Abstract
The paradigm for tissue specific homing of leukocytes is the “area code” hypothesis, which predicts that a specific combination of adhesive interactions and chemokine signals from the endothelium directs leukocyte migration into specific tissue sites. This area code hypothesis has been supported by studies from previous HLDA workshops where endothelial specific cell antigens have been studied. Similarly, a clear haematopoietic "stem cell code" comprising the chemokine SDF-1 (CXCL12) and the adhesion receptor VCAM-1 (CD106) has been shown to contribute to the stem cell niche within bone marrow [1]. HLDA 7 included a section devoted to stem cell antigens, which began to define additional antigens important in these processes. During the course of HLDA 8 we have extended these observations to determine whether a more global stromal address code defined by fibroblasts, exists in variety of different tissues [2]. The stromal cell section in HLDA 8 was designed to complement the malignant cell, endothelial cell, and stem cell/progenitor cell sections. Seven new CD numbers were assigned to antibodies included in this section at the HLDA 8 Workshop meeting held during December 2004.
1. Introduction
1.1. What are stromal cells?
Two broad historical definitions of stromal cells exist. The first is that they are cells of mesenchymal origin that are non-epithelium, non-endothelium, and non-haematopoietic. The second is that they are the cells within the stroma and therefore include fibroblasts, endothelial cells, and tissue resident leukocytes. Within both these definitions, some stromal cells, particularly leukocytes and endothelial cells, have been covered by previous HLDA workshops. However, fibroblasts have not been previously covered and as a consequence it is these cells that have been the focus of the stromal cell section in HLDA8.
1.2. What is a fibroblast?
The most abundant cells of the stroma are fibroblasts, which are responsible for the synthesis and remodelling of extracellular matrix components. In addition, their ability to produce and respond to growth factors allows reciprocal interactions with other stromal cell types, and with adjacent epithelial and endothelial structures. As a consequence, fibroblasts play a critical role during tissue development and homeostasis, and are often described as having a “sentinel” or “landscaping” function. Moreover, these functions contribute to the pathology of many diseases either directly for example by overproduction of matrix components during fibrosis and/or indirectly by influencing the behaviour of neighbouring cell types. In particular, it is now well recognized that fibroblasts and their secreted products are critical in tumour development and the progression of inflammatory diseases [3-7].
1.3. Not all fibroblasts are the same
Fibroblasts are a diverse cell type and display clear topographic differentiation and positional memory that is transcriptionally imprinted [8,9]. Despite this heterogeneity there are very few selective markers that allow clear discrimination between fibroblast subtypes. What is known is that fibroblasts are extremely versatile connective tissue cells and display a remarkable capacity to differentiate into other members of the connective tissue family including cartilage, bone, adipocyte, and smooth muscle cells. Further, not all fibroblasts are mesodermal in origin. For example, fibroblasts in the head and neck region are derived from the neural crest (ectoderm). Even within a single tissue there is growing evidence that fibroblasts are not a homogeneous population, but exist as subsets of cells, much like tissue macrophages and dendritic cells [10,11], It is likely that connective tissue contains a mixture of distinct fibroblast lineages with mature fibroblasts existing side by side with immature fibroblasts (often called mesenchymal fibroblasts) that are capable of differentiating into other connective tissue cells. Tantalizing evidence now suggests that as is the case for endothelial cells, fibroblast precursors (termed fibrocytes) circulate in peripheral blood. These cells share many properties of bone marrow stromal stem cells and are capable of differentiating into several cell lineages. This diversity in phenotype and function that characterizes fibroblasts from different anatomical sites may play a significant role in the intrinsic susceptibility of different organs to inflammatory insults. It may also provide the molecular basis for the well described but as yet poorly understood clinical finding that relapses in chronic inflammation are often tissue and site specific. Furthermore, recent studies have shown that thymic fibroblasts play an important role in early T cell development, providing a molecular explanation for long standing observations that destruction of the cephalic neural crest results in retarded lymphoid development in the thymus, as well as producing craniofacial and cardiac defects [3].
A critical advance to this field will be to identify and characterize fibroblast subsets, and to determine the relative contribution of these different subsets to tissue homeostasis and disease progression in diseases such as chronic inflammation and cancer. Therefore, the aims of the stromal cell section in HLDA 8 were:
Identify fibroblast specific antibodies (or at least those with expression mainly limited to fibroblasts).
Identify antibodies that can discriminate between fibroblasts from different sites.
Identify antibodies that can discriminate between normal tissue fibroblasts from one site and diseased tissue (fibroblasts) from the same site.
2. Methods
Antibodies were solicited from scientists in the field as well as open recruitment during the period January 2001 to June 2004. This resulted in 62 potential antibodies being assigned to the HLDA8 stromal cell section. These 62 antibodies were screened by immunohistochemistry of frozen sections of tonsil, synovium, liver, and skin as well as by flow cytometry of peripheral blood and tonsil lymphocytes. The aim of the screen was to identify those antibodies that recognized epitopes that were relatively restricted to stromal cells (endothelium, epithelium, and fibroblasts) and were not expressed on leucocytes. In some cases where expression was confined to monocytes (CD14 positive) and/or tissue infiltrating leucocytes and not any other peripheral blood leucocytes, these antibodies were considered for further evaluation as there is now accumulating evidence that some fibroblasts can be derived from a circulating peripheral blood monocytes [12]. From the 62 antibodies submitted (Table 1), 18 antibodies plus 2 extra antibodies 80324 and 80448 from the stem cell section of HLDA 8, were selected and subjected to further screens by three independent laboratories in the United Kingdom (CDB, SH, DH, GR, CMI) Netherlands (RT), and France (V JDV, DB-B). These additional screens were designed to (a) determine their subcellular localization and their differential distribution on primary fibroblasts isolated from different tissues (bone marrow, spleen, liver synovium, lung) (b) determine whether the antigens recognized by these antibodies were cation and protease sensitive. Cation and protease sensitivity add biochemical data (for example cell surface integrins have cation sensitive epitopes), and protease sensitivity helps to confirm that the epitope recognized by the antibody is a protein.
Table 1.
Details of the 62 antibodies submitted to the stromal section of HLDA 8
| Workshop number | Antibody | Isotype | Immunogen | Specificity |
|---|---|---|---|---|
| 80100 | MIMA-24 | IgG1 | Plasmid cDNA/transfected 293T cells | Kell protein |
| 80101 | MIMA-52 | IgG2a | Plasmid cDNA/transfected 293T cells | Dombrock protein ART4 |
| 80102 | MIMA-53 | IgG2a | Plasmid cDNA/transfected 293T cells | Dombrock protein ART4 |
| 80103 | MIMA-46 | IgM | Transfected 293T cells | I-like |
| 80104 | MIMA-51 | IgG2b | DTT-treated hRBCs | Rh:17 |
| 80105 | NBL-1 | IgG1 | Peptides | Xg(a) |
| 80106 | BANR S10 | IgA | Hu erythrocytes (male) | CD99 |
| 80107 | MSG-B1 | IgG2b | Synthetic peptides | CD99 |
| 80111 | ZCH-4D5 | IgG1 | KG1a cell line | ?CD45 |
| 80114 | Y129 | IgG2a | Human myeloma cell line, KPC-32 | Human natural HM 1.24 |
| 80465 | RS38E | IgG1 | Hu BST-2 expressed BALB 3T3 cells | Human BST-2 |
| 80466 | K5Cl | IgG1 | Recombinant human HM1.24 | Human recombinant HM1.24 |
| 80117 | HUTS-21 | IgG2a | Purified β1 integrins | CD29 |
| 80142 | 1-456 | IgG1 | Myeloid derived-DC | CD58 |
| 80143 | 5-341 | IgG2a | Myeloid derived-DC | CD54 |
| 80160 | N6 B6 | IgG2a | Nalm-1 | CD164 |
| 80162 | 67 D2 | IgG1 | T-47D breast tumour cells | CD164 |
| 80163 | B1 D5 | IgG2a | SIRPβ1 transfected NIH-3T3 cells | CD172b |
| 80164 | B4 B6 | IgG1 | SIRPβ1 transfected NIH-3T3 cells | CD172b |
| 80167 | 67 A4 | IgG1 | T-47D breast tumour cells | E-cadherin |
| 80168 | 9 C4 | IgG2b | DU-4475 breast tumour cell line | Ep-CAM |
| 80169 | 57 D2 | IgG1 | TF-1 erythroleukemia cell line | Unknown |
| 80170 | W4A5 | Subsets of mesenchymal stem cells +neuronal progenitor cells |
||
| 80171 | W8B2B10 | Subsets of mesenchymal stem cells | ||
| 80172 | W8C3B3 | Subsets of mesenchymal stem cells | ||
| 80201 | W1B9 | IgM | Patient derived (no immunization) | RBC membrane |
| 80202 | 3A11 | IgG1 | HBL-100 cells (human) | Novel CD6 ligand |
| 80203 | ZCH-2G7 | IgG1 | Fresh TdT + AML blasts | Unknown CD, non-lineage |
| 80204 | ZCH-5E2 | IgG2b | KG1a cell line | Unknown CD, non-lineage |
| 80205 | ZCH-4B6 | IgG1 | KG1a cell line | Unknown CD, non-lineage |
| 80206 | ZCH-8Dla | IgG2a | KG1a cell line | Unknown CD, non-lineage |
| 80207 | ZCH-9C7 | IgM | KG1a cell line | Unknown CD, non-lineage |
| 80208 | ZCH-2H7b | IgG1 | KG1a cell line | Unknown CD, non-lineage |
| 80209 | ZCH-3B8 | IgG1 | KG1a cell line | Unknown CD, non-lineage |
| 80210 | ZCH-4E3 | IgG1 | KG1a cell line | Unknown CD, non-lineage |
| 80211 | ZCH-3B12 | IgG1 | KG1a cell line | Unknown CD, non-lineage |
| 80212 | ZCH-5H8 | IgG2b | KG1a cell line | Unknown CD, non-lineage |
| 80213 | ZCH-2B8a | IgG2a | KG1a cell line | Unknown CD, non-lineage |
| 80214 | ZCH-2F10 | IgG1 | Fresh TdT + AML blasts | Unknown CD, non-lineage |
| 80226 | ZCH-2D3 | IgG1 | Fresh TdT + AML blasts | Unknown CD, non-lineage |
| 80268 | B-L28 | ?CD58 | ||
| 80270 | B-D15 | ?CD29 | ||
| 80273 | A1 | Hu BM derived stromal cells | Bone marrow derived stromal | |
| 80274 | A8 | Hu BM derived stromal cells | Bone marrow derived stromal | |
| 80275 | A2 | Hu BM derived stromal cells | Bone marrow derived stromal | |
| 80276 | E5 | Hu BM derived stromal cells | Bone marrow derived stromal | |
| 80277 | E6 | Hu BM derived stromal cells | Bone marrow derived stromal | |
| 80310 | FB21 | IgM | Hu lymphoid cell line | |
| 80314 | CUB 1 | ?CDCP1 | ||
| 80315 | CUB 2 | ?CDCP1 | ||
| 80317 | CUB 4 | ?CDCP1 | ||
| 80337 | P1B5 | IgGl, k | HT 1080 fibrosarcoma cells | α3 subunit of integrin α3β1 |
| 80338 | P4G9 | IgG3, k | Jurkat T lymphoblasts | α4 subunit of integrin α4β1 |
| 80339 | P1D6 | IgG3, k | Lymphokine activated killer cells | α5 subunit of integrin α5β1 |
| 80359 | NCH-38 | IgG1, k | E-cadherin (uvornorulin) | 120kDa of mature E-cadherin + 82kDa fragment of E-cadherin |
| 80392 | 8D6 | Follicular dendritic cells | ||
| 80393 | 3C8 | Follicular dendritic cells | ||
| 80394 | 4G10 | Follicular dendritic cells | ||
| 80437 | 11G5a | IgG1,k | CD151 | |
| 80462 | 188331 | IgG2b | EC domain of human jagged-1 (aa I-296) | Human jagged-1 |
| 80464 | 87908 | IgG2b | EC domain of human BMPR-lα | Human BMPR-1α |
| 80465 | 88614 | IgG2b | EC domain of human BST-2 | Human BMPR-1β |
3. Results
An example of how the data was collected for each antibody in the primary screen is shown for antibody 80167 (E-Cadherin) in Fig. 1. Of the 20 antibodies that passed the first screen (relatively restricted expression on stromal cells) three were found to have epitopes expressed on peripheral blood leucocytes and were then identified to recognize the previously designated CD antigens CD13 (80274), CD44 (80394), and CD166 (80273) Fig. 2. One of the antibodies was demonstrated to be against an intracellular enzyme prostaglandin synthase (80393) Fig. 3. Seven antibodies were assigned new CD numbers at the workshop based on the fact that the antigen had been cloned and did not already have a CD number (80167, 80168, 80324, 80392, 80448, 80646, 80645). Of the remaining nine antibodies, insufficient information (the antigen was not cloned and there was no molecular or biochemical data available) precluded the assignment of CD numbers at this workshop (80169, 80170, 80171, 80172, 80202, 80213, 80275, 80276, 80277). Examples of three of these non-designated antibodies (80169), (80170), (80202) are shown in Fig. 4. In the secondary screens, no antibody was found that could clearly discriminate between subsets of fibroblasts (i.e., had distinct biphasic distribution on flow cytometric analysis of primary fibroblasts) or between fibroblasts isolated from different sites (data not shown). However, there were clear differences between antibodies that recognized extracellular epitopes as well as differences between antibodies in terms of cation and protease sensitivity (summarized in Table 2).
Fig. 1.
Example of data accumulated during primary screen on all 62 antibodies submitted. Information in the spreadsheet format includes data from immunohistochemistry screens on tonsil and liver sections (green is the test antibody and red is nuclear counter stain) as well as screens on leucocytes isolated from tonsil and peripheral blood. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this paper.)
Fig. 2.
Examples of three antibodies which recognized non-stromal cells and were subsequently found 10 recognize CD13 (A), CD44 (B), and CD166 (C). In the immunofluorescence pictures, green is the test antibody and red is the nuclear counterstain. (see Ref. [14] for more information on (B)). (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this paper.)
Fig. 3.
Example of an antibody that appeared to be stromal specific but when cloned was found to identify the intracellular enzyme prostaglandin synthase ([15] and personal communication). In the immunofluorescence pictures, green is the test antibody and red is the nuclear counterstain. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this paper.)
Fig. 4.
Examples of three of the nine antibodies that remain unclassified and did not receive CD numbers at the workshop. (A) 80169, (B) 80170, and (C) 80202. In the immunofluorescence pictures, green is the test antibody and red is the nuclear counterstain. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this paper.)
Table 2.
Details of the 20 antibodies that passed the first screen and were then analyzed for expression on a range of primary fibroblasts as well as cation sensitivity, protease resistance, and intracellular or extracellular expression
| Workshop number |
Antibody | Isotype | Immunogen | Specificity | Cation sensitive |
Trypsin sensitive |
Extracellular or intracellular |
CD number |
|---|---|---|---|---|---|---|---|---|
| 80167 | 67 A4 | IgG1 | T-47D breast tumour cells | E-cadherin [16] | No | No | Extracellular | CD324 |
| 80168 | 9 C4 | IgG2b | DU-4475 breast tumour cell line | Ep-CAM [17] | No | No | Extracellular | CD326 |
| 80169 | 57 D2 | IgG1 | TF-1 erythroleukemia cell line | Unknown | ? | ? | ? | – |
| 80170 | W4A5 | IgG1 | WER1-RB-1 retinoblastoma cell line | Subsets of mesenchymal stem cells + neuronal progenitor cells |
No | No | extracellular | – |
| 80171 | W8B2B10 | IgG1 | WERI-RB-1 retinoblastoma cell line | Subsets of mesenchymal stem cells | No | No | Extracellular | – |
| 80172 | W8C3B3 | IgG1 | WERI-RB-1 retinoblastoma cell line | Subsets of mesenchymal stem cells | ? | ? | Extracellular | – |
| 80202 | 3A11 | IgG1 | HBL-100 cells (human) | Novel CD6 ligand | No | Yes | Extracellular | – |
| 80213 | ZCH-2B8a | IgG2a | KG1a cell line | Unknown CD, non-lineage | ? | ? | ? | |
| 80273 | A1 | Hu BM derived stromal cells | CD166 (pers. comm.) | No | No | Extracellular | – | |
| 80274 | A8 | Hu BM derived stromal cells | CD13 (pers. comm.) | No | No | Extracellular | – | |
| 80275 | A2 | Hu BM derived stromal cells | Bone marrow derived stromal | Yes | No | Extracellular | – | |
| 80276 | E5 | Hu BM derived stromal cells | Bone marrow derived stromal | No | No | ? | – | |
| 80277 | E6 | Hu BM derived stromal cells | Bone marrow derived stromal | No | No | Extracellular | – | |
| 80324 | E1/183 | IgG1 | AG1523 human fibroblasts | Endo180/uPARAP [18] | ? | No | Extracellular | CD280 |
| 80392 | 8D6 | Follicular dendritic cells | 8D6 transmembrane antigen [19] | No | No | Extracellular | CD320 | |
| 80393 | 3C8 | Follicular dendritic cells | Prostaglandin synthase ([15]; and pers. comm.) | No | No | Intracellular | – | |
| 80394 | 4G10 | Follicular dendritic cells | CD44 [14] | No | No | Extracellular | – | |
| 80448 | Bl/473 | IgG1 | AG1523 human fibroblasts | Endosialin ([13]) | ? | Yes | Extracellular | CD248 |
| 80464 | 87908 | IgG2b | EC domain of hu BMPR-1α | Human BMPR-1α | No | No | Extracellular | CD292 |
| 80645 | RS38E | IgG1 | Hu BST-2 expressed in 3T3 cells | Human BST-2 | ? | ? | ? | CD317 |
4. Conclusions
The low number of antibodies analyzed in this section was insufficient to obtain an overall description of fibroblast cell surface antigens. However from the antibodies that were studied it was notable that (a) although antibodies were characterized as recognizing antigens that were predominantly expressed by fibroblasts, no fibroblast specific antibodies were identified, (b) no antibodies were identified that discriminated between fibroblasts from different anatomical sites. It remains to be determined whether the antibodies that have been characterized discriminate between fibroblasts from diseased and normal tissue [13].
The relatively low number of antibodies submitted to the stromal cell section reflects two important issues. First, that classification of fibroblast cell surface proteins remains an immature field. Second, workers in the field have increasingly employed transcriptional profiling to characterize fibroblasts and other stromal cells rather than an antibody based approach (for examples see Refs. [8,9]). However, the problem with the latter approach is that antibodies to some of the proteins identified using transcriptional profiling are frequently not available to validate results and to further analyze antigen distribution. Furthermore, transcriptional profiling does not permit the isolation and further functional characterization of fibroblast isolated ex vivo. As a consequence, it is our opinion that an antibody based approach to characterizing fibroblast cell surface proteins is still a valid and valuable one. Moreover with increasing interest in the role of stromal cells such as fibroblasts in disease progression (for example cancer and chronic inflammation), we would encourage others in the field to continue to generate antibodies and characterize stromal cell surface antigens so that these reagents can form the basis of further HLDA workshops.
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