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Science 302 (5647): 1041-1043

Copyright © 2003 by the American Association for the Advancement of Science

Control of Effector CD8+ T Cell Function by the Transcription Factor Eomesodermin

Erika L. Pearce,1 Alan C. Mullen,1 Gislâine A. Martins,1 Connie M. Krawczyk,1 Anne S. Hutchins,1 Valerie P. Zediak,1 Monica Banica,1 Catherine B. DiCioccio,1 Darrick A. Gross,1 Chai-an Mao,4 Hao Shen,2 Nezih Cereb,5 Soo Y. Yang,5 Tullia Lindsten,1 Janet Rossant,4 Christopher A. Hunter,3 Steven L. Reiner1*

Abstract: Activated CD8+ T cells play a critical role in host defense against viruses, intracellular microbes, and tumors. It is not clear if a key regulatory transcription factor unites the effector functions of CD8+ T cells. We now show that Eomesodermin (Eomes), a paralogue of T-bet, is induced in effector CD8+ T cells in vitro and in vivo. Ectopic expression of Eomes was sufficient to invoke attributes of effector CD8+ T cells, including interferon-{gamma} (IFN-{gamma}), perforin, and granzyme B. Loss-of-function analysis suggests Eomes may also be necessary for full effector differentiation of CD8+ T cells. We suggest that Eomesodermin is likely to complement the actions of T-bet and act as a key regulatory gene in the development of cell-mediated immunity.

1 Abramson Family Cancer Research Institute, and Department of Medicine, University of Pennsylvania, Philadelphia, PA 19104, USA.
2 Department of Microbiology, University of Pennsylvania, Philadelphia, PA 19104, USA.
3 Department of Pathobiology, University of Pennsylvania, Philadelphia, PA 19104, USA.
4 Samuel Lunenfeld Research Institute, and Mount Sinai Hospital, University of Toronto, Toronto, Ontario, Canada M5G 1X5.
5 Histogenetics, and Center for Genetic Polymorphism, Ossining, NY 10562, USA.

* To whom correspondence should be addressed. E-mail: sreiner{at}mail.med.upenn.edu

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IL-21-Mediated Potentiation of Antitumor Cytolytic and Proinflammatory Responses of Human V{gamma}9V{delta}2 T Cells for Adoptive Immunotherapy.
A. Thedrez, C. Harly, A. Morice, S. Salot, M. Bonneville, and E. Scotet (2009)
J. Immunol. 182, 3423-3431
   Abstract »    Full Text »    PDF »
Eomesodermin Requires Transforming Growth Factor-{beta}/Activin Signaling and Binds Smad2 to Activate Mesodermal Genes.
P. Picozzi, F. Wang, K. Cronk, and K. Ryan (2009)
J. Biol. Chem. 284, 2397-2408
   Abstract »    Full Text »    PDF »
Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs.
F. Cruz-Guilloty, M. E. Pipkin, I. M. Djuretic, D. Levanon, J. Lotem, M. G. Lichtenheld, Y. Groner, and A. Rao (2009)
J. Exp. Med. 206, 51-59
   Abstract »    Full Text »    PDF »
The cytolytic enzymes granyzme A, granzyme B, and perforin: expression patterns, cell distribution, and their relationship to cell maturity and bright CD57 expression.
P. K. Chattopadhyay, M. R. Betts, D. A. Price, E. Gostick, H. Horton, M. Roederer, and S. C. De Rosa (2009)
J. Leukoc. Biol. 85, 88-97
   Abstract »    Full Text »    PDF »
T-bet and Eomesodermin Play Critical Roles in Directing T Cell Differentiation to Th1 versus Th17.
Y. Yang, J. Xu, Y. Niu, J. S. Bromberg, and Y. Ding (2008)
J. Immunol. 181, 8700-8710
   Abstract »    Full Text »    PDF »
Self-Antigen Prevents CD8 T Cell Effector Differentiation by CD134 and CD137 Dual Costimulation.
S. Bandyopadhyay, M. Long, H. Z. Qui, A. T. Hagymasi, A. M. Slaiby, M. A. Mihalyo, H. L. Aguila, R. S. Mittler, A. T. Vella, and A. J. Adler (2008)
J. Immunol. 181, 7728-7737
   Abstract »    Full Text »    PDF »
CD8+ Th17 Mediate Costimulation Blockade-Resistant Allograft Rejection in T-bet-Deficient Mice.
B. E. Burrell, K. Csencsits, G. Lu, S. Grabauskiene, and D. K. Bishop (2008)
J. Immunol. 181, 3906-3914
   Abstract »    Full Text »    PDF »
Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity.
X. Zhou, L. T. Jeker, B. T. Fife, S. Zhu, M. S. Anderson, M. T. McManus, and J. A. Bluestone (2008)
J. Exp. Med. 205, 1983-1991
   Abstract »    Full Text »    PDF »
CD4 T cells: fates, functions, and faults.
J. Zhu and W. E. Paul (2008)
Blood 112, 1557-1569
   Abstract »    Full Text »    PDF »
Phenotype and Functional Characterization of Long-term gp100-Specific Memory CD8+ T Cells in Disease-Free Melanoma Patients Before and After Boosting Immunization.
E. B. Walker, D. Haley, U. Petrausch, K. Floyd, W. Miller, N. Sanjuan, G. Alvord, B. A. Fox, and W. J. Urba (2008)
Clin. Cancer Res. 14, 5270-5283
   Abstract »    Full Text »    PDF »
Identification of an Evolutionarily Conserved Transcriptional Signature of CD8 Memory Differentiation That Is Shared by T and B Cells.
W. N. Haining, B. L. Ebert, A. Subrmanian, E. J. Wherry, Q. Eichbaum, J. W. Evans, R. Mak, S. Rivoli, J. Pretz, J. Angelosanto, et al. (2008)
J. Immunol. 181, 1859-1868
   Abstract »    Full Text »    PDF »
Anomalous Type 17 Response to Viral Infection by CD8+ T Cells Lacking T-bet and Eomesodermin.
A. M. Intlekofer, A. Banerjee, N. Takemoto, S. M. Gordon, C. S. DeJong, H. Shin, C. A. Hunter, E. J. Wherry, T. Lindsten, and S. L. Reiner (2008)
Science 321, 408-411
   Abstract »    Full Text »    PDF »
T-Bet Plays a Key Role in NK-Mediated Control of Melanoma Metastatic Disease.
M. B. F. Werneck, G. Lugo-Villarino, E. S. Hwang, H. Cantor, and L. H. Glimcher (2008)
J. Immunol. 180, 8004-8010
   Abstract »    Full Text »    PDF »
Histone Acetylation Facilitates Rapid and Robust Memory CD8 T Cell Response through Differential Expression of Effector Molecules (Eomesodermin and Its Targets: Perforin and Granzyme B).
Y. Araki, M. Fann, R. Wersto, and N.-p. Weng (2008)
J. Immunol. 180, 8102-8108
   Abstract »    Full Text »    PDF »
IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy.
C. S. Hinrichs, R. Spolski, C. M. Paulos, L. Gattinoni, K. W. Kerstann, D. C. Palmer, C. A. Klebanoff, S. A. Rosenberg, W. J. Leonard, and N. P. Restifo (2008)
Blood 111, 5326-5333
   Abstract »    Full Text »    PDF »
Effector CD8 T Cell Development: A Balancing Act between Memory Cell Potential and Terminal Differentiation.
N. S. Joshi and S. M. Kaech (2008)
J. Immunol. 180, 1309-1315
   Abstract »    Full Text »    PDF »

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