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The Journal of Immunology, 2002, 169: 4712-4716.
Copyright © 2002 by The American Association of Immunologists

Cutting Edge

Cutting Edge: CD4+CD25+ Regulatory T Cells Suppress Antigen-Specific Autoreactive Immune Responses and Central Nervous System Inflammation During Active Experimental Autoimmune Encephalomyelitis1

Adam P. Kohm, Pamela A. Carpentier, Holly A. Anger and Stephen D. Miller2

Department of Microbiology-Immunology and Interdepartmental Immunobiology Center, Northwestern University Medical School, Chicago, IL 60611


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Autoreactive CD4+ T cells exist in normal individuals and retain the capacity to initiate autoimmune disease. The current study investigates the role of CD4+CD25+ T-regulatory (TR) cells during autoimmune disease using the CD4+ T cell-dependent myelin oligodendrocyte glycoprotein (MOG)-specific experimental autoimmune encephalomyelitis model of multiple sclerosis. In vitro, TR cells effectively inhibited both the proliferation of and cytokine production by MOG35–55-specific Th1 cells. In vivo, adoptive transfer of TR cells conferred significant protection from clinical experimental autoimmune encephalomyelitis which was associated with normal activation of autoreactive Th1 cells, but an increased frequency of MOG35–55-specific Th2 cells and decreased CNS infiltration. Lastly, transferred TR cells displayed an enhanced ability to traffic to the peripheral lymph nodes and expressed increased levels of the adhesion molecules ICAM-1 and P-selectin that may promote functional interactions with target T cells. Collectively, these findings suggest that TR cells contribute notably to the endogenous mechanisms that regulate actively induced autoimmune disease.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
An essential characteristic of intrathymic CD4+ T cell development is the generation of TCR diversity which permits T cells to respond to a huge number of foreign Ags. However, one consequence of TCR diversity is the inevitable emergence of autoreactive T cell populations that persist in normal individuals with the capacity of mediating various autoimmune diseases (1). To combat this, regulatory cell populations and other protective mechanisms, such as clonal deletion and activation-induced anergy, have evolved with the collective goal of inhibiting the generation and/or function of autoreactive CD4+ T cells.

CD4+ T-regulatory (TR)3 cells display a mixed phenotype of naive and activated cell surface markers, e.g., CD4+CD25+CD62Lhigh (2). Importantly, the TR cell population does not contain previously activated CD4+ T cells (3) and inhibits T cell proliferation in a TCR-dependent manner, possibly via direct T-T cell interactions. Although the exact mechanism by which TR cells exert their inhibitory influence is still unknown, IL-10 production, surface CTLA-4 expression, IL-2 binding, costimulatory molecule blockade, and surface TGF-{beta} expression are all proposed mechanisms by which TR cells may down-regulate CD4+ T cell responses (2).

Consistent with their proposed role as active regulators of autoimmune responses, the depletion of TR cells in neonatal animals results in the spontaneous induction of autoimmune gastritis in both the thymectomy and nu/nu model systems (4, 5). Importantly, TR cells also block the gastritis resulting from the transfer of H/K ATPase-specific effector T cells (4, 5). Similarly, the transfer of CD4+CD25+ TR cells in an adoptive model of diabetes conferred significant protection against the onset of spontaneous diabetes (6), and transfer of either CD4+CD25- or CD4+CD25+ TR cells has been reported to suppress spontaneous experimental autoimmune encephalomyelitis (EAE) mediated by naive myelin basic protein (MOG)-specific T cells in recombination-activating gene-1-deficient TCR-transgenic mice (7, 8). Collectively, these findings suggest that TR cells may block both the initiation of autoimmune responses and inhibit the function of established autoreactive effector cells.

In this study, we investigate the role of TR cells in regulating the progression of active EAE in conventional C57BL/6 mice. MOG35–55-specific EAE (9), a mouse model of multiple sclerosis, is a CD4+ Th1-mediated autoimmune disease (10) in which autoreactive T cells specific for myelin components enter the CNS, initiating a cascade of inflammation and demyelination. We report here that CD4+CD25+ TR cells inhibit both the proliferation of and IFN-{gamma} production by a MOG35–55-specific T cell line in vitro. In addition, supplementation of TR cell numbers by adoptive transfer before active and adoptive EAE induction significantly reduced the severity of clinical disease potentially by promoting a disease-protective Th2 immune response and preventing CNS inflammation via a mechanism that may involve up-regulated expression of ICAM-1 and P-selectin. Together, these findings support a role for TR cells in protection from the onset/progression of autoimmune demyelination in wild-type mice induced by active MOG35–55/CFA immunization or adoptive transfer of differentiated autoreactive Th1 cells.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Mice

Female C57BL/6 mice, 5–6 wk old, were purchased from The Jackson Laboratory (Bar Harbor, ME). Mice were maintained on standard laboratory food and water ad libitum. Paralyzed animals were afforded easier access to food and water.

TR cells

Peripheral lymph nodes (LNs) were harvested from 6- to 7-wk-old mice, mechanically disassociated, and depleted of APC populations before positive selection of CD25+ TR cells using anti-CD25 Ab (7D4), anti-rat {kappa} microbeads (Miltenyi Biotec, Auburn, CA), and an AutoMACs (Miltenyi Biotec). The resulting population consisted of between 85 and 95% CD4+CD25+CD62Lhigh T cells.

In vitro proliferation and ELISPOT assay

Draining LN cells or MOG35–55-specific T cells (AG1) (11) were cultured with medium alone or different concentrations of MOG35–55 (MEVGWYRSPFSRVVHLYRNGK; Genemed Synthesis, San Francisco, CA) for 72 h and then pulsed with 1 µCi/well [3H]TdR for the final 24 h of culture. [3H]TdR uptake was detected using a Topcount Microplate Scintillation Counter, and results are expressed as the mean of triplicate cultures ± SEM. ELISPOT assays were performed as previously described (11).

Induction and clinical evaluation of MOG35–55-induced EAE

Female mice 6–7 wk old were immunized s.c. with 200 µl of an emulsion containing 800 µg of Mycobacterium tuberculosis H37Ra (Difco, Detroit, MI) and 200 µg of MOG35–55 distributed over three spots on the flank. Each mouse additionally received 200 ng of pertussis toxin (List Biological Laboratories, Campbell, CA) in 200 µl of PBS i.p. on days 0 and 2 postimmunization. For adoptive transfer, 5 x 106 MOG35–55 blasts were coinjected i.v. with either 2.5 x 106 TR (CD25+) or non-TR (CD25-) cells into naive C56BL/6 mice (11). Individual animals were observed daily, and clinical scores were assessed in a blinded manner on a scale of 0–5 as follows: 0 = no abnormality; 1 = limp tail; 2 = limp tail and hind limb weakness; 3 = hind limb paralysis; 4 = hind limb paralysis and forelimb weakness; and 5 = moribund. Data are reported as the mean daily clinical score. Mice were age and sex matched for all experiments.

Immunohistochemistry and immunofluorescence

CNS immunohistochemistry was performed as previously described (11). For immunofluorescence, single-cell suspensions were washed and incubated with fluorescently tagged Abs directed against a panel of cell surface markers (BD PharMingen, San Diego, CA). Fluorescent staining was analyzed using a FACSCalibur and CellQuest Pro (BD Biosciences, San Jose, CA).

Statistical analysis

Comparisons of clinical scores and ELISPOT frequencies between the various treatment groups were analyzed by unpaired Student’s t test. Values of p < 0.01 were considered significant.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
CD4+CD25+ TR cells suppress the proliferation of both CD4+ and CD8+ T cells; however, the exact mechanism by which these cells exert their effector function remains elusive. To elucidate the potential of TR cells for regulating the induction and/or progression of EAE, we first determined whether TR cells could suppress the in vitro proliferation of a T cell line (11) specific for an immunodominant epitope of MOG (MOG35–55) known to initiate EAE in C57BL/6 mice. As seen in Fig. 1GoA, coculture of a fixed number of a MOG35–55-specific Th1 line with an increasing number of TR cells isolated from naive C57BL/6 mice inhibited the level of T cell proliferation, regardless of whether the TR cells were isolated from either the LN or spleen. Overnight culture of LN TR cells with recombinant IL-2, before coculture with target cells, also had no observed effects on suppressive function. In addition to effects on cellular proliferation, TR cells (E:T ratio, 2:1) also reduced the level of IFN-{gamma} secreted by the MOG35–55-specific Th1 cell line (Fig. 1GoB), which is the predominant cytokine produced by this line as determined by gene array analysis (data not shown). As with cellular proliferation, TR-mediated suppression of IFN-{gamma} production was directly proportional to the E:T ratio (data not shown). Thus, TR cells appear to be competent in suppressing MOG35–55-specific T cell proliferation and IFN-{gamma} production in vitro.



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  		FIGURE 1. Effect of TR cells on MOG35–55-specific CD4+ Th1 function. A, TR cells isolated from LN or spleen cells were cultured overnight in either the presence or absence of rIL-2. An increasing number of TR cells (effector cells) were added to a fixed number (5 x 105/well) of MOG35–55-specific T cells (target cells), irradiated APC (5 x 106/well), and MOG35–55 (10 µM). Data are presented as percent inhibition of proliferation in comparison with groups cocultured with equivalent numbers of CD4+CD25- T cells. B, Effect of TR cell coculture on Ag-specific IFN-{gamma} production. Ninety-six hours after coculture of MOG35–55-specific T cells with either TR or non-TR CD4+ cells (E:T ratio, 2:1), supernatant levels of IFN-{gamma} were determined by ELISA. Data are presented as picograms per milliliter of IFN-{gamma} after serial dilution of supernatants and are representative of two separate experiments.

 
On the basis of the above findings, we next investigated the role of TR cells in modulating EAE disease progression in vivo. First, TR cells were isolated from LNs of naive C57BL/6 donors, and 2 x 106 TR cells were adoptively transferred into naive recipients 3 days before active induction of EAE. Supplementation of TR cells conferred significant protection from the development of clinical EAE (Fig. 2GoA), in comparison with mice receiving either no cells or non-TR CD4+ T cells. Surprisingly, the number of cells secreting disease-promoting Th1 cytokines, such as IFN-{gamma} and TNF-{alpha} (12), were similar in the LNs (Fig. 2GoB) and spleens (data not shown) at the peak of disease in all groups of mice. Of potential importance, the number of MOG35–55-specific IL-2-secreting cells was significantly diminished (Fig. 2GoC), and the number of IL-4 and IL-5-secreting cells was elevated in regulatory cell recipients (Fig. 2Go, D and E). Lastly, we examined the capacity of TR cells to regulate the effector function of previously activated autoreactive T cells by coinjecting TR or non-TR cells with MOG35–55-specific T cell blasts. Clinical symptoms in mice receiving TR cells were reduced by ~50% in comparison with mice receiving non-TR cells (Fig. 2GoF). Thus, supplementation of TR cell numbers conferred protection against both active and passive EAE disease progression, in the absence of any observable effect on the frequency of T cells producing disease-promoting cytokines, whereas the number of cells secreting disease-protective Th2 cytokines was elevated.



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  		FIGURE 2. Active and passive EAE disease progression after supplementation of TR cells. A, Two x 106 TR or non-TR cells were isolated from LNs of naive donors and transferred i.v. into recipients 3 days before active EAE induction with MOG35–55/CFA. Data are presented as the mean clinical score of five mice per group and are representative of three separate experiments. B–E, Effect of TR cells on cytokine production by MOG35–55-specific T cells during EAE. At the peak of EAE (15–20 days postimmunization), LN cells were harvested and cocultured with irradiated APC and stimulated (Stim) with 2 concentrations of MOG35–55, 1 µM (Mog1) and 10 µM (Mog10), or anti-CD3 Ab (2C11, 0.5 µg/106 cells) for 24–36 h. Data are presented as the number of MOG35–55-specific IFN-{gamma} (B), IL-2 (C), IL-4 (D), and IL-5 (E)-secreting cells. F, Five x 106 MOG35–55 blasts were coinjected i.v. with either 2.5 x 106 TR (CD25+) or non-TR (CD25-) cells into naive C56BL/6 mice. Data are presented as the mean clinical score of five mice per group and are representative of three separate experiments. *, Significant differences, p < 0.01.

 
As previously discussed, CNS inflammation is a characteristic of EAE disease progression. The degree of lymphocyte infiltration correlates with both the level of macrophage infiltration/activation and disease severity (13). In agreement with this, CD4+ T cell infiltration and F4/80+ APC activation/infiltration was substantially reduced in the spinal cords of TR recipients (Fig. 3Go) despite the normal frequency of peripheral MOG35–55-specific Th1 cells. These findings raised the possibility that TR cells may enter the CNS to locally regulate immune cell activation and inflammation. To address this possibility, we examined the peripheral lymphoid organs and CNS tissues of individual mice for the presence of the transferred TR cells. Although the number of non-TR CD4+ T cells was markedly reduced 6- to 12-fold within the CNS of TR cell recipients (Fig. 4GoA), we failed to detect the transferred TR cell population within either the brain or spinal cord during the peak of EAE. In contrast, there were 3.5-fold more donor cells in the LNs of TR vs non-TR recipients, suggesting differential trafficking of these populations. This finding may be explained by differential adhesion molecule expression on TR cells, which expressed elevated levels of both surface P-selectin (CD62P) and ICAM-1 (Fig. 4GoB). Therefore, TR cells appear to confer protection to mice against progression of EAE by a mechanism involving enhanced Th2 cytokine production and inhibition of CNS inflammation, which may be dependent on expression of specific adhesion molecules.



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  		FIGURE 3. TR cells diminish CNS inflammation during EAE. Spinal cord tissues from mice sacrificed days 15–20 postpriming were examined for the presence of CD4+, CD8+, B220+, and F4/80+ (APC) cells (red). Tissues were also counterstained with DAPI (blue). No positive staining was observed in isotype-matched controls (data not shown). x100 magnification.

 


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  		FIGURE 4. In vivo homing properties and adhesion molecule expression on TR cells. A, Homing properties of Tr cells. A total of 2 x 106 TR or non-TR cells isolated from Thy1.2+ wild-type C57BL/6 mice were adoptively transferred into Thy1.1+-congenic mice 3 days before active EAE disease induction. At the peak of clinical disease, mice were perfused before harvest of spinal cords, brains, spleens, and peripheral LNs and adhesion molecule analysis. Data are presented from individual mice as recipient (Thy1.1) vs donor (Th1.2) CD4+ T cells. The percent of the CD4+ T cell population originating from donor cells is indicated in each upper left quadrant. Data are representative of three separate animals in three separate experiments. B, Adhesion molecule expression on TR and non-TR CD4+ T cells. LN cells isolated from naive mice were stained with Abs specific for CD4, CD25, CD62L, and a panel of adhesion molecules. Data are presented as the relative fluorescence of each adhesion molecule on both TR and non-TR cells and are representative of three separate experiments.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
It is currently believed that TCR ligation enables TR cells to nonspecifically inhibit CD4+ T cell proliferation both in vitro and in vivo (3). However, there is a surprising deficiency in the literature concerning the effects of TR cells on additional functional measures such as cytokine production and cellular differentiation. We report that coculture of MOG35–55-specific T cells with TR cells inhibits the level of both Ag-specific proliferation and IFN-{gamma} production. TR cells appear not to prevent the initial activation of target CD4+ T cells but subsequently induce cell cycle arrest (3). In light of these findings, it is not clear whether the measured reduction in IFN-{gamma} production is the result of direct effects on cytokine production or whether it results from inhibition of Ag-specific cell expansion. Previous studies indicate that TR cells must be activated via TCR ligation before exerting their immunosuppressive phenotype (14); however, the limiting frequency of MOG35–55-specific TR cells undoubtedly present in our in vitro culture system suggests that TR cells are more efficient inhibitors of Ag-specific than mitogen-induced T cell responses and/or that these cells become activated as a result of the isolation process.

To investigate the role of TR cells in regulating the progression of autoimmune diseases, we used a model system in which the TR cell population in naive C57BL/6 mice was supplemented before both active and passive induction of EAE. Augmentation of TR cell numbers by ~50–75% (2 x 106 TR cells transferred to naive recipients normally containing an estimated 2.5–3 x 106 TR cells) conferred significant protection against EAE induction/progression as measured by both disease score and the promotion of protective Th2 cytokines. In addition, we observed markedly less CD4+ T cell infiltration into the CNS at the peak of disease in TR cell recipients which corresponded with decreased levels of APC infiltration/activation within the CNS (Fig. 3Go). One explanation of these findings is that TR cells inhibit the expansion of MOG-specific T cells in peripheral lymphoid organs. This possibility is supported by the decreased frequency of MOG35–55-specific IL-2-producing cells in TR cell recipients, but not by the normal numbers of Ag-specific IFN-{gamma} ELISPOTs (Fig. 2Go). Alternatively, we detected an increased frequency of cells producing Th2-like cytokines in the LNs and spleens of TR cell recipients after disease initiation. Therefore, it is possible that TR cells differentially influence either the differentiation or effector function of Th1 and Th2 cells, with the normal frequency of Th1 cells better supporting the latter possibility. In addition, the elevated number of MOG35–55-specific Th2 cells in TR recipients may result from inhibition of the pathogenic Th1-like responses, subsequently allowing the progression of bystander Th2 responses. This possibility is further supported by our findings that mitogenic (anti-CD3 Ab) simulation of LN and spleen cells isolated from TR recipients induced a significant increase in the number of cells producing Th2-like cytokines in comparison with cells stimulated with the specific MOG35–55 peptide (Fig. 2Go). However, further study is necessary to gain a better understanding of the exact effector mechanisms of TR cells during EAE disease progression.

Little is currently known about the homing patterns and site(s) of TR cell function in vivo. During EAE, TR cells may traffic to the CNS to inhibit the local activation of myelin-specific autoreactive T cells, a prerequisite for development of inflammatory demyelination (11). However, we failed to detect donor TR within the CNS at a time corresponding with the peak of disease in non-TR cell recipients (Fig. 4GoA), whereas TR cell populations were detectable in recipient spleen and LNs. This finding supports the hypothesis that TR cells may influence the activation of autoreactive T cells within peripheral lymphoid organs and/or the homing of activated lymphocytes to the CNS. This latter hypothesis gains further support from current findings (Fig. 2GoF) and those of others (4, 5) showing that TR cells inhibit the in vivo function of previously activated T cells. It is possible that the numbers of regulatory cells within the CNS were below our detection limits or that the kinetics of TR cell homing was such that these cells may be detected within the CNS either earlier or later than currently measured.

Chemokine gradients are an obvious mechanism that may regulate TR cell trafficking in vivo (8, 15). In addition, TR homing may be influenced by differential expression of adhesion molecules. Our findings support this possibility, because TR cells expressed elevated levels of both ICAM-1 and P-selectin in comparison with non-TR cells (Fig. 4GoB). The detection of P-selectin expression on TR cells was surprising, because previous reports have indicated that expression is limited to activated platelets and endothelium (16). However, because P-selectin facilitates endothelium-T cell interactions (17), P-selectin expression may prove to be one mechanism promoting the direct interaction of TR cells with target CD4+ T cells in vivo. This is an attractive hypothesis in light of previous findings suggesting that TR cells must directly interact with target T cells to exert their suppressive phenotype and that P-selectin glycoprotein ligand-1 is expressed preferentially on Th1 cells (18). This is supported by our recent studies showing that TR from P-selectin-deficient mice are functionally defective in vitro (data not shown). We are currently exploring the dependence of P-selectin/P-selectin glycoprotein ligand-1 interactions, as well as other adhesion molecules, in governing TR function both in vitro and in vivo.


   Footnotes
 
1 This work was supported in part by U.S. Public Health Service National Institutes of Health Research Grants NS30871 and NS26543. Back

2 Address correspondence and reprint requests to Dr. Stephen D. Miller, Department of Microbiology-Immunology, Northwestern University Medical School, 303 East Chicago Avenue, Chicago, IL 60611. E-mail address: s-d-miller{at}northwestern.edu Back

3 Abbreviations used in this paper: TR cell, CD4+CD25+ T-regulatory cell; EAE, experimental autoimmune encephalomyelitis; MOG, myelin oligodendrocyte glycoprotein; LN, lymph node. Back

Received for publication August 12, 2002. Accepted for publication September 11, 2002.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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  5. Sakaguchi, S., N. Sakaguchi, M. Asano, M. Itoh, M. Toda. 1995. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor {alpha}-chains (CD25): breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155:1151.[Abstract]
  6. Salomon, B., D. J. Lenschow, L. Rhee, N. Ashourian, B. Singh, A. Sharpe, J. A. Bluestone. 2000. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431.[Medline]
  7. Furtado, G. C., D. Olivares-Villagomez, M. A. Curotto de Lafaille, A. K. Wensky, J. A. Latkowski, J. J. Lafaille. 2001. Regulatory T cells in spontaneous autoimmune encephalomyelitis. Immunol. Rev. 182:122.[Medline]
  8. Hori, S., M. Haury, A. Coutinho, J. Demengeot. 2002. Specificity requirements for selection and effector functions of CD25+4+ regulatory T cells in anti-myelin basic protein T cell receptor transgenic mice. Proc. Natl. Acad. Sci. USA 99:8213.[Abstract/Free Full Text]
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Matrix Metalloproteinase-12 Deficiency Worsens Relapsing-Remitting Experimental Autoimmune Encephalomyelitis in Association with Cytokine and Chemokine Dysregulation
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A. L. Barnard, A. P. Chidgey, C. C. Bernard, and R. L. Boyd
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Blood, January 1, 2009; 113(1): 204 - 213.
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CCR6 Regulates the Migration of Inflammatory and Regulatory T Cells
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H. H. Hofstetter, O. Stuve, and H.-P. Hartung
Fine-tuning the Homeostasis of Regulatory T Cells: New Mechanism of Immunomodulatory Therapy in Multiple Sclerosis
Arch Neurol, November 1, 2008; 65(11): 1417 - 1418.
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M. Korporal, J. Haas, B. Balint, B. Fritzsching, A. Schwarz, S. Moeller, B. Fritz, E. Suri-Payer, and B. Wildemann
Interferon Beta-Induced Restoration of Regulatory T-Cell Function in Multiple Sclerosis Is Prompted by an Increase in Newly Generated Naive Regulatory T Cells
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Mycobacterium bovis Bacille Calmette-Guerin Infection in the CNS Suppresses Experimental Autoimmune Encephalomyelitis and Th17 Responses in an IFN-{gamma}-Independent Manner
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X. Luo, K. L. Pothoven, D. McCarthy, M. DeGutes, A. Martin, D. R. Getts, G. Xia, J. He, X. Zhang, D. B. Kaufman, et al.
ECDI-fixed allogeneic splenocytes induce donor-specific tolerance for long-term survival of islet transplants via two distinct mechanisms
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CD28 Costimulation Is Essential for Human T Regulatory Expansion and Function
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J. Ochoa-Reparaz, A. Rynda, M. A. Ascon, X. Yang, I. Kochetkova, C. Riccardi, G. Callis, T. Trunkle, and D. W. Pascual
IL-13 Production by Regulatory T Cells Protects against Experimental Autoimmune Encephalomyelitis Independently of Autoantigen
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J. H. Mills, L. F. Thompson, C. Mueller, A. T. Waickman, S. Jalkanen, J. Niemela, L. Airas, and M. S. Bynoe
CD73 is required for efficient entry of lymphocytes into the central nervous system during experimental autoimmune encephalomyelitis
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 EndocrinologyHome page
S.-C. Tzou, I. Lupi, M. Landek, A. Gutenberg, Y.-M. Tzou, H. Kimura, G. Pinna, N. R. Rose, and P. Caturegli
Autoimmune Hypophysitis of SJL Mice: Clinical Insights from a New Animal Model
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S. Reinwald, C. Wiethe, A. M. Westendorf, M. Breloer, M. Probst-Kepper, B. Fleischer, A. Steinkasserer, J. Buer, and W. Hansen
CD83 Expression in CD4+ T Cells Modulates Inflammation and Autoimmunity
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 Rheumatology (Oxford)Home page
M. Thewissen and J. W. Cohen Tervaert
Leptin and ANCA-associated vasculitis: a healthy link?
Rheumatology, April 1, 2008; 47(4): 387 - 389.
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J. Wang, H. Takeuchi, Y. Sonobe, S. Jin, T. Mizuno, S. Miyakawa, M. Fujiwara, Y. Nakamura, T. Kato, H. Muramatsu, et al.
Inhibition of midkine alleviates experimental autoimmune encephalomyelitis through the expansion of regulatory T cell population
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R. K. Selvaraj and T. L. Geiger
Mitigation of Experimental Allergic Encephalomyelitis by TGF-{beta} Induced Foxp3+ Regulatory T Lymphocytes through the Induction of Anergy and Infectious Tolerance
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R. P. Singh, A. La Cava, and B. H. Hahn
pConsensus Peptide Induces Tolerogenic CD8+ T Cells in Lupus-Prone (NZB x NZW)F1 Mice by Differentially Regulating Foxp3 and PD1 Molecules
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Y.-H. Lee, Y. Ishida, M. Rifa'i, Z. Shi, K.-i. Isobe, and H. Suzuki
Essential Role of CD8+CD122+ Regulatory T Cells in the Recovery from Experimental Autoimmune Encephalomyelitis
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Neuroprotective activities of CD4+CD25+ regulatory T cells in an animal model of Parkinson's disease
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R. J. DiPaolo, C. Brinster, T. S. Davidson, J. Andersson, D. Glass, and E. M. Shevach
Autoantigen-Specific TGFbeta-Induced Foxp3+ Regulatory T Cells Prevent Autoimmunity by Inhibiting Dendritic Cells from Activating Autoreactive T Cells
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A. L. Christy and M. A. Brown
The Multitasking Mast Cell: Positive and Negative Roles in the Progression of Autoimmunity
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R. A. O'Connor, K. H. Malpass, and S. M. Anderton
The Inflamed Central Nervous System Drives the Activation and Rapid Proliferation of Foxp3+ Regulatory T Cells
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S. Brahmachari and K. Pahan
Sodium Benzoate, a Food Additive and a Metabolite of Cinnamon, Modifies T Cells at Multiple Steps and Inhibits Adoptive Transfer of Experimental Allergic Encephalomyelitis
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B. D. Sather, P. Treuting, N. Perdue, M. Miazgowicz, J. D. Fontenot, A. Y. Rudensky, and D. J. Campbell
Altering the distribution of Foxp3+ regulatory T cells results in tissue-specific inflammatory disease
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M. K. Mann, K. Maresz, L. P. Shriver, Y. Tan, and B. N. Dittel
B Cell Regulation of CD4+CD25+ T Regulatory Cells and IL-10 Via B7 is Essential for Recovery From Experimental Autoimmune Encephalomyelitis
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J. Ochoa-Reparaz, C. Riccardi, A. Rynda, S. Jun, G. Callis, and D. W. Pascual
Regulatory T Cell Vaccination without Autoantigen Protects against Experimental Autoimmune Encephalomyelitis
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S. E. Cabbage, E. S. Huseby, B. D. Sather, T. Brabb, D. Liggitt, and J. Goverman
Regulatory T Cells Maintain Long-Term Tolerance to Myelin Basic Protein by Inducing a Novel, Dynamic State of T Cell Tolerance
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S. Hirata, H. Matsuyoshi, D. Fukuma, A. Kurisaki, Y. Uemura, Y. Nishimura, and S. Senju
Involvement of Regulatory T Cells in the Experimental Autoimmune Encephalomyelitis-Preventive Effect of Dendritic Cells Expressing Myelin Oligodendrocyte Glycoprotein plus TRAIL
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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.
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R. C. Axtell, L. Xu, S. R. Barnum, and C. Raman
CD5-CK2 Binding/Activation-Deficient Mice Are Resistant to Experimental Autoimmune Encephalomyelitis: Protection Is Associated with Diminished Populations of IL-17-Expressing T Cells in the Central Nervous System
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S. Schif-Zuck, G. Wildbaum, and N. Karin
Coadministration of Plasmid DNA Constructs Encoding an Encephalitogenic Determinant and IL-10 Elicits Regulatory T Cell-Mediated Protective Immunity in the Central Nervous System
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 BrainHome page
D. Tischner, A. Weishaupt, J. v. d. Brandt, N. Muller, N. Beyersdorf, C. W. Ip, K. V. Toyka, T. Hunig, R. Gold, T. Kerkau, et al.
Polyclonal expansion of regulatory T cells interferes with effector cell migration in a model of multiple sclerosis
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Q. Ding, L. Lu, B. Wang, Y. Zhou, Y. Jiang, X. Zhou, L. Xin, Z. Jiao, and K.-Y. Chou
B7H1-Ig Fusion Protein Activates the CD4+ IFN-{gamma} Receptor+ Type 1 T Regulatory Subset through IFN-{gamma}-Secreting Th1 Cells
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E. H. Tran, Y.-T. Azuma, M. Chen, C. Weston, R. J. Davis, and R. A. Flavell
Inactivation of JNK1 enhances innate IL-10 production and dampens autoimmune inflammation in the brain
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K. J. Scalapino, Q. Tang, J. A. Bluestone, M. L. Bonyhadi, and D. I. Daikh
Suppression of Disease in New Zealand Black/New Zealand White Lupus-Prone Mice by Adoptive Transfer of Ex Vivo Expanded Regulatory T Cells
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C. Cassan, E. Piaggio, J. P. Zappulla, L. T. Mars, N. Couturier, F. Bucciarelli, S. Desbois, J. Bauer, D. Gonzalez-Dunia, and R. S. Liblau
Pertussis Toxin Reduces the Number of Splenic Foxp3+ Regulatory T Cells
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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.
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A. Rolland, E. Jouvin-Marche, C. Viret, M. Faure, H. Perron, and P. N. Marche
The Envelope Protein of a Human Endogenous Retrovirus-W Family Activates Innate Immunity through CD14/TLR4 and Promotes Th1-Like Responses.
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J. Cabarrocas, C. Cassan, F. Magnusson, E. Piaggio, L. Mars, J. Derbinski, B. Kyewski, D.-A. Gross, B. L. Salomon, K. Khazaie, et al.
Foxp3+ CD25+ regulatory T cells specific for a neo-self-antigen develop at the double-positive thymic stage
PNAS, May 30, 2006; 103(22): 8453 - 8458.
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X. Zhang, J. Reddy, H. Ochi, D. Frenkel, V. K. Kuchroo, and H. L. Weiner
Recovery from experimental allergic encephalomyelitis is TGF-{beta} dependent and associated with increases in CD4+LAP+ and CD4+CD25+ T cells
Int. Immunol., April 1, 2006; 18(4): 495 - 503.
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E. Gonzalez-Rey, A. Fernandez-Martin, A. Chorny, J. Martin, D. Pozo, D. Ganea, and M. Delgado
Therapeutic Effect of Vasoactive Intestinal Peptide on Experimental Autoimmune Encephalomyelitis: Down-Regulation of Inflammatory and Autoimmune Responses
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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
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T. Koya, T. Kodama, K. Takeda, N. Miyahara, E.-S. Yang, C. Taube, A. Joetham, J.-W. Park, A. Dakhama, and E. W. Gelfand
Importance of Myeloid Dendritic Cells in Persistent Airway Disease after Repeated Allergen Exposure
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R. Liu, A. La Cava, X.-F. Bai, Y. Jee, M. Price, D. I. Campagnolo, P. Christadoss, T. L. Vollmer, L. Van Kaer, and F.-D. Shi
Cooperation of Invariant NKT Cells and CD4+CD25+ T Regulatory Cells in the Prevention of Autoimmune Myasthenia
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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
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M. S. Wilson, M. D. Taylor, A. Balic, C. A.M. Finney, J. R. Lamb, and R. M. Maizels
Suppression of allergic airway inflammation by helminth-induced regulatory T cells
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A. Chorny, E. Gonzalez-Rey, A. Fernandez-Martin, D. Pozo, D. Ganea, and M. Delgado
Vasoactive intestinal peptide induces regulatory dendritic cells with therapeutic effects on autoimmune disorders
PNAS, September 20, 2005; 102(38): 13562 - 13567.
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M. J. McGeachy, L. A. Stephens, and S. M. Anderton
Natural Recovery and Protection from Autoimmune Encephalomyelitis: Contribution of CD4+CD25+ Regulatory Cells within the Central Nervous System
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D. J. Mekala, R. S. Alli, and T. L. Geiger
IL-10-dependent infectious tolerance after the treatment of experimental allergic encephalomyelitis with redirected CD4+CD25+ T lymphocytes
PNAS, August 16, 2005; 102(33): 11817 - 11822.
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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
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T. L. Denning, G. Kim, and M. Kronenberg
Cutting Edge: CD4+CD25+ Regulatory T Cells Impaired for Intestinal Homing Can Prevent Colitis
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Y. Chen, C. Cuda, and L. Morel
Genetic Determination of T Cell Help in Loss of Tolerance to Nuclear Antigens
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J. G. Heuer, T. Zhang, J. Zhao, C. Ding, M. Cramer, K. L. Justen, S. L. Vonderfecht, and S. Na
Adoptive Transfer of In Vitro-Stimulated CD4+CD25+ Regulatory T Cells Increases Bacterial Clearance and Improves Survival in Polymicrobial Sepsis
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A. P. Kohm, J. S. Williams, A. L. Bickford, J. S. McMahon, L. Chatenoud, J.-F. Bach, J. A. Bluestone, and S. D. Miller
Treatment with Nonmitogenic Anti-CD3 Monoclonal Antibody Induces CD4+ T Cell Unresponsiveness and Functional Reversal of Established Experimental Autoimmune Encephalomyelitis
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S. P. Zehntner, C. Brickman, L. Bourbonniere, L. Remington, M. Caruso, and T. Owens
Neutrophils That Infiltrate the Central Nervous System Regulate T Cell Responses
J. Immunol., April 15, 2005; 174(8): 5124 - 5131.
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G. Matarese, P. B. Carrieri, A. La Cava, F. Perna, V. Sanna, V. De Rosa, D. Aufiero, S. Fontana, and S. Zappacosta
Leptin increase in multiple sclerosis associates with reduced number of CD4+CD25+ regulatory T cells
PNAS, April 5, 2005; 102(14): 5150 - 5155.
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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.
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S. Schif-Zuck, J. Westermann, N. Netzer, Y. Zohar, M. Meiron, G. Wildbaum, and N. Karin
Targeted Overexpression of IL-18 Binding Protein at the Central Nervous System Overrides Flexibility in Functional Polarization of Antigen-Specific Th2 Cells
J. Immunol., April 1, 2005; 174(7): 4307 - 4315.
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M. R. Walker, B. D. Carson, G. T. Nepom, S. F. Ziegler, and J. H. Buckner
De novo generation of antigen-specific CD4+CD25+ regulatory T cells from human CD4+CD25- cells
PNAS, March 15, 2005; 102(11): 4103 - 4108.
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 Rheumatology (Oxford)Home page
A. Loughry, S. Fairchild, N. Athanasou, J. Edwards, and F. C. Hall
Inflammatory arthritis and dermatitis in thymectomized, CD25+ cell-depleted adult mice
Rheumatology, March 1, 2005; 44(3): 299 - 308.
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 BloodHome page
D. J. Mekala and T. L. Geiger
Immunotherapy of autoimmune encephalomyelitis with redirected CD4+CD25+ T lymphocytes
Blood, March 1, 2005; 105(5): 2090 - 2092.
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A. Matejuk, C. Hopke, A. A. Vandenbark, P. D. Hurn, and H. Offner
Middle-Age Male Mice Have Increased Severity of Experimental Autoimmune Encephalomyelitis and Are Unresponsive to Testosterone Therapy
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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}
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N. Taylor, K. McConnachie, C. Calder, R. Dawson, A. Dick, J. D. Sedgwick, and J. Liversidge
Enhanced Tolerance to Autoimmune Uveitis in CD200-Deficient Mice Correlates with a Pronounced Th2 Switch in Response to Antigen Challenge
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T. Kubo, R. D. Hatton, J. Oliver, X. Liu, C. O. Elson, and C. T. Weaver
Regulatory T Cell Suppression and Anergy Are Differentially Regulated by Proinflammatory Cytokines Produced by TLR-Activated Dendritic Cells
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 Proc. Natl. Acad. Sci. USAHome page
J. Kipnis, H. Avidan, R. R. Caspi, and M. Schwartz
Dual effect of CD4+CD25+ regulatory T cells in neurodegeneration: A dialogue with microglia
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N. Sarween, A. Chodos, C. Raykundalia, M. Khan, A. K. Abbas, and L. S. K. Walker
CD4+CD25+ Cells Controlling a Pathogenic CD4 Response Inhibit Cytokine Differentiation, CXCR-3 Expression, and Tissue Invasion
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M. J. Polanczyk, B. D. Carson, S. Subramanian, M. Afentoulis, A. A. Vandenbark, S. F. Ziegler, and H. Offner
Cutting Edge: Estrogen Drives Expansion of the CD4+CD25+ Regulatory T Cell Compartment
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M. R. Ehrenstein, J. G. Evans, A. Singh, S. Moore, G. Warnes, D. A. Isenberg, and C. Mauri
Compromised Function of Regulatory T Cells in Rheumatoid Arthritis and Reversal by Anti-TNF{alpha} Therapy
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A. P. Kohm, J. S. Williams, and S. D. Miller
Cutting Edge: Ligation of the Glucocorticoid-Induced TNF Receptor Enhances Autoreactive CD4+ T Cell Activation and Experimental Autoimmune Encephalomyelitis
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S. Gregori, N. Giarratana, S. Smiroldo, and L. Adorini
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