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CUTTING EDGE |
Abteilung für Immunologie, Medizinische Klinik, Universitätskrankenhaus Eppendorf, Hamburg, Germany
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResults and DiscussionReferences |
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, MIP-1ß, and RANTES were
efficient chemoattractants for Th1 cells, inducing a dose-dependent
transmigration, Th2 cells were not attracted by these chemokines.
Another CC-chemokine, JE/monocyte chemoattractant protein (MCP)-1, and
a CXC-chemokine, stromal cell-derived factor (SDF)-1, exerted
chemotactic effects on both Th1 and Th2 cells, but differences in
sensitivity and the percentage of responding cells were recorded
between both subsets. These results indicate that chemokines play a
distinct role in the regulation of local immune reactions by
influencing the local balance between proinflammatory and
antiinflammatory T cell subsets. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Besides adhesion molecules such as selectins and integrins, chemokines are thought to be involved in the multi step process of extravasation by the triggering of integrins and chemotactic attraction of cell subsets (2, 3). The diversity of chemokines that potentially attract different cell populations makes them interesting candidates for the regulation of effector cell recruitment. Indeed, CC-chemokines especially are inducible and up-regulated in inflammatory lesions, suggesting a role for the recruitment of activated and proinflammatory T cell subsets into these sites.
In vivo, a role for chemokines in B cell migration and germinal center
formation (4), as well as for the colonization of lymphoid and
nonlymphoid tissues of SCID mice by T cells, has been shown (5).
Chemokines such as stromal cell-derived factor
(SDF)3-1 (6), the
recently described dendritic cell chemokine (DC-CK)-1 (7), and liver
and activation-regulated chemokine (LARC) (8) have been shown to
preferentially attract naive T lymphocytes, whereas others such as
RANTES or monocyte chemoattractant protein-1 (MCP-1) were found to act
predominantly on activated/memory stages of T cells (9, 10). In
addition, differential effects on CD4+ vs CD8+
cells were reported for macrophage inflammatory protein (MIP)-1 and
MIP-1ß (11, 12).
Whether chemokines are involved in a differential recruitment of key
effector subsets of T cells such as Th1 and Th2 is largely unknown.
Recently, selective expression of the chemokine receptor CC-chemokine
receptor (CCR)3 has been demonstrated in human Th2 cells (13). Here, we
studied the ability of chemokines to differentially attract Th1 and Th2
cells in a chemotaxis assay. As the representativeness of long term
lines or clones is questionable, we used primary cell populations
generated by cytokine-induced differentiation in vitro (14, 15).
Several members of the CC and CXC subgroups were analyzed. The data
show a selective response of Th1 cells toward MIP-1, MIP-1ß, and
RANTES, whereas other chemokines such as MCP-1 and SDF-1 were
chemoattractant for both Th1 and Th2 cells, although with differing
potency and efficacy.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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Purified recombinant chemokines were obtained from the following
sources: murine MIP-1, MIP-1ß, JE/MCP-1, eotaxin,
CRG-2/interferon-inducible protein-10 (IP-10), MIG, and KC from R&D
Systems (Minneapolis, MN); human RANTES and SDF-1 from Peprotech
(Rocky Hill, NJ); cytokines IL-2, IL-4, and IL-12 as well as
unconjugated or phycoerythrin-/FITC-coupled anti-IFN-
(clone
XMG1.2) and anti-IL-4 (clone 11B11) from PharMingen (San Diego,
CA). mAbs applied in the panning procedure were either used as
supernatants or purified. Hybridomas were obtained from the American
Type Culture Collection (Rockville, MD). Hamster anti-CD28 mAb
(clone 37.51) was a gift of J. P. Allison through E. Schmitt
(University of Mainz, Mainz, Germany). Murine fibronectin was obtained
from Sigma (St. Louis, MO), BSA from Life Technologies (Paisley, U.K.),
and rabbit anti-rat Ig from Dako (Glostrup, Denmark).
Cell preparation and culture
Th1 and Th2 cells were generated as described (1). In short,
CD4+ T cells were purified from peripheral and
mesenteric lymph node cells of 8- to 15-wk-old
specific-pathogen-free-reared female BALB/c mice by panning using
anti-CD8 (53-6.72), anti-CD25 (PC 61 5.3), anti-FcR II/III
(2.4G2), and anti-MAC-1 (M1/70) mAbs and rabbit anti-rat
Ig-coated plates (16). The purified cells were >96% CD4+,
>99% CD3+, and largely (85–95%) of naive phenotype
(L-selectinhigh, CD45RBhigh,
IL-2Rneg). Cells were activated on six-well plates
precoated with 3 µg/ml of anti-CD3 (145-2C11) in RPMI 1640 plus
10% FCS supplemented with either IL-12 (5 ng/ml), IFN- (20 ng/ml),
and anti-IL-4 (1 µg/ml) for generation of Th1 cells, or IL-2 (5
ng/ml), IL-4 (10 ng/ml), and anti-IFN- (2 µg/ml) for Th2
cells, respectively. After 2 days, cells were transferred onto uncoated
plates without a change of medium and cultured for an additional 4 days
to allow the cells to return to a resting state.
Effector cells generated under these conditions express levels of L-selectin and CD45RB comparable with naive cells, increased levels of CD44 and LFA-1, and are predominantly in a resting state as judged by low IL-2R expression (specific fluorescence units 4–8, compared with 20–30 for fully activated CD4+ T cells) and cell size. They actively home in vivo, in contrast to fully activated cells that circulate rather poorly (1, 16, 17).
Intracellular staining of Th1/Th2 subsets was performed after
restimulation on plates precoated with 2 µg/ml of anti-CD3 and
anti-CD28 overnight as previously described (1, 18). Stained cells
were analyzed using a FACScan flow cytometer (Becton Dickinson,
Heidelberg, Germany). In the generated Th1 cell population, 30 to 60%
of the cells produced high amounts of IFN- and no IL-4. In the Th2
cell culture, a significant fraction of cells produced high levels of
IL-4, whereas very few cells contained IFN- (Fig. 1
B). In general, not
all cells in such primary cultures are inducible; the number of
cytokine-producing cells detected seems to be partially dependent on
the conditions of restimulation, among other factors (18, 19).
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For use in the transmigration assay, Th1 and Th2 cells were collected on day 6 and, after removal of dead cells by density centrifugation on 17% isotonic Nycodenz (Nycomed Pharma, Oslo, Norway), resuspended in assay medium (RPMI 1640 plus 0.5% BSA) at 5 x 106 cells/ml. Polyvinylpyrrolidone-free polycarbonate Transwell culture inserts of 6.5 mm diameter and 5 µm pore size (Costar, Cambridge, MA) were coated with 50 µl of distilled water containing 10 µg/ml fibronectin for 1 h in 5% CO2 at 37°C. After removing the liquid, filters were dried for 2 h at 37°C. Either chemokines diluted in assay medium or assay medium alone was added to the lower chamber in a final volume of 600 µl. The filter inserts were placed in the wells, 5 x 105 of either Th1 or Th2 cells were added to the top chamber in a volume of 100 µl, and the chambers were incubated for 1 h in 5% CO2 at 37°C. Cells that transmigrated into the lower chamber were suspended and counted using a Casy TT cell counter (Schärfe System, Reutlingen, Germany). At a minimum, all determinations were performed in triplicate. Statistical analysis was performed using Student’s t test.
For an analysis restricted to the very producers of cytokines, Th1 and
Th2 cells were mixed in a ratio of 1:2 and subjected to a chemotaxis
assay toward either medium or 10 ng/ml MIP-1. The cells from upper
and lower compartments (30 chambers per sample were pooled) were
washed, restimulated with PMA/ionomycin for 5 h, and then the
absolute numbers of IFN or IL-4-producing cells were determined by
intracellular staining.
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Results and Discussion |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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A surprisingly high level of intrinsic migratory activity was
found for resting T effector cells compared with naive
CD4+ T cells. In the absence of chemokines, 5.3
± 2.3% of Th1 cells and 7.9 ± 2.6% of Th2 cells (mean of 12
experiments, range 3–11%) had migrated after 1 h through
fibronectin-coated filters, while freshly isolated CD4+ T
cells showed transmigration below 3% (Fig. 1
A).
Extension of the assay for 4 h resulted in continuous
migration of the effector cell populations with up to 35% of the cells
found in the lower well. In contrast, no additional significant
increase was observed with fresh CD4+ T cells, suggesting
that it is predominantly the small fraction of effector/memory cells
present among lymph node CD4+ cells that migrates
spontaneously. This observation is consistent with the correlation
between migratory capacity and the T cell differentiation stage
demonstrated previously (20, 21).
The differences between fresh CD4+ cells and the effector cell populations were not simply due to different activation states; the used protocol results in largely resting Th1 or Th2 cells, as judged by low IL-2R and high L-selectin expression (16). Moreover, fully activated effector cells displayed a significantly lower migratory capacity than the resting population used here (not shown). This observation indicates that effector cells in this stage are destined to migrate through the tissue much more actively than naive cells.
When the spontaneous migration of Th1 and Th2 cells through
fibronectin-coated filters was compared, clear differences could be
observed (Fig. 1A). In 10 of 12 1-h experiments and
all 4-h experiments, Th2 cells migrated to a higher degree than Th1
cells. After 1 h, from 1.2- to over 2-fold more Th2 than Th1 cells
were found in the lower compartment, the difference being significant
with p < 0.001 (12 experiments). Again, the effect
could not be explained by differences in the activity state, because
IL-2R and L-selectin expression of Th1 and Th2 cells were similar.
Preliminary data point to a supportive role of fibronectin on
spontaneous Th2, but not on Th1 cell transmigration. Studies on
migration through endothelial monolayers revealed similar differences
in the transmigratory activity of Th1 vs Th2 cells (J. T. Siveke
and B. Engelhardt, unpublished data). Thus, differences in the
intrinsic migratory activity between the Th1 and Th2 effector cell
populations might contribute to their differential trafficking in vivo
as reported previously (1).
Selective chemoattraction of Th1 cells by MIP-1, MIP-1ß, and
RANTES
Chemotactic signals are assumed to be of critical importance for
the recruitment of leukocyte subsets. We therefore investigated
possible differences in the response of Th cell subsets toward
different chemokines. Th1 cells were found to display a clear response
to MIP-1 in the transmigration assay. As shown in Figure 2, the directed migration was dose
dependent, reaching a maximum between 1 and 10 ng/ml. Optimal
concentrations of MIP-1 induced more than a threefold increase in
migration of Th1 cells (14–18% cells migrated) compared with
spontaneous migration without MIP-1 of 4 to 7% in three
experiments.
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. Interestingly, at the highest concentrations tested, the
number of transmigrating Th2 cells was consistently diminished below
background levels (Fig. 2). The reduction was significant in all three
experiments (with p < 0.002, p <
0.002, and p < 0.02, respectively).
The differential response of Th1 vs Th2 cells toward MIP-1 was not
dependent on the activation stage; similar responses (albeit at a lower
level) were observed with fully activated Th1/Th2 cell populations
(data not shown).
MIP-1ß had largely similar effects to MIP-1 on Th1 cells.
Migration was highest at 10 ng/ml with detectable chemoattractant
activity at 1 and 100 ng/ml. As for MIP-1, approximately threefold
more cells migrated compared with background.
Previous reports have shown that MIP-1, MIP-1ß, and
RANTES are ligands for murine CCR5 (22). Similar to MIP-1
and MIP-1ß, human RANTES was found to induce a dose-dependent
response in Th1 cells with an optimum response at 10 ng/ml.
In primary effector cell cultures, only a fraction of cells can be
induced to produce cytokine. To confirm that the observed specific
migration indeed applies to cells with a proven cytokine phenotype, we
enumerated cells producing either IFN- (Th1) or IL-4 (Th2) after
migration of a mixed population toward either medium or 10 ng/ml
MIP-1 in the respective compartments. As shown in Figure 3B, the chemotactic response
toward MIP-1 was almost completely restricted to IFN-
producers.
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A, migration of Th1 cells toward MIP-1 could
be completely blocked when 100 ng/ml MIP-1 or MIP-1ß was added to
the upper well. In contrast, migration toward MIP-1ß could be blocked
completely by MIP-1 (not shown). Thus, induced migration toward
MIP-1 and MIP-1ß is due to directed migration rather than to an
increase in random motility of the cells. This directed migration, as
well as the short duration of the assay used in this study, excluded
indirect effects of the chemokines, e.g., by inducing the synthesis of
other soluble factors.
A slight increase in the migration of Th2 cells at concentrations
exceeding 100 ng/ml could be observed for MIP-1ß, in contrast to the
effects of MIP-1 (difference between 1000 ng and control values was
significant with p < 0.001 in three experiments). At
most, this increase was twofold above background but never did reach
levels observed with Th1 cells (Fig. 2). Th2 cells also showed a
slightly increased migration in the intermediate concentration range
(1–100 ng/ml) toward RANTES.
The chemotactic response of Th2 cells to high concentrations of
MIP-1ß, but not to MIP-1, points to differential biologic effects
of these chemokines, although the checkerboard analysis suggested that
both chemokines were competing for the same receptors under these
conditions. In other studies, the two chemokines were found to have
both partly overlapping and partly differing biologic activities in
chemotaxis, activation, or hemopoiesis. Studies of T cells revealed
preferential chemotactic migration of CD8+ T cells toward
MIP-1, and of CD4+ T cells toward MIP-1ß (11, 12). A
unique function of MIP-1 has been demonstrated in vivo (23). These
data point to CCR5 as a good candidate for the selective
chemoattraction of the Th1 subset by MIP-1, MIP-1ß, and RANTES.
The small effects of MIP-1ß (at high concentrations) and of RANTES
(at intermediate concentrations) on Th2 cells both suggest the presence
of other receptors such as CCR1 or CCR3 on Th2 cells. Low receptor
affinity, density, or signaling of the receptors might restrict their
biologic responsiveness in this subset.
The selective expression of CCR3 by human Th2 cells has recently been shown (13). This receptor binds eotaxin and RANTES. The small effects of both RANTES and eotaxin (not shown) on the chemotaxis of Th2 cells support this finding, but predict a rather low expression or function of this receptor among murine Th2 cells.
Both Th1 and Th2 cells are attracted by JE/MCP-1 and
SDF-1 but show qualitative and quantitative
differences in responsiveness.
To test whether other CC-chemokines are involved in a selective
recruitment of Th1 or Th2 cells, JE, the murine homologue of human
MCP-1, was tested in the chemotaxis assay. MCP-1 has been reported to
be a major attractant for CD4+ T cells of
activated/memory phenotype (10, 24), and JE/MCP-1 has also been shown
to bind to a receptor different from that of MIP-1 (25). As shown in
Figure 2, both Th1 and Th2 cells were attracted by JE, yet the
dose-response curve differed between the two populations. Th1 cells
were effectively attracted (threefold higher) only at high
concentrations. Thus, JE is as effective as MIP-1 and MIP-1ß for
Th1 cells but not as potent, because higher levels of chemokines were
required for an optimal response. Th2 cells, on the other hand, were
slightly less efficiently attracted and had a smaller response window
with highest migration between 1 and 10 ng/ml, dropping to baseline
levels at higher concentrations (Fig. 2). In three experiments
performed, the migration of Th2 cells toward JE/MCP-1 at optimal
conditions did not reach the maximal Th1 levels (maximal responses
differed with p < 0.05). Thus, JE/MCP-1 is a
chemoattractant for both populations with a preference for Th1 cells at
high concentrations only.
As mentioned above, CCR3 has been found on human Th2, but not on Th1 cells (13). Eotaxin is a CC-chemokine binding selectively to CCR3. Indeed, we found no effects of eotaxin on the migration of Th1 cells, and its effects on Th2 cells were only very modest (data not shown).
As a classical CXC-chemokine, we tested KC, the suggested murine homologue of human GRO that binds to the mouse IL-8R type B (26). KC was not able to induce a significant increase in the migration of both Th1 and Th2 cells (data not shown), supporting previous reports showing that memory T cells respond to CC-chemokines, rather than to CXC-chemokines such as IL-8 and IP-10 (27). Other CXC-chemokines such as CRG-2 (IP-10) or MIG revealed a weak but significant chemotactic activity for Th1 cells at high concentrations (1000 ng/ml), whereas Th2 cells showed no significant increase in migration (data not shown).
SDF-1, recently described as being a highly efficacious chemokine for
lymphocytes (6), induced the highest migration of all chemokines
tested. At 1000 ng/ml, 15% of Th1 cells and 39% of Th2 cells had
migrated (Fig. 2), while no effects were seen at low concentrations.
Consistently, the response of Th2 cells to SDF-1 at 1000 ng/ml was
higher than that of Th1 cells. Supernatant of the murine bone marrow
stromal cell line MS-5, which contains high amounts of SDF-1 (6),
induced the largest increase in Th1 migration, up to 35% (Fig. 2),
whereas the response of Th2 cells toward MS-5 was similar to their
response toward 1000 ng SDF-1. Whether this difference between Th1
and Th2 cells is indeed due to a differential responsiveness toward
SDF-1, whether additional factors secreted by the stromal cell line are
the cause, or whether the very high migration of Th2 cells had already
reached a maximal value limited by the type of assay must still be
determined.
In our study, SDF-1 had the strongest effect of all chemokines
tested and attracted Th1 as well as Th2 cells. In contrast to the
inflammation-related CC-chemokines, it has been suggested that SDF-1
plays a role in recirculation and immune surveillance, rather than in
inflammation, because of its wide expression in many tissues
independent of inflammatory stimuli (28, 29) and because of the
preferential expression of its receptor CXCR4 on naive T cells (30).
SDF-1 was the only tested chemokine that exerted a stronger effect
on Th2 than on Th1 cells. Previously, we found that Th2 cells had a
greater preference for trafficking into the spleen (1). Preliminary
observations also indicate that the migration within this tissue
differs between Th1 and Th2 cells (our unpublished observations). It is
tempting to suggest that SDF-1 might play a role in these migratory
properties of Th2 cells.
The results of this work show a preferential responsiveness of the proinflammatory Th1 subset toward CC-chemokines. Many studies have demonstrated the eminent importance of the Th1 and Th2 subsets on the outcome of immune responses. The selective attraction of Th1 cells by CC-chemokines that are produced in sites of inflammation can be considered as a new mechanism that contributes to the local balance between these subsets and shapes the immune reaction within inflamed tissue. Our data suggest selective differences in the expression or function of chemokine receptors among Th subsets.
Interestingly, recent reports show a secretion of CC-chemokines in Th1
cells, but not in Th2 cells in humans (31, 32). Together, these
findings could indicate the existence of a positive feedback loop that
links the production of MIP-1 with a chemotactic response toward
MIP-1 in Th1 cells.
In conclusion, this study provides evidence for a selective control of T effector cell recruitment mediated by chemokines. It confirms conclusions drawn from previous studies on in vivo migration and the selective use of adhesion molecules among Th1/Th2 cells by establishing an additional molecular level on which specific trafficking of lymphocytes can be regulated.
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Acknowledgments |
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Footnotes |
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2 Address correspondence and reprint requests to Dr. Alf Hamann, Abteilung für Immunologie, Medizinische Klinik, Universitätskrankenhaus Eppendorf, 20246 Hamburg, Germany. E-mail address:
3 Abbreviations used in this paper: SDF, stromal cell-derived factor; MCP-1, monocyte chemoattractant protein 1; MIP, macrophage inflammatory protein; CCR, CC-chemokine receptor; IP-10, IFN-inducible protein-10.
Received for publication September 9, 1997. Accepted for publication November 13, 1997.
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References |
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TopAbstractIntroductionMaterials and MethodsResults and DiscussionReferences |
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and is inhibited by transforming growth factor-ß. Eur. J. Immunol. 24:793.[Medline]
and in interleukin-4-expressing cells. Eur. J. Immunol. 24:1097.[Medline]
, MIP-1ß, and RANTES is associated with a type 1 immune response. J. Immunol. 157:3598.[Abstract]
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M. Odendahl, H. Mei, B. F. Hoyer, A. M. Jacobi, A. Hansen, G. Muehlinghaus, C. Berek, F. Hiepe, R. Manz, A. Radbruch, et al. Generation of migratory antigen-specific plasma blasts and mobilization of resident plasma cells in a secondary immune response Blood, February 15, 2005; 105(4): 1614 - 1621. [Abstract] [Full Text] [PDF]
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M. Apostolaki and N. A. Williams Nasal Delivery of Antigen with the B Subunit of Escherichia coli Heat-Labile Enterotoxin Augments Antigen-Specific T-Cell Clonal Expansion and Differentiation Infect. Immun., July 1, 2004; 72(7): 4072 - 4080. [Abstract] [Full Text] [PDF]
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M. A. Holsti, T. Chitnis, R. J. Panzo, R. T. Bronson, H. Yagita, M. H. Sayegh, and A. O. Tzianabos Regulation of Postsurgical Fibrosis by the Programmed Death-1 Inhibitory Pathway J. Immunol., May 1, 2004; 172(9): 5774 - 5781. [Abstract] [Full Text] [PDF]
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 J. D. van Buul and P. L. Hordijk Signaling in Leukocyte Transendothelial Migration Arterioscler Thromb Vasc Biol, May 1, 2004; 24(5): 824 - 833. [Abstract] [Full Text]
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H. Xu, A. Manivannan, H.-R. Jiang, J. Liversidge, P. F. Sharp, J. V. Forrester, and I. J. Crane Recruitment of IFN-{gamma}-Producing (Th1-Like) Cells into the Inflamed Retina In Vivo Is Preferentially Regulated by P-Selectin Glycoprotein Ligand 1:P/E-Selectin Interactions J. Immunol., March 1, 2004; 172(5): 3215 - 3224. [Abstract] [Full Text] [PDF]
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K. Muller, S. Bischof, F. Sommer, M. Lohoff, W. Solbach, and T. Laskay Differential Production of Macrophage Inflammatory Protein 1{gamma} (MIP-1{gamma}), Lymphotactin, and MIP-2 by CD4+ Th Subsets Polarized In Vitro and In Vivo Infect. Immun., November 1, 2003; 71(11): 6178 - 6183. [Abstract] [Full Text] [PDF]
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 M. Crittenden, M. Gough, K. Harrington, K. Olivier, J. Thompson, and R. G. Vile Expression of Inflammatory Chemokines Combined with Local Tumor Destruction Enhances Tumor Regression and Long-term Immunity Cancer Res., September 1, 2003; 63(17): 5505 - 5512. [Abstract] [Full Text] [PDF]
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V. Veckman, M. Miettinen, S. Matikainen, R. Lande, E. Giacomini, E. M. Coccia, and I. Julkunen Lactobacilli and streptococci induce inflammatory chemokine production in human macrophages that stimulates Th1 cell chemotaxis J. Leukoc. Biol., September 1, 2003; 74(3): 395 - 402. [Abstract] [Full Text] [PDF]
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 S. Senechal, P. de Nadai, N. Ralainirina, A. Scherpereel, H. Vorng, P. Lassalle, A.-B. Tonnel, A. Tsicopoulos, and B. Wallaert Effect of Diesel on Chemokines and Chemokine Receptors Involved in Helper T Cell Type 1/Type 2 Recruitment in Patients with Asthma Am. J. Respir. Crit. Care Med., July 15, 2003; 168(2): 215 - 221. [Abstract] [Full Text] [PDF]
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K. Sasaki, T. Tsuji, T. Jinushi, J. Matsuzaki, T. Sato, K. Chamoto, Y. Togashi, T. Koda, and T. Nishimura Differential regulation of VLA-2 expression on Th1 and Th2 cells: a novel marker for the classification of Th subsets Int. Immunol., June 1, 2003; 15(6): 701 - 710. [Abstract] [Full Text] [PDF]
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J. R. Bleharski, V. Kiessler, C. Buonsanti, P. A. Sieling, S. Stenger, M. Colonna, and R. L. Modlin A Role for Triggering Receptor Expressed on Myeloid Cells-1 in Host Defense During the Early-Induced and Adaptive Phases of the Immune Response J. Immunol., April 1, 2003; 170(7): 3812 - 3818. [Abstract] [Full Text] [PDF]
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M. Kleinhans, A. Tun-Kyi, M. Gilliet, M. E. Kadin, R. Dummer, G. Burg, and F. O. Nestle Functional expression of the eotaxin receptor CCR3 in CD30+ cutaneous T-cell lymphoma Blood, February 15, 2003; 101(4): 1487 - 1493. [Abstract] [Full Text] [PDF]
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 D. Huang, M. Tani, J. Wang, Y. Han, T. T. He, J. Weaver, I. F. Charo, V. K. Tuohy, B. J. Rollins, and R. M. Ransohoff Pertussis Toxin-Induced Reversible Encephalopathy Dependent on Monocyte Chemoattractant Protein-1 Overexpression in Mice J. Neurosci., December 15, 2002; 22(24): 10633 - 10642. [Abstract] [Full Text] [PDF]
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E. Roman, E. Miller, A. Harmsen, J. Wiley, U. H. von Andrian, G. Huston, and S. L. Swain CD4 Effector T Cell Subsets in the Response to Influenza: Heterogeneity, Migration, and Function J. Exp. Med., October 7, 2002; 196(7): 957 - 968. [Abstract] [Full Text] [PDF]
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K. Suetomi, D. Rojo, and J. Navarro Identification of a Signal Transduction Switch in the Chemokine Receptor CXCR1 J. Biol. Chem., August 23, 2002; 277(35): 31563 - 31566. [Abstract] [Full Text] [PDF]
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 R. Abdi, R. N. Smith, L. Makhlouf, N. Najafian, A. D. Luster, H. Auchincloss Jr., and M. H. Sayegh The Role of CC Chemokine Receptor 5 (CCR5) in Islet Allograft Rejection Diabetes, August 1, 2002; 51(8): 2489 - 2495. [Abstract] [Full Text] [PDF]
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A. E. Hauser, G. F. Debes, S. Arce, G. Cassese, A. Hamann, A. Radbruch, and R. A. Manz Chemotactic Responsiveness Toward Ligands for CXCR3 and CXCR4 Is Regulated on Plasma Blasts During the Time Course of a Memory Immune Response J. Immunol., August 1, 2002; 169(3): 1277 - 1282. [Abstract] [Full Text] [PDF]
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 J. N. Kline, K. Kitagaki, T. R. Businga, and V. V. Jain Treatment of established asthma in a murine model using CpG oligodeoxynucleotides Am J Physiol Lung Cell Mol Physiol, July 1, 2002; 283(1): L170 - L179. [Abstract] [Full Text] [PDF]
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G. F. Debes, U. E. Hopken, and A. Hamann In Vivo Differentiated Cytokine-Producing CD4+ T Cells Express Functional CCR7 J. Immunol., June 1, 2002; 168(11): 5441 - 5447. [Abstract] [Full Text] [PDF]
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O. Fahy, S. Senechal, J. Pene, A. Scherpereel, P. Lassalle, A.-B. Tonnel, H. Yssel, B. Wallaert, and A. Tsicopoulos Diesel Exposure Favors Th2 Cell Recruitment by Mononuclear Cells and Alveolar Macrophages from Allergic Patients by Differentially Regulating Macrophage-Derived Chemokine and IFN-{gamma}-Induced Protein-10 Production J. Immunol., June 1, 2002; 168(11): 5912 - 5919. [Abstract] [Full Text] [PDF]
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B. D. Medoff, A. Sauty, A. M. Tager, J. A. Maclean, R. N. Smith, A. Mathew, J. H. Dufour, and A. D. Luster IFN-{gamma}-Inducible Protein 10 (CXCL10) Contributes to Airway Hyperreactivity and Airway Inflammation in a Mouse Model of Asthma J. Immunol., May 15, 2002; 168(10): 5278 - 5286. [Abstract] [Full Text] [PDF]
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A. Y. Karulin, M. D. Hesse, H. C. Yip, and P. V. Lehmann Indirect IL-4 Pathway in Type 1 Immunity J. Immunol., January 15, 2002; 168(2): 545 - 553. [Abstract] [Full Text] [PDF]
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 G. Adamus, M. Manczak, and M. Machnicki Expression of CC Chemokines and Their Receptors in the Eye in Autoimmune Anterior Uveitis Associated with EAE Invest. Ophthalmol. Vis. Sci., November 1, 2001; 42(12): 2894 - 2903. [Abstract] [Full Text] [PDF]
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H. P. Jones, L. M. Hodge, K. Fujihashi, H. Kiyono, J. R. McGhee, and J. W. Simecka The Pulmonary Environment Promotes Th2 Cell Responses After Nasal-Pulmonary Immunization with Antigen Alone, but Th1 Responses Are Induced During Instances of Intense Immune Stimulation J. Immunol., October 15, 2001; 167(8): 4518 - 4526. [Abstract] [Full Text] [PDF]
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M. A. Olszewski, G. B. Huffnagle, T. R. Traynor, R. A. McDonald, D. N. Cook, and G. B. Toews Regulatory Effects of Macrophage Inflammatory Protein 1{alpha}/CCL3 on the Development of Immunity to Cryptococcus neoformans Depend on Expression of Early Inflammatory Cytokines Infect. Immun., October 1, 2001; 69(10): 6256 - 6263. [Abstract] [Full Text] [PDF]
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G. Iezzi, D. Scheidegger, and A. Lanzavecchia Migration and Function of Antigen-Primed Nonpolarized T Lymphocytes in Vivo J. Exp. Med., April 16, 2001; 193(8): 987 - 994. [Abstract] [Full Text] [PDF]
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B. Qiu, K. A. Frait, F. Reich, E. Komuniecki, and S. W. Chensue Chemokine Expression Dynamics in Mycobacterial (Type-1) and Schistosomal (Type-2) Antigen-Elicited Pulmonary Granuloma Formation Am. J. Pathol., April 1, 2001; 158(4): 1503 - 1515. [Abstract] [Full Text] [PDF]
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D. Huang, J. Wang, P. Kivisakk, B. J. Rollins, and R. M. Ransohoff Absence of Monocyte Chemoattractant Protein 1 in Mice Leads to Decreased Local Macrophage Recruitment and Antigen-Specific T Helper Cell Type 1 Immune Response in Experimental Autoimmune Encephalomyelitis J. Exp. Med., March 19, 2001; 193(6): 713 - 726. [Abstract] [Full Text] [PDF]
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A. M. Schmidt and D. M. Stern Chemokines on the Rise : MCP-1 and Restenosis Arterioscler Thromb Vasc Biol, March 1, 2001; 21(3): 297 - 299. [Full Text] [PDF]
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R. E. Wiley, K. Palmer, B. U. Gajewska, M. R. Stampfli, D. Alvarez, A. J. Coyle, J.-C. Gutierrez-Ramos, and M. Jordana Expression of the Th1 Chemokine IFN-{{gamma}}-Inducible Protein 10 in the Airway Alters Mucosal Allergic Sensitization in Mice J. Immunol., February 15, 2001; 166(4): 2750 - 2759. [Abstract] [Full Text] [PDF]
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H. Yamagami, T. Matsumoto, N. Fujiwara, T. Arakawa, K. Kaneda, I. Yano, and K. Kobayashi Trehalose 6,6'-Dimycolate (Cord Factor) of Mycobacterium tuberculosis Induces Foreign-Body- and Hypersensitivity-Type Granulomas in Mice Infect. Immun., February 1, 2001; 69(2): 810 - 815. [Abstract] [Full Text] [PDF]
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X. Shang, B. Qiu, K. A. Frait, J. S. Hu, J. Sonstein, J. L. Curtis, B. Lu, C. Gerard, and S. W. Chensue Chemokine Receptor 1 Knockout Abrogates Natural Killer Cell Recruitment and Impairs Type-1 Cytokines in Lymphoid Tissue during Pulmonary Granuloma Formation Am. J. Pathol., December 1, 2000; 157(6): 2055 - 2063. [Abstract] [Full Text] [PDF]
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M. A. Olszewski, G. B. Huffnagle, R. A. McDonald, D. M. Lindell, B. B. Moore, D. N. Cook, and G. B. Toews The Role of Macrophage Inflammatory Protein-1{alpha}/CCL3 in Regulation of T Cell-Mediated Immunity to Cryptococcus neoformans Infection J. Immunol., December 1, 2000; 165(11): 6429 - 6436. [Abstract] [Full Text] [PDF]
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K. A. Papadakis, J. Prehn, V. Nelson, L. Cheng, S. W. Binder, P. D. Ponath, D. P. Andrew, and S. R. Targan The Role of Thymus-Expressed Chemokine and Its Receptor CCR9 on Lymphocytes in the Regional Specialization of the Mucosal Immune System J. Immunol., November 1, 2000; 165(9): 5069 - 5076. [Abstract] [Full Text] [PDF]
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Z.-Z. Pan, L. Parkyn, A. Ray, and P. Ray Inducible lung-specific expression of RANTES: preferential recruitment of neutrophils Am J Physiol Lung Cell Mol Physiol, October 1, 2000; 279(4): L658 - L666. [Abstract] [Full Text] [PDF]
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S. Zhang, N. W. Lukacs, V. A. Lawless, S. L. Kunkel, and M. H. Kaplan Cutting Edge: Differential Expression of Chemokines in Th1 and Th2 Cells Is Dependent on Stat6 But Not Stat4 J. Immunol., July 1, 2000; 165(1): 10 - 14. [Abstract] [Full Text] [PDF]
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S. K. Bromley, D. A. Peterson, M. D. Gunn, and M. L. Dustin Cutting Edge: Hierarchy of Chemokine Receptor and TCR Signals Regulating T Cell Migration and Proliferation J. Immunol., July 1, 2000; 165(1): 15 - 19. [Abstract] [Full Text] [PDF]
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K. J. Maloy, C. Burkhart, T. M. Junt, B. Odermatt, A. Oxenius, L. Piali, R. M. Zinkernagel, and H. Hengartner Cd4+ T Cell Subsets during Virus Infection: Protective Capacity Depends on Effector Cytokine Secretion and on Migratory Capability J. Exp. Med., June 19, 2000; 191(12): 2159 - 2170. [Abstract] [Full Text] [PDF]
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P. G. Andres, P. L. Beck, E. Mizoguchi, A. Mizoguchi, A. K. Bhan, T. Dawson, W. A. Kuziel, N. Maeda, R. P. MacDermott, D. K. Podolsky, et al. Mice with a Selective Deletion of the CC Chemokine Receptors 5 or 2 Are Protected from Dextran Sodium Sulfate-Mediated Colitis: Lack of CC Chemokine Receptor 5 Expression Results in a NK1.1+ Lymphocyte-Associated Th2-Type Immune Response in the Intestine J. Immunol., June 15, 2000; 164(12): 6303 - 6312. [Abstract] [Full Text] [PDF]
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M. C. Bosco, A. Rapisarda, S. Massazza, G. Melillo, H. Young, and L. Varesio The Tryptophan Catabolite Picolinic Acid Selectively Induces the Chemokines Macrophage Inflammatory Protein-1{alpha} and -1{beta} in Macrophages J. Immunol., March 15, 2000; 164(6): 3283 - 3291. [Abstract] [Full Text] [PDF]
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B. Clissi, D. D'Ambrosio, J. Geginat, L. Colantonio, A. Morrot, N. W. Freshney, J. Downward, F. Sinigaglia, and R. Pardi Chemokines Fail to Up-Regulate {beta}1 Integrin-Dependent Adhesion in Human Th2 T Lymphocytes J. Immunol., March 15, 2000; 164(6): 3292 - 3300. [Abstract] [Full Text] [PDF]
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E. H. Tran, E. N. Prince, and T. Owens IFN-{gamma} Shapes Immune Invasion of the Central Nervous System Via Regulation of Chemokines J. Immunol., March 1, 2000; 164(5): 2759 - 2768. [Abstract] [Full Text] [PDF]
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A. Matsukawa, N. W. Lukacs, T. J. Standiford, S. W. Chensue, and S. L. Kunkel Adenoviral-Mediated Overexpression of Monocyte Chemoattractant Protein-1 Differentially Alters the Development of Th1 and Th2 Type Responses In Vivo J. Immunol., February 15, 2000; 164(4): 1699 - 1704. [Abstract] [Full Text] [PDF]
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N.-H. Cho, S.-Y. Seong, M.-S. Huh, T.-H. Han, Y.-S. Koh, M.-S. Choi, and I.-S. Kim Expression of Chemokine Genes in Murine Macrophages Infected with Orientia tsutsugamushi Infect. Immun., February 1, 2000; 68(2): 594 - 602. [Abstract] [Full Text] [PDF]
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 M. Castro, D. D. Chaplin, M. J. Walter, and M. J. Holtzman Could Asthma Be Worsened by Stimulating the T-helper Type 1 Immune Response? Am. J. Respir. Cell Mol. Biol., February 1, 2000; 22(2): 143 - 146. [Full Text]
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Philip. L. Shields, C. M. Morland, M. Salmon, S. Qin, S. G. Hubscher, and D. H. Adams Chemokine and Chemokine Receptor Interactions Provide a Mechanism for Selective T Cell Recruitment to Specific Liver Compartments Within Hepatitis C-Infected Liver J. Immunol., December 1, 1999; 163(11): 6236 - 6243. [Abstract] [Full Text] [PDF]
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S. Yamagami, D. Miyazaki, S. J. Ono, and M. R. Dana Differential Chemokine Gene Expression in Corneal Transplant Rejection Invest. Ophthalmol. Vis. Sci., November 1, 1999; 40(12): 2892 - 2897. [Abstract] [Full Text] [PDF]
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S. Mukai, J. Kjargaard, S. Shu, and G. E. Plautz Infiltration of Tumors by Systemically Transferred Tumor-Reactive T Lymphocytes Is Required for Antitumor Efficacy Cancer Res., October 1, 1999; 59(20): 5245 - 5249. [Abstract] [Full Text] [PDF]
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T. Kawai, M. Seki, K. Hiromatsu, J. W. Eastcott, G. F. M. Watts, M. Sugai, D. J. Smith, S. A. Porcelli, and M. A. Taubman Selective Diapedesis of Th1 Cells Induced by Endothelial Cell RANTES J. Immunol., September 15, 1999; 163(6): 3269 - 3278. [Abstract] [Full Text] [PDF]
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C. Abbal, P. Jourdan, T. Hori, J. Bousquet, H. Yssel, and J. Pene TCR-mediated activation of allergen-specific CD45RO+ memory T lymphocytes results in down-regulation of cell-surface CXCR4 expression and a strongly reduced capacity to migrate in response to stromal cell-derived factor-1 Int. Immunol., September 1, 1999; 11(9): 1451 - 1462. [Abstract] [Full Text] [PDF]
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S. W. Chensue, K. S. Warmington, E. J. Allenspach, B. Lu, C. Gerard, S. L. Kunkel, and N. W. Lukacs Differential Expression and Cross-Regulatory Function of RANTES During Mycobacterial (Type 1) and Schistosomal (Type 2) Antigen-Elicited Granulomatous Inflammation J. Immunol., July 1, 1999; 163(1): 165 - 173. [Abstract] [Full Text] [PDF]
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J. Galon, C. Sudarshan, S. Ito, D. Finbloom, and J. J. O'Shea IL-12 Induces IFN Regulating Factor-1 (IRF-1) Gene Expression in Human NK and T Cells J. Immunol., June 15, 1999; 162(12): 7256 - 7262. [Abstract] [Full Text] [PDF]
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S. K. Bliss, A. J. Marshall, Y. Zhang, and E. Y. Denkers Human Polymorphonuclear Leukocytes Produce IL-12, TNF-{alpha}, and the Chemokines Macrophage-Inflammatory Protein-1{alpha} and -1{beta} in Response to Toxoplasma gondii Antigens J. Immunol., June 15, 1999; 162(12): 7369 - 7375. [Abstract] [Full Text] [PDF]
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B. Vester, K. Muller, W. Solbach, and T. Laskay Early Gene Expression of NK Cell-Activating Chemokines in Mice Resistant to Leishmania major Infect. Immun., June 1, 1999; 67(6): 3155 - 3159. [Abstract] [Full Text] [PDF]
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M. J. Dobrzanski, J. B. Reome, and R. W. Dutton Therapeutic Effects of Tumor-Reactive Type 1 and Type 2 CD8+ T Cell Subpopulations in Established Pulmonary Metastases J. Immunol., June 1, 1999; 162(11): 6671 - 6680. [Abstract] [Full Text] [PDF]
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S. Sur, J. S. Wild, B. K. Choudhury, N. Sur, R. Alam, and D. M. Klinman Long Term Prevention of Allergic Lung Inflammation in a Mouse Model of Asthma by CpG Oligodeoxynucleotides J. Immunol., May 15, 1999; 162(10): 6284 - 6293. [Abstract] [Full Text] [PDF]
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S. L. Kunkel Promiscuous Chemokine Receptors and Their Redundant Ligands Play an Enigmatic Role during HIV-1 Infection Am. J. Respir. Cell Mol. Biol., May 1, 1999; 20(5): 859 - 860. [Full Text]
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K. S. Warmington, L. Boring, J. H. Ruth, J. Sonstein, C. M. Hogaboam, J. L. Curtis, S. L. Kunkel, I. R. Charo, and S. W. Chensue Effect of C-C Chemokine Receptor 2 (CCR2) Knockout on Type-2 (Schistosomal Antigen-Elicited) Pulmonary Granuloma Formation : Analysis of Cellular Recruitment and Cytokine Responses Am. J. Pathol., May 1, 1999; 154(5): 1407 - 1416. [Abstract] [Full Text] [PDF]
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H. A. Doyle and J. W. Murphy Role of the C-C Chemokine, TCA3, in the Protective Anticryptococcal Cell-Mediated Immune Response J. Immunol., April 15, 1999; 162(8): 4824 - 4833. [Abstract] [Full Text] [PDF]
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N. Suzuki, A. Nakajima, S. Yoshino, K. Matsushima, H. Yagita, and K. Okumura Selective accumulation of CCR5+ T lymphocytes into inflamed joints of rheumatoid arthritis Int. Immunol., April 1, 1999; 11(4): 553 - 559. [Abstract] [Full Text] [PDF]
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R. L. Rabin, M. K. Park, F. Liao, R. Swofford, D. Stephany, and J. M. Farber Chemokine Receptor Responses on T Cells Are Achieved Through Regulation of Both Receptor Expression and Signaling J. Immunol., April 1, 1999; 162(7): 3840 - 3850. [Abstract] [Full Text] [PDF]
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L. M. Bradley, V. C. Asensio, L.-K. Schioetz, J. Harbertson, T. Krahl, G. Patstone, N. Woolf, I. L. Campbell, and N. Sarvetnick Islet-Specific Th1, But Not Th2, Cells Secrete Multiple Chemokines and Promote Rapid Induction of Autoimmune Diabetes J. Immunol., March 1, 1999; 162(5): 2511 - 2520. [Abstract] [Full Text] [PDF]
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F. Liao, R. L. Rabin, C. S. Smith, G. Sharma, T. B. Nutman, and J. M. Farber CC-Chemokine Receptor 6 Is Expressed on Diverse Memory Subsets of T Cells and Determines Responsiveness to Macrophage Inflammatory Protein 3{alpha} J. Immunol., January 1, 1999; 162(1): 186 - 194. [Abstract] [Full Text] [PDF]
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A. J. Wagers, C. M. Waters, L. M. Stoolman, and G. S. Kansas Interleukin 12 and Interleukin 4 Control T Cell Adhesion to Endothelial Selectins through Opposite Effects on {alpha}1,3-fucosyltransferase VII Gene Expression J. Exp. Med., December 21, 1998; 188(12): 2225 - 2231. [Abstract] [Full Text] [PDF]
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A. Zingoni, H. Soto, J. A. Hedrick, A. Stoppacciaro, C. T. Storlazzi, F. Sinigaglia, D. D'Ambrosio, A. O'Garra, D. Robinson, M. Rocchi, et al. Cutting Edge: The Chemokine Receptor CCR8 Is Preferentially Expressed in Th2 But Not Th1 Cells J. Immunol., July 15, 1998; 161(2): 547 - 551. [Abstract] [Full Text] [PDF]
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M. Taguchi, D. Sampath, T. Koga, M. Castro, D. C. Look, S. Nakajima, and M. J. Holtzman Patterns for RANTES Secretion and Intercellular Adhesion Molecule 1 Expression Mediate Transepithelial T Cell Traffic Based on Analyses In Vitro and In Vivo J. Exp. Med., June 15, 1998; 187(12): 1927 - 1940. [Abstract] [Full Text] [PDF]
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