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The Journal of Immunology, 2000, 164: 3460-3464.
Copyright © 2000 by The American Association of Immunologists

CUTTING EDGE

Cutting Edge: Identification of the Orphan Receptor G-Protein-Coupled Receptor 2 as CCR10, a Specific Receptor for the Chemokine ESkine1 ,2

David I. Jarmin*, Miriam Rits*, Dalena Bota*, Norma P. Gerard*, Gerard J. Graham{dagger}, Ian Clark-Lewis{ddagger} and Craig Gerard3,*

* Ina Sue Perlmutter Laboratory, Children’s Hospital, Harvard Medical School, Boston, MA 02115; {dagger} The Beatson Institute for Cancer Research, Cancer Research Campaign Laboratories, Glasgow, Scotland, United Kingdom; and {ddagger} Biomed Research Center, University of British Columbia, Vancouver, British Columbia, Canada


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
A number of orphan G-protein coupled receptors (GPR) have been reported as putative chemokine receptors. One previously reported orphan receptor is an incomplete PCR clone, called GPR2. Here we report the cloning of full-length human (h)GPR2 and mouse (m)GPR2 cDNAs, and the identification of GPR2 as a receptor for a novel CC chemokine called ESkine. hGPR2 is expressed at high levels in testis and small intestine, and at lower levels in other tissues. mGPR2 was expressed at high levels in small intestine, colon, lymph nodes, and Peyer’s patches and at lower levels in thymus and spleen. Stimulation of L1.2/hGPR2 transfectants with hESkine induced their migration and resulted in intracellular calcium mobilization. These results provide evidence that GPR2 is a specific receptor for ESkine. We propose that GPR2 be renamed as CCR10. The expression pattern of mGPR2/CCR10 suggests that it may play a role in the homing/trafficking of leukocytes within intestinal and lymphoid environments.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
Chemokines are believed to play a critical role in the trafficking, homing, and activation of leukocytes, as well as mediating a wide range of other functions (1). At present they are classified into four separate subfamilies on the basis of the spacing of conserved cysteine residues within their N-terminal regions: these are known as the CC, CXC, C, and CX3C subfamilies (1, 2). Chemokines mediate their functions through their binding to specific cell-surface receptors, and these receptors are members of the seven transmembrane spanning G protein-coupled-receptor (GPR)4 superfamily. To date, this interaction appears subfamily specific, and receptors have been identified for CC chemokines (CCR1–9), CXC (CXCR1–5), C (XCR1), and CX3C (CX3CR1) (1, 2, 3, 4, 5, 6). In addition to the known chemokine/receptor pairings, a number of orphan GPRs have been reported (7, 8, 9). Several chemokines have also been identified, for which the specific receptor(s) is not yet known (10, 11, 12).

One orphan receptor previously reported as having homology to known chemokine receptors is GPR2 (13). The GPR2 gene cloned previously from human genomic DNA lacked an initiating methionine, suggesting the existence of an intron in the 5' region. No positive data on the expression of GPR2 has been reported to date. Here we report that GPR2 is a specific receptor for the novel CC chemokine known as ESkine/ALP/ILC/CTACK (14, 15, 16, 17). ESkine induced chemotaxis of the murine pre-B cell line L1.2, when transfected with human (h)GPR2. Moreover, calcium flux assays demonstrated that hGPR2 and mouse (m)GPR2 transfectants responded to human or murine ESkine. Here we also report the low-level constitutive expression of GPR2 RNA in a variety of tissues and, in particular, higher levels of mGPR2 RNA expression in the intestine, colon, lymph node, Peyer’s patches, spleen, and thymus. Previous reports have indicated that those chemokines and their receptors (namely EBI1-ligand chemokine (ELC)/secondary lymphoid tissue chemokine (SLC)/CCR7, liver- and activation-regulated chemokine (LARC)/CCR6, and thymus-expressed chemokine (TECK)/CCR9), whose expression is relatively lymphoid restricted, appear to play critical roles in the homing and localization of leukocytes (18, 19, 20). Therefore, we speculate that GPR2 may also play a similar role. Using the current nomenclature rules for chemokine receptors, we propose that GPR2 be designated as CCR10.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
Cloning and sequencing of human and mouse GPR2 cDNAs

The full-length cDNA for hGPR2 was cloned from a CEMx 174 cell line (T cell/B cell hybrid) cDNA library, while the mGPR2 cDNA was cloned from a Peyer’s patch cDNA library. The cDNA libraries were constructed using the Superscript plasmid kit (Life Technologies, Grand Island, NY) according to the manufacturer’s instructions. The cDNA libraries were screened with 32P-labeled PCR-derived probe fragments encoding the 5' regions of hGPR2 and mGPR2 (human, 5'-GTTTCCTGGGCCATTAC-3' and 5'-ACAGCGTCGTTGGCCTTC-3'; mouse, 5'-GTCTCCTGGGGACTTTAC-3' and 5[pime]-GCTGAAAGAAAGCGCAGG-3'). The murine probe sequence was derived from an incomplete cDNA clone derived from a murine Th1 cDNA library (our unpublished data), whose sequence was homologous to the clone previously reported (13). Positive cDNA inserts were subcloned into the pcDNA 3 vector (Stratagene, La Jolla, CA) (human, EcoRI and XbaI; mouse, NotI and XbaI) and sequenced fully.

Chemokines and cells

Chemokines were purchased from PeproTech (Rocky Hill, NJ) or R&D Systems (Minneapolis, MN). Mouse and human ESkine were chemically synthesized as previously described (14). hGPR2 and mGPR2 were transfected into the murine pre-B cell line L1.2 by electroporation, and stable transfectants were obtained after G418 selection, as described (21).

Northern blot analysis

Multiple tissue Northern blots (Clontech Laboratories, Palo Alto, CA) were probed with a 32P-labeled 5' hGPR2-specific DNA probe, according to the suppliers instructions. Total RNA from 4- to 8-wk-old BALB/c mouse tissues were stored in RNA Later (Ambion, Austin, TX) before their extraction using the RNAqueous kit (Ambion). Next, 15 µg of each sample was electrophoresed on a denaturing formaldehyde-agarose gel and blotted onto Hybond N membranes (Amersham Pharmacia Biotech, Piscataway, NJ). The membranes were prehybridized using an SDS/phosphate buffer before hybridization with a 32P-labeled 5' mGPR2-specific DNA probe, as described (22). After washing, the blots were exposed to BioMax MR film using BioMax MS intensifying screens (Eastman Kodak, Rochester, NJ).

Chemotaxis and calcium mobilization

Calcium mobilization studies were performed on untransfected L1.2 cells, hGPR2/L1.2 transfectants, or mGPR2 transfectants loaded with fura-2AM (Molecular Probes, Eugene, OR), as previously described (21). A 2-ml aliquot of cells, containing 4 x 106 cells, was used for each analysis. For pertussis toxin sensitivity, cells were stimulated for 2 h with 100 ng/ml pertussis toxin (Sigma, St. Louis, MO), and the cells were then washed twice with RPMI 1640/1% FBS and then used in mobilization studies. Chemotaxis assays were also performed on untransfected L1.2 cells, hGPR2/L1.2 transfectants, or mGPR2 transfectants in Costar 5.0-µm 24-well cluster transwells (Corning, Corning, NY) as described (21). The number of migrating cells was determined by comparison against a standard curve derived from a dilution series of a known number of cells, and the number of migrated cells was expressed as a percentage of the total number of input cells.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
Comparison of the hGPR2 sequence to known chemokine receptors suggests that this orphan receptor may be a putative chemokine receptor. We examined the expression of mGPR2 RNA in various mouse tissues and determined that it was expressed at low levels in the thymus. This data prompted us to further characterize GPR2.

Cloning of full-length hGPR2 and mGPR2 cDNAs

Expression of mGPR2 RNA in the thymus suggested that hGPR2 would be expressed in human T cells. Therefore, we screened a CEMx 174 cell cDNA library and identified several GPR2-like clones. The nucleic sequence of one of these clones encoded an additional 8 aa at the amino terminus, compared with the previously published sequence of the hGPR2 gene (13) (Fig. 1GoA). In this report, it was speculated that there was an exon in the 5' terminal region of hGPR2, and our data supports this conclusion.



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  		FIGURE 1. A, Alignment of the predicted amino acid sequences of human and mouse GPR2. Transmembrane domains (TM) are outlined with lines above the corresponding amino acids. The eight additional N-terminal amino acids are indicated with a bold line. B, Schematic of mGPR2 cDNA clones. Two forms of mGPR2 are shown. Potential exons are indicated above boxes

 
Further analysis of mGPR2 RNA expression revealed a striking level of expression in Peyer’s patches (see below, and Fig. 2GoB). Therefore, we constructed a cDNA library from murine Peyer’s patches. Two murine clones were identified and sequenced. Conceptual translation of one of the cDNA clones revealed that the encoded protein was 8 aa longer than that previously reported in the cloning of the human genomic GPR2 clone (13). Fig. 1GoA shows an alignment of the predicted amino acid sequences for the hGPR2 and mGPR2 proteins. These appear to be 86% identical at the level of amino acid sequence. The second clone was incomplete as it lacked an initiating methionine, but it also had an additional 465 bp at the 3' end with a classical poly(A)+ tail. The first clone represents a full-length cDNA, composed of at least 3 exons. The second clone represents an incomplete cDNA with an alternative 3' region. Fig. 1GoB shows a schematic of the structure of the two mouse clones. The hGPR2 gene has previously been reported to be localized to chromosome 17q21, next to a human homologue for the Drosophila enhancer of zeste gene (13, 23).



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  		FIGURE 2. Analysis of hGPR2 and mGPR2 RNA expression. A, Membranes with poly(A)+ RNA from the indicated human tissues were hybridized with a 5' hGPR2 probe. Following exposure, blots were stripped and loading levels confirmed with a hß-actin probe. B, Total RNA from the indicated mouse tissues was hybridized with a mGPR2 probe. Blots were also stripped and loading levels confirmed with a hß-actin probe.

 
Analysis of the expression of hGPR2 and mGPR2

The expression of hGPR2 and mGPR2 RNA in various mouse and human tissues was investigated using Northern blot analysis of either human poly(A)+ RNA or mouse total RNA (Fig. 2Go). Analysis of hGPR2 showed a high level of expression in the adult testis and small intestine (Fig. 2GoA). In addition, relatively high levels of expression were detected in fetal lung and fetal kidney. Weaker expression was also observed in many other adult tissues including spleen, thymus, lymph node, colon, heart, ovary, peripheral blood lymphocytes, and spinal cord. The primary transcript size was ~1.4 kb in size, but a second ~2 kb transcript was also visible in most of the same tissues. These transcripts are of similar sizes to the two forms of mGPR2, suggesting that they represent alternatively spliced forms of hGPR2. In contrast to the high levels observed in human testis, mGPR2 expression was not detected in testis. However, high levels of expression were observed in small intestine, colon, lymph node, and Peyer’s patches (Fig. 2GoB). In addition, weak expression was observed in spleen and thymus. This appeared to be a single transcript of ~1.4 kb. Longer exposure of murine tissue blots revealed very faint expression levels in other tissues (such as spinal cord and ovary), as well as very faint expression of a second larger size transcript visible in Peyer’s patches and small intestine. The relevance of the discrepancy observed between the high level of expression in human testis and the apparent absence of any expression in murine testis is unclear; however, this may simply reflect the different analysis using the more sensitive poly(A)+ vs total RNA or that species differences may exist per se. The observation that GPR2 is expressed at moderate to strikingly high levels in lymphoid, secondary lymphoid, and intestinal tissues is of particular interest, given the known importance of chemokines and their receptors in homing and trafficking of leukocytes. It has been previously speculated that CCR9, CCR7, and CCR6 may form a second CC chemokine receptor subfamily (4), as their expression is relatively restricted to lymphoid and intestinal tissues (20, 24, 25). Like GPR2, these receptors also share a common structural feature in that their coding sequences are interrupted by introns.

ESkine induces migration of L1.2 cells transfected with GPR2

To investigate the potential of known chemokines to function as specific ligands for GPR2, we tested 18 chemokines (see Fig. 3GoA) for their ability to induce migration of GPR2-expressing L1.2 cell transfectants in chemotaxis assays. Only the addition of human ESkine (hESkine) resulted in the dose-dependent chemotaxis of hGPR2/L1.2 cells, relative to untransfected L1.2 cells (Fig. 3GoB). This migration of hGPR2/L1.2 cells in response to hESkine began at around 10–30 nM and was maximal at ~300 nM.



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  		FIGURE 3. Migration assays. A, Chemokines tested in migration assays. B, hESkine-induced migration of L1.2 cells transfected with hGPR2. Mean values of duplicate measurements are shown; bars, SD. Data shown is representative of three separate experiments.

 
ESkine induces calcium mobilization of GPR2-expressing L1.2 cells

We next investigated the ability of ESkine to mobilize intracellular calcium in GPR2-expressing L1.2 cells. The addition of 100 nM hESkine to hGPR2/L1.2 cells resulted in a significant calcium flux, and this response was dose dependent down to at least 1 nM (Fig. 4GoA), although a 10-nM dose appeared to be as effective as 100 nM. The addition of 100 nM SLC to hGPR2-expressing L1.2 cells (which express endogenous CCR7) also resulted in a significant mobilization (Fig. 4Go). Murine ESkine was also able to induce a strong calcium flux in mGPR2-expressing L1.2 cells (Fig. 4GoB), as well as in hGPR2/L1.2 cells (data not shown). The addition of 100 nM hESkine or mESkine resulted in desensitization of hGPR2/L1.2 cells to a second stimulus of ESkine of the same dose (Fig. 4GoC). The addition of SLC did not result in the desensitization of hGPR2/L1.2 cells to a subsequent hESkine stimulation and vice versa (Fig. 4GoD). The response of hGPR2 to hESkine was also pertussis toxin sensitive (Fig. 4GoE).



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  		FIGURE 4. ESkine-induced mobilization of intracellular calcium in L1.2 cells stably expressing GPR2. A, Dose response of hGPR2/L1.2 cells to hESkine (top three traces). L1.2 cells expressing hGPR2 treated with SLC as a positive control and untransfected L1.2 cells were stimulated with 100 nM hESkine (bottom trace). B, mGPR2/L1.2 cells and untransfected L1.2 cells were stimulated with 100 nM mESkine. C, hGPR2/L1.2 cells were stimulated with 100 nM of either hESkine or mESkine, followed by a second identical stimulation. D, Desensitization experiments. hGPR2/L1.2 cells were stimulated with 100 nM SLC followed by a second stimulation of 100 nM hESkine (top trace) or vice versa (bottom trace). E, Pertussis toxin-sensitivity. hGPR2/L1.2 cells either previously treated with 100 ng/ml pertussis toxin (PTX) (bottom trace) or left untreated (top trace) were stimulated with 100 nM Eskine. Arrows indicate the time of the additions. Un.L1.2, Untransfected L1.2 control cells.

 
Taken together, the data we report herein strongly support the conclusion that GPR2 is a specific receptor for the novel CC chemokine ESkine, and that this occurs cross-species in both human and murine systems. Currently, 10 CC chemokine receptors have been designated, and we propose that GPR2 be redesignated as CCR10, according to the guidelines established for chemokine nomenclature at the 1997 Gordon Conference on Chemokines. We are currently further investigating the nature of the cells expressing GPR2 and how this relates to ESkine expression/function. Interestingly, a large number of ESkine-like expressed sequence tags that are derived from epidermal tissues have been identified; therefore, it is likely that the skin is a major source of ESkine expression. Indeed, during the preparation of this manuscript, ESkine was independently isolated as CTACK and shown to preferentially attract skin homing CLA+ memory T cells (17). However, in addition to CLA+ T cells, ESkine is also functional on activated (but not naive) CD4+ T cells (14). We have been unable to demonstrate the expression of mGPR2 in murine skin, either by Northern blot analysis or by RT-PCR (data not shown). However, this does not preclude the expression of low levels of GPR2 in a rare circulating population of cells, such as CLA+ memory T cells. Therefore, the pairing of GPR2 with ESkine is an intriguing one, particularly given the highly unusual nature of the ligand as recently reported (14, 17) and the strong lymphoid and intestinal expression observed for GPR2 as reported herein. Although ESkine was the only chemokine that seemed to function as a specific ligand for GPR2, we cannot exclude the fact that additional novel ligands for GPR2 are likely to exist, and indeed it is also likely that additional receptors exist for ESkine. Interestingly, although ESkine is highly divergent from other CC chemokines, it is most highly homologous to LARC and TECK, the ligands for CCR6 and CCR9, respectively (14). Both CCR6 and CCR9 are expressed in lymphoid tissues (24, 20), and, in addition, CCR9 is selectively expressed on intestinal homing T lymphocytes and mucosal lymphocytes. Hopefully, the exact role of CCR10/GPR2 and ESkine will become more evident following further characterization of the ESkine ligand, identification of the cell types expressing GPR2 and responding to ESkine, and by the generation of mice lacking the CCR10/GPR2 gene.


   Footnotes
 
1 This work was supported in part by a grant from The Wellcome Trust, U.K. (053125; to D.I.J.), National Institutes of Health Grant HL39579 (to C.G.), and by the Rubenstein/Cable Fund at the Perlmutter Laboratory. Back

2 The sequences presented in this article have been submitted to GenBank under accession numbers AF215981 (hCCR10), AF215982, and AF215983 (mCCR10). Back

3 Address correspondence and reprint requests to Dr. Craig Gerard, Ina Sue Perlmutter Laboratory, Enders Suite 144, Children’s Hospital, 320 Longwood Avenue, Boston, MA 02115. E-mail address: Back

4 Abbreviations used in this paper: GPR, G-protein-coupled receptor, h, human; m, mouse; SLC, secondary lymphoid-tissue chemokine, ELC, EBI1-ligand chemokine; LARC, liver- and activation-regulated chemokine; TECK, thymus-expressed chemokine. Back

Received for publication December 13, 1999. Accepted for publication February 2, 2000.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
 References
 

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