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The Journal of Immunology, 2001, 167: 1137-1140.
Copyright © 2001 by The American Association of Immunologists


Cutting Edge

Cutting Edge: Control of CD8+ T Cell Activation by CD4+CD25+ Immunoregulatory Cells

Ciriaco A. Piccirillo and Ethan M. Shevach1

Laboratory of Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892

CD4+CD25+ regulatory T cells inhibit organ-specific autoimmune diseases induced by CD4+CD25- T cells and are potent suppressors of CD4+CD25- T cell activation in vitro. We demonstrate that CD4+CD25+ T cells also suppress both proliferation and IFN-{gamma} production by CD8+ T cells induced either by polyclonal or Ag-specific stimuli. CD4+CD25+ T cells inhibit the activation of CD8+ responders by inhibiting both IL-2 production and up-regulation of IL-2R{alpha}-chain (CD25) expression. Suppression is mediated via a T-T interaction as activated CD4+CD25+ T cells suppress the responses of TCR-transgenic CD8+ T cells stimulated with soluble peptide-MHC class I tetramers in the complete absence of APC. These results broaden the immunoregulatory role played by CD4+CD25+ T cells in the prevention of autoimmune diseases, but also raise the possibility that they may hinder the induction of effector CD8+ T cells to tumor or foreign Ags.




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T. Boettler, H. C. Spangenberg, C. Neumann-Haefelin, E. Panther, S. Urbani, C. Ferrari, H. E. Blum, F. von Weizsacker, and R. Thimme
T Cells with a CD4+CD25+ Regulatory Phenotype Suppress In Vitro Proliferation of Virus-Specific CD8+ T Cells during Chronic Hepatitis C Virus Infection
J. Virol., June 15, 2005; 79(12): 7860 - 7867.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
C. Kudo-Saito, J. Schlom, K. Camphausen, C. N. Coleman, and J. W. Hodge
The Requirement of Multimodal Therapy (Vaccine, Local Tumor Radiation, and Reduction of Suppressor Cells) to Eliminate Established Tumors
Clin. Cancer Res., June 15, 2005; 11(12): 4533 - 4544.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. Karim, G. Feng, K. J. Wood, and A. R. Bushell
CD25+CD4+ regulatory T cells generated by exposure to a model protein antigen prevent allograft rejection: antigen-specific reactivation in vivo is critical for bystander regulation
Blood, June 15, 2005; 105(12): 4871 - 4877.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
H. Kojima, Y. Kanno, H. Hase, and T. Kobata
CD4+CD25+ Regulatory T Cells Attenuate the Phosphatidylinositol 3-Kinase/Akt Pathway in Antigen-Primed Immature CD8+ CTLs during Functional Maturation
J. Immunol., May 15, 2005; 174(10): 5959 - 5967.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
D. Lundsgaard, T. L. Holm, L. Hornum, and H. Markholst
In Vivo Control of Diabetogenic T-Cells by Regulatory CD4+CD25+ T-Cells Expressing Foxp3
Diabetes, April 1, 2005; 54(4): 1040 - 1047.
[Abstract] [Full Text] [PDF]


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J. Virol.Home page
O. Franzese, P. T. F. Kennedy, A. J. Gehring, J. Gotto, R. Williams, M. K. Maini, and A. Bertoletti
Modulation of the CD8+-T-Cell Response by CD4+ CD25+ Regulatory T Cells in Patients with Hepatitis B Virus Infection
J. Virol., March 15, 2005; 79(6): 3322 - 3328.
[Abstract] [Full Text] [PDF]


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Cancer Res.Home page
L. A. Ormandy, T. Hillemann, H. Wedemeyer, M. P. Manns, T. F. Greten, and F. Korangy
Increased Populations of Regulatory T Cells in Peripheral Blood of Patients with Hepatocellular Carcinoma
Cancer Res., March 15, 2005; 65(6): 2457 - 2464.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. Zhou, S. J. Balin, M. Mashayekhi, K. W. Hwang, D. A. Palucki, and M.-L. Alegre
Transplantation Tolerance in NF-{kappa}B-Impaired Mice Is Not Due to Regulation but Is Prevented by Transgenic Expression of Bcl-xL
J. Immunol., March 15, 2005; 174(6): 3447 - 3453.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. A. Antony, C. A. Piccirillo, A. Akpinarli, S. E. Finkelstein, P. J. Speiss, D. R. Surman, D. C. Palmer, C.-C. Chan, C. A. Klebanoff, W. W. Overwijk, et al.
CD8+ T Cell Immunity Against a Tumor/Self-Antigen Is Augmented by CD4+ T Helper Cells and Hindered by Naturally Occurring T Regulatory Cells
J. Immunol., March 1, 2005; 174(5): 2591 - 2601.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
T. Alvaro, M. Lejeune, M. T. Salvado, R. Bosch, J. F. Garcia, J. Jaen, A. H. Banham, G. Roncador, C. Montalban, and M. A. Piris
Outcome in Hodgkin's Lymphoma Can Be Predicted from the Presence of Accompanying Cytotoxic and Regulatory T Cells
Clin. Cancer Res., February 15, 2005; 11(4): 1467 - 1473.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
P. E. Rao, A. L. Petrone, and P. D. Ponath
Differentiation and Expansion of T Cells with Regulatory Function from Human Peripheral Lymphocytes by Stimulation in the Presence of TGF-{beta}
J. Immunol., February 1, 2005; 174(3): 1446 - 1455.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
M.-L. Chen, M. J. Pittet, L. Gorelik, R. A. Flavell, R. Weissleder, H. von Boehmer, and K. Khazaie
Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-{beta} signals in vivo
PNAS, January 11, 2005; 102(2): 419 - 424.
[Abstract] [Full Text] [PDF]


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DiabetesHome page
S. Lindley, C. M. Dayan, A. Bishop, B. O. Roep, M. Peakman, and T. I.M. Tree
Defective Suppressor Function in CD4+CD25+ T-Cells From Patients With Type 1 Diabetes
Diabetes, January 1, 2005; 54(1): 92 - 99.
[Abstract] [Full Text] [PDF]


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BloodHome page
L. Weiss, V. Donkova-Petrini, L. Caccavelli, M. Balbo, C. Carbonneil, and Y. Levy
Human immunodeficiency virus-driven expansion of CD4+CD25+ regulatory T cells, which suppress HIV-specific CD4 T-cell responses in HIV-infected patients
Blood, November 15, 2004; 104(10): 3249 - 3256.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
E. Belnoue, C. Guettier, M. Kayibanda, S. Le Rond, A.-M. Crain-Denoyelle, C. Marchiol, M. Ziol, D. Fradelizi, L. Renia, and M. Viguier
Regression of Established Liver Tumor Induced by Monoepitopic Peptide-Based Immunotherapy
J. Immunol., October 15, 2004; 173(8): 4882 - 4888.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
G. L. Stephens, R. S. McHugh, M. J. Whitters, D. A. Young, D. Luxenberg, B. M. Carreno, M. Collins, and E. M. Shevach
Engagement of Glucocorticoid-Induced TNFR Family-Related Receptor on Effector T Cells by its Ligand Mediates Resistance to Suppression by CD4+CD25+ T Cells
J. Immunol., October 15, 2004; 173(8): 5008 - 5020.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Z. Liu and L. Lefrancois
Intestinal Epithelial Antigen Induces Mucosal CD8 T Cell Tolerance, Activation, and Inflammatory Response
J. Immunol., October 1, 2004; 173(7): 4324 - 4330.
[Abstract] [Full Text] [PDF]


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JEMHome page
A. L. Kinter, M. Hennessey, A. Bell, S. Kern, Y. Lin, M. Daucher, M. Planta, M. McGlaughlin, R. Jackson, S. F. Ziegler, et al.
CD25+CD4+ Regulatory T Cells from the Peripheral Blood of Asymptomatic HIV-infected Individuals Regulate CD4+ and CD8+ HIV-specific T Cell Immune Responses In Vitro and Are Associated with Favorable Clinical Markers of Disease Status
J. Exp. Med., August 2, 2004; 200(3): 331 - 343.
[Abstract] [Full Text] [PDF]


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Mult SclerHome page
P. W Denton, C. M Tello, and R. W Melvold
CD8 + T cells reduce in vitro interferon-g production in Theiler's murine encephalomyelitis virus-induced demyelinating disease model
Multiple Sclerosis, August 1, 2004; 10(4): 370 - 375.
[Abstract] [PDF]


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J. Immunol.Home page
E. A. Wohlfert, M. K. Callahan, and R. B. Clark
Resistance to CD4+CD25+ Regulatory T Cells and TGF-{beta} in Cbl-b-/- Mice
J. Immunol., July 15, 2004; 173(2): 1059 - 1065.
[Abstract] [Full Text] [PDF]


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J. Gen. Virol.Home page
P. M. Stuart, B. Summers, J. E. Morris, L. A. Morrison, and D. A. Leib
CD8+ T cells control corneal disease following ocular infection with herpes simplex virus type 1
J. Gen. Virol., July 1, 2004; 85(7): 2055 - 2063.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Stassen, H. Jonuleit, C. Muller, M. Klein, C. Richter, T. Bopp, S. Schmitt, and E. Schmitt
Differential Regulatory Capacity of CD25+ T Regulatory Cells and Preactivated CD25+ T Regulatory Cells on Development, Functional Activation, and Proliferation of Th2 Cells
J. Immunol., July 1, 2004; 173(1): 267 - 274.
[Abstract] [Full Text] [PDF]


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BloodHome page
S. Vigouroux, E. Yvon, E. Biagi, and M. K. Brenner
Antigen-induced regulatory T cells
Blood, July 1, 2004; 104(1): 26 - 33.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. Mamura, W. Lee, T. J. Sullivan, A. Felici, A. L. Sowers, J. P. Allison, and J. J. Letterio
CD28 disruption exacerbates inflammation in Tgf-{beta}1-/- mice: in vivo suppression by CD4+CD25+ regulatory T cells independent of autocrine TGF-{beta}1
Blood, June 15, 2004; 103(12): 4594 - 4601.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
T. L. Sumpter and D. S. Wilkes
Role of autoimmunity in organ allograft rejection: a focus on immunity to type V collagen in the pathogenesis of lung transplant rejection
Am J Physiol Lung Cell Mol Physiol, June 1, 2004; 286(6): L1129 - L1139.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. A. Lyman, S. Aung, J. A. Biggs, and L. A. Sherman
A Spontaneously Arising Pancreatic Tumor Does Not Promote the Differentiation of Naive CD8+ T Lymphocytes into Effector CTL
J. Immunol., June 1, 2004; 172(11): 6558 - 6567.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
B. K. Choi, J. S. Bae, E. M. Choi, W. J. Kang, S. Sakaguchi, D. S. Vinay, and B. S. Kwon
4-1BB-dependent inhibition of immunosuppression by activated CD4+CD25+ T cells
J. Leukoc. Biol., May 1, 2004; 75(5): 785 - 791.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. Suvas, A. K. Azkur, B. S. Kim, U. Kumaraguru, and B. T. Rouse
CD4+CD25+ Regulatory T Cells Control the Severity of Viral Immunoinflammatory Lesions
J. Immunol., April 1, 2004; 172(7): 4123 - 4132.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
S. M. Blois, C. D. Alba Soto, M. Tometten, B. F. Klapp, R. A. Margni, and P. C. Arck
Lineage, Maturity, and Phenotype of Uterine Murine Dendritic Cells Throughout Gestation Indicate a Protective Role in Maintaining Pregnancy
Biol Reprod, April 1, 2004; 70(4): 1018 - 1023.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Z. Jaffar, T. Sivakuru, and K. Roberts
CD4+CD25+ T Cells Regulate Airway Eosinophilic Inflammation by Modulating the Th2 Cell Phenotype
J. Immunol., March 15, 2004; 172(6): 3842 - 3849.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Hesse, C. A. Piccirillo, Y. Belkaid, J. Prufer, M. Mentink-Kane, M. Leusink, A. W. Cheever, E. M. Shevach, and T. A. Wynn
The Pathogenesis of Schistosomiasis Is Controlled by Cooperating IL-10-Producing Innate Effector and Regulatory T Cells
J. Immunol., March 1, 2004; 172(5): 3157 - 3166.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. G. Zheng, J. H. Wang, M. N. Koss, F. Quismorio Jr., J. D. Gray, and D. A. Horwitz
CD4+ and CD8+ Regulatory T Cells Generated Ex Vivo with IL-2 and TGF-{beta} Suppress a Stimulatory Graft-versus-Host Disease with a Lupus-Like Syndrome
J. Immunol., February 1, 2004; 172(3): 1531 - 1539.
[Abstract] [Full Text] [PDF]




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