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The Journal of Immunology, 2001, 167: 1245-1253.
Copyright © 2001 by The American Association of Immunologists

CD4+CD25high Regulatory Cells in Human Peripheral Blood1

Clare Baecher-Allan2,*, Julia A. Brown{dagger}, Gordon J. Freeman{dagger} and David A. Hafler*

* Laboratory of Molecular Immunology, Center for Neurologic Diseases, Brigham and Women’s Hospital, and {dagger} Department of Adult Oncology, Dana Farber Cancer Institute and Harvard Medical School, Boston, MA 02115

Thymectomy in mice on neonatal day 3 leads to the development of multiorgan autoimmune disease due to loss of a CD+CD25+ T cell regulatory population in their peripheral lymphoid tissues. Here, we report the identification of a CD4+ population of regulatory T cells in the circulation of humans expressing high levels of CD25 that exhibit in vitro characteristics identical with those of the CD4+CD25+ regulatory cells isolated in mice. With TCR cross-linking, CD4+CD25high cells did not proliferate but instead totally inhibited proliferation and cytokine secretion by activated CD4+CD25- responder T cells in a contact-dependent manner. The CD4+CD25high regulatory T cells expressed high levels of CD45RO but not CD45RA, akin to the expression of CD45RBlow on murine CD4+CD25+ regulatory cells. Increasing the strength of signal by providing either costimulation with CD28 cross-linking or the addition of IL-2 to a maximal anti-CD3 stimulus resulted in a modest induction of proliferation and the loss of observable suppression in cocultures of CD4+CD25high regulatory cells and CD4+CD25- responder cells. Whereas higher ratios of CD4+CD25high T cells are required to suppress proliferation if the PD-L1 receptor is blocked, regulatory cell function is shown to persist in the absence of the PD-1/PD-L1 or CTLA-4/B7 pathway. Thus, regulatory CD4 T cells expressing high levels of the IL-2 receptor are present in humans, providing the opportunity to determine whether alterations of these populations of T cells are involved in the induction of human autoimmune disorders.




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J. Virol.Home page
L. E. Pereira, F. Villinger, N. Onlamoon, P. Bryan, A. Cardona, K. Pattanapanysat, K. Mori, S. Hagen, L. Picker, and A. A. Ansari
Simian Immunodeficiency Virus (SIV) Infection Influences the Level and Function of Regulatory T Cells in SIV-Infected Rhesus Macaques but Not SIV-Infected Sooty Mangabeys
J. Virol., May 1, 2007; 81(9): 4445 - 4456.
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Am. J. Physiol. Heart Circ. Physiol.Home page
C. Schmidt-Lucke, A. Aicher, P. Romagnani, B. Gareis, S. Romagnani, A. M. Zeiher, and S. Dimmeler
Specific recruitment of CD4+CD25++ regulatory T cells into the allograft in heart transplant recipients
Am J Physiol Heart Circ Physiol, May 1, 2007; 292(5): H2425 - H2431.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
S. P. Hilchey, A. De, L. M. Rimsza, R. B. Bankert, and S. H. Bernstein
Follicular Lymphoma Intratumoral CD4+CD25+GITR+ Regulatory T Cells Potently Suppress CD3/CD28-Costimulated Autologous and Allogeneic CD8+CD25- and CD4+CD25- T Cells
J. Immunol., April 1, 2007; 178(7): 4051 - 4061.
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J. Immunol.Home page
J. Bayry, F. Triebel, S. V. Kaveri, and D. F. Tough
Human Dendritic Cells Acquire a Semimature Phenotype and Lymph Node Homing Potential through Interaction with CD4+CD25+ Regulatory T Cells
J. Immunol., April 1, 2007; 178(7): 4184 - 4193.
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Arterioscler. Thromb. Vasc. Bio.Home page
A. Mor, D. Planer, G. Luboshits, A. Afek, S. Metzger, T. Chajek-Shaul, G. Keren, and J. George
Role of Naturally Occurring CD4+CD25+ Regulatory T Cells in Experimental Atherosclerosis
Arterioscler Thromb Vasc Biol, April 1, 2007; 27(4): 893 - 900.
[Abstract] [Full Text] [PDF]


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Clin. Cancer Res.Home page
S. A. Siddiqui, X. Frigola, S. Bonne-Annee, M. Mercader, S. M. Kuntz, A. E. Krambeck, S. Sengupta, H. Dong, J. C. Cheville, C. M. Lohse, et al.
Tumor-Infiltrating Foxp3-CD4+CD25+ T Cells Predict Poor Survival in Renal Cell Carcinoma
Clin. Cancer Res., April 1, 2007; 13(7): 2075 - 2081.
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J. Am. Soc. Nephrol.Home page
M. Noris, F. Casiraghi, M. Todeschini, P. Cravedi, D. Cugini, G. Monteferrante, S. Aiello, L. Cassis, E. Gotti, F. Gaspari, et al.
Regulatory T Cells and T Cell Depletion: Role of Immunosuppressive Drugs
J. Am. Soc. Nephrol., March 1, 2007; 18(3): 1007 - 1018.
[Abstract] [Full Text] [PDF]


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BloodHome page
M. I. Garin, C.-C. Chu, D. Golshayan, E. Cernuda-Morollon, R. Wait, and R. I. Lechler
Galectin-1: a key effector of regulation mediated by CD4+CD25+ T cells
Blood, March 1, 2007; 109(5): 2058 - 2065.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
A. Kinter, J. McNally, L. Riggin, R. Jackson, G. Roby, and A. S. Fauci
Suppression of HIV-specific T cell activity by lymph node CD25+ regulatory T cells from HIV-infected individuals
PNAS, February 27, 2007; 104(9): 3390 - 3395.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
X. Valencia, C. Yarboro, G. Illei, and P. E. Lipsky
Deficient CD4+CD25high T Regulatory Cell Function in Patients with Active Systemic Lupus Erythematosus
J. Immunol., February 15, 2007; 178(4): 2579 - 2588.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
E. Kekalainen, H. Tuovinen, J. Joensuu, M. Gylling, R. Franssila, N. Pontynen, K. Talvensaari, J. Perheentupa, A. Miettinen, and T. P. Arstila
A Defect of Regulatory T Cells in Patients with Autoimmune Polyendocrinopathy-Candidiasis-Ectodermal Dystrophy
J. Immunol., January 15, 2007; 178(2): 1208 - 1215.
[Abstract] [Full Text] [PDF]


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Br J OphthalmolHome page
H Keino, M Takeuchi, Y Usui, T Hattori, N Yamakawa, T Kezuka, J-I Sakai, and M Usui
Supplementation of CD4+CD25+ regulatory T cells suppresses experimental autoimmune uveoretinitis
Br J Ophthalmol, January 1, 2007; 91(1): 105 - 110.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
M. Battaglia, A. Stabilini, B. Migliavacca, J. Horejs-Hoeck, T. Kaupper, and M.-G. Roncarolo
Rapamycin Promotes Expansion of Functional CD4+CD25+FOXP3+ Regulatory T Cells of Both Healthy Subjects and Type 1 Diabetic Patients
J. Immunol., December 15, 2006; 177(12): 8338 - 8347.
[Abstract] [Full Text] [PDF]


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BloodHome page
P. Hoffmann, R. Eder, T. J. Boeld, K. Doser, B. Piseshka, R. Andreesen, and M. Edinger
Only the CD45RA+ subpopulation of CD4+CD25high T cells gives rise to homogeneous regulatory T-cell lines upon in vitro expansion
Blood, December 15, 2006; 108(13): 4260 - 4267.
[Abstract] [Full Text] [PDF]


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BloodHome page
H. Tuovinen, J. T. Salminen, and T. P. Arstila
Most human thymic and peripheral-blood CD4+CD25+ regulatory T cells express 2 T-cell receptors
Blood, December 15, 2006; 108(13): 4063 - 4070.
[Abstract] [Full Text] [PDF]


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JCOHome page
J. Yang
In Reply
J. Clin. Oncol., December 1, 2006; 24(34): 5470 - 5471.
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J. Immunol.Home page
L. Zhu, F. Ji, Y. Wang, Y. Zhang, Q. Liu, J. Z. Zhang, K. Matsushima, Q. Cao, and Y. Zhang
Synovial Autoreactive T Cells in Rheumatoid Arthritis Resist IDO-Mediated Inhibition
J. Immunol., December 1, 2006; 177(11): 8226 - 8233.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. M. Miller, K. Lundberg, V. Ozenci, A. H. Banham, M. Hellstrom, L. Egevad, and P. Pisa
CD4+CD25high T Cells Are Enriched in the Tumor and Peripheral Blood of Prostate Cancer Patients
J. Immunol., November 15, 2006; 177(10): 7398 - 7405.
[Abstract] [Full Text] [PDF]


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Eur Heart JHome page
A. Mor, G. Luboshits, D. Planer, G. Keren, and J. George
Altered status of CD4+CD25+ regulatory T cells in patients with acute coronary syndromes
Eur. Heart J., November 1, 2006; 27(21): 2530 - 2537.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. A. Cavassani, A. P. Campanelli, A. P. Moreira, J. O. Vancim, L. H. Vitali, R. C. Mamede, R. Martinez, and J. S. Silva
Systemic and Local Characterization of Regulatory T Cells in a Chronic Fungal Infection in Humans
J. Immunol., November 1, 2006; 177(9): 5811 - 5818.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
Z.-W. Xia, W.-W. Zhong, L.-Q. Xu, J.-L. Sun, Q.-X. Shen, J.-G. Wang, J. Shao, Y.-Z. Li, and S.-C. Yu
Heme Oxygenase-1-Mediated CD4+CD25high Regulatory T Cells Suppress Allergic Airway Inflammation
J. Immunol., November 1, 2006; 177(9): 5936 - 5945.
[Abstract] [Full Text] [PDF]


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Ann Rheum DisHome page
A Suarez, P Lopez, J Gomez, and C Gutierrez
Enrichment of CD4+ CD25high T cell population in patients with systemic lupus erythematosus treated with glucocorticoids
Ann Rheum Dis, November 1, 2006; 65(11): 1512 - 1517.
[Abstract] [Full Text] [PDF]


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PediatricsHome page
A. Bernasconi, R. Marino, A. Ribas, J. Rossi, M. Ciaccio, M. Oleastro, A. Ornani, R. Paz, M. A. Rivarola, M. Zelazko, et al.
Characterization of Immunodeficiency in a Patient With Growth Hormone Insensitivity Secondary to a Novel STAT5b Gene Mutation
Pediatrics, November 1, 2006; 118(5): e1584 - e1592.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Hirahara, L. Liu, R. A. Clark, K.-i. Yamanaka, R. C. Fuhlbrigge, and T. S. Kupper
The Majority of Human Peripheral Blood CD4+CD25highFoxp3+ Regulatory T Cells Bear Functional Skin-Homing Receptors
J. Immunol., October 1, 2006; 177(7): 4488 - 4494.
[Abstract] [Full Text] [PDF]


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J. Am. Soc. Nephrol.Home page
M. Lopez, M. R. Clarkson, M. Albin, M. H. Sayegh, and N. Najafian
A Novel Mechanism of Action for Anti-Thymocyte Globulin: Induction of CD4+CD25+Foxp3+ Regulatory T Cells
J. Am. Soc. Nephrol., October 1, 2006; 17(10): 2844 - 2853.
[Abstract] [Full Text] [PDF]


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Rheumatology (Oxford)Home page
C. A. Lawson, A. K. Brown, V. Bejarano, S. H. Douglas, C. H. Burgoyne, A. S. Greenstein, A. W. Boylston, P. Emery, F. Ponchel, and J. D. Isaacs
Early rheumatoid arthritis is associated with a deficit in the CD4+CD25high regulatory T cell population in peripheral blood
Rheumatology, October 1, 2006; 45(10): 1210 - 1217.
[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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