J. Exp. Med., Volume 186, Number 9, November 3, 1997 1407-1418

Phenotypic and Functional Separation of Memory and Effector Human CD8⁺ T Cells

By Dörte Hamann, Paul A. Baars, Martin H.G. Rep, Berend Hooibrink, Susana R. Kerkhof-Garde, Michèl R. Klein, and René A.W. van Lier

From the Department of Clinical Viro-Immunology, Central Laboratory of the Netherlands Red Cross Blood Transfusion Service, and Laboratory of Experimental and Clinical Immunology of the University of Amsterdam, 1066 CX Amsterdam, The Netherlands

Human CD8⁺ memory- and effector-type T cells are poorly defined. We show here that, next to a naive compartment, two discrete primed subpopulations can be found within the circulating human CD8⁺ T cell subset. First, CD45RACD45R0⁺ cells are reminiscent of memory-type T cells in that they express elevated levels of CD95 (Fas) and the integrin family members CD11a, CD18, CD29, CD49d, and CD49e, compared to naive CD8⁺ T cells, and are able to secrete not only interleukin (IL) 2 but also interferon , tumor necrosis factor , and IL-4. This subset does not exert cytolytic activity without prior in vitro stimulation but does contain virus-specific cytotoxic T lymphocyte (CTL) precursors. A second primed population is characterized by CD45RA expression with concomitant absence of expression of the costimulatory molecules CD27 and CD28. The CD8⁺CD45RA⁺CD27 population contains T cells expressing high levels of CD11a, CD11b, CD18, and CD49d, whereas CD62L (L-selectin) is not expressed. These T cells do not secrete IL-2 or -4 but can produce IFN- and TNF-. In accordance with this finding, cells contained within this subpopulation depend for proliferation on exogenous growth factors such as IL-2 and -15. Interestingly, CD8⁺CD45RA⁺CD27 cells parallel effector CTLs, as they abundantly express Fas-ligand mRNA, contain perforin and granzyme B, and have high cytolytic activity without in vitro prestimulation. Based on both phenotypic and functional properties, we conclude that memory- and effector-type T cells can be separated as distinct entities within the human CD8⁺ T cell subset.

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• Willinger, T., Freeman, T., Hasegawa, H., McMichael, A. J., Callan, M. F. C. (2005). Molecular Signatures Distinguish Human Central Memory from Effector Memory CD8 T Cell Subsets. J. Immunol. 175: 5895-5903 [Abstract] [Full Text]  
• Ahn, J. K., Chung, H., Lee, D.-s., Yu, Y. S., Yu, H. G. (2005). CD8brightCD56+ T Cells Are Cytotoxic Effectors in Patients with Active Behcet's Uveitis. J. Immunol. 175: 6133-6142 [Abstract] [Full Text]  
• Bachmann, M. F., Wolint, P., Schwarz, K., Jager, P., Oxenius, A. (2005). Functional Properties and Lineage Relationship of CD8+ T Cell Subsets Identified by Expression of IL-7 Receptor {alpha} and CD62L. J. Immunol. 175: 4686-4696 [Abstract] [Full Text]  
• Elkord, E., Williams, P. E., Kynaston, H., Rowbottom, A. W. (2005). Differential CTLs specific for prostate-specific antigen in healthy donors and patients with prostate cancer. Int Immunol 17: 1315-1325 [Abstract] [Full Text]  
• Thimme, R., Appay, V., Koschella, M., Panther, E., Roth, E., Hislop, A. D., Rickinson, A. B., Rowland-Jones, S. L., Blum, H. E., Pircher, H. (2005). Increased Expression of the NK Cell Receptor KLRG1 by Virus-Specific CD8 T Cells during Persistent Antigen Stimulation. J. Virol. 79: 12112-12116 [Abstract] [Full Text]  
• van Leeuwen, E. M. M., de Bree, G. J., Remmerswaal, E. B. M., Yong, S.-L., Tesselaar, K., Berge, I. J. M. t., van Lier, R. A. W. (2005). IL-7 receptor {alpha} chain expression distinguishes functional subsets of virus-specific human CD8+ T cells. Blood 106: 2091-2098 [Abstract] [Full Text]  
• Salazar, J. C., Pope, C. D., Moore, M. W., Pope, J., Kiely, T. G., Radolf, J. D. (2005). Lipoprotein-Dependent and -Independent Immune Responses to Spirochetal Infection. CVI 12: 949-958 [Abstract] [Full Text]  
• Humphreys, T. L., Baldridge, L. A., Billings, S. D., Campbell, J. J., Spinola, S. M. (2005). Trafficking Pathways and Characterization of CD4 and CD8 Cells Recruited to the Skin of Humans Experimentally Infected with Haemophilus ducreyi. Infect. Immun. 73: 3896-3902 [Abstract] [Full Text]  
• Schilbach, K., Kerst, G., Walter, S., Eyrich, M., Wernet, D., Handgretinger, R., Xie, W., Rammensee, H.-G., Muller, I., Buhring, H.-J., Niethammer, D. (2005). Cytotoxic minor histocompatibility antigen HA-1-specific CD8+ effector memory T cells: artificial APCs pave the way for clinical application by potent primary in vitro induction. Blood 106: 144-149 [Abstract] [Full Text]  
• Sacre, K., Carcelain, G., Cassoux, N., Fillet, A.-M., Costagliola, D., Vittecoq, D., Salmon, D., Amoura, Z., Katlama, C., Autran, B. (2005). Repertoire, diversity, and differentiation of specific CD8 T cells are associated with immune protection against human cytomegalovirus disease. JEM 201: 1999-2010 [Abstract] [Full Text]  
• Ruprecht, C. R., Gattorno, M., Ferlito, F., Gregorio, A., Martini, A., Lanzavecchia, A., Sallusto, F. (2005). Coexpression of CD25 and CD27 identifies FoxP3+ regulatory T cells in inflamed synovia. JEM 201: 1793-1803 [Abstract] [Full Text]  
• Jiang, Y., Jolly, P. E., Ellis, W. O., Wang, J.-S., Phillips, T. D., Williams, J. H. (2005). Aflatoxin B1 albumin adduct levels and cellular immune status in Ghanaians. Int Immunol 17: 807-814 [Abstract] [Full Text]  
• Monceaux, V., Viollet, L., Petit, F., Fang, R. H. T., Cumont, M.-C., Zaunders, J., Hurtrel, B., Estaquier, J. (2005). CD8+ T Cell Dynamics during Primary Simian Immunodeficiency Virus Infection in Macaques: Relationship of Effector Cell Differentiation with the Extent of Viral Replication. J. Immunol. 174: 6898-6908 [Abstract] [Full Text]  
• Holmes, S., He, M., Xu, T., Lee, P. P. (2005). Memory T cells have gene expression patterns intermediate between naive and effector. Proc. Natl. Acad. Sci. USA 102: 5519-5523 [Abstract] [Full Text]  
• Rock, M. T., Yoder, S. M., Wright, P. F., Talbot, T. R., Edwards, K. M., Crowe, J. E. Jr (2005). Differential Regulation of Granzyme and Perforin in Effector and Memory T Cells following Smallpox Immunization. J. Immunol. 174: 3757-3764 [Abstract] [Full Text]  
• Sabbaj, S., Ghosh, M. K., Edwards, B. H., Leeth, R., Decker, W. D., Goepfert, P. A., Aldrovandi, G. M. (2005). Breast Milk-Derived Antigen-Specific CD8+ T Cells: An Extralymphoid Effector Memory Cell Population in Humans. J. Immunol. 174: 2951-2956 [Abstract] [Full Text]  
• Harari, A., Vallelian, F., Meylan, P. R., Pantaleo, G. (2005). Functional Heterogeneity of Memory CD4 T Cell Responses in Different Conditions of Antigen Exposure and Persistence. J. Immunol. 174: 1037-1045 [Abstract] [Full Text]  
• Powell, D. J. Jr, Dudley, M. E., Robbins, P. F., Rosenberg, S. A. (2005). Transition of late-stage effector T cells to CD27+ CD28+ tumor-reactive effector memory T cells in humans after adoptive cell transfer therapy. Blood 105: 241-250 [Abstract] [Full Text]  
• Kim, Y.-J., Stringfield, T. M., Chen, Y., Broxmeyer, H. E. (2005). Modulation of cord blood CD8+ T-cell effector differentiation by TGF-{beta}1 and 4-1BB costimulation. Blood 105: 274-281 [Abstract] [Full Text]  

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