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CUTTING EDGE |
Laboratory of Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
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Abstract |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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, and IL-2R
deficient (–/–) mice all die early in life of severe lymphoproliferation and autoimmune disease (2, 3, 4) and IL-2 and IL-2R–/– mice have few or no CD4+CD25+ cells. Furthermore, while STAT5-deficient mice have very few CD4+CD25+ cells, mice transgenic for the active form of STAT5 possess a greater frequency of these cells (5, 6), thus confirming the requirement for IL-2 signaling in CD4+CD25+ T cell homeostasis. Recent studies suggest that the IL-2/IL-2R pathway is important for CD4+CD25+ T cells at several stages. CD4+CD25+ cell numbers are restored and the induction of autoimmune disease is prevented when an IL-2R transgene is expressed solely in the thymus of IL-2R–/– mice, indicating that an intact IL-2/IL-2R pathway is required in the thymus for generation of CD4+CD25+ cells (7). IL-2 signaling in the periphery is also required for the expansion of CD4+CD25+ cells. Although the transfer of wild-type CD4+CD25+ cells to IL-2R–/– mice resulted in a marked expansion of the transferred cells and prevented the induction of disease, the transfer of wild-type CD4+CD25+ cells into IL-2–/– mice did not lead to engraftment or expansion of CD4+CD25+ cells and did not prevent autoimmune disease or death, suggesting that IL-2 is needed for the expansion and/or homeostasis of CD4+CD25+ cells. Similarly, Furtado et al. (8) demonstrated that CD4+ T cells from IL-2–/– mice protected mice from spontaneous experimental autoimmune encephalomyelitis, while CD4+ T cells from CD25–/– mice did not; thus, IL-2 derived from the recipient drove expansion of IL-2–/– cells, but was unable to drive the expansion of CD4+CD25–/– cells. Other factors may also control the homeostasis of CD4+CD25+ T cells, as mice with defects in delivery or receipt of costimulation (CD28–/–, CD80/CD86–/–, CD40–/–), may have quantitative or qualitative defects in CD4+CD25+-mediated functions (9, 10). Some of these defects appear to be independent of IL-2 (11). Although IL-2 and its receptor clearly play a critical role in the homeostasis of CD4+CD25+ T cells in vivo, the potential contribution of IL-2 to their suppressive function remains elusive. Indeed, the molecular basis for suppression of T cell activation by CD4+CD25+ T cells in vitro is inhibition of IL-2 gene transcription in the CD4+CD25– responder T cells. Furthermore, addition of IL-2 or the enhancement of costimulation by the addition of anti-CD28 are thought to break the anergic state of the CD4+CD25+ T cells and abrogate their suppressive function. One of the major problems with interpretation of this data is that T cell proliferation has been used as the major readout of suppression and both CD4+CD25+ and CD4+CD25– cells proliferate under these conditions. In this study, we have used a quantitative assay of suppression of IL-2 transcription to re-evaluate the role of IL-2 in the suppressor function of CD4+CD25+ T cells. We demonstrate that transcription of IL-2 mRNA remains fully suppressed in the presence of high concentrations of exogenous IL-2 and in the presence of proliferation of both the CD4+CD25+ suppressors and the CD4+CD25– responders. In contrast, the addition of anti-CD28 to the suppression assay results in abrogation of suppression as transcription of IL-2 mRNA is partially restored. Thus, abrogation of the anergic state of CD4+CD25+ cells does not break suppression, as previously thought. Most importantly, the addition of anti-IL-2 completely abrogates the suppressive effects of CD4+CD25+ T cells on IL-2 mRNA transcription and demonstrates that IL-2 is not only required for the generation and peripheral maintenance of CD4+CD25+ cells, but is also required for the acquisition of suppressor function. The implications of these findings for the in vivo effects of CD4+CD25+ T cells are discussed.
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Materials and Methods |
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Female BALB/c mice were obtained from the National Cancer Institute (Frederick, MD). BALB/c Thy1.1 congenic mice were obtained from R. A. Seder (National Institutes of Health, Bethesda, MD) and were bred and maintained in National Institute of Allergy and Infectious Diseases/National Institutes of Health animal facilities.
Media, reagents, and Abs
Cells were grown in RPMI 1640 (Biofluids, Rockville, MD) supplemented with 10% heat-inactivated FCS, penicillin (100 µg/ml), streptomycin (100 µg/ml), 2 mM L-glutamine, 10 mM HEPES, 0.1 mM nonessential amino acids, 1 mM sodium pyruvate (all Biofluids), and 50 µM 2-ME (Sigma-Aldrich, St. Louis, MO). Biotin-anti-CD25 (7D4), PE-streptavidin, anti-CD3 (2C11), anti-CD28, and anti-IL-2 (S4B6) were purchased from BD PharMingen (San Diego, CA). Anti-CD90 (Thy1.2), anti-CD8, and anti-PE magnetic beads were purchased from Miltenyi Biotec (Auburn, CA). Human rIL-2 was obtained from the Preclinical Repository of the Biological Resources Branch, National Cancer Institute. IL-4 was purchased from R&D Systems (Minneapolis, MN). Flow cytometry analysis to assess cell purity was performed using CellQuest software (BD PharMingen).
Cell purification
CD4+CD25– and CD4+CD25+ cells were purified as previously reported (12), unless stated otherwise. Purity ranged from 95 to 98%. T-depleted spleen cells (T
S) were used as APC and were prepared by lysing erythrocytes with ACK lysis buffer (Biofluids), followed by depletion of CD90+ cells on an autoMACS (Miltenyi Biotec). APC were irradiated with 3000R.
Proliferation assays
CD4+CD25– cells (5 x 104), CD4+CD25+ cells (5 x 104), or CD4+CD25– cells (5 x 104) cocultured with CD4+CD25+ cells (2.5 x 104) were cultured in 96-well plates (0.2 ml) with APC (5 x 104) and 0.25 µg/ml anti-CD3 for 72 h at 37°C/7% CO2 in the presence of any indicated reagents. IL-2 was used at 50 U/ml, IL-4 at 20 ng/ml, and anti-CD28 at 0.5 µg/ml. Cultures were pulsed with [3H]TdR for the last 6 h of culture. All experiments were set up in triplicate.
CFSE labeling
Thy 1.1 CD4+CD25– or Thy 1.2 CD4+CD25+ cells were labeled with 2 µM CFSE for 8 min at room temperature. Cells were set up as in standard 96-well proliferation assays in triplicate. At 70 h, the triplicates were pooled and analyzed by flow cytometry.
Quantitative IL-2 mRNA analysis
CD4+CD25– cells, CD4+CD25+ cells, or CD4+CD25– cells cocultured with CD4+CD25+ cells were cultured with APC and 0.25 µg/ml anti-CD3 in the presence of indicated reagents for 44 h. Reactions were set up in 96-well plates as for the proliferation assays and the contents of one plate (
5 x 106 cells) pooled at 44 h. Total RNA was prepared with an RNeasy kit (Qiagen, Valencia, CA) during which on-column DNase I treatment (Qiagen) was performed. cDNA was made using Superscript II (Invitrogen, Carlsbad, CA) with random primers (Invitrogen). Primers and FAM-labeled probe for IL-2 and IL-4 were purchased from Applied Biosystems (Foster City, CA). As an internal control for normalization, 18S ribosomal RNA (rRNA) (Applied Biosystems) was used. Standard curves were set up for IL-2 and 18S rRNA. For each sample, the results of IL-2 gene expression were normalized relative to its 18s rRNA. The IL-2 gene expression of normalized unstimulated CD4+CD25– cells was given an arbitrary value of 1.0 and the remaining samples were plotted relative to that value. All PCRs were performed in triplicate with a TaqMan Universal PCR Master Mix (Applied Biosystems). An ABI Prism 7700 Sequence Detection System (Applied Biosystems) was used for 40 cycles of PCR. Each experiment was performed at least three times and a representative experiment is shown.
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Results |
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As previously shown, coculture of CD4+CD25+ and CD4+CD25– T cells results in inhibition of the proliferative response of CD4+CD25– cells, which is reversed to varying extents by the addition of IL-2, IL-4, or anti-CD28 (Fig. 1A) (13, 14, 15). As purified CD4+CD25+ T cells proliferate when stimulated with anti-CD3 and IL-2 (13, 14), it has been assumed that when the in vitro nonresponsive state of the CD4+CD25+ cells is broken, their suppressive function is abolished. However, it is possible that CD4+CD25+ cells retain their suppressive function, and proliferation of both the CD4+CD25+ and CD4+CD25– populations is driven by the addition of the exogenous agents. To address this possibility, we used CFSE dilution experiments to independently examine the proliferation of CD4+CD25– and CD4+CD25+ cells under coculture conditions. As shown in Fig. 1B, CD4+CD25– cells manifested a significant proliferative response which was enhanced by the addition of IL-2, IL-4, and anti-CD28. CD4+CD25+ cells cultured with anti-CD3 alone or with anti-CD3/CD28 did not divide significantly, but as was observed in the [3H]TdR uptake assays, proliferated vigorously when stimulated with anti-CD3 and IL-2 or IL-4. In the cocultures, CD4+CD25+ cells markedly inhibited division of CD4+CD25– cells. However, both the CD4+CD25– and CD4+CD25+ populations divided when IL-2, IL-4, or anti-CD28 were added to the cocultures. Although the division of CD4+CD25– cells led to distinct peaks of CFSE dilution, the division of CD4+CD25+ cells consistently showed a more diffuse pattern of CFSE dilution.
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Although both CD4+CD25– and CD4+CD25+ cells proliferated in the presence of exogenous IL-2, IL-4, and anti-CD28, the possibility remained that the CD4+CD25+ cells remained functional with respect to their ability to inhibit IL-2 mRNA. When measured by quantitative PCR (qPCR), 3 maximum levels of IL-2 mRNA were observed under these limiting culture conditions after 44 h of stimulation (data not shown). Fig. 2 is divided into two parts with the results of the [3H]TdR uptake assay on the left side and the corresponding qPCR analysis of the same cell populations on the right. In agreement with our previous Northern analysis (14), the transcription of IL-2 mRNA in CD4+CD25– cells was inhibited in the presence of CD4+CD25+ cells (Fig. 2A). When IL-2 (Fig. 2A) or IL-4 (Fig. 2B) were added to the cultures, the levels of IL-2 mRNA were not significantly different in CD4+CD25– cells stimulated in the absence of CD4+CD25+ cells and were never induced in CD4+CD25+ cells alone. However, IL-2 mRNA (Fig. 2A) and IL-4 mRNA (data not shown) were still inhibited. Thus, the proliferative response detected by [3H]TdR uptake and CFSE dilution was solely driven by the exogenous cytokines as CD4+CD25+ cells were functional and suppressed IL-2 mRNA. In these experiments, CD4+CD25– cells were not purified after coculture with CD4+CD25+ cells and it was possible that the decrease in IL-2 mRNA was a result of dilution from the additional cells. However, CD4+CD25+ cells comprise 33% of the sample while IL-2 mRNA inhibition was always greater than 80%. Furthermore, in preliminary experiments not depicted, greater than 75% inhibition of IL-2 mRNA was observed when CD4+CD25+ cells comprised only 20% of the coculture.
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60% of CD4+CD25– cells alone as well (data not shown). Thus, the addition of anti-CD28 partially abrogates the suppressive effect of the CD4+CD25+ T cells on IL-2 mRNA transcription in the CD4+CD25– responders. CD4+CD25+ cells require IL-2 to inhibit IL-2 transcription in CD4+CD25– cells
As recent in vivo experiments have strongly suggested that IL-2 is required for the generation and function of CD4+CD25+ T cells (17), we examined IL-2 mRNA in our coculture system in the presence of anti-IL-2 to determine whether IL-2 was also required for the activation of suppressor function. Although the addition of anti-IL-2 completely blocked the proliferation of CD4+CD25– cells alone (Fig. 3A), the addition of anti-IL-2 did not block the transcription of IL-2 mRNA (Fig. 3B), allowing us to examine the effect of anti-IL-2 on CD4+CD25+ function. The addition of anti-IL-2 to the coculture restored IL-2 mRNA (Fig. 3B). Thus, a certain level of IL-2 production by CD4+CD25– cells appears to be required to induce CD4+CD25+-mediated inhibition of IL-2 mRNA production. As IL-4 in the presence of a TCR signal can stimulate proliferation of CD4+CD25+ cells and induce CD4+CD25+ suppressor function (15), we also examined whether IL-4 could substitute for IL-2 in the induction of CD4+CD25+-mediated suppression. In the presence of IL-4 alone, the results were similar to those shown in Fig. 2B (data not shown). However, when IL-4 was added to the cocultures in the presence of anti-IL-2, IL-2 mRNA was not restored, indicating that IL-4 can substitute for IL-2 in vitro in inducing CD4+CD25+ suppressor function.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionReferences |
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A clear role for IL-2 in the generation, maintenance, and expansion of CD4+CD25+ cells in vivo has been convincingly established (17). The only exception to this is the observation that CD4+CD25+ T cells from mice that express the IL-2R chain only in the thymus, and cannot respond to IL-2 in the periphery, exist in normal numbers and are capable of suppressing the development of the autoimmune syndrome that normally develops in IL-2R chain-deficient mice. However, it remains possible that the output of these cells from the thymus is abnormally high secondary to the transgenic expression of the IL-2R chain and that they retain their capacity to suppress for a certain period of time after receiving the IL-2 signal in the thymus. Their failure to survive and suppress autoimmunity upon transfer to IL-2–/– mice is consistent with this scenario.
We have demonstrated here, for the first time, that IL-2 is also required for the activation of suppressor function of CD4+CD25+ T cells in vitro and that IL-4 can substitute for IL-2 in this process. An alternative explanation for this result is that IL-2/IL-4 function only as critical survival factors for CD4+CD25+ T cells in vitro. We believe this explanation is unlikely as we have recently demonstrated (15) that activation of suppressor function during preculture of CD4+CD25+ cells before their coculture with CD4+CD25– cells also required the presence of IL-2, yet no difference in the recovery of cells at 1 or 2 days was observed in the presence or absence of IL-2. In the present study, IL-2 mRNA was measured at 40 h of culture, when the effects of IL-2 on cell recovery were minimal.
It might be regarded as paradoxical that the action of one or the other of the two major T cell growth factors is required for subsequent suppression of their own production. However, the initial activation of effector CD4+CD25– T cells with resultant production of IL-2/IL-4 may be needed for regulation of the function of CD4+CD25+ T cells for two distinct purposes. First, it may facilitate the nonspecific expansion of the CD4+CD25+ T cells in situ at the site of the response. Although CD4+CD25+ T cells are nonresponsive to IL-2/IL-4 alone, they express high levels of the glucocorticoid-induced TNFR (GITR) and engagement of the GITR by an agonistic mAb (19) or its ligand 3 in the presence of IL-2 or IL-4 results in their proliferation in vitro. Recently, it has been shown that the GITR-L is expressed at high levels on resting APC, particularly B lymphocytes (20, 21). Second, the requirement for initial activation of effector cells before induction of suppressor function imposes a time constraint on when suppression can become manifest. Indeed, it would be highly desirable in the immune response to infectious agents that a certain level of effector function be established before induction of suppressor function which subsequently would lead to a down-modulation of effector function and the prevention of an overexuberant immune response (22).
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Footnotes |
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2 Current address: Department of Microbiology and Immunology, McGill University, Montreal, Quebec, Canada, H3A2B4.
3 Abbreviations used in this paper: qPCR, quantitative PCR; GITR, glucocorticoid-induced TNFR.
4 G. L. Stephens, R. S. McHugh, M. J. Whitters, D. A. Young, M. Collins, and E. M. Shevach. Engagement of GITR on effector T cells by its ligand mediates resistance to suppression by CD4+CD25+ T cells. Submitted for publication.
Received for publication February 9, 2004. Accepted for publication March 29, 2004.
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References |
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. Science 268:1472. chain regulates the size and content of the peripheral lymphoid compartment. Immunity 3:521.[Medline]
-deficient mice: implications for the nonredundant function of IL-2. Immunity 17:167.[Medline]
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 T. Bopp, C. Becker, M. Klein, S. Klein-Hessling, A. Palmetshofer, E. Serfling, V. Heib, M. Becker, J. Kubach, S. Schmitt, et al. Cyclic adenosine monophosphate is a key component of regulatory T cell mediated suppression J. Exp. Med., June 11, 2007; 204(6): 1303 - 1310. [Abstract] [Full Text] [PDF]
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K. G. Chan, M. Mayer, E. M. Davis, S. A. Halperin, T.-J. Lin, and S. F. Lee Role of D-Alanylation of Streptococcus gordonii Lipoteichoic Acid in Innate and Adaptive Immunity Infect. Immun., June 1, 2007; 75(6): 3033 - 3042. [Abstract] [Full Text] [PDF]
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J. Yates, F. Rovis, P. Mitchell, B. Afzali, J.-S Tsang, M. Garin, R. Lechler, G. Lombardi, and O. Garden The maintenance of human CD4+CD25+ regulatory T cell function: IL-2, IL-4, IL-7 and IL-15 preserve optimal suppressive potency in vitro Int. Immunol., June 1, 2007; 19(6): 785 - 799. [Abstract] [Full Text] [PDF]
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L. Xu, A. Kitani, I. Fuss, and W. Strober Cutting Edge: Regulatory T Cells Induce CD4+CD25-Foxp3- T Cells or Are Self-Induced to Become Th17 Cells in the Absence of Exogenous TGF-beta J. Immunol., June 1, 2007; 178(11): 6725 - 6729. [Abstract] [Full Text] [PDF]
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I. Kryczek, S. Wei, L. Zou, S. Altuwaijri, W. Szeliga, J. Kolls, A. Chang, and W. Zou Cutting Edge: Th17 and Regulatory T Cell Dynamics and the Regulation by IL-2 in the Tumor Microenvironment J. Immunol., June 1, 2007; 178(11): 6730 - 6733. [Abstract] [Full Text] [PDF]
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J. Andersson, I. Stefanova, G. L. Stephens, and E. M. Shevach CD4+CD25+ regulatory T cells are activated in vivo by recognition of self Int. Immunol., April 1, 2007; 19(4): 557 - 566. [Abstract] [Full Text] [PDF]
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T. S. Davidson, R. J. DiPaolo, J. Andersson, and E. M. Shevach Cutting Edge: IL-2 Is Essential for TGF-beta-Mediated Induction of Foxp3+ T Regulatory Cells J. Immunol., April 1, 2007; 178(7): 4022 - 4026. [Abstract] [Full Text] [PDF]
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A. L. Bayer, A. Yu, and T. R. Malek Function of the IL-2R for Thymic and Peripheral CD4+CD25+ Foxp3+ T Regulatory Cells J. Immunol., April 1, 2007; 178(7): 4062 - 4071. [Abstract] [Full Text] [PDF]
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J. Dai, B. Liu, S. M. Ngoi, S. Sun, A. T. Vella, and Z. Li TLR4 Hyperresponsiveness via Cell Surface Expression of Heat Shock Protein gp96 Potentiates Suppressive Function of Regulatory T Cells J. Immunol., March 1, 2007; 178(5): 3219 - 3225. [Abstract] [Full Text] [PDF]
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F. Marangoni, S. Trifari, S. Scaramuzza, C. Panaroni, S. Martino, L. D. Notarangelo, Z. Baz, A. Metin, F. Cattaneo, A. Villa, et al. WASP regulates suppressor activity of human and murine CD4+CD25+FOXP3+ natural regulatory T cells J. Exp. Med., February 19, 2007; 204(2): 369 - 380. [Abstract] [Full Text] [PDF]
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M. H. Maillard, V. Cotta-de-Almeida, F. Takeshima, D. D. Nguyen, P. Michetti, C. Nagler, A. K. Bhan, and S. B. Snapper The Wiskott-Aldrich syndrome protein is required for the function of CD4+CD25+Foxp3+ regulatory T cells J. Exp. Med., February 19, 2007; 204(2): 381 - 391. [Abstract] [Full Text] [PDF]
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S. G. Zheng, J. Wang, P. Wang, J. D. Gray, and D. A. Horwitz IL-2 Is Essential for TGF-beta to Convert Naive CD4+CD25- Cells to CD25+Foxp3+ Regulatory T Cells and for Expansion of These Cells J. Immunol., February 15, 2007; 178(4): 2018 - 2027. [Abstract] [Full Text] [PDF]
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J. Bodor, Z. Fehervari, B. Diamond, and S. Sakaguchi Regulatory T cell-mediated suppression: potential role of ICER J. Leukoc. Biol., January 1, 2007; 81(1): 161 - 167. [Abstract] [Full Text] [PDF]
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Y. Carrier, J. Yuan, V. K. Kuchroo, and H. L. Weiner Th3 Cells in Peripheral Tolerance. II. TGF-beta-Transgenic Th3 Cells Rescue IL-2-Deficient Mice from Autoimmunity J. Immunol., January 1, 2007; 178(1): 172 - 178. [Abstract] [Full Text] [PDF]
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M. A. Burchill, J. Yang, C. Vogtenhuber, B. R. Blazar, and M. A. Farrar IL-2 Receptor beta-Dependent STAT5 Activation Is Required for the Development of Foxp3+ Regulatory T Cells J. Immunol., January 1, 2007; 178(1): 280 - 290. [Abstract] [Full Text] [PDF]
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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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T. L. Sukiennicki and D. J. Fowell Distinct Molecular Program Imposed on CD4+ T Cell Targets by CD4+CD25+ Regulatory T Cells J. Immunol., November 15, 2006; 177(10): 6952 - 6961. [Abstract] [Full Text] [PDF]
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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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A. Yu and T. R. Malek Selective Availability of IL-2 Is a Major Determinant Controlling the Production of CD4+CD25+Foxp3+ T Regulatory Cells J. Immunol., October 15, 2006; 177(8): 5115 - 5121. [Abstract] [Full Text] [PDF]
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P. Grimbert, S. Bouguermouh, N. Baba, T. Nakajima, Z. Allakhverdi, D. Braun, H. Saito, M. Rubio, G. Delespesse, and M. Sarfati Thrombospondin/CD47 Interaction: A Pathway to Generate Regulatory T Cells from Human CD4+CD25- T Cells in Response to Inflammation J. Immunol., September 15, 2006; 177(6): 3534 - 3541. [Abstract] [Full Text] [PDF]
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A. Toda and C. A. Piccirillo Development and function of naturally occurring CD4+CD25+ regulatory T cells J. Leukoc. Biol., September 1, 2006; 80(3): 458 - 470. [Abstract] [Full Text] [PDF]
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E. Zorn, E. A. Nelson, M. Mohseni, F. Porcheray, H. Kim, D. Litsa, R. Bellucci, E. Raderschall, C. Canning, R. J. Soiffer, et al. IL-2 regulates FOXP3 expression in human CD4+CD25+ regulatory T cells through a STAT-dependent mechanism and induces the expansion of these cells in vivo Blood, September 1, 2006; 108(5): 1571 - 1579. [Abstract] [Full Text] [PDF]
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K. Rezvani, S. Mielke, M. Ahmadzadeh, Y. Kilical, B. N. Savani, J. Zeilah, K. Keyvanfar, A. Montero, N. Hensel, R. Kurlander, et al. High donor FOXP3-positive regulatory T-cell (Treg) content is associated with a low risk of GVHD following HLA-matched allogeneic SCT Blood, August 15, 2006; 108(4): 1291 - 1297. [Abstract] [Full Text] [PDF]
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S. Wei, I. Kryczek, and W. Zou Regulatory T-cell compartmentalization and trafficking Blood, July 15, 2006; 108(2): 426 - 431. [Abstract] [Full Text] [PDF]
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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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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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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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 H. Liu, M. Komai-Koma, D. Xu, and F. Y. Liew Toll-like receptor 2 signaling modulates the functions of CD4+CD25+ regulatory T cells PNAS, May 2, 2006; 103(18): 7048 - 7053. [Abstract] [Full Text] [PDF]
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R Duchmann and M Zeitz T regulatory cell suppression of colitis: the role of TGF-{beta} Gut, May 1, 2006; 55(5): 604 - 606. [Full Text] [PDF]
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P. A. Antony, C. M. Paulos, M. Ahmadzadeh, A. Akpinarli, D. C. Palmer, N. Sato, A. Kaiser, C. Heinrichs, C. A. Klebanoff, Y. Tagaya, et al. Interleukin-2-Dependent Mechanisms of Tolerance and Immunity In Vivo J. Immunol., May 1, 2006; 176(9): 5255 - 5266. [Abstract] [Full Text] [PDF]
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L. Pace, S. Rizzo, C. Palombi, F. Brombacher, and G. Doria Cutting Edge: IL-4-Induced Protection of CD4+CD25- Th Cells from CD4+CD25+ Regulatory T Cell-Mediated Suppression J. Immunol., April 1, 2006; 176(7): 3900 - 3904. [Abstract] [Full Text] [PDF]
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K. Ebata, Y. Shimizu, Y. Nakayama, M. Minemura, J. Murakami, T. Kato, S. Yasumura, T. Takahara, T. Sugiyama, and S. Saito Immature NK Cells Suppress Dendritic Cell Functions during the Development of Leukemia in a Mouse Model J. Immunol., April 1, 2006; 176(7): 4113 - 4124. [Abstract] [Full Text] [PDF]
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A. P. Kohm, J. S. McMahon, J. R. Podojil, W. S. Begolka, M. DeGutes, D. J. Kasprowicz, S. F. Ziegler, and S. D. Miller Cutting Edge: Anti-CD25 Monoclonal Antibody Injection Results in the Functional Inactivation, Not Depletion, of CD4+CD25+ T Regulatory Cells J. Immunol., March 15, 2006; 176(6): 3301 - 3305. [Abstract] [Full Text] [PDF]
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C. Lyddane, B. U. Gajewska, E. Santos, P. D. King, G. C. Furtado, and M. Sadelain Cutting Edge: CD28 Controls Dominant Regulatory T Cell Activity during Active Immunization J. Immunol., March 15, 2006; 176(6): 3306 - 3310. [Abstract] [Full Text] [PDF]
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M. Ahmadzadeh and S. A. Rosenberg IL-2 administration increases CD4+CD25hi Foxp3+ regulatory T cells in cancer patients Blood, March 15, 2006; 107(6): 2409 - 2414. [Abstract] [Full Text] [PDF]
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I. P. Lewkowich, N. S. Herman, K. W. Schleifer, M. P. Dance, B. L. Chen, K. M. Dienger, A. A. Sproles, J. S. Shah, J. Kohl, Y. Belkaid, et al. CD4+CD25+ T cells protect against experimentally induced asthma and alter pulmonary dendritic cell phenotype and function J. Exp. Med., December 5, 2005; 202(11): 1549 - 1561. [Abstract] [Full Text] [PDF]
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R. J. DiPaolo, D. D. Glass, K. E. Bijwaard, and E. M. Shevach CD4+CD25+ T Cells Prevent the Development of Organ-Specific Autoimmune Disease by Inhibiting the Differentiation of Autoreactive Effector T Cells J. Immunol., December 1, 2005; 175(11): 7135 - 7142. [Abstract] [Full Text] [PDF]
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D. K. Sojka, A. Hughson, T. L. Sukiennicki, and D. J. Fowell Early Kinetic Window of Target T Cell Susceptibility to CD25+ Regulatory T Cell Activity J. Immunol., December 1, 2005; 175(11): 7274 - 7280. [Abstract] [Full Text] [PDF]
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C. Brinster and E. M. Shevach Bone Marrow-Derived Dendritic Cells Reverse the Anergic State of CD4+CD25+ T Cells without Reversing Their Suppressive Function J. Immunol., December 1, 2005; 175(11): 7332 - 7340. [Abstract] [Full Text] [PDF]
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A. S. Krupnick, A. E. Gelman, W. Barchet, S. Richardson, F. H. Kreisel, L. A. Turka, M. Colonna, G. A. Patterson, and D. Kreisel Cutting Edge: Murine Vascular Endothelium Activates and Induces the Generation of Allogeneic CD4+25+Foxp3+ Regulatory T Cells J. Immunol., November 15, 2005; 175(10): 6265 - 6270. [Abstract] [Full Text] [PDF]
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L. Li, W. R. Godfrey, S. B. Porter, Y. Ge, C. H. June, B. R. Blazar, and V. A. Boussiotis CD4+CD25+ regulatory T-cell lines from human cord blood have functional and molecular properties of T-cell anergy Blood, November 1, 2005; 106(9): 3068 - 3073. [Abstract] [Full Text] [PDF]
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L.-X. Wang, S. Shu, and G. E. Plautz Host Lymphodepletion Augments T Cell Adoptive Immunotherapy through Enhanced Intratumoral Proliferation of Effector Cells Cancer Res., October 15, 2005; 65(20): 9547 - 9554. [Abstract] [Full Text] [PDF]
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N. Beyersdorf, S. Gaupp, K. Balbach, J. Schmidt, K. V. Toyka, C.-H. Lin, T. Hanke, T. Hunig, T. Kerkau, and R. Gold Selective targeting of regulatory T cells with CD28 superagonists allows effective therapy of experimental autoimmune encephalomyelitis J. Exp. Med., August 1, 2005; 202(3): 445 - 455. [Abstract] [Full Text] [PDF]
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I. L. King and B. M. Segal Cutting Edge: IL-12 Induces CD4+CD25- T Cell Activation in the Presence of T Regulatory Cells J. Immunol., July 15, 2005; 175(2): 641 - 645. [Abstract] [Full Text] [PDF]
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B. Bienvenu, B. Martin, C. Auffray, C. Cordier, C. Becourt, and B. Lucas Peripheral CD8+CD25+ T Lymphocytes from MHC Class II-Deficient Mice Exhibit Regulatory Activity J. Immunol., July 1, 2005; 175(1): 246 - 253. [Abstract] [Full Text] [PDF]
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M. M. Freeman and H. K. Ziegler Simultaneous Th1-Type Cytokine Expression Is a Signature of Peritoneal CD4+ Lymphocytes Responding to Infection with Listeria monocytogenes J. Immunol., July 1, 2005; 175(1): 394 - 403. [Abstract] [Full Text] [PDF]
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C. R. Ruprecht, M. Gattorno, F. Ferlito, A. Gregorio, A. Martini, A. Lanzavecchia, and F. Sallusto Coexpression of CD25 and CD27 identifies FoxP3+ regulatory T cells in inflamed synovia J. Exp. Med., June 6, 2005; 201(11): 1793 - 1803. [Abstract] [Full Text] [PDF]
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M. T. Abreu, M. Fukata, and M. Arditi TLR Signaling in the Gut in Health and Disease J. Immunol., April 15, 2005; 174(8): 4453 - 4460. [Abstract] [Full Text] [PDF]
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M. D. Taylor, L. LeGoff, A. Harris, E. Malone, J. E. Allen, and R. M. Maizels Removal of Regulatory T Cell Activity Reverses Hyporesponsiveness and Leads to Filarial Parasite Clearance In Vivo J. Immunol., April 15, 2005; 174(8): 4924 - 4933. [Abstract] [Full Text] [PDF]
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B. Valzasina, C. Guiducci, H. Dislich, N. Killeen, A. D. Weinberg, and M. P. Colombo Triggering of OX40 (CD134) on CD4+CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR Blood, April 1, 2005; 105(7): 2845 - 2851. [Abstract] [Full Text] [PDF]
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A. Bushell, E. Jones, A. Gallimore, and K. Wood The Generation of CD25+CD4+ Regulatory T Cells That Prevent Allograft Rejection Does Not Compromise Immunity to a Viral Pathogen J. Immunol., March 15, 2005; 174(6): 3290 - 3297. [Abstract] [Full Text] [PDF]
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H. Nishikawa, T. Kato, I. Tawara, K. Saito, H. Ikeda, K. Kuribayashi, P. M. Allen, R. D. Schreiber, S. Sakaguchi, L. J. Old, et al. Definition of target antigens for naturally occurring CD4+ CD25+ regulatory T cells J. Exp. Med., March 7, 2005; 201(5): 681 - 686. [Abstract] [Full Text] [PDF]
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R. Setoguchi, S. Hori, T. Takahashi, and S. Sakaguchi Homeostatic maintenance of natural Foxp3+ CD25+ CD4+ regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization J. Exp. Med., March 7, 2005; 201(5): 723 - 735. [Abstract] [Full Text] [PDF]
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A. L. Bayer, A. Yu, D. Adeegbe, and T. R. Malek Essential role for interleukin-2 for CD4+CD25+ T regulatory cell development during the neonatal period J. Exp. Med., March 7, 2005; 201(5): 769 - 777. [Abstract] [Full Text] [PDF]
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T. Barthlott, H. Moncrieffe, M. Veldhoen, C. J. Atkins, J. Christensen, A. O'Garra, and B. Stockinger CD25+CD4+ T cells compete with naive CD4+ T cells for IL-2 and exploit it for the induction of IL-10 production Int. Immunol., March 1, 2005; 17(3): 279 - 288. [Abstract] [Full Text] [PDF]
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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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J. Nacsa, Y. Edghill-Smith, W.-P. Tsai, D. Venzon, E. Tryniszewska, A. Hryniewicz, M. Moniuszko, A. Kinter, K. A. Smith, and G. Franchini Contrasting Effects of Low-Dose IL-2 on Vaccine-Boosted Simian Immunodeficiency Virus (SIV)-Specific CD4+ and CD8+ T Cells in Macaques Chronically Infected with SIVmac251 J. Immunol., February 15, 2005; 174(4): 1913 - 1921. [Abstract] [Full Text] [PDF]
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Z. Liu, Q. Liu, H. Hamed, R. M. Anthony, A. Foster, F. D. Finkelman, J. F. Urban Jr, and W. C. Gause IL-2 and Autocrine IL-4 Drive the In Vivo Development of Antigen-Specific Th2 T Cells Elicited by Nematode Parasites J. Immunol., February 15, 2005; 174(4): 2242 - 2249. [Abstract] [Full Text] [PDF]
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T. Bopp, A. Palmetshofer, E. Serfling, V. Heib, S. Schmitt, C. Richter, M. Klein, H. Schild, E. Schmitt, and M. Stassen NFATc2 and NFATc3 transcription factors play a crucial role in suppression of CD4+ T lymphocytes by CD4+ CD25+ regulatory T cells J. Exp. Med., January 18, 2005; 201(2): 181 - 187. [Abstract] [Full Text] [PDF]
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