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The Journal of Immunology, 1999, 163: 5211-5218.
Copyright © 1999 by The American Association of Immunologists

Induction of Tumor Immunity by Removing CD25+CD4+ T Cells: A Common Basis Between Tumor Immunity and Autoimmunity1

Jun Shimizu*, Sayuri Yamazaki{dagger} and Shimon Sakaguchi2,*,{dagger}

* Department of Immunopathology, Tokyo Metropolitan Institute of Gerontology, Tokyo, Japan; and {dagger} Department of Experimental Pathology, Institute for Frontier Medical Sciences, Kyoto University, Kyoto, Japan

This study shows that removal of a T cell subpopulation can evoke effective tumor immunity in otherwise nonresponding animals. Elimination of CD25-expressing T cells, which constitute 5–10% of peripheral CD4+ T cells in normal naive mice, elicited potent immune responses to syngeneic tumors in vivo and eradicated them. The responses were mediated by tumor-specific CD8+ CTLs and tumor-nonspecific CD4-8- cytotoxic cells akin to NK cells. Furthermore, in vitro culture of CD25+4+ T cell-depleted splenic cell suspensions prepared from tumor-unsensitized normal mice led to spontaneous generation of similar CD4-8- cytotoxic cells capable of killing a broad spectrum of tumors; reconstitution of CD25+4+ T cells inhibited the generation. In this culture, self-reactive CD25-4+ T cells responding to self peptides/class II MHC complexes on APCs spontaneously proliferated upon removal of CD25+4+ T cells, secreting large amounts of IL-2. The IL-2 thus produced appeared to be responsible for the generation of CD4-8- NK cells as lymphokine-activated killer cells, because direct addition of an equivalent amount of IL-2 to the culture of CD4-8- cells generated similar lymphokine-activated killer/NK cells, whereas coculture of normal CD4-8- cells with CD25-4+ T cells from IL-2-deficient mice did not. Thus, removal of immunoregulatory CD25+4+ T cells can abrogate immunological unresponsiveness to syngeneic tumors in vivo and in vitro, leading to spontaneous development of tumor-specific effector cells as well as tumor-nonspecific ones. This novel way of evoking tumor immunity would help to devise effective immunotherapy for cancer in humans.




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Cancer Res.Home page
A. Chen, S. Liu, D. Park, Y. Kang, and G. Zheng
Depleting Intratumoral CD4+CD25+ Regulatory T Cells via FasL Protein Transfer Enhances the Therapeutic Efficacy of Adoptive T Cell Transfer
Cancer Res., February 1, 2007; 67(3): 1291 - 1298.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
N. Kobayashi, N. Hiraoka, W. Yamagami, H. Ojima, Y. Kanai, T. Kosuge, A. Nakajima, and S. Hirohashi
FOXP3+ Regulatory T Cells Affect the Development and Progression of Hepatocarcinogenesis
Clin. Cancer Res., February 1, 2007; 13(3): 902 - 911.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Nair, D. Boczkowski, M. Fassnacht, D. Pisetsky, and E. Gilboa
Vaccination against the Forkhead Family Transcription Factor Foxp3 Enhances Tumor Immunity
Cancer Res., January 1, 2007; 67(1): 371 - 380.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
N. Ralainirina, A. Poli, T. Michel, L. Poos, E. Andres, F. Hentges, and J. Zimmer
Control of NK cell functions by CD4+CD25+ regulatory T cells
J. Leukoc. Biol., January 1, 2007; 81(1): 144 - 153.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. Charalambous, M. Oks, G. Nchinda, S. Yamazaki, and R. M. Steinman
Dendritic Cell Targeting of Survivin Protein in a Xenogeneic Form Elicits Strong CD4+ T Cell Immunity to Mouse Survivin
J. Immunol., December 15, 2006; 177(12): 8410 - 8421.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. J. Dobrzanski, J. B. Reome, J. C. Hylind, and K. A. Rewers-Felkins
CD8-Mediated Type 1 Antitumor Responses Selectively Modulate Endogenous Differentiated and Nondifferentiated T Cell Localization, Activation, and Function in Progressive Breast Cancer
J. Immunol., December 1, 2006; 177(11): 8191 - 8201.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
Z.-Z. Yang, A. J. Novak, S. C. Ziesmer, T. E. Witzig, and S. M. Ansell
Attenuation of CD8+ T-Cell Function by CD4+CD25+ Regulatory T Cells in B-Cell Non-Hodgkin's Lymphoma.
Cancer Res., October 15, 2006; 66(20): 10145 - 10152.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. Read, R. Greenwald, A. Izcue, N. Robinson, D. Mandelbrot, L. Francisco, A. H. Sharpe, and F. Powrie
Blockade of CTLA-4 on CD4+CD25+ Regulatory T Cells Abrogates Their Function In Vivo
J. Immunol., October 1, 2006; 177(7): 4376 - 4383.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
L. Melencio, R. J. McKallip, H. Guan, R. Ramakrishnan, R. Jain, P. S. Nagarkatti, and M. Nagarkatti
Role of CD4+CD25+ T regulatory cells in IL-2-induced vascular leak
Int. Immunol., October 1, 2006; 18(10): 1461 - 1471.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
N. Hiraoka, K. Onozato, T. Kosuge, and S. Hirohashi
Prevalence of FOXP3+ Regulatory T Cells Increases During the Progression of Pancreatic Ductal Adenocarcinoma and Its Premalignant Lesions.
Clin. Cancer Res., September 15, 2006; 12(18): 5423 - 5434.
[Abstract] [Full Text] [PDF]


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Ann. Surg. Oncol.Home page
C. T. Viehl, T. T. Moore, U. K. Liyanage, D. M. Frey, J. P. Ehlers, T. J. Eberlein, P. S. Goedegebuure, and D. C. Linehan
Depletion of CD4+CD25+ Regulatory T Cells Promotes a Tumor-Specific Immune Response in Pancreas Cancer-Bearing Mice
Ann. Surg. Oncol., September 1, 2006; 13(9): 1252 - 1258.
[Abstract] [Full Text] [PDF]


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Evid Based Complement Alternat MedHome page
A. Vojdani and J. Erde
Regulatory T Cells, a Potent Immunoregulatory Target for CAM Researchers: Modulating Tumor Immunity, Autoimmunity and Alloreactive Immunity (III)
Evid. Based Complement. Altern. Med., September 1, 2006; 3(3): 309 - 316.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
G. Lizee, L. G. Radvanyi, W. W. Overwijk, and P. Hwu
Improving Antitumor Immune Responses by Circumventing Immunoregulatory Cells and Mechanisms.
Clin. Cancer Res., August 15, 2006; 12(16): 4794 - 4803.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. Maksimow, M. Miiluniemi, F. Marttila-Ichihara, S. Jalkanen, and A. Hanninen
Antigen targeting to endosomal pathway in dendritic cell vaccination activates regulatory T cells and attenuates tumor immunity
Blood, August 15, 2006; 108(4): 1298 - 1305.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
E. Ambrosino, M. Spadaro, M. Iezzi, C. Curcio, G. Forni, P. Musiani, W.-Z. Wei, and F. Cavallo
Immunosurveillance of erbb2 carcinogenesis in transgenic mice is concealed by a dominant regulatory T-cell self-tolerance.
Cancer Res., August 1, 2006; 66(15): 7734 - 7740.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
N. Sugimoto, T. Oida, K. Hirota, K. Nakamura, T. Nomura, T. Uchiyama, and S. Sakaguchi
Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis
Int. Immunol., August 1, 2006; 18(8): 1197 - 1209.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. Beyer and J. L. Schultze
Regulatory T cells in cancer
Blood, August 1, 2006; 108(3): 804 - 811.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
J. D. Bui, R. Uppaluri, C.-S. Hsieh, and R. D. Schreiber
Comparative Analysis of Regulatory and Effector T Cells in Progressively Growing versus Rejecting Tumors of Similar Origins.
Cancer Res., July 15, 2006; 66(14): 7301 - 7309.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
P. E. Fecci, A. E. Sweeney, P. M. Grossi, S. K. Nair, C. A. Learn, D. A. Mitchell, X. Cui, T. J. Cummings, D. D. Bigner, E. Gilboa, et al.
Systemic Anti-CD25 Monoclonal Antibody Administration Safely Enhances Immunity in Murine Glioma without Eliminating Regulatory T Cells.
Clin. Cancer Res., July 15, 2006; 12(14): 4294 - 4305.
[Abstract] [Full Text] [PDF]


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BloodHome page
R. Zeiser, V. H. Nguyen, A. Beilhack, M. Buess, S. Schulz, J. Baker, C. H. Contag, and R. S. Negrin
Inhibition of CD4+CD25+ regulatory T-cell function by calcineurin-dependent interleukin-2 production
Blood, July 1, 2006; 108(1): 390 - 399.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
S. Oniki, H. Nagai, T. Horikawa, J. Furukawa, M. L. Belladonna, T. Yoshimoto, I. Hara, and C. Nishigori
Interleukin-23 and interleukin-27 exert quite different antitumor and vaccine effects on poorly immunogenic melanoma.
Cancer Res., June 15, 2006; 66(12): 6395 - 6404.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
T. Ishida, T. Ishii, A. Inagaki, H. Yano, H. Komatsu, S. Iida, H. Inagaki, and R. Ueda
Specific Recruitment of CC Chemokine Receptor 4-Positive Regulatory T Cells in Hodgkin Lymphoma Fosters Immune Privilege
Cancer Res., June 1, 2006; 66(11): 5716 - 5722.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. Ramirez-Montagut, A. Chow, D. Hirschhorn-Cymerman, T. H. Terwey, A. A. Kochman, S. Lu, R. C. Miles, S. Sakaguchi, A. N. Houghton, and M. R. M. van den Brink
Glucocorticoid-Induced TNF Receptor Family Related Gene Activation Overcomes Tolerance/Ignorance to Melanoma Differentiation Antigens and Enhances Antitumor Immunity.
J. Immunol., June 1, 2006; 176(11): 6434 - 6442.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Offner, S. Subramanian, S. M. Parker, C. Wang, M. E. Afentoulis, A. Lewis, A. A. Vandenbark, and P. D. Hurn
Splenic Atrophy in Experimental Stroke Is Accompanied by Increased Regulatory T Cells and Circulating Macrophages.
J. Immunol., June 1, 2006; 176(11): 6523 - 6531.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. Nishioka, J. Shimizu, R. Iida, S. Yamazaki, and S. Sakaguchi
CD4+CD25+Foxp3+ T Cells and CD4+CD25-Foxp3+ T Cells in Aged Mice.
J. Immunol., June 1, 2006; 176(11): 6586 - 6593.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Veldhoen, H. Moncrieffe, R. J. Hocking, C. J. Atkins, and B. Stockinger
Modulation of Dendritic Cell Function by Naive and Regulatory CD4+ T Cells
J. Immunol., May 15, 2006; 176(10): 6202 - 6210.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Nishikawa, F. Qian, T. Tsuji, G. Ritter, L. J. Old, S. Gnjatic, and K. Odunsi
Influence of CD4+CD25+ Regulatory T Cells on Low/High-Avidity CD4+ T Cells following Peptide Vaccination
J. Immunol., May 15, 2006; 176(10): 6340 - 6346.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. Beyer, M. Kochanek, T. Giese, E. Endl, M. R. Weihrauch, P. A. Knolle, S. Classen, and J. L. Schultze
In vivo peripheral expansion of naive CD4+CD25high FoxP3+ regulatory T cells in patients with multiple myeloma
Blood, May 15, 2006; 107(10): 3940 - 3949.
[Abstract] [Full Text] [PDF]


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BloodHome page
D.-M. Zhao, A. M. Thornton, R. J. DiPaolo, and E. M. Shevach
Activated CD4+CD25+ T cells selectively kill B lymphocytes
Blood, May 15, 2006; 107(10): 3925 - 3932.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
A. D. Cohen, A. Diab, M.-A. Perales, J. D. Wolchok, G. Rizzuto, T. Merghoub, D. Huggins, C. Liu, M. J. Turk, N. P. Restifo, et al.
Agonist Anti-GITR Antibody Enhances Vaccine-Induced CD8+ T-Cell Responses and Tumor Immunity.
Cancer Res., May 1, 2006; 66(9): 4904 - 4912.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
O. Saitoh and Y. Nagayama
Regulation of Graves' Hyperthyroidism with Naturally Occurring CD4+CD25+ Regulatory T Cells in a Mouse Model
Endocrinology, May 1, 2006; 147(5): 2417 - 2422.
[Abstract] [Full Text] [PDF]


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BloodHome page
Z.-Z. Yang, A. J. Novak, M. J. Stenson, T. E. Witzig, and S. M. Ansell
Intratumoral CD4+CD25+ regulatory T-cell-mediated suppression of infiltrating CD4+ T cells in B-cell non-Hodgkin lymphoma
Blood, May 1, 2006; 107(9): 3639 - 3646.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
C. Casati, C. Camisaschi, F. Rini, F. Arienti, L. Rivoltini, F. Triebel, G. Parmiani, and C. Castelli
Soluble Human LAG-3 Molecule Amplifies the In vitro Generation of Type 1 Tumor-Specific Immunity.
Cancer Res., April 15, 2006; 66(8): 4450 - 4460.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
B. Valzasina, S. Piconese, C. Guiducci, and M. P. Colombo
Tumor-Induced Expansion of Regulatory T Cells by Conversion of CD4+CD25- Lymphocytes Is Thymus and Proliferation Independent.
Cancer Res., April 15, 2006; 66(8): 4488 - 4495.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Ono, J. Shimizu, Y. Miyachi, and S. Sakaguchi
Control of Autoimmune Myocarditis and Multiorgan Inflammation by Glucocorticoid-Induced TNF Receptor Family-Related Proteinhigh, Foxp3-Expressing CD25+ and CD25- Regulatory T Cells.
J. Immunol., April 15, 2006; 176(8): 4748 - 4756.
[Abstract] [Full Text] [PDF]




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