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Involvement of orphan nuclear receptor COUP-TFII in cadherin-6 and cadherin-11 regulation: Implications in development and cancer Pierre-Paul Bringuier a,b,c,*,1, Jack A. Schalken d, Valérie Hervieu a,c, Laurence A. Giroldi b,**,1 a

Université Claude Bernard Lyon1, F-69622 Villeurbanne, France INSERM, U865, IFR62, F-69 372 Lyon, France c Cancer Research Center of Lyon, UMR 1052, INSERM, 69 372, Lyon cedex 08, France d Department of Urology, Nijmegen Medical Centre, Radboud University, Nijmegen, The Netherlands b

A R T I C L E

I N F O

A B S T R A C T

Article history:

Changes in cadherin expression are instrumental both in embryonic development and disease,

Received 16 December 2014

underlining the importance of understanding how cadherin expression is controlled. Kidney

Received in revised form

development is characterized by a mesenchymal–epithelial transition underlain by a cadherin-

3 February 2015

11 to cadherin-6 switch, the regulation mechanisms of which are presently unexplained.

Accepted 10 February 2015

Using transfection and RNA-interference we demonstrate that COUP-TFII (NR2F2) induces

Available online 14 February 2015

down-regulation of cadherin-6 and up-regulation of cadherin-11 in cultured cell lines. Double immunolabeling of mouse embryos provides indirect evidence that COUP-TFII negatively

Keywords:

controls the cadherin-11 to cadherin-6 switch underlying the kidney developmental

Cadherins

mesenchymal–epithelial transition. Furthermore, we found high expression of COUP-TFII

Kidney mesenchymal–epithelial

in some gastric and oesophageal adenocarcinomas, correlating with abnormal cadherin-

transition

11 expression and suggesting reactivation of embryonic pathways linked to COUP-TFII in

Gastric/oesophageal cancer

these tumors. Altogether, our data shed new light upon the role of COUP-TFII in develop-

Implantation

ment and in cancer. © 2015 Elsevier Ireland Ltd. All rights reserved.

Fibrosis

1.

Introduction

Cadherin cell–cell adhesion molecules display more or less stringent tissue specialization. Changes in expressed cadherins (cadherin switching) underlie several developmental milestones such as gastrulation and neurulation. Both these events involve down regulation of E-cadherin and replacement by N-cadherin in a group of cells (Stemmler, 2008)

suggesting a coordinated regulation.These changes in cadherin expression impart new properties to cells which acquire the capacity to detach from their tissue of origin to migrate and colonize distant sites in the body, a process called epithelial– mesenchymal transition (EMT). E- to N-cadherin switching and associated EMT are hijacked during disease such as cancer and are known to account partly for metastatic occurrence (Wheelock et al., 2008). Hence, cadherin switching is instrumental both in organogenesis and cancer spreading, stressing the

1 These authors contributed equally to this work. * Corresponding author. Université Claude Bernard Lyon1, F-69622 Villeurbanne, France. Tel: +33 478 78 56 33. E-mail address: [email protected] (P.-P. Bringuier). ** Corresponding author. INSERM, U865, IFR62, F-69 372 Lyon, France. E-mail address: [email protected] (L.A. Giroldi). http://dx.doi.org/10.1016/j.mod.2015.02.001 0925-4773/© 2015 Elsevier Ireland Ltd. All rights reserved.

m e c h a n i s m s o f d e v e l o p m e n t 1 3 6 ( 2 0 1 5 ) 6 4 –7 2

importance of clarifying how cadherin expression is regulated to understand development orchestration and cancer progression. E-cadherin, being a prominent cadherin molecule and a major actor of EMT, has been the subject of many studies aimed at elucidating the control of its expression and the transcription factors involved have been shown to operate both in development and cancer EMT (Yang and Weinberg, 2008). Interestingly, the embryonic factor TWIST was shown to both repress E-cadherin and induce N-cadherin expression, providing a unifying explanation for the observed coordinated regulation of these two cadherins (Alexander et al., 2006; Yang et al., 2004). Other cadherin expression changes, in disease as well as development, are less well understood. Cadherin-11, a mesenchymal cadherin, is abnormally switched on in the progression of some carcinoma, participating in EMT (Sarrio et al., 2008; Tomita et al., 2000). Undue cadherin-11 expression is also associated with kidney fibrosis, another pathology involving EMT (Forino et al., 2006). Interestingly, during development, loss of cadherin-11 expression is often coordinated with appearance of cadherin-6 expression. For instance a cadherin-11 to cadherin-6 switch underlies the kidney mesenchymal to epithelial transition (MET) (Schmidt-Ott et al., 2006). A similar cadherin change occurs during the formation of motoneurons (Marthiens et al., 2002). Intriguingly, both kidney development and motoneurons formation have been shown to involve the orphan nuclear receptor COUP-TFII (NR2F2) (Lutz et al., 1994; Suh et al., 2006) although no mechanistic insight was provided. COUP-TFII is a developmentally expressed mesenchymal molecule that is known to regulate several organogenetic processes (Lin et al., 2011). Interestingly, it has been recently reported to drive prostate cancer progression albeit not through cadherin regulation (Qin et al., 2013) and to promote metastasis of colon carcinoma by up-regulating Snail (Bao et al., 2014). In this report, we investigated the possibility that COUPTFII regulate cadherin-11 and cadherin-6 expression.

2.

Materials and methods

2.1.

Plasmid constructs

COUP-TFII coding sequence was PCR generated (see Electronic Supplementary Material Table S1 for primer sequences) and cloned into pcDNA4/TO (Invitrogen) either alone (pcDNA4/ TO-ONR) or with an N-terminal Xpress tag (pcDNA4/TO-XpressONR). For RNA interference (RNAi), three different oligonucleotides targeting COUP-TFII were cloned in pTER (a gift from van de Wetering et al., 2003): pTER onr881, pTER onr791 and pTER onr911 (see Table S1 for sequences).

2.2.

Cell culture and transfections

MDCK 2 (Dukes et al., 2011), SW800 (Giroldi et al., 1999) and TPC1 (Ishizaka et al., 1990) cells were cultured in RPMI. Human cell lines have been authenticated by Multiplexion. All transfection experiments were performed using Fugene

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(Roche). We used the tetracycline-regulated expression system T-REx (Invitrogen). Cells were transfected with pcDNA6/ TR and selected using 2 µg/ml (MDCK 2 and SW800) or 3 µg/ ml (TPC1) blasticidin. TetR positive clones (assessed with antibody TET01 (MoBiTec)) were then transfected with pcDNA4/TO-Xpress-ONR (MDCK), pcDNA4/TO-ONR (MDCK, TPC1), pTER ONR 881, pTER ONR 791 and pTER ONR 911 (SW800). Positive clones were selected with 100 µg/ml zeocin. The expression of the constructs was induced with 0.5 µg/ml doxycycline (Dox).

2.3.

Antibodies, western blot and immunofluorescence

Primary antibodies used are detailed in Table S2. Santa Cruz secondary antibodies were used at 1/10,000 to 1/40,000 and revealed with Covalight (Covalab) or West Femto (Pierce) chemiluminescent substrates. For western blot (WB), total protein samples were obtained by solubilizing cells or frozen tumors in Laemmli reagent and nuclear extracts were prepared using a protocol adapted from Dignam’s method. Protein concentration was assessed using Quant-iT protein assay (Invitrogen) and loadings were systematically controlled by amido-black staining of the blot. We find this more accurate than probing the blot for highly expressed housekeeping genes such as tubulin, which saturate both membranes and films equalizing the signal in all lanes thus giving a false impression of equal loading (see Fig. S1). For immunofluorescence, cells were cultured on slides, fixed with 3% paraformaldehyde in PBS and permeabilized with 0.1% Triton X-100. Tumor samples and E12.5–15.5 mouse embryos were fixed in formalin, paraffin embedded and cut at 4 µm. Antigen unmasking was performed in 20 mM Tris pH9 at 98 °C for 1 hour. Immunoreactivity was revealed either with a 1/1000 dilution of Alexa Fluor 488 F(ab′)2 fragment of anti-mouse or anti-rabbit IgG (Molecular Probes) or with a biotinylated anti-mouse or antirabbit IgG (Vector) followed by streptavidin Alexa Fluor 594. When necessary, nuclei were stained with DAPI. For immunoperoxydase, an ABC kit (Vector) was used after biotinylated secondary antibodies. In tumors, nuclear staining of endothelial cells was used as internal positive control for COUP-TFII.

2.4.

mRNA analyses

Northern blots were performed as previously described (Giroldi et al., 1999). Probes were PCR generated (see Table S1) using either SW800 cDNA (cadherin-11) or MDCK cDNA (dog cadherin-6). Two cadherin-6 cDNAs have been obtained; the one used as probe encodes the full coding sequence and the other one lacks exon 5 (accession number: HQ845962). For real time quantitative PCR, three micrograms RNA were treated with DNase (RQ1 DNase, Promega). Half of it was saved as negative control and half was retro-transcribed using Superscript II (Invitrogen) and random primers. RT-PCR was carried out on a Lightcycler (Roche) using LightCycler FastStart DNA Master SYBER Green I (Roche). Cyclophillin A was used as control gene. Relative mRNA levels, calculated with the Ct method are represented as bar graphs; uninduced cells have been set to 100%. Primers used are in Table S1.

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3.

Results

3.1. COUP-TFII regulates cadherin-6 and cadherin-11 expression To functionally characterize COUP-TFII with respect to cadherin regulation in cultured cell lines, we used cell lines with low COUP-TFII expression (i.e. trace or negative on WB) to perform forced expression and cell lines with clear-cut high COUP-TFII expression for RNAi. A summary of the experiments performed on cell lines is provided in Table S3. MDCK 2 cells, being tubular kidney cells, express both E-cadherin and cadherin-6 (Stewart et al., 2000). Upon induction of COUP-TFII, no change in E-cadherin expression level was seen but a dramatic decrease of cadherin-6 was evidenced on WB, corresponding with the disappearance of cadherin-6 honeycomb staining of the cells (Fig. 1a). We also observed the repression of cadherin-6 expression by COUPTFII in the human kidney cell line SKRC 28 (Ebert et al., 1990) (data not shown) but we did not work further with these cells because they have a very long doubling time (over 4 days). SW800 cells are a bladder carcinoma cell line expressing cadherin-11, and N-cadherin (Giroldi et al., 1999). We found that they express high level of COUP-TFII and abrogation of COUPTFII expression through RNAi induced down-regulation of cadherin-11 (Fig. 1b) but did not influence N-cadherin level significantly. To get insight into the mechanisms involved in these cadherin expression changes, we performed northern blot analyses which revealed an overall decrease of cadherin-6 mRNA (four transcripts as previously described by Giroldi et al., 1999) in MDCK cells and a clear decrease of cadherin-11 mRNA level in SW800 cells (Fig. 1c and d). qRT-PCR on a clone subset measured a twofold reduction of cadherin-6 mRNA and a fourfold decrease of cadherin-11 mRNA (Fig. 1c and d).

3.2. COUP-TFII triggers a cadherin-6 to cadherin-11 switch in TPC1 cells The above data are in agreement with a model in which COUP-TFII can both inhibit cadherin-6 and promote cadherin11 expression. However, WB analysis and RT-PCR did not reveal induction of cadherin-6 in SW800 cells deprived of COUP-

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TFII nor did cadherin-11 appear in MDCK cells over-expressing COUP-TFII (data not shown). We hypothesized that COUPTFII cannot by itself switch on a cadherin gene that has been completely shut off but would be able to enhance a gene expression persisting in a cell on a low basal level. Among the cell lines we screened, the thyroid line TPC1 appeared as a tool of choice to test this hypothesis as it displays a fair amount of cadherin-6 but weak levels of both COUP-TFII and cadherin11. A transfection experiment yielded three positive clones overexpressing COUP-TFII upon induction. As anticipated, induction of COUP-TFII expression was associated with induction of cadherin-11 expression together with extinction of cadherin-6 expression (Fig. 2a and b); qRT-PCR revealed mRNA switching accordingly (Fig. 2c).

3.3. Arrest of COUP-TFII expression matches the cadherin switch on kidney development Remarkably, cadherin-11 to cadherin-6 switches have been reported during motoneuron differentiation and kidney embryogenesis (Marthiens et al., 2002; Schmidt-Ott et al., 2006) but the regulatory mechanisms have remained undisclosed. As both developmental events were shown to involve COUPTFII (Lutz et al., 1994; Suh et al., 2006), our above findings strengthen our initial surmise that COUP-TFII is implicated in these cadherin switches. To get insight into this, we assessed the spatiotemporal pattern of COUP-TFII, cadherin-6 and cadherin-11 expressions during kidney embryogenesis, by performing double labelings of COUP-TFII and cadherin-11 on one hand and COUPTFII and cadherin-6 on the other hand, in the developing kidney of mouse embryos. We show that the arrest of COUP-TFII signal matches the disappearance of cadherin-11 and the induction of cadherin-6 in cells becoming epithelial (Fig. 3a–d). As we have shown previously that COUP-TFII both can repress cadherin-6 and support cadherin-11 expression, it may be speculated that COUP-TFII blocks the cadherin-11 to cadherin-6 switch occurring during the kidney mesenchymal–epithelial transition.

3.4. Gastric and esophageal adenocarcinomas with high COUP-TFII expression also display cadherin-11 expression Cadherin switching has long been implicated in tumor development and progression. Particularly, aberrant cadherin-

Fig. 1 – COUP-TFII regulates cadherin-6 and cadherin-11. (a) COUP-TFII represses cadherin-6 expression in MDCK cells. Left: WB of total proteins from MDCK clones before (−) and after (+) induction of COUP-TFII expression for 2 days (826-17) or 4 days (ONRfl-22). COUP-TFII is untagged (46 kDa) in 826-17 and Xpress-tagged (~56 kDa) in ONRfl-22. Right: Immunofluorescence staining of cadherin-6 before (−Dox) and after (+Dox) induction of COUP-TFII. (b) COUP-TFII ablation turns off cadherin-11 in SW800 cells. Left: WB of SW800 clones before (−) and after (+) abrogation of COUP-TFII expression by RNAi using oligos 791, 911 or 881. Three different targeting oligos were used to avoid off targeting artifacts. Dox treatment was for 4 days. Two clones are shown in each case. Cadherin-11 was evaluated on total proteins and COUP-TFII on nuclear extracts. Right: Immunofluorescence staining of cadherin-11 before (−Dox) and after (+Dox) extinction of COUPTFII expression. (c) Analysis of cadherin-6 mRNA in MDCK clones. Left: northern blot (upper and lower parts of the same blot are shown); as previously reported there are 4 cadherin-6 mRNA species (Giroldi et al., 1999). LacZ-6 is a transfection control clone expressing β-galactosidase upon induction. ONRfl-22, -9 and -17 are clones expressing Xpress-tagged COUPTFII upon induction (+). Two independent experiments are shown for each clone. G3PDH: loading control. Right: qRT-PCR in clone ONRfl-22 (mean ± standard error). (d) Analysis of cadherin-11 mRNA expression in SW800 clones after inhibition of COUP-TFII expression (+). Left: northern blot; G3PDH: loading control. Right: qRT-PCR (mean ± standard error).

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Fig. 2 – COUP-TFII triggers a cadherin-6 to cadherin-11 switch in TPC1 cells. (a) Immunofluorescence staining of cadherin11 and cadherin-6 before (−Dox) and after (+Dox) induction of COUP-TFII expression. (b) WB of total proteins from TPC1 clones before (−) and after (+) induction of COUP-TFII expression for 3 days (a longer film exposure is shown for clone 9). (c) qRT-PCR in clone 9 (mean ± standard error).

11 expression has been reported in aggressive breast and prostate tumors (Sarrio et al., 2008; Tomita et al., 2000) and is alleged to explain the tendency for bone metastasis of these tumors (Huang et al., 2010; Tamura et al., 2008). Interestingly, COUP-TFII was recently implicated in prostate and colon cancer progression (Bao et al., 2014; Qin et al., 2013). We wondered

whether COUP-TFII expression is frequent in carcinoma. To this end, we screened a few tumors of different origins (bladder, colon, oesophagus, stomach, lung, thyroid and kidney), using IHC, to determine if and where COUP-TFII is overexpressed. It immediately appeared that gastric and oesophageal adenocarcinomas frequently display prominent

m e c h a n i s m s o f d e v e l o p m e n t 1 3 6 ( 2 0 1 5 ) 6 4 –7 2

expression of COUP-TFII in some areas (Fig. 3e). We assessed cadherin-11 expression in all of the six samples (three gastric and three oesophageal) with high COUP-TFII expression. Remarkably, all of them also display cadherin-11 immunoreactivity matching the areas expressing COUP-TFII, although the staining is not strong (Fig. 3f) and often with a focal pattern. Although this corresponds to the staining pattern reported in the literature for cadherin-11 positive tumors (Tomita et al., 2000), we further assessed cadherin-11 expression by WB, using the only COUP-TFII positive adenocarcinoma available as a frozen sample. Only one band with the expected size was obtained, confirming cadherin-11 expression (Fig. 3h). On the other hand, all of the eight COUP-TFII negative tumors (three gastric and five oesophageal) were clearly negative for cadherin-11 (p = 0.03% using Fisher exact test). Characteristics of the screened tumors are provided in Table S4. COUP-TFII was not frequently expressed in other tumor types in the limited series we analyzed.

4.

Discussion

We have shown that COUP-TFII regulates cadherin-6 and cadherin-11 in cultured cell lines. As COUP-TFII is a transcription factor, it may be hypothesized this regulation to be direct, particularly since COUP-TFII binds to DNA in a rather promiscuous way (Benoit et al., 2006; Lou et al., 1999). Cadherin-6 and -11 regulatory sequences not being defined yet, we did not address to this question in this paper. Moreover, the possibility also exists that the regulation be indirect like the negative regulation of E-cadherin by TWIST that goes through SNAIL1 (Casas et al., 2011). A recently released paper describes positive regulation of SNAIL1 by COUP-TFII with consequent downregulation of E-cadherin expression in colon cell lines (Bao et al., 2014). Although SNAIL2 has been shown to down-regulate cadherin-6 gene directly by binding to E-boxes in his regulatory sequences (Taneyhill et al., 2007), it seems unlikely that the regulation of cadherin-6 by COUP-TFII in MDCK cells goes through a SNAIL family member because E-cadherin expression remains very stable. Furthermore, the regulation of E-cadherin by COUP-TFII is certainly context dependent as we did not observe down-regulation in several epithelial cancer cell lines (Bringuier and Giroldi, 2014). COUP-TFII is known to interact with a plethora of molecular partners to positively or negatively modulate gene expression (Benoit et al., 2006) and it is likely that its effect is dependent on the partners available in different cell lines. As a matter of fact, we observed it can modulate cadherin-6 or cadherin-11 expression only in cell lines already expressing these cadherins. Our data suggest that COUP-TFII curbs the kidney MET through maintenance of cadherin-11 expression and inhibition of cadherin-6 expression in the metanephric mesenchyme. Indeed, cadherin-6 expression is instrumental in the kidney MET (Mah et al., 2000). Hence, the kidney developmental MET possibly involves arrest of COUP-TFII expression as one triggering signal. Definitive evidence of this should require mice genetically engineered to continue expressing COUP-TFII in cells of the developing kidney after the endogenous COUP-TFII molecule has been switched off. Moreover, the reverse phenomenon, i.e. EMT and consequently fibrosis, might involve undue reexpression of COUP-TFII in the adult kidney.

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Importantly, also motoneurons express both COUP-TFII and cadherin-11 at early stages of development and later lose both COUP-TFII and cadherin-11 and start expressing cadherin-6 in some populations, although these studies have been performed in chicken as far as COUP-TFII is concerned (Lutz et al., 1994) and in mouse with regard to cadherin-6 and -11 (Marthiens et al., 2002). We speculate that COUP-TFII is involved in the control of the coordinated variations of cadherin-6 and cadherin-11 expressions reported in nervous system development. Hence, it might be useful to follow the motoneurons developmental expression pattern of all three molecules in the same species. Complementary expression of cadherin-6 and -11 also occur in endometrial stromal cells where progesterone regulates the mRNA levels of both these cadherins (Getsios et al., 1998), a regulation possibly involving COUP-TFII (see below). To our knowledge, this is the first report of a frequent expression of COUP-TFII in gastric and esophageal tumors, associated with cadherin-11 expression; this suggests reactivation of embryonic pathways linked to COUP-TFII in these tumors. Studies concerning COUP-TFII expression in tumors are still scarce. Our findings and the recent involvement of COUP-TFII in prostate adenocarcinoma progression (Qin et al., 2013) suggest COUP-TFII might be responsible for the abnormal expression of cadherin-11 by certain prostate tumors. Also breast tumors often express cadherin-11 in connection with the basal-like phenotype, EMT, and metastasis to bone (Sarrio et al., 2008) and a previous report about breast tumors claims COUP-TFII expression is a bad prognosis factor (Nagasaki et al., 2009). Abnormal expression of Cadherin-11 by prostate or breast tumor cells is thought to favor the anchoring and invasion into the bone tissue which physiologically expresses this cadherin. This is reminiscent of a proposed physiological function of Cadherin-11 that would be to mediate the interaction between trophoblast cells and the decidualized endometrium, thus enabling throphoblast invasion and implantation of the embryo (MacCalman et al., 1996). As already mentioned, the endometrial stroma is another example of a tissue expressing both cadherin-6 and cadherin-11 in a coordinated manner controlled by progesterone (Getsios et al., 1998), the accumulation of cadherin-11 correlating with decidualization (MacCalman et al., 1996). Significantly, COUP-TFII has been reported to mediate progesterone regulation of uterine implantation with defective decidualization in uterus-targeted COUP-TFII KO animals (Kurihara et al., 2007). We surmise this might result partly from lack of cadherin-11. Although COUP-TFII has long been known as a key factor in development, acting through pleiotropic mechanisms (Lin et al., 2011) this report is the first to show its involvement in cadherin-6 and -11 regulation in relation with morphogenetic processes. The hijacking of embryonic pathways based on cadherin switching being largely documented in cancer and fibrosis, our data suggest COUP-TFII is a player in this field.

Acknowledgements We thank WJ Nelson, RM Mège and M van de Wetering for providing reagents. We acknowledge G Clain’s help with cutting the embryos and we thank Marie Chanal and Clémentine

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Fig. 3 – In vivo COUP-TFII and cadherins expression data. (a–d) Coordinated expression of COUP-TFII, cadherin-6 and cadherin-11 observed during kidney development. E13.5 (a and b) and 15.5 (c and d) mouse embryos labeled for COUP-TFII (red) and cadherin-6 (a and c, green) or cadherin-11 (b and d, green). Cadherin-11 is co-expressed with COUP-TFII in mesenchyme (b, d) and both molecules stop being expressed in cells undergoing mesenchymal–epithelial transition whereas cadherin-6 rises (c, a, arrows). Cells having completed their epithelial transition express high levels of cadherin-6 (c, a, arrowheads). Ureteric buds express E-cadherin and do not express COUP-TFII (not shown). (e–h) Co-expression of COUP-TFII and cadherin-11 in tumors. Serial sections of a gastric adenocarcinoma stained for COUP-TFII (e) or cadherin-11 (f); (g): no primary antibody. Cells with nuclear expression of COUP-TFII also express cadherin-11 in their cytoplasm. (h) WB analysis of cadherin-11 expression in a gastric adenocarcinoma not expressing COUP-TFII (T neg), a gastric adenocarcinoma expressing COUP-TFII (T pos) and the cell line TPC1 used as positive control (Ctl). Lower panel: A pancytokeratin antibody has been used to check equal epithelial content of tumor samples.

Moreau for technical assistance. We are very grateful to J Samarut for advices and to Frank Smit and JY Scoazec for support. This work was supported by the Association for International Cancer Research (98-54) (LAG) and the Ligue Nationale Française contre le Cancer (PPB).

Appendix: Supplementary material Supplementary data to this article can be found online at doi:10.1016/j.mod.2015.02.001.

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Involvement of orphan nuclear receptor COUP-TFII in cadherin-6 and cadherin-11 regulation: implications in development and cancer.

Changes in cadherin expression are instrumental both in embryonic development and disease, underlining the importance of understanding how cadherin ex...
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