ARTICLE |
Correspondence to: Ziedonis Skobe, The Forsyth Institute, 140 the Fenway, Boston, MA 02115. E-mail: zskobe@forsyth.org
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Summary |
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E-cadherin, a calcium-dependent cellcell adhesion molecule, is expressed in highly specific spatiotemporal patterns throughout metazoan development, notably at sites of embryonic induction. E-cadherin also plays a critical role in regulating cell motility/adhesion, cell proliferation, and apoptosis. We have used the continuously erupting rat incisor as a system for examining the expression of E-cadherin and the associated catenins [-, ß-,
-catenin (plakoglobin) and p120ctn] during amelogenesis. Using immunhistochemical techniques, we observed expression of
-catenin and
-catenin in ameloblasts throughout amelogenesis. In contrast, expression of E-cadherin, ß-catenin, and p120ctn was strong in presecretory, transitional, and reduced stage ameloblasts (Stages I, III, and V) but was dramatically lower in secretory and maturation stage ameloblasts (Stages II and IV). This expression alternates with the expression pattern we previously reported for the adenomatous polyposis coli protein (APC), a tumor suppressor that competes with E-cadherin for binding to ß-catenin. We suggest that alternate expression of APC and the cadherincatenin complex is critical for the alterations in cellcell adhesion and other differentiated cellular characteristics, such as cytoskeletal alterations, that are required for the formation of enamel by ameloblasts. (J Histochem Cytochem 48:397406, 2000)
Key Words: cadherin, catenin, plakoglobin, APC, p120ctn, tooth development, ameloblast, enamel, amelogenesis
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Introduction |
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Tooth development, like most morphogenetic processes, requires iterative inductive interactions between apposed groups of epithelial and mesenchymal cells. In tooth development, these are initiated by in-migrating neural crest cells, which induce a thickening of the stomadeal epithelium forming the dental lamina (
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The epithelial cadherins, E- and P-cadherin, have been reported to be expressed early in amelogenesis (-catenin (the latter is identical to plakoglobin) (
-catenin, which interacts directly (
Dramatic changes in E-cadherin expression occur at sites of embryonic induction (
ß-Catenin can interact with a variety of proteins in addition to the cadherins and -catenin (
-catenin (
The interaction of ß-catenin with the transcription factor LEF-1 may also be important in tooth development. ß-Catenin interacts with LEF-1 to alter transcriptional activation by LEF-1 (
The importance of E-cadherin, ß-catenin, and APC in cell differentiation and morphogenesis in a variety of systems suggested that these three proteins might also play important roles in tooth development and amelogenesis. A study of early first molar development in the mouse showed that E-cadherin is expressed in cells of the outer enamel epithelium, stellate reticulum, and stratum intermedium in bud, cap, and early bell stages, and P-cadherin is expressed in inner enamel epithelium (-actinin and vinculin (
-actinin, and vinculin were localized only in basal (proximal) and apical (distal) terminal web complexes (
-actinin, vinculin, and desmoplakin I/II, are oriented primarily perpendicular to the longitudinal axis of the incisor (
Given the dramatic alterations in APC expression during the ameloblast life cycle, the known ability of APC to compete with E-cadherin for ß-catenin binding, and the roles of all three proteins in regulation of cell motility/adhesion and in morphogenetic activities, including differentiative signaling, it seemed likely that the cadherincatenin complex, as well as APC, would play a critical role in amelogenesis. As a first step towards investigating this possibility, we describe here the expression patterns of E-cadherin and the catenins in the continuously erupting rat incisor.
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Materials and Methods |
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All animals used in this work were housed in an AAALAC-approved facility and all operations were performed in accord with protocols approved by The Forsyth Institute's IACUC.
Antibodies
Anti-E-cadherin (clones 34 or 36) and monoclonal antibodies to -catenin (clone 5), ß-catenin (clone 14),
-catenin (clone 15), and p120ctn (clone 98) were obtained from Transduction Laboratories (Lexington, KY). Anti-APC antibody (CC-1) was obtained from Calbiochem (Cambridge, MA). Peroxidase-conjugated anti-mouse secondary antibody and the Vectastain Elite ABC kit were obtained from Vector Laboratories (Burlingame, CA).
Electrophoresis and Western Blotting
Human gingival tissue was waste tissue from patients undergoing surgery for periodontal disease, obtained under an IRB-approved protocol. Enamel organs (four maxillary and four mandibular) were dissected from euthanized adult inbred Rowett rats.
A-431 cells were obtained from the ATCC (Rockville, MD) and were grown in Dulbecco's modified Eagle's medium containing 10% heat-inactivated fetal calf serum. Immortalized human gingival keratinocytes (IHGK;
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Immunohistochemistry
Maxillary and mandibular incisors obtained from euthanized adult inbred Rowett rats were fixed in 5% neutral formal/saline overnight, incubated in PBS containing 0.1% Triton X-100 for 8 hr, rinsed overnight with running water, and decalcified in 20% sodium citrate/45% formic acid for 2 weeks. This and all subsequent incubations were at ambient temperature unless otherwise indicated. The incisors were dehydrated in a graded series of ethanols and embedded in paraffin for sectioning. Deparaffinized and rehydrated sections were quenched with 0.3% H2O2 in methanol for 30 min, rinsed with PBS, and blocked with 5% horse serum in PBS for 30 min. The sections were then incubated with primary antibody (see above) at concentrations of either 1 µg/ml or 5 µg/ml for 1 hr at room temperature (anti-E-cadherin, anti-ß-catenin, and anti-p120ctn) or overnight at 4C (anti--catenin, and anti-
-catenin). Sections of human and rat gingivae were used as positive control (Fig 3). Sections incubated without primary antibody were used as negative controls, and consistently did not show any staining. Antibody binding was visualized using the Vectastain ABC Elite Universal kit (Vector Laboratories) with Sigma Fast DAB (Sigma; St Louis, MO) as the substrate. Sections were counterstained with 0.1% Fast Green in PBS for 2 min, dehydrated, and mounted. Sections for double staining were rinsed in water and PBS after DAB staining following the first primary antibody, blocked with 5% normal horse serum, and incubated with the second primary antibody overnight at 4C. The sections were rinsed in PBS and developed using the Vectastain Elite ABC kit with Vector VIP as the enzyme substrate, counterstained, dehydrated, and mounted.
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Results |
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Antibody Specificity and Western Blotting
Enamel organ extracts were subjected to Western blotting to verify the antibody specificities and the presence of the antigens in the enamel organ. As shown in Fig 2, Coomassie blue staining (CB) detected a large number of high molecular weight proteins in extracts of both enamel organ and immortalized human gingival keratinocytes (IHGK). Similar results were obtained for the A-431 cell extract. The antibodies detected bands with the expected migrations, confirming that the antibody specificities were as indicated by the manufacturers and that the antigens were present in the enamel organ. Anti-E-cadherin recognized a single band migrating at 124 kD in extracts of both rat enamel organ and A-431 cells. Anti-ß-catenin recognized a single band migrating at 99 kD. The anti-p120ctn antibody recognized bands migrating at 110 and 120 kD. The more rapidly migrating form is probably one of the alternatively spliced forms of p120ctn (-catenin recognized the expected band migrating at 102 kD, and anti-
-catenin recognized a single band migrating at 85 kD.
Immunohistochemistry
No reaction was observed in control sections incubated without primary antibody. Moderate staining with the antibodies against -catenin and
-catenin was seen in ameloblasts at all stages of amelogenesis (Fig 4). Immunohistochemical staining using the monoclonal antibodies against E-cadherin, ß-catenin, or p120ctn resulted in intense staining (brown/black) of cell contact sites in the middle layers of human oral epithelium (Fig 3). Similar reaction was observed in rat epithelium (not shown) in sections of forming rat incisors, confirming reactivity of the antibody with both species. Antibodies to
-catenin and
-catenin moderately stained cellcell surfaces most strongly in middle layers of human epithelium, with weaker staining of basal cells (Fig 3).
Presecretory stage ameloblasts (Stage I) and stratum intermedium cells showed strong expression of E-cadherin (Fig 5A) and ß-catenin (Fig 5B). Ameloblasts, but not stratum intermedium cells, bound anti-p120ctn at this stage (Fig 5C). Although diffuse staining was observed throughout the cytoplasm of ameloblasts, staining was concentrated along basolateral cell membranes. Odontoblasts weakly expressed ß-catenin (Fig 5B) but not E-cadherin (Fig 5A).
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In early secretory-stage ameloblasts, the expression of E-cadherin, ß-catenin, and p120ctn decreased at the stage where Tomes' processes were seen in the sections (Fig 5). Expression of E-cadherin and ß-catenin persisted longer in stratum intermedium cells than in ameloblasts (Fig 6A and Fig 6B), but staining of the former was greatly reduced in the late secretory stage (Fig 7A and Fig 7B).
Transition-stage ameloblasts (Stage III) showed strong reactions with the anti-E-cadherin (Fig 7A), anti-ß-catenin (Fig 7B), and anti-p120ctn (Fig 7C) antibodies, with the most intense staining along the lateral cell membranes. We observed no staining with these antibodies of any other cell type in the transition-stage enamel organ.
In Stage IV (maturation stage), weak expression of E-cadherin was observed along lateral borders of ameloblasts and in the apical and terminal web junctional complexes (Fig 8A). At this stage, the only significant reaction observed with the anti-ß-catenin antibody was with the distal papillary cells (Fig 8B). Proximal papillary cells (those adjacent to the ameloblasts) showed little or no reaction with either the anti-E-cadherin or the anti-ß-catenin antibody (Fig 8A and Fig 8B). A slight reaction was observed with the anti-p120ctn antibody in maturation-stage ameloblasts and distal papillary cells.
In the late maturation stage (Fig 9A) and in the reduced stage (Fig 10A), ameloblasts showed strong membrane-localized expression of E-cadherin, but the papillary cells reacted weakly. In late maturation and the reduced stage, both ameloblasts and papillary cells reacted with anti-ß-catenin (Fig 9B and Fig 10B) and p120ctn (Fig 9C and Fig 10C).
Double staining with anti-E-cadherin (purple) and anti-APC (dark brown) confirmed the alternating expression of these two proteins (Fig 11). E-cadherin was expressed in ameloblasts in the early presecretory stage, and APC was expressed as ameloblasts differentiated into the secretory stage, at the site where dentin formation is first seen in the sections.
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Discussion |
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E-cadherin expression in mouse embryo craniofacial development has been reported as early as Day 14 (-catenin and
-catenin during amelogenesis were less dramatic (Fig 4).
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We observed high levels of E-cadherin and ß-catenin expression in cells altering their differentiation status but participating in relatively stable adhesion (presecretory, transition, and reduced stages, or Stages I, III, and V). This is consistent with the importance of E-cadherin and ß-catenin in mediating the formation of relatively stable junctions between epithelial cells and in transmitting differentiative signals. It contrasts sharply with the low expression of E-cadherin and ß-catenin, but high levels of APC expression were observed in secretory-stage cells (Stage II) that are actively moving relative to their neighbors or in maturation-stage cells (Stage IV) that frequently alter their apical and basal junctions (
APC has been reported to perform more than one function within the same cell (
In summary, -catenin and
-catenin are present in ameloblasts throughout amelogenesis. The staining intensity of the other components of the cadherincatenin complex alternates through the stages of the enamel organ life cycle. Presecretory-stage (I) ameloblasts, undergoing their initial differentiation, express E-cadherin strongly (Fig 5A) but have no detectable APC expression (
The rat incisor enamel organ is the only tissue we are aware of in which the expression of APC and the cadherincatenin complex alternates several times during the life cycle of the cells. The continuously erupting rat incisor thus offers obvious advantages for studying both the mechanisms of regulation of expression of these proteins during development and their functions.
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Acknowledgments |
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Supported by The Forsyth Institute and by the Colgate Palmolive Company.
Received for publication May 27, 1999; accepted October 28, 1999.
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