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Department of Medicine, Division of Immunology and Rheumatology, Stanford University School of Medicine, Stanford, CA 94305
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionReferences |
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), lymphoid
chemokines, whereas
CD4+CD25+CD62L- splenocytes
preferentially express CCR2, CCR4, and CXCR3 and migrate toward the
corresponding inflammatory chemokines. These data demonstrate that
CD4+CD25+CD62L+, but not
CD4+CD25+CD62L-, splenocytes delay
diabetes transfer, and that CD4+CD25+
suppressor T cells are comprised of at least two subpopulations that
behave differently in cotransfer in vivo and express distinct chemokine
receptor and chemotactic response profiles despite demonstrating
equivalent suppressor functions in vitro. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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CD4+CD25+ T cells have been
shown to be potent regulatory cells in a number of mouse models as well
as in rats and humans (9, 11, 12, 13, 14, 15). The mechanism of action
by which CD4+CD25+ T cells
prevent the development of autoimmune disease is not completely
understood. CD4+CD25+ T
cells, activated in vitro, suppress the proliferation of responder
CD4+CD25- T cells in a
cell contact-dependent manner (16). Their effect in vivo
appears (in some, but not all, systems) to depend on IL-10 and/or
TGF- expression (17). Very little is known about the
trafficking behavior of
CD4+CD25+ T cells or the
site where they exert their regulatory activity in vivo.
CD4+CD25+ T cells can be
easily found in secondary lymphoid organs.
CD4+CD25+ splenocytes
express high levels of CCR5 and are attracted by activated APCs
that express macrophage inflammatory protein-1 (ligand for CCR5).
This may be essential for maintaining normal humoral immune responses
in the secondary lymphoid tissues (18). At the same time,
CD4+CD25+ T cells from
human peripheral blood selectively express CCR8 and CCR4 and show a
strong chemotactic response to ligands for CCR4, monocyte-derived
chemokine (MDC), and thymus- and activation-regulated chemokine (TARC).
These chemokines are produced at high levels by activated APC and
attract activated T cells, suggesting that
CD4+CD25+ T cells may be
attracted to inflamed tissues to regulate or prevent autoimmune disease
(19).
In this manuscript we demonstrate that CD4+CD25+CD62L+, and not CD4+CD25+CD62L-, splenocytes inhibit diabetes transfer into immune-compromised NOD mice, whereas both subsets are equally effective in suppression assays in vitro. We address whether differential trafficking of these two subsets may explain these seemingly contradictory results.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Female NOD mice were obtained from Taconic Farms (Germantown, NY). Female NOD.SCID mice were obtained from The Jackson Laboratory (Bar Harbor, ME) and were used as recipients between 4–6 wk of age. All animals were maintained under specific pathogen-free conditions at the Department of Comparative Medicine, Stanford University School of Medicine (Stanford, CA).
Antibodies
Purified anti-CD3 (145-2C11) and anti-CD28 (37.51), FITC-labeled anti-CD4 (GK1.5), anti-CD62L (MEL-14), PE-labeled anti-CD25 (PC61), biotinylated anti-CD25 (7D4), and CyChrome-labeled anti-CD4 (RM4-5) were purchased from BD PharMingen (San Diego, CA). PE-conjugated streptavidin was purchased from Caltag Laboratories (Burlingame, CA).
Lymphocyte preparation
Single cells containing IIC were prepared from the pancreata of 11-wk-old NOD mice using a procedure previously described (20). CD4+CD25+ and CD4+CD25- cells were prepared from single-cell suspensions by CD4 enrichment using anti-CD4 magnetic Microbeads (Miltenyi Biotec, Auburn, CA), followed by FACS sorting. CD4+CD25+CD62L+ and CD4+CD25+CD62L- cells were prepared as single-cell suspensions from splenocytes stained with PE-labeled anti-CD25, enriched with anti-PE magnetic Microbeads (Miltenyi Biotec), and then sorted by FACS as CD4+CD25+CD62L+ and CD4+CD25+CD62L- cells. The purity of these sorted cell populations was routinely >95%.
FACS analysis and FACS sorting
Cell preparation was performed in PBS (Life Technologies, Gaithersburg, MD) plus 5% heat-inactivated FBS (HyClone, Logan, UT). Cells were sorted aseptically on a FACStar cell sorter (BD Biosciences, Mountain View, CA) in the Shared FACS Facility, Center for Molecular and Genetic Medicine, Stanford University. The data were analyzed using the Herzenberg desk facility (Stanford University), FloJo 2.7.8 (TreeStar, San Carlos, CA).
Cell transfer procedure
Cells were resuspended in PBS and were injected i.p. at the numbers indicated. NOD.SCID recipients were checked for glucosurea using Glucostix (Roche, Indianapolis, IN) twice a week. If glucosurea was observed, blood glucose was measured with a One Touch Basic glucometer (Johnson & Johnson, Milpitas, CA). Mice with glucosurea and blood glucose 250 mg/dl were considered diabetic. Glucosurea always coincided with high blood glucose levels.
In vitro proliferation assays
RPMI-C, i.e., RPMI 1640 (BioWhittaker, Walkersville, MD) supplemented with 10% heat-inactivated FBS, 10 mM HEPES, 1% nonessential amino acids, 1 mM sodium pyruvate, 100 U/ml penicillin plus 100 µg/ml streptomycin, 2 mM L-glutamine (all obtained from Life Technologies), and 50 µM 2-ME (Sigma, St. Louis, MO), was used for in vitro cultures. Cells were incubated with equal number of anti-CD3- and anti-CD28-coated beads in RPMI-C in 96-well U-bottom plates (BD Biosciences). Beads were coated as described previously (21) using 2.5 µg/ml anti-CD3 and 2.5 µg/ml anti-CD28 mAbs. Cells were pulsed with 1 µCi [3H]thymidine (Amersham Pharmacia Biotech, Piscataway, NJ)/well for the last 15 h of the 72-h culture. Cells were then harvested onto filter membranes using a Wallac harvester (PerkinElmer, Gaithersburg, MD), and the amount of incorporated [3H]thymidine was measured with a Wallac Betaplate counter (PerkinElmer).
Analysis of chemokine receptor mRNA by RNase protection assay
Sorted cells were washed in PBS, pelleted, and frozen. RNA was
extracted using the RNeasy kit (Qiagen, Valencia, CA). Probes were
labeled with [
-32-P]UTP and hybridized with
the isolated RNA. Two custom-designed probe sets (BD PharMingen) were
used. One set detects CCR1, CXCR4, CCR5, BLR-1, CCR8, CCR6, L32, and
GAPDH. The other set detects CXCR2, CCR3, CCR4, CCR2, CCR7, CXCR3, L32,
and GAPDH. After digestion of ssRNA, the protected fragments were
separated by PAGE. Controls included the probe set hybridized to tRNA
only and to tRNA plus a pool of synthetic sense RNAs complementary to
the probe set. For quantification, autoradiographs were scanned on a
PhosphorImager (Molecular Dynamics, Sunnyvale, CA), and band density
was assessed with ImageQuant image software (Molecular Dynamics,
Sunnyvale, CA). The arbitrary units of expression levels for the
chemokine receptors are the values obtained from the densitometer and
normalized against GAPDH.
Chemotaxis assays
Sorted cells were allowed to incubate in RPMI-C for 1 h at
37°C. Migration assays were performed in Costar 24-well plate tissue
culture inserts with 5-µm pore size polycarbonate filters (Corning,
Corning, NY). All recombinant mouse chemokines were purchased from R&D
Systems (Minneapolis, MN) and were used at the following final
concentrations: ELC (macrophage-inflammatory protein-3), 100 nM;
secondary lymphoid tissue chemokine (SLC), 100 nM; monokine induced by
IFN-
, 100 nM; IFN--inducible protein 10, 25 nM; MDC 100 nM; and
TARC, 100 nM. Six hundred microliters of the diluted chemokine solution
was placed in the lower well, and 100 µl medium containing cells
(1 x 105) was placed in the upper chamber.
Migration was conducted in equilibrated RPMI-C at 37°C with 6%
CO2 for 90 min. After removal of the Transwell
insert, 400 µl of the medium in the lower well containing the
migrated cells was mixed with 5 x 104
PE-streptavidin (Caltag Laboratories)-labeled latex beads (Interfacial
Dynamics, Portland, OR) and analyzed by FACS. The percentage of cells
that had migrated through the filter was determined by counting the
proportion of cells vs PE-positive beads, taking into account the
volumes. Background/nonspecific migration was assessed by migration to
plain medium.
Statistical analysis
For comparison of disease onset times, the Mann-Whitney U test was used.
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Prompted by the previous observations that IIC from prediabetic
NOD mice rapidly transferred diabetes into NOD.SCID recipients
(3) and that total splenocytes from prediabetic NOD mice
inhibited this transfer of disease (4), we attempted to
identify the splenocyte subset that mediated this protective effect. We
tested the effects of CD4+,
CD4+CD25+, or
CD4+CD25- splenocytes on
diabetes onset following cotransfer with IIC from inflamed pancreatic
islets (Fig. 1
). Seven of eight NOD.SCID
recipients that received 500,000 IIC from 11-wk-old NOD mice became
diabetic by 36 days post-transfer. Cotransfer of 5 million
CD4+ splenocytes from 6-wk-old NOD mice
significantly delayed the onset of diabetes (p
= 0.0485). This regulatory capacity appeared to be contained primarily
within the CD4+CD25+
subpopulation, as cotransfer of 500,000
CD4+CD25+ splenocytes,
i.e., the fraction of
CD4+CD25+ cells within 5
million CD4+ cells, similarly delayed the onset
of disease (p = 0.0070). Five million
cotransferred CD4+CD25-
splenocytes did not have a significant impact on disease
(p = 0.2828). Our results confirm the
regulatory function of
CD4+CD25+ T cells in this
particular disease model (9). Interestingly, neither
CD4+CD25+ nor total
CD4+ splenocytes blocked the transfer of diabetes
completely. Six of eight mice receiving IIC together with
CD4+CD25+ cells, and four
of four mice receiving IIC together with CD4+
total cells became diabetic by 110 days after transfer. This temporary
effect may be due to a limited regulatory capacity of
CD4+CD25+ T cells to
inhibit the pathogenic IIC or to a loss of
CD4+CD25+ regulatory T cell
function with time. Our studies do not exclude the possibility that a
statistically significant delay in the onset of diabetes might be
achieved with a larger number of
CD4+CD25- splenocytes (>5
million) or a much larger number of recipient mice. However, this
delaying effect would be modest in comparison with that seen with only
500,000 CD4+CD25+ cells. As
previously reported
CD4+CD25- peripheral
lymphocytes depleted of recent thymic emigrants could protect against
the development of diabetes in rats, suggesting that some regulatory
activity is present in the
CD4+CD25- compartment
(14). Similarly, in the BDC2.5 transgenic system the
abrupt onset of diabetes in BDC2.5/RAG2-/- mice
could be delayed with both
CD4+CD25+ and
CD4+CD25- cells from NOD
mice (22). Whether these putative
CD4+CD25- regulatory T
cells are related to
CD4+CD25+ T cells or
represent a separate lineage is not known.
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It has previously been reported that CD4+CD62L+ and CD4+CD45RBlow splenocytes from prediabetic NOD mice could inhibit diabetes transfer using splenocytes from diabetic NOD mice in cotransfer into immune-incompetent NOD.SCID recipients (6, 7, 8), and a possible overlap between CD4+CD25+, CD4+CD62L+, and CD4+CD45RBlow regulatory cells in the NOD mouse has been suggested (5, 10). We therefore analyzed the surface expression of activation/memory markers on CD4+CD25+ splenocytes in 6-wk-old NOD mice. NOD CD4+CD25+ T cells were uniformly CD45RBlow and CD44medium, but heterogeneous for the expression of CD62L (25% CD62L- and 75% CD62L+) and CD69 (85% CD69- and 15% CD69+; data not shown).
We then tested whether CD62L expression on
CD4+CD25+ T cells would
allow a more precise definition of the regulatory splenocyte population
in our adoptive cotransfer model of diabetes. To this end we
transferred 500,000 IIC alone or together with 500,000
CD4+CD25+CD62L+,
CD4+CD25+CD62L-,
or CD4+CD25+ splenocytes
into NOD.SCID recipients (Fig. 2A).
CD4+CD25+ splenocytes
significantly delayed the onset of diabetes (p
= 0.0021).
CD4+CD25+CD62L+
cells similarly delayed the onset of diabetes
(p = 0.0147), whereas
CD4+CD25+
CD62L- splenocytes showed a slight, but
nonsignificant, delay (p = 0.0892). This
demonstrates that in NOD mice
CD4+CD25+ T cells can be
separated into two functionally distinct subpopulation based upon the
expression of a third surface marker.
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The idea of distinguishing regulatory from activated nonregulatory
CD4+CD25+ T cells based on
the expression of other surface markers has been tested in normal mice.
CD4+CD25+CD62L-
and
CD4+CD25+CD62L+
T cells were found to be equally suppressive in vitro (23, 24). However, it remained possible that in NOD mice there exists
a large population of autoantigen-activated conventional
CD4+CD25+ T cells within
the CD62L- subpopulation that might not have
suppressor qualities. Thus, we sorted
CD4+CD25+CD62L+
or
CD4+CD25+CD62L-
NOD splenocytes and cultured them with anti-CD3- and anti-CD28
mAb-coated beads as surrogate APC (21) either alone or
together with CD4+CD25-
splenocytes at decreasing ratios to test their function in vitro. Data
presented in Fig. 2
B show that in contrast to the findings
in vivo, both populations were equally anergic and suppressive in
vitro.
It is possible that this assay is not sensitive enough to detect a mild contamination with nonregulatory T cells that nonetheless may be significant in vivo. In addition, the polyclonal stimulus neglects potential Ag-specific effects. However, an alternative explanation takes into account the specific nature of the CD62L molecule. CD62L (L-selectin) is an adhesion molecule that mediates lymphocyte extravasation through high endothelial venules (HEV) into lymph nodes and Peyer’s patches as well as into chronically inflamed tissues through HEV-like structures (25). We reasoned that the functional difference between CD4+CD25+CD62L- and CD4+CD25+CD62L+ T cells in their capacity to delay diabetes transfer might be due to differential trafficking patterns of the two subpopulations.
CD4+CD25+CD62L+, but not CD62L-, cells express high levels of CCR7
Lymphocyte trafficking through the endothelium is a sequence of events involving adhesion molecules (such as CD62L), chemokine receptors, and integrins. Lymphoid chemokines are critical for trafficking into lymph nodes and within lymphoid compartments, whereas inflammatory chemokines attract lymphocytes into inflamed peripheral tissue (26).
To test whether
CD4+CD25+CD62L+
and
CD4+CD25+CD62L-
splenocytes differ in their chemotactic properties, we analyzed
the expression of chemokine receptors in these subsets using RNase
protection assays (Fig. 3A).
Different expression levels between the two subpopulations were
apparent for CCR7 expression (higher in CD62L+ T
cells) and CCR2, CCR4, and CXCR3 expression (higher in
CD62L- T cells). These bands were quantified by
densitometry (Fig. 3B);
CD4+CD25+CD62L+
cells expressed 3.1-fold higher levels of CCR7 than
CD4+CD25+CD62L-
cells. CCR4, CCR2, and CXCR3 expression levels in
CD4+CD25+CD62L-
cells were 1.9-, 2.8-, and 4.4-fold higher, respectively, than that
expressed on
CD4+CD25+CD62L+
cells. There was no significant difference in the expression levels of
the other chemokine receptors examined. CCR4, CCR8, and CCR5 have been
suggested to be specific for
CD4+CD25+ cells (18, 19). We found that
CD4+CD25+ NOD splenocytes
expressed all these chemokine receptors. While there was no difference
between the expression levels of CCR8 and CCR5 in
CD4+CD25+CD62L+
and
CD4+CD25+CD62L-
cells, the latter subpopulations expressed 1.9-fold higher levels of
CCR4. This suggests that
CD4+CD25+ cells may not be
homogenous in terms of their trafficking properties.
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We then tested whether the differences observed in chemokine
receptor mRNA expression of
CD4+CD25+CD62L+
and
CD4+CD25+CD62L-
splenocytes were reflected in the differential chemotactic activity of
these cells in response to the corresponding chemokine ligands in a
cell migration assay in vitro. In agreement with the chemokine receptor
expression data, migration of
CD4+CD25+CD62L+
cells toward ELC and SLC (ligands for CCR7) was 3.6- and 1.9-fold
higher, respectively, than was migration of
CD4+CD25+CD62L-
cells.
CD4+CD25+CD62L+
cells migrated preferentially to monokine induced by IFN- and
IFN--inducible protein 10 (ligands for CXCR3), and MDC and TARC
(ligands for CCR4; Fig. 4).
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How do these findings relate to the differential outcome in
diabetes development following cotransfer of
CD4+CD25+CD62L-
or
CD4+CD25+CD62+
splenocytes and IIC into immune-incompetent NOD mice? The events
following adoptive transfer of IIC into immune-incompetent NOD mice are
complex. Islet-reactive lymphocytes are believed to be primed in the
pancreatic lymph nodes by APC that present islet Ags (32).
Following activation, islet-reactive lymphocytes home to the pancreas
and initiate -cell destruction. We hypothesize that the specific
adhesion molecule and chemokine receptor expression profile of the
CD4+CD25+CD62L+
cells allows them to more efficiently enter the pancreatic lymph nodes
where they can productively interact with and potentially inhibit the
activation of IIC.
Our data are suggestive, but not conclusive. We have tried to follow the early migration of the transferred cell population using CFSE-labeled cells. However, the nature of the system (difficulties to generate requisite cell numbers) makes it hard to generate appropriate and controlled data. Chemokine receptor knockout mice on an NOD background are not available. Finally, Abs and small molecule inhibitors of chemokine receptors (even if they were available) would not be helpful, as they would unselectively affect both IIC as well as CD4+CD25+ T cells.
Conclusion
CD4+CD25+ splenocytes are composed of two subsets based upon differential expression of CD62L and CCR7. CD4+CD25+ cells that express CD62L and high levels of CCR7 preferentially migrate to lymphoid chemokines, while those that are CD62L- express CCR4, CCR2, and CXCR3 and preferentially migrate toward inflammatory chemokines. CD4+ splenocytes that most efficiently inhibit adoptive transfer of diabetes in cotransfer with IIC are CD4+CD25+CD62L+. This differential chemokine receptor expression and migration pattern of CD4+CD25+CD62L+ compared with CD4+CD25+CD62L- splenocytes might explain why the CD4+CD25+CD62L+ NOD splenocytes delay diabetes upon cotransfer with IIC despite the fact that both subsets are equally suppressive in vitro.
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Acknowledgments |
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Footnotes |
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2 Address correspondence and reprint requests to Dr. C. Garrison Fathman, Stanford University School of Medicine, CCSR Building, Room 2225, 300 Pasteur Drive, Stanford, CA 94305-5166. E-mail address: cfathman{at}stanford.edu
3 Abbreviations used in this paper: DC, dendritic cell; HEV, high endothelial venule; IIC, islet-infiltrating cell; MDC, monocyte-derived chemokine; SLC, secondary lymphoid tissue chemokine; TARC, thymus- and activation-regulated chemokine.
Received for publication May 9, 2002. Accepted for publication July 10, 2002.
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References |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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S. M. Pop, C. P. Wong, Q. He, Y. Wang, M. A. Wallet, K. S. Goudy, and R. Tisch The Type and Frequency of Immunoregulatory CD4+ T-Cells Govern the Efficacy of Antigen-Specific Immunotherapy in Nonobese Diabetic Mice Diabetes, May 1, 2007; 56(5): 1395 - 1402. [Abstract] [Full Text] [PDF]
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M. A. Schneider, J. G. Meingassner, M. Lipp, H. D. Moore, and A. Rot CCR7 is required for the in vivo function of CD4+ CD25+ regulatory T cells J. Exp. Med., April 16, 2007; 204(4): 735 - 745. [Abstract] [Full Text] [PDF]
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J. R. Kocks, A. C. M. Davalos-Misslitz, G. Hintzen, L. Ohl, and R. Forster Regulatory T cells interfere with the development of bronchus-associated lymphoid tissue J. Exp. Med., April 16, 2007; 204(4): 723 - 734. [Abstract] [Full Text] [PDF]
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V. H. Nguyen, R. Zeiser, D. L. daSilva, D. S. Chang, A. Beilhack, C. H. Contag, and R. S. Negrin In vivo dynamics of regulatory T-cell trafficking and survival predict effective strategies to control graft-versus-host disease following allogeneic transplantation Blood, March 15, 2007; 109(6): 2649 - 2656. [Abstract] [Full Text] [PDF]
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 D. O'Mahony, J. C. Morris, C. Quinn, W. Gao, W. H. Wilson, B. Gause, S. Pittaluga, S. Neelapu, M. Brown, T. A. Fleisher, et al. A Pilot Study of CTLA-4 Blockade after Cancer Vaccine Failure in Patients with Advanced Malignancy Clin. Cancer Res., February 1, 2007; 13(3): 958 - 964. [Abstract] [Full Text] [PDF]
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A. Joetham, K. Takada, C. Taube, N. Miyahara, S. Matsubara, T. Koya, Y.-H. Rha, A. Dakhama, and E. W. Gelfand Naturally Occurring Lung CD4+CD25+ T Cell Regulation of Airway Allergic Responses Depends on IL-10 Induction of TGF-beta J. Immunol., February 1, 2007; 178(3): 1433 - 1442. [Abstract] [Full Text] [PDF]
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K. V. Tarbell, L. Petit, X. Zuo, P. Toy, X. Luo, A. Mqadmi, H. Yang, M. Suthanthiran, S. Mojsov, and R. M. Steinman Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice J. Exp. Med., January 22, 2007; 204(1): 191 - 201. [Abstract] [Full Text] [PDF]
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D. Golshayan, S. Jiang, J. Tsang, M. I. Garin, C. Mottet, and R. I. Lechler In vitro-expanded donor alloantigen-specific CD4+CD25+ regulatory T cells promote experimental transplantation tolerance Blood, January 15, 2007; 109(2): 827 - 835. [Abstract] [Full Text] [PDF]
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I. Goldstein, S. Ben-Horin, A. Koltakov, H. Chermoshnuk, V. Polevoy, Y. Berkun, N. Amariglio, and I. Bank {alpha}1beta1 Integrin+ and Regulatory Foxp3+ T Cells Constitute Two Functionally Distinct Human CD4+ T Cell Subsets Oppositely Modulated by TNF{alpha} Blockade J. Immunol., January 1, 2007; 178(1): 201 - 210. [Abstract] [Full Text] [PDF]
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G. M. Venturi, R. M. Conway, D. A. Steeber, and T. F. Tedder CD25+CD4+ Regulatory T Cell Migration Requires L-Selectin Expression: L-Selectin Transcriptional Regulation Balances Constitutive Receptor Turnover J. Immunol., January 1, 2007; 178(1): 291 - 300. [Abstract] [Full Text] [PDF]
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J. H. Lee, S. G. Kang, and C. H. Kim FoxP3+ T Cells Undergo Conventional First Switch to Lymphoid Tissue Homing Receptors in Thymus but Accelerated Second Switch to Nonlymphoid Tissue Homing Receptors in Secondary Lymphoid Tissues J. Immunol., January 1, 2007; 178(1): 301 - 311. [Abstract] [Full Text] [PDF]
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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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B. J. Chen Treg-cell expansion: better to be "naive" Blood, December 15, 2006; 108(13): 3963 - 3964. [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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J.-L. Hillebrands, B. Whalen, J. T. J. Visser, J. Koning, K. D. Bishop, J. Leif, J. Rozing, J. P. Mordes, D. L. Greiner, and A. A. Rossini A Regulatory CD4+ T Cell Subset in the BB Rat Model of Autoimmune Diabetes Expresses Neither CD25 Nor Foxp3 J. Immunol., December 1, 2006; 177(11): 7820 - 7832. [Abstract] [Full Text] [PDF]
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S. Brode, T. Raine, P. Zaccone, and A. Cooke Cyclophosphamide-Induced Type-1 Diabetes in the NOD Mouse Is Associated with a Reduction of CD4+CD25+Foxp3+ Regulatory T Cells J. Immunol., November 15, 2006; 177(10): 6603 - 6612. [Abstract] [Full Text] [PDF]
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E. Yurchenko, M. Tritt, V. Hay, E. M. Shevach, Y. Belkaid, and C. A. Piccirillo CCR5-dependent homing of naturally occurring CD4+ regulatory T cells to sites of Leishmania major infection favors pathogen persistence J. Exp. Med., October 30, 2006; 203(11): 2451 - 2460. [Abstract] [Full Text] [PDF]
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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 J. Immunol., August 1, 2006; 177(3): 1451 - 1459. [Abstract] [Full Text] [PDF]
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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 J. Immunol., August 1, 2006; 177(3): 1552 - 1560. [Abstract] [Full Text] [PDF]
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H. W. Lim, H. E. Broxmeyer, and C. H. Kim Regulation of Trafficking Receptor Expression in Human Forkhead Box P3+ Regulatory T Cells J. Immunol., July 15, 2006; 177(2): 840 - 851. [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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 W.-J. Chae, O. Henegariu, S.-K. Lee, and A. L. M. Bothwell The mutant leucine-zipper domain impairs both dimerization and suppressive function of Foxp3 in T cells PNAS, June 20, 2006; 103(25): 9631 - 9636. [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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H. Waldner, R. A. Sobel, N. Price, and V. K. Kuchroo The Autoimmune Diabetes Locus Idd9 Regulates Development of Type 1 Diabetes by Affecting the Homing of Islet-Specific T Cells J. Immunol., May 1, 2006; 176(9): 5455 - 5462. [Abstract] [Full Text] [PDF]
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 B. Valzasina, S. Piconese, C. Guiducci, and M. P. Colombo Tumor-Induced Expansion of Regulatory T Cells by Conversion of CD4+CD25- Lymphocytes Is Thymus and Proliferation Independent. Cancer Res., April 15, 2006; 66(8): 4488 - 4495. [Abstract] [Full Text] [PDF]
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G. Raimondi, W. J. Shufesky, D. Tokita, A. E. Morelli, and A. W. Thomson Regulated Compartmentalization of Programmed Cell Death-1 Discriminates CD4+CD25+ Resting Regulatory T Cells from Activated T Cells. J. Immunol., March 1, 2006; 176(5): 2808 - 2816. [Abstract] [Full Text] [PDF]
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U. C. Rogner, F. Lepault, M.-C. Gagnerault, D. Vallois, J. Morin, P. Avner, and C. Boitard The Diabetes Type 1 Locus Idd6 Modulates Activity of CD4+CD25+ Regulatory T-Cells Diabetes, January 1, 2006; 55(1): 186 - 192. [Abstract] [Full Text] [PDF]
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K. Siegmund, M. Feuerer, C. Siewert, S. Ghani, U. Haubold, A. Dankof, V. Krenn, M. P. Schon, A. Scheffold, J. B. Lowe, et al. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo Blood, November 1, 2005; 106(9): 3097 - 3104. [Abstract] [Full Text] [PDF]
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C. A. Wysocki, Q. Jiang, A. Panoskaltsis-Mortari, P. A. Taylor, K. P. McKinnon, L. Su, B. R. Blazar, and J. S. Serody Critical role for CCR5 in the function of donor CD4+CD25+ regulatory T cells during acute graft-versus-host disease Blood, November 1, 2005; 106(9): 3300 - 3307. [Abstract] [Full Text] [PDF]
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H. Kitade, M. Kawai, O. Rutgeerts, W. Landuyt, M. Waer, C. Mathieu, and J. Pirenne Early Presence of Regulatory Cells in Transplanted Rats Rendered Tolerant by Donor-Specific Blood Transfusion J. Immunol., October 15, 2005; 175(8): 4963 - 4970. [Abstract] [Full Text] [PDF]
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T. Hiura, H. Kagamu, S. Miura, A. Ishida, H. Tanaka, J. Tanaka, F. Gejyo, and H. Yoshizawa Both Regulatory T Cells and Antitumor Effector T Cells Are Primed in the Same Draining Lymph Nodes during Tumor Progression J. Immunol., October 15, 2005; 175(8): 5058 - 5066. [Abstract] [Full Text] [PDF]
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M. Beyer, M. Kochanek, K. Darabi, A. Popov, M. Jensen, E. Endl, P. A. Knolle, R. K. Thomas, M. von Bergwelt-Baildon, S. Debey, et al. Reduced frequencies and suppressive function of CD4+CD25hi regulatory T cells in patients with chronic lymphocytic leukemia after therapy with fludarabine Blood, September 15, 2005; 106(6): 2018 - 2025. [Abstract] [Full Text] [PDF]
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L.-F. Lu, D. C. Gondek, Z. A. Scott, and R. J. Noelle NF{kappa}B-Inducing Kinase Deficiency Results in the Development of a Subset of Regulatory T Cells, which Shows a Hyperproliferative Activity upon Glucocorticoid-Induced TNF Receptor Family-Related Gene Stimulation J. Immunol., August 1, 2005; 175(3): 1651 - 1657. [Abstract] [Full Text] [PDF]
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Y. Chen, C. Cuda, and L. Morel Genetic Determination of T Cell Help in Loss of Tolerance to Nuclear Antigens J. Immunol., June 15, 2005; 174(12): 7692 - 7702. [Abstract] [Full Text] [PDF]
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 D. T. Nardelli, J. P. Cloute, K. H. K. Luk, J. Torrealba, T. F. Warner, S. M. Callister, and R. F. Schell CD4+ CD25+ T Cells Prevent Arthritis Associated with Borrelia Vaccination and Infection Clin. Vaccine Immunol., June 1, 2005; 12(6): 786 - 792. [Abstract] [Full Text] [PDF]
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S. You, M. Belghith, S. Cobbold, M.-A. Alyanakian, C. Gouarin, S. Barriot, C. Garcia, H. Waldmann, J.-F. Bach, and L. Chatenoud Autoimmune Diabetes Onset Results From Qualitative Rather Than Quantitative Age-Dependent Changes in Pathogenic T-Cells Diabetes, May 1, 2005; 54(5): 1415 - 1422. [Abstract] [Full Text] [PDF]
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I. Suffia*, S. K. Reckling*, G. Salay*, and Y. Belkaid* A Role for CD103 in the Retention of CD4+CD25+ Treg and Control of Leishmania major Infection J. Immunol., May 1, 2005; 174(9): 5444 - 5455. [Abstract] [Full Text] [PDF]
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S. M. Pop, C. P. Wong, D. A. Culton, S. H. Clarke, and R. Tisch Single cell analysis shows decreasing FoxP3 and TGF{beta}1 coexpressing CD4+CD25+ regulatory T cells during autoimmune diabetes J. Exp. Med., April 18, 2005; 201(8): 1333 - 1346. [Abstract] [Full Text] [PDF]
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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. Ermann, P. Hoffmann, M. Edinger, S. Dutt, F. G. Blankenberg, J. P. Higgins, R. S. Negrin, C. G. Fathman, and S. Strober Only the CD62L+ subpopulation of CD4+CD25+ regulatory T cells protects from lethal acute GVHD Blood, March 1, 2005; 105(5): 2220 - 2226. [Abstract] [Full Text] [PDF]
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R. K. Gregg, J. J. Bell, H.-H. Lee, R. Jain, S. J. Schoenleber, R. Divekar, and H. Zaghouani IL-10 Diminishes CTLA-4 Expression on Islet-Resident T Cells and Sustains Their Activation Rather Than Tolerance J. Immunol., January 15, 2005; 174(2): 662 - 670. [Abstract] [Full Text] [PDF]
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M. Afanasyeva, D. Georgakopoulos, D. F. Belardi, D. Bedja, D. Fairweather, Y. Wang, Z. Kaya, K. L. Gabrielson, E. R. Rodriguez, P. Caturegli, et al. Impaired up-regulation of CD25 on CD4+ T cells in IFN-{gamma} knockout mice is associated with progression of myocarditis to heart failure PNAS, January 4, 2005; 102(1): 180 - 185. [Abstract] [Full Text] [PDF]
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S. Liang, P. Alard, Y. Zhao, S. Parnell, S. L. Clark, and M. M. Kosiewicz Conversion of CD4+ CD25- cells into CD4+ CD25+ regulatory T cells in vivo requires B7 costimulation, but not the thymus J. Exp. Med., January 3, 2005; 201(1): 127 - 137. [Abstract] [Full Text] [PDF]
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R. K. Gregg, R. Jain, S. J. Schoenleber, R. Divekar, J. J. Bell, H.-H. Lee, P. Yu, and H. Zaghouani A Sudden Decline in Active Membrane-Bound TGF-{beta} Impairs Both T Regulatory Cell Function and Protection against Autoimmune Diabetes J. Immunol., December 15, 2004; 173(12): 7308 - 7316. [Abstract] [Full Text] [PDF]
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P. A. Taylor, A. Panoskaltsis-Mortari, J. M. Swedin, P. J. Lucas, R. E. Gress, B. L. Levine, C. H. June, J. S. Serody, and B. R. Blazar L-Selectinhi but not the L-selectinlo CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection Blood, December 1, 2004; 104(12): 3804 - 3812. [Abstract] [Full Text] [PDF]
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W. Yang, S. Hussain, Q.-S. Mi, P. Santamaria, and T. L. Delovitch Perturbed Homeostasis of Peripheral T Cells Elicits Decreased Susceptibility to Anti-CD3-Induced Apoptosis in Prediabetic Nonobese Diabetic Mice J. Immunol., October 1, 2004; 173(7): 4407 - 4416. [Abstract] [Full Text] [PDF]
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D. Yadav, V. Judkowski, M. Flodstrom-Tullberg, L. Sterling, W. L. Redmond, L. Sherman, and N. Sarvetnick B7-2 (CD86) Controls the Priming of Autoreactive CD4 T Cell Response against Pancreatic Islets J. Immunol., September 15, 2004; 173(6): 3631 - 3639. [Abstract] [Full Text] [PDF]
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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 J. Immunol., September 1, 2004; 173(5): 2942 - 2951. [Abstract] [Full Text] [PDF]
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N. Giarratana, G. Penna, S. Amuchastegui, R. Mariani, K. C. Daniel, and L. Adorini A Vitamin D Analog Down-Regulates Proinflammatory Chemokine Production by Pancreatic Islets Inhibiting T Cell Recruitment and Type 1 Diabetes Development J. Immunol., August 15, 2004; 173(4): 2280 - 2287. [Abstract] [Full Text] [PDF]
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P. Hoffmann, R. Eder, L. A. Kunz-Schughart, R. Andreesen, and M. Edinger Large-scale in vitro expansion of polyclonal human CD4+CD25high regulatory T cells Blood, August 1, 2004; 104(3): 895 - 903. [Abstract] [Full Text] [PDF]
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S. Mendez, S. K. Reckling, C. A. Piccirillo, D. Sacks, and Y. Belkaid Role for CD4+ CD25+ Regulatory T Cells in Reactivation of Persistent Leishmaniasis and Control of Concomitant Immunity J. Exp. Med., July 19, 2004; 200(2): 201 - 210. [Abstract] [Full Text] [PDF]
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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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K. V. Tarbell, S. Yamazaki, K. Olson, P. Toy, and R. M. Steinman CD25+ CD4+ T Cells, Expanded with Dendritic Cells Presenting a Single Autoantigenic Peptide, Suppress Autoimmune Diabetes J. Exp. Med., June 7, 2004; 199(11): 1467 - 1477. [Abstract] [Full Text] [PDF]
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N. A. Danke, D. M. Koelle, C. Yee, S. Beheray, and W. W. Kwok Autoreactive T Cells in Healthy Individuals J. Immunol., May 15, 2004; 172(10): 5967 - 5972. [Abstract] [Full Text] [PDF]
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V. Viglietta, C. Baecher-Allan, H. L. Weiner, and D. A. Hafler Loss of Functional Suppression by CD4+CD25+ Regulatory T Cells in Patients with Multiple Sclerosis J. Exp. Med., April 5, 2004; 199(7): 971 - 979. [Abstract] [Full Text] [PDF]
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F. J. Clark, R. Gregg, K. Piper, D. Dunnion, L. Freeman, M. Griffiths, G. Begum, P. Mahendra, C. Craddock, P. Moss, et al. Chronic graft-versus-host disease is associated with increased numbers of peripheral blood CD4+CD25high regulatory T cells Blood, March 15, 2004; 103(6): 2410 - 2416. [Abstract] [Full Text] [PDF]
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J. Huehn, K. Siegmund, J. C.U. Lehmann, C. Siewert, U. Haubold, M. Feuerer, G. F. Debes, J. Lauber, O. Frey, G. K. Przybylski, et al. Developmental Stage, Phenotype, and Migration Distinguish Naive- and Effector/Memory-like CD4+ Regulatory T Cells J. Exp. Med., February 2, 2004; 199(3): 303 - 313. [Abstract] [Full Text] [PDF]
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L. A. Stephens, A. N. Barclay, and D. Mason Phenotypic characterization of regulatory CD4+CD25+ T cells in rats Int. Immunol., February 1, 2004; 16(2): 365 - 375. [Abstract] [Full Text] [PDF]
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M.-A. Alyanakian, S. You, D. Damotte, C. Gouarin, A. Esling, C. Garcia, S. Havouis, L. Chatenoud, and J.-F. Bach Diversity of regulatory CD4+T cells controlling distinct organ-specific autoimmune diseases PNAS, December 23, 2003; 100(26): 15806 - 15811. [Abstract] [Full Text] [PDF]
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S. Gregori, N. Giarratana, S. Smiroldo, and L. Adorini Dynamics of Pathogenic and Suppressor T Cells in Autoimmune Diabetes Development J. Immunol., October 15, 2003; 171(8): 4040 - 4047. [Abstract] [Full Text] [PDF]
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S. Fisson, G. Darrasse-Jeze, E. Litvinova, F. Septier, D. Klatzmann, R. Liblau, and B. L. Salomon Continuous Activation of Autoreactive CD4+ CD25+ Regulatory T Cells in the Steady State J. Exp. Med., September 2, 2003; 198(5): 737 - 746. [Abstract] [Full Text] [PDF]
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G. Rajagopalan, Y. C. Kudva, L. Chen, L. Wen, and C. S. David Autoimmune diabetes in HLA-DR3/DQ8 transgenic mice expressing the co-stimulatory molecule B7-1 in the {beta} cells of islets of Langerhans Int. Immunol., September 1, 2003; 15(9): 1035 - 1044. [Abstract] [Full Text] [PDF]
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K. S. Goudy, B. R. Burkhardt, C. Wasserfall, S. Song, M. L. Campbell-Thompson, T. Brusko, M. A. Powers, M. J. Clare-Salzler, E. S. Sobel, T. M. Ellis, et al. Systemic Overexpression of IL-10 Induces CD4+CD25+ Cell Populations In Vivo and Ameliorates Type 1 Diabetes in Nonobese Diabetic Mice in a Dose-Dependent Fashion J. Immunol., September 1, 2003; 171(5): 2270 - 2278. [Abstract] [Full Text] [PDF]
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T. Mizobuchi, K. Yasufuku, Y. Zheng, M. A. Haque, K. M. Heidler, K. Woods, G. N. Smith Jr., O. W. Cummings, T. Fujisawa, J. S. Blum, et al. Differential Expression of Smad7 Transcripts Identifies the CD4+CD45RChigh Regulatory T Cells That Mediate Type V Collagen-Induced Tolerance to Lung Allografts J. Immunol., August 1, 2003; 171(3): 1140 - 1147. [Abstract] [Full Text] [PDF]
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