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CUTTING EDGE |
*
DNAX Research Institute, Palo Alto, CA 94304;
Department of Dermatology, University of Düsseldorf, Düsseldorf, Germany;
Schering Plough, Laboratory for Immunological Research, Dardilly, France; and
§
Instituto Nacional de la Nutrición Salvador Zubirán, México City, México
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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and IL-1ß. CCR10 is not expressed by keratinocytes and is
instead expressed by melanocytes, dermal fibroblasts, and dermal
microvascular endothelial cells. CCR10 was also detected in T cells as
well as in skin-derived Langerhans cells. Taken together, these
observations suggest a role for this novel ligand/receptor pair in both
skin homeostasis as well as a potential role in inflammatory
responses. |
Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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Here, we report that the previously orphan G protein-coupled receptor-2 (GPR-2)4 binds CCL27. Furthermore, we explored the expression pattern of this ligand/receptor pair in normal and inflamed skin. Our results suggest both a homeostatic and an inflammatory role for CCL27/CCR10 in the skin.
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Materials and Methods |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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Full-length human CCR10 (GPR-2) was cloned from a cDNA library generated from a human B cell EBV-positive tumor cell line (B103) using a 1064-bp probe amplified from human genomic DNA. This fragment was generated by PCR using the partial sequence of CCR10 (GPR-2) as reported by Marchese et al. (8). The sequence of full-length human GPR-2 has been deposited in GenBank under accession number AF208237. To generate stable transfectants, full-length expression constructs were made in BAF/3 cells. Human CCR10 (GPR-2) was cloned into the retroviral vector, pMX-CD8-myc. Transfectants underwent selection in G418 and were further enriched by FACS-sorting using an anti-myc Ab (PharMingen, San Diego).
Calcium mobilization assays
To identify the CCL27 receptor, we tested a panel of known human (CCR1, 2, 3, 4, 5, 6, 7, 8, 9; XCR1; CX3CR; CXCR1, 2, 3, 4, 5) chemokine and orphan (STRL33, GPR-15, GPR-2) GPCR transfectants for signaling using a calcium mobilization assay as described previously (9). Mouse CCL27 was obtained from R&D Systems (Minneapolis, MN), and human CCL27 was chemically synthesized by Gryphon Sciences (South San Francisco, CA).
Transwell chemotaxis assay
The transwell chemotaxis assays were performed using 106 BAF/3-hCCR10(GPR-2) transfectant or parental cells as previously described (4).
Cell isolation and cell culture
Human primary epidermal keratinocytes, dermal fibroblasts,
melanocytes, and dermal microvascular endothelial cells were purchased
from Clonetics (San Diego, CA) and cultured in keratinocyte,
fibroblast, melanocyte, or endothelial cell growth medium (Clonetics,
San Diego, CA). Cells were treated with TNF- (10 ng/ml)/IL-1ß (5
ng/ml), IFN-
(20 ng/ml), IL-4 (50 ng/ml), IL-10 (100 ng/ml) (R&D
Systems), or left untreated. The epidermal 
T cell line, 7-17,
was kindly provided by Richard Boismenu (The Scripps Institute, La
Jolla, CA) and cultured as described (10). Epidermal
T cells were left untreated or stimulated with Con A, TNF-
(10 ng/ml)/IL-1ß (5 ng/ml), for 6 or 18 h. Generation of
dendritic cells either from cord blood CD34+
hemopoietic progenitor cells or from peripheral blood monocytes was
performed as described (11). Human skin-derived Langerhans
cells (LC) were isolated form normal skin of patients undergoing
plastic surgery (12). Enrichment of LC was achieved as
described (12). PBMCs were isolated using standard
techniques, and T cell enrichment was performed using T cell enrichment
columns (R&D Systems).
Biopsy samples
Six-millimeter punch biopsies were taken, after obtaining informed consent, from either lesional skin of patients with psoriasis (n = 21), atopic dermatitis (n = 10), or cutaneous lupus erythematosus (n = 10), or from normal (n = 10) healthy individuals. Skin samples were immediately frozen in liquid nitrogen and stored at -80°C. This study was approved by local ethics committees.
Real-time quantitative PCR (TaqMan) analysis of CCL27 and CCR10 mRNA expression
RNA from both homogenized skin samples or human cells was extracted using RNA STAT 60 according to the manufacturer’s protocol (Tel-Test, Friedensburg, TX). Four micrograms of RNA were treated with DNase I (Boehringer Mannheim, Mannheim, Germany) and reverse transcribed with oligo dT14–18 (Life Technologies, Gaithersburg, MD) and random hexamer primers (Promega, Madison, WI) using standard protocols. cDNA was diluted to a final concentration of 10 ng/µl. cDNA was analyzed for the expression of human CCL27 and CCR10 (GPR-2) genes by the fluorogenic 5'-nuclease PCR assay (13) using a Perkin-Elmer ABI Prism 7700 Sequence Detection System (Perkin-Elmer, Foster City, CA). Briefly, 10 µl cDNA (100 ng) were amplified in the presence of 12.5 µl TaqMan universal master mix (Perkin-Elmer), 0.625 µl gene-specific TaqMan probe, 0.5 µl gene-specific forward and reverse primers, and 0.5 µl water. As an internal positive control, 0.125 µl 18S RNA-specific TaqMan probe and 0.125 µl 18S RNA-specific forward and reverse primers were added to each reaction. Specific primers and probes for CCL27, CCR10, and the other chemokine receptors measured were obtained from Perkin-Elmer. Samples underwent the following stages: stage 1, 50°C for 2 min; stage 2, 95°C for 10 min; and stage 3, 95°C for 15 s followed by 60°C for 1 min. Stage 3 was repeated 40 times. Gene-specific PCR products were measured by means of an ABI PRISM 7700 Sequence Detection System (Perkin-Elmer) continuously during 40 cycles. Standard curves for CCL27 and CCR10 expression were generated amplifying 10-fold serial dilutions of known quantities of CCL27 and CCR10 plasmid DNA. Quantification of target gene expression was obtained using sequence detector system software (Perkin-Elmer). Human cDNA libraries used in this study were generated as described previously (1, 4, 14, 15). For analyses using cDNA libraries, a human GAPDH-specific primer/probe pair was used as internal positive control.
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Results |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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shows the sequence of a
clone of human GPR-2, which was established from a cDNA library
prepared from the 103 human B cell line. Comparison with the original
published sequence (8) indicates that the first 8 aa were
missing from the NH2 terminus of the original
sequence (Fig. 1).
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, A and C show
that both human and mouse CCL27 induced a specific calcium flux in the
transfectants but not the parental BAF/3 cells, indicating that CCL27
binds GPR-2. Furthermore, CCL27 induced a strong chemotactic response
in GPR-2 transfectants but not on the parental cells (Fig. 2B). Mouse CCL27 desensitized the response induced by human
CCL27 and vice versa (Fig. 2C) demonstrating that they
recognize the same receptor. BAF/3 cells are known to express CXCR4
endogenously, so we also tested the ligand of this receptor,
CXCL12/SDF-1, and observed the expected specific calcium flux in
both the transfectants and the parental line. However, the latter
response could not be desensitized by CCL27 in the transfectants,
indicating that CXCL12 and CCL27 act through different chemokine
receptors (Fig. 2C). Taken together, these results indicate
that GPR-2 is a receptor for CCL27. Therefore, we have renamed this
receptor CCR10, following the established chemokine receptor
nomenclature. No other chemokine from a panel of 35 known human
chemokines gave a response like CCL27 in the CCR10 transfectants (data
not shown). Thus, CCR10 appears to be a specific CCL27 receptor. As
mentioned above, transfectants of the cDNA clone encoding the short
version (lacking the first 8 aa; Fig. 1
) of CCR10 did not respond to
CCL27, suggesting that the amino terminus of CCR10 may be important for
either receptor translation, stability, transportation to the cell
surface, or direct ligand binding.
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Given that secreted CCL27 is mainly expressed in skin, we investigated
the expression of CCR10 and CCL27 in more detail in skin-related
tissues including tissue samples from patients with psoriasis, atopic
dermatitis, and cutaneous lupus erythematosus. To this end, we prepared
cDNA from total RNA derived from these tissues that we then used for
quantitative real-time RT-PCR analyses. We observed that CCL27 is
constitutively and markedly expressed in normal or inflamed human skin
(Fig. 3A). No significant
difference in CCL27 expression using real-time quantitative PCR was
observed between normal (n = 10) vs lesional skin from
either psoriatic (n = 21), atopic dermatitis
(n = 10), or lupus erythematosus patients
(n = 10). We then analyzed the expression of hCCR10 in
these samples (Fig. 3B) and observed uniformly low
expression, which is not significantly up-regulated in any of the
different inflammatory skin conditions. We also studied the expression
of both CCL27 and CCR10 in various cellular components of the skin
(Fig. 3C). CCL27 is exclusively expressed by human primary
keratinocytes, although its expression is markedly up-regulated by
IL-1ß and TNF-. Interestingly, IL-1ß/TNF--induced CCL27 mRNA
expression was down-regulated by additional IL-10 treatment (Fig. 3C). In contrast to CCL27, CCR10 is not expressed by
keratinocytes (Fig. 3C) but is instead constitutively
expressed in human primary melanocytes, dermal fibroblasts, and dermal
microvascular endothelial cells. It also appears to be up-regulated in
those cells upon induction with IL-1ß and TNF- (Fig. 3C). We also studied its expression levels in cDNA derived
from PBMCs, T cells, and dendritic cells (Fig. 3D). CCR10 is
expressed in PBMCs, T cells, and LC, but not in either
CD34+ hemopoietic progenitor-derived or
monocyte-derived dendritic cells.
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Discussion |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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C).
Interestingly, CCR10 expression was detected in skin as well as in
several other tissues including small intestine, colon, brain, lung,
liver, and testes (data not shown). CCL27 has at least two forms
(6), but only one bears a signal peptide and is the form
associated with predominant skin expression (3, 4). At
this point, we do not know if the other intracellular forms of CCL27
bind CCR10 or if the latter receptor has any role in the physiology of
the intracellular forms of CCL27. Given the predominant and selective
expression of the secreted form of CCL27 in the skin (3, 4) by keratinocytes (Fig. 3C), it was surprising to
find that CCR10 is expressed in various organs. This observation
suggests that either CCL27 may be expressed in these tissues by a
restricted cellular component under specific inflammatory or other
pathogenic conditions, or there exists another ligand (which is either
not a chemokine or not a known chemokine) for CCR10 that could be
expressed in these tissues.
We focused our studies on the expression of CCR10 and CCL27 in human
skin samples. In agreement with the discrete expression pattern of
CCL27, we found CCR10 expressed in various normal cellular components
of the skin including melanocytes, dermal fibroblasts, and dermal
microvascular endothelial cells. CCR10 expression is induced in these
cells by TNF- and IL-1ß, suggesting that CCL27 may play a role in
the organization of cutaneous cellular components during inflammation.
It is possible that CCL27/CCR10 may play a role in wound repair.
Keratinocytes do not express CCR10, suggesting that CCL27/CCR10
represent a mechanism by which keratinocytes control the migration
and/or differentiation of other cellular components of the skin in
either normal or inflammatory conditions.
CCL27 is strongly expressed in both normal and inflamed skin. This
suggests a homeostatic role as discussed above. CCR10 was also detected
in both normal and diseased skin but at lower levels. This is
consistent with other chemokine receptors, which, in contrast to
chemokine ligands, do not represent abundant transcripts in the
expressing cells. Lastly, we should consider the contribution of CCR10
expressed by T cells, because we first identified that CCL27
preferentially chemoattracts CLA+ T cells
(4). Our data (Fig. 3) are consistent with the presence of
CCR10 in a small population of peripheral blood T cells, as we
predicted from our previous studies (4). Future
experiments will aim at exploring its role in T cells. In conclusion,
we have identified a novel chemokine receptor that is likely to be
involved in both normal homeostasis as well as in inflammatory
conditions of the skin.
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Note Added in Proof. |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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Acknowledgments |
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Footnotes |
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2 B.H. and W.W. contributed equally to this paper.
3 Address correspondence and reprint requests to Dr. Albert Zlotnik, Department of Immunobiology, DNAX Research Institute, 901 California Avenue, Palo Alto, CA 94303-1104. E-mail address:
4 Abbreviations used in this paper: GPR, G protein-coupled receptor; LC, Langerhans cell.
Received for publication December 23, 1999. Accepted for publication February 2, 2000.
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionNote Added in Proof.References |
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and MIP-3ß. J. Immunol. 158:1033.[Abstract]
-locus chemokine (ILC), which is located on chromosome 9p13 and a potential homologue of a CC chemokine encoded by Molluscum contagiosum virus. FEBS Lett. 460:544.[Medline]
T cells: implications for the recruitment of inflammatory cells to damaged epithelia. J. Immunol. 157:985.[Abstract]
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