Expression analysis of the mouse S100A7/psoriasin gene in skin inflammation and mammary tumorigenesis
© Webb et al; licensee BioMed Central Ltd. 2005
Received: 27 October 2004
Accepted: 17 February 2005
Published: 17 February 2005
The human psoriasin (S100A7) gene has been implicated in inflammation and tumor progression. Implementation of a mouse model would facilitate further investigation of its function, however little is known of the murine psoriasin gene. In this study we have cloned the cDNA and characterized the expression of the potential murine ortholog of human S100A7/psoriasin in skin inflammation and mammary tumorigenesis.
On the basis of chromosomal location, phylogenetic analysis, amino acid sequence similarity, conservation of a putative Jab1-binding motif, and similarities of the patterns of mouse S100A7/psoriasin gene expression (measured by RT-PCR and in-situ hybridization) with those of human S100A7/psoriasin, we propose that mouse S100A7/psoriasin is the murine ortholog of human psoriasin/S100A7.
Although mouse S100A7/psoriasin is poorly conserved relative to other S100 family members, its pattern of expression parallels that of the human psoriasin gene. In murine skin S100A7/psoriasin was significantly upregulated in relation to inflammation. In murine mammary gland expression is also upregulated in mammary tumors, where it is localized to areas of squamous differentiation. This mirrors the context of expression in human tumor types where both squamous and glandular differentiation occur, including cervical and lung carcinomas. Additionally, mouse S100A7/psoriasin possesses a putative Jab1 binding motif that mediates many downstream functions of the human S100A7 gene.
These observations and results support the hypothesis that the mouse S100A7 gene is structurally and functionally similar to human S100A7 and may offer a relevant model system for studying its normal biological function and putative role in tumor progression.
Human S100A7 or psoriasin was first identified as an over-expressed secreted protein in psoriatic skin. More recently its expression in both pre-invasive (ductal carcinoma in situ, DCIS) and invasive human breast cancer was demonstrated . Although highly expressed in DCIS and generally down-regulated in invasive breast cancer, the expression of psoriasin/S100A7 in both in-situ and invasive breast cancer is correlated with markers of poor prognosis [3, 4] and in invasive carcinoma also with poor clinical outcome . Support for psoriasin/S100A7 having a functional role in this aggressive phenotype is shown by the observation of increased growth and tumorigenesis when breast cancer cells over-expressing psoriasin/S100A7 are grown as xenografts in nude mice . This activity may in part be mediated by the ability of psoriasin/S100A7 to interact with c-Jun activation domain-binding protein 1 (Jab1)  and enhance pro-survival pathways  and protect against anoikis in human breast and head and neck squamous cancer cells . However, further investigation of the physiological and pathophysiological function of psoriasin/S100A7 can only be effectively undertaken using genetic manipulation of an animal model. To undertake such studies we need to characterize and clone the mouse psoriasin gene. Interestingly, during the preparation of this manuscript Marenholz etal.,  have argued that the possible ancestral homolog of the human S100A7 paralogs  has been identified in the mouse on the basis of genome sequence analysis and gene orientation, but has not been characterized fully as yet. The following study provides evidence of the cloning of a cDNA of the putative mouse ortholog of human psoriasin/S100A7, investigates its expression under conditions of mouse mammary tumorigenesis and skin inflammation, and confirms that the factors involved in its regulation are comparable to those involved in regulation of the human counterpart.
Murine studies were conducted in accordance with the principles and procedures recommended and approved by the University of Manitoba Animal Care Review Board. Mammary tumors in CD1 mice were generated chemically using 7, 12-dimethylbenz anthracine (DMBA) as previously described . Freshly dissected mouse tissues were either stored frozen at -70°C, or processed to generate formalin fixed paraffin-embedded tissue blocks.
Acute dermatitis in C57/B6 mice was induced by the topical application of 20% croton oil (dissolved in dimethyl sulfoxide) to a 1 cm length mid-tail portion . The tail skins were stimulated continuously with croton oil every 4 hours for 24 hours. Mice were divided into five time-groups (each containing 3 mice) that were designated 0, 4, 8, 16, and 24 hours. At each time-point, the mice were sacrificed. The tail-skins were harvested and paired specimens of normal and inflamed skin tissue were fixed in 3.7% formaldehyde in 0.1 M phosphate buffered saline for 16–18 hours, followed by paraffin embedding.
Sections from the above blocks were used for preparation of haematoxylin and eosin stained sections for light microscopic examination, in situ hybridization (ISH), and immunohistochemistry (IHC).
Human tumor tissues were obtained from the Department of Pathology, University of Manitoba. All cases were coded and therefore anonymous and prior approval was obtained from the University of Manitoba Research Ethics Board and the Pathology Access to Tissue Committee. Different cervical tumor pathologies (total n = 39 cases) including in-situ adenocarcinoma (n = 10) and squamous cell carcinoma (n = 9), as well as invasive adenocarcinoma (n = 10) and squamous carcinoma (n = 10) were selected for one cohort study. In addition, different invasive lung tumor types (total n = 78 cases) including mesothelioma (n = 10), small cell carcinoma (n = 15), adenocarcinoma (n = 28), and squamous carcinoma (n = 25) were selected to form another study cohort. Squamous differentiation within both murine and human tumors was determined by standard morphological criteria including cytoplasmic keratinization and cellular stratification relative to keratin pearls.
Paraffin embedded 5 μm tissue sections were analyzed by in-situ hybridization according to a previously described protocol . The plasmid pCR4-TOPO-mPsor-ORF, consisted of pCR4-TOPO plasmid (Invitrogen Canada Inc, Burlington, ON) containing a 344 base pair insert of the mouse psoriasin cDNA, also known as mouse S100A15 (from nucleotide 94 to 437 as numbered in AY465109, and from 1 to 344 as numbered in AY582964). One microgram of linearized template DNA was used to generate 35S-UTP-labeled sense and antisense cRNA probes using the Riboprobe System (Promega, Madison, WI) according to the manufacturer's instructions. Sense probes were used as controls. In-situ hybridization and washing conditions were as previously described. Sections were developed using Kodak NTB-2 photographic emulsion and counter-stained with Lee's stain after 2–6 weeks.
Levels of mouse S100A7/psoriasin RNA expression were assessed by microscopic examination at low power magnification and with reference to the negative sense control. This was done by scoring the estimated average signal intensity (on a scale of 0 to 3), where 0 is no expression and 3 is a high proportion of strong focal expression.
Immunohistochemistry (IHC) was performed on serial 5 μm sections from a representative, formalin fixed paraffin embedded tissue block from each tumor. For human tumor blocks, psoriasin/S100A7 IHC was performed essentially as described  and human psoriasin/S100A7 was detected using a previsouly characterized rabbit polyclonal antibody [3, 5]. For murine tumors estrogen receptor-alpha (ERα) was detected using an affinity purified rabbit polyclonal antibody, MC-20, raised against a C-terminal peptide of mouse ERα (#sc-542, Santa Cruz Biotechnology Inc, CA). Antibodies were applied using an automated tissue immunostainer (Discovery module, Ventana Medical System), 3, 3-diaminobenzidine IHC kit and bulk reagents were supplied by the manufacturer. Briefly, the Discovery staining protocol was set to "Standard Cell Conditioning", followed by 60 minutes incubation at 42°C with primary antibody and 30 minutes incubation at 42°C with secondary antibody (goat anti-rabbit-IgG-HRP, Jackson Immuno Research Labs Inc). Primary antibody concentrations initially applied to the Ventana instrument were 1:200 for ERα and 1:200 for the secondary antibody translating into final dilutions of 1:600 after 1:3 dilution with buffer dispensed onto the slide with the primary antibody. Slides were counterstained with hematoxylin.
Levels of psoriasin/S100A7 and ERα expression were scored semi-quantitatively in tissue sections, under the light microscope. Scores were obtained by estimating average signal intensity (scale of 0 to 3) and the proportion of epithelial cells showing a positive signal (0–100%). The intensity and proportion scores were then multiplied to give an overall IHC-score.
RNA extraction and reverse transcription
Total mouse RNA was extracted using Trizol™ reagent (Invitrogen) according to the manufacturer's instructions, and the integrity of the RNA was confirmed by denaturing gel electrophoresis as previously described . RNAs from the various frozen tissues were reverse transcribed. One μg of total RNA was reverse transcribed in a final volume of 30 μl composed of 50 mM Tris-HC1 (pH 8.3), 75 mM KC1, 3 mM MgC12, 0.5 μM random hexamers (Invitrogen) 0.5 mM dNTPs, 0.01 mM DTT in the presence of 300 units of MMLV-RT (Invitrogen), and 4 units RNase inhibitor at 37°C for 1 hour, followed by 5 minutes at 95°C and kept at -20°C until used.
The primer pairs used were as follows;
Mouse S100A7/psoriasin C-terminus
5'-ATG CCA GAC ACA CCA GTG GAG-3' (sense; nucleotides 111–131 in GenBank acc. AY465109) and 5'-GGT AGT CCT TCA CCA GCT TGC-3' (antisense; nucleotides 358–378).
Mouse S100A7/psoriasin open reading frame
5'-TGA AGG GTC CAT CAG TCA-3' (sense; nucleotides 94–111 in GenBank acc. AY465109) and 5'-CTA GTA GAG GCT GTG CT-3' (antisense; nucleotides 421–437).
Primers were designed according to the mRNA sequence (GenBank acc. NM_007393): 5'-TCT ACG AGG GCT ATG CTC TCC-3' (sense; nucleotides 574–594) and 5'-GGA TGC CAC AGG ATT CCA TAC-3' (antisense; nucleotides 883–903). According to the chromosome 5 genomic contig sequence (GenBank acc. NT_039324), these primers span an 87-bp intron with the antisense primer binding across the intron-exon boundary.
PCR reactions were performed essentially as previously described . To amplify cDNA corresponding to mouse S100A7/psoriasin, an initial 2 minutes at 94°C was followed by 36 cycles (30 seconds at 94°C, 30 seconds at 56°C, 30 seconds at 72°C). Twenty six cycles were used to amplify β-actin cDNA (30 seconds at 94°C, 30 seconds at 58°C, 30 seconds at 72°C). PCR products were separated on 1.5% agarose gels containing ethidium bromide (0.1 μg/ml) as previously described . Identity of the 344 bp product corresponding to mouse S100A7/psoriasin and the 330 bp product corresponding to β-actin were confirmed by subcloning and sequencing as described previously .
Semi-quantitative PCR analyses were performed using three independent PCRs for each sample for both mouse S100A7/psoriasin and β-actin. Signals visualized with UV irradiation on a GelDoc2000/ChemiDoc System (Bio-Rad), were quantified by densitometry using the Quantity One software (version 4.2; Bio-Rad). Mouse S100A7/psoriasin expression was standardized to β-actin expression assessed from the same cDNA in separate PCR reactions and run in parallel on separate gels. The standardized mean of each triplicate PCR was then expressed relative to the levels in a "moderately expressing" sample selected for each batch of cDNAs to be analyzed.
Amino acid sequences of S100 family genes were aligned using Clustal X . This alignment was used to construct a phylogenetic tree based on a Poisson corrected neighbour-joining distance method  available in the computer software package MEGA v3.0 . The reliability of the phylogeny's interior branches was tested by a bootstrap test with 1000 replications . The human sequences used, were GenBank Accession numbers: AAH05019 (S100A14), NP_789793 (5100A15), NP_006262 (S100A1), NP_005969 (S100A2), NP_002951 (S100A3), AAH00838 (S100A4), NP_002953 (S100A5), AAH09017 (S100A6), AAH34687 (S100A7), XP_060509 (S100A7L-2), AAH05928 (S100A8), AAH47681 (S100A9), AAH15973 (S100A10), AAH14354 (S100A11), NP_005612 (S100A12), NP_002952 (S100A13). The mouse sequences used, were GenBank Accession numbers: NP_035439 (S100A1), NP_035440 (S100A3), NP_035441 (S100A4), NP_035442 (S100A5), AAH03832 (S100A6), NP_955454 (S100A7/15), NP_038678 (S100A8), AAH27635 (S100A9), AAH25044 (S100A10), AAH21916 (S100A11), NP_033139 (S100A13), AAH25607 (S100A14).
Identification and cloning of mouse S100A7/psoriasin cDNA
Presence of putative Jab1 binding motif in mouse S100A7/psoriasin
A notable structural feature of the human psoriasin/S100A7 gene is a consensus Jab1-binding domain sequence that we have speculated may confer the ability of human psoriasin/S100A7 to interact with Jab1 and so play an important role in the mechanism by which human psoriasin/S100A7 medicates its action . Jab1 was originally identified as a factor influencing c-Jun transcription of AP-1 regulated genes . It is now known that Jab1 is a component of a multimeric protein complex (the CSN/COP9 signalosome) and that Jab1 interacts with many components of cell signalling pathways . This may be in the context of either phosphorylation or proteasomal activities as Jab1 is also the only known deneddylating protein active in control of the SCF-cullin ubiquitin ligases .
Expression of mouse S100A7/psoriasin during mouse mammary tumorigenesis
Our initial results shown in Figure 2 suggest that the expression of mouse S100A7/psoriasin may be upregulated during mammary tumorigenesis. This was of interest since we and others have previously found that human psoriasin/S100A7 expression is highly up-regulated in human breast cancer compared to normal breast tissue [2, 24]. To confirm and extend this observation, further analysis of murine mammary tumors was conducted by both semi-quantitative RT-PCR and by in situ hybridization.
cDNAs were generated from matched normal mammary gland and mammary gland tumors from DMBA-treated CD1 wild-type mice (n = 6, same as in Figure 2A). Semi-quantitative RT-PCR analysis showed significantly increased expression of mouse S100A7/psoriasin mRNA in mammary gland tumors relative to matched normal mammary gland (p < 0.05) by Wilcoxon signed-rank test, one-sided (Figure 2B).
Correlation of mouse S100A7/psoriasin expression using RT-PCR and in situ hydridization in normal mammary gland and DMBA-induced mammary tumors Mouse S100A7/psoriasin mRNA levels were determined in extracts from frozen tissue samples of matched normal mammary gland and DMBA-induced mammary tumors (n = 6) by semi-quantitative RT-PCR as described in Materials and Methods. Sections from the corresponding adjacent tissue samples which had been formalin fixed and paraffin-embedded, where used for in situ hybridization (ISH) with 35S-labelled antisense mouse S100A7/psoriasin probes. Specific hybridization was scored on a scale of 0 to 3 as described in Materials and Methods. Results of the two analyses were correlated using Spearmans test (r = 0.63, p < 0.02).
Relative mouse S100A7/psoriasin expression
Although up-regulation of mouse S100A7/psoriasin expression occurred in DMBA induced tumors compared to adjacent normal mammary gland tissue, expression levels showed a wide-scatter amongst the mammary tumors (Figure 2). This was of interest since ERα has been reported to have variable expression in chemical carcinogen induced tumors [25–27] and we have previously shown an inverse association of human psoriasin/S100A7 expression with ERα in breast cancer [3, 5]. We therefore compared the expression of mouse S100A7/psoriasin as determined by in situ hydridization with ERα expression assessed by IHC in adjacent sections from the same tumors. An inverse association between mouse S100A7/psoriasin and ERα expression was clearly evident but categorical contingency analysis did not reach statistical significance (Fisher's exact test, p = 0.073), likely due to small numbers. However detailed comparison within tumors showed that in tumors that expressed both genes, mouse S100A7/psoriasin expression was restricted to areas within heterogeneously positive ERα tumors that lacked ERα expression. Interestingly, mouse mammary tumors that develop due to targeting of the neu oncogene to the mouse mammary gland (MMTV-neu) did not express mouse S100A7/psoriasin RNA nor ERα (data not shown).
Expression of mouse S100A7/psoriasin in a model of skin inflammation
Inflammatory response to topical application of croton oil to the skin.
0 hours median [range]
24 hours median [range]
Expression of human psoriasin/S100A7 in relation to differentiation in human tumors
We have used structural and expression analysis to show that a gene currently classified as mouse S100A15 (GenBank acc. AY465110) which maps within the murine S100 cluster on chromosome 3 (see acc. NT_078386, NCBI Map View Link and LOC381493)  should be reclassified as mouse S100A17/psoriasin, as suggested by Marenholz et al. . This gene is not highly conserved relative to other members of the S100 family (~40% amino acid sequence similarity of mouse S100A7 with either human S100A7 and/or human S100A15, compared to >60% amino acid sequence similarity of most other known mouse S100A proteins to their human counterparts, unpublished data) . However, phylogenetic analysis shows that while mouse retained an ancestral S100A7/psoriasin gene, the human ortholog underwent duplication and functional differentiation making the assignment of orthology/paralogy only on the basis of phyogenetic information uncertain.
In the human, the closely related psoriasin/S100A7 and S100A15 appear to be functionally distinct. Although both were isolated as overexpressed genes in human psoriatic skin [1, 20], we have previously identified S100A7 to be differentially expressed in neoplastic mammary gland . Neither gene is substantially detectable in database analysis of the available normal human mammary gland libraries, and only psoriasin/S100A7 is present at high copy numbers (up to 2,300 tags per 200,000) in several mammary gland neoplasia libraries, whereas S100A15 is absent or rarely detectable (<10 tags per 200,000) . Additionally, psoriasin/S100A7 is expressed in several SAGE database libraries representing human skin neoplasia, while S100A15 is not detected (data not shown). Thus, despite some similarities in their occurrence and expression in association with psoriasis  these closely related human genes show dissimilar expression patterns in mammary tumors suggesting distinct functional roles. In contrast, our studies show that the pattern of gene expression of mouse S100A7/psoriasin during mammary tumorigenesis and skin inflammation occurs in a similar pattern to that seen with human psoriasin/S100A7 [2, 3]. Furthermore, while mouse S100A7/psoriasin shows approximately equivalent amino acid sequence similarity to both human S100A7 and human S100A15 proteins, both mouse S100A7/psoriasin and human psoriasin/S100A7 contain a putative Jab1-binding motif that is functionally significant in the human at least [6, 7] but this motif is not found in human S100A15. We conclude on the basis of chromosomal location, phylogenetic analysis, amino acid sequence similarity, conservation of a putative Jab1-binding motif, and similarities in patterns of expression, that mouse S100A7/ psoriasin is the murine ortholog of human psoriasin/S100A7.
Expression of human psoriasin/S100A7 was originally attributed to skin pathologies where abnormal squamous differentiation occurs . In breast tumors where psoriasin/S100A7 is also expressed, overt squamous differentiation is rare. However it has been detected and suggested as a marker of squamous differentiation in a subtype of bladder cancer . Extending the latter finding our data here shows that in cervix and lung, two tissues where squamous and glandular differentiation are both common differentiation pathways for carcinomas, psoriasin/S100A7 is commonly expressed and almost exclusively associated with squamous tumor subtypes. The parallel finding that mouse S100A7/psoriasin was distinctively associated with areas of squamous differentiation within murine breast adenocarcinomas suggests that similar factors are involved in the regulation of both psoriasin/S100A7 and murine S100A7/psoriasin genes, and is in keeping with a similar role for the murine gene.
A role for human psoriasin/S100A7 in inflammation has been suggested, since psoriasin/S100A7 can be secreted and was shown to be chemotactic for neutrophils and CD4+ T-cells in vitro . Our current data from a model of mouse skin inflammation is also consistent with such a role, since a significant upregulation in mouse S100A7/psoriasin expression occurs simultaneously with the acute phase of skin inflammation after application of croton oil to the mouse tail skin. The role for psoriasin/S100A7 in tumorigenesis may be related to the activity of pro-survival pathways  and acquisition of apoptosis resistance . Our results here also provide indirect support for this hypothesis, as mouse S100A7/psoriasin RNA was expressed in keratinocytes at the margin of squamous differentiation, where resistance to apoptotic stimuli may be an important component of the sequence of differentiation and to allow time for production of large amounts of keratin before finally undergoing desquamation, denucleation and cell death .
Finally, psoriasin has been implicated in human breast cancer progression. Specifically, psoriasin/S100A7 has been associated with the pre-invasive DCIS phenotype , augmentation of several characteristics of malignancy in vitro and in vivo [4, 6] and with poor outcome in invasive estrogen receptor-negative tumors [3, 5]. Our current results also support the involvement of S100A7/psoriasin in murine mammary tumorigenesis. Additionally, differential expression of mouse S100A7/psoriasin was observed between DMBA and MMTV-neu induced mammary tumors, and a strong trend towards a negative correlation between mouse S100A7/psoriasin and estrogen receptor alpha expression emerged in the DMBA induced mammary tumors. Such data are consistent with the pattern of expression of human psoriasin/S100A7 in human breast tumors, and are consistent with the view that mouse S100A7/psoriasin subserves similar roles to human psoriasin/S100A7 in mammary tumorigenesis and breast cancer progression. It is nevertheless possible that human psoriasin/S100A7 and mouse S100A7/psoriasin have several functions, depending on cellular context. This is reflected by differences already observed in localization of expression in different cell types within a tissue or subcellular localization, since psoriasin has been found in the nucleus, in the cytoplasm, at the cell periphery/plasma membrane and it can also be secreted [33, 34].
S100 proteins have been known to be differentially expressed during tumorigenesis as well as other disease states for some time. However, the functional roles they may play in disease processes are poorly understood [33, 34]. In breast cancer, psoriasin/S100A7 is associated with important biological and clinical aspects of the disease  and the identification of its potential ortholog in the mouse is an important step to facilitate understanding of its function and mechanism of action. The results presented in this study strongly support the hypothesis that mouse S100A7 is the murine ortholog of human psoriasin/S100A7, and provide a rationale for the manipulation of mouse S100A7/psoriasin in mice to gain important insights into the function of human psoriasin/S100A7.
This work was supported by grants from the Canadian Institutes for Health Research (CIHR), the Canadian Breast Cancer Research Alliance (CBCRA) and the Canadian Foundation for Innovation (CFI). P. H. W. is a CIHR/MRC Scientist. Y.M. is an MMSF career awardee. E.E. is a recipient of a Terry Fox research studentship from the National Cancer Institute of Canada.
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