275: 16730-16737 [Abstract] [Full Text]
Santana, M. A., Pedraza-Alva, G., Olivares-Zavaleta, N., Madrid-Marina, V., Horejsi, V., Burakoff, S. J., Rosenstein, Y. (2000). CD43-mediated Signals Induce DNA Binding Activity of AP-1, NF-AT, and NFkappa B Transcription Factors in Human T Lymphocytes. J. Biol. Chem. 275: 31460-31468 [Abstract] [Full Text]