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J Dent Res 82(1): 17-22, 2003
© 2003 International and American Associations for Dental Research

RESEARCH REPORT
Biological

Cadherin-related Neuronal Receptors in Incisor Development

E. Fukumoto1,*, H. Sakai2, S. Fukumoto3, T. Yagi4, O. Takagi1, and Y. Kato2

1 Department of Preventive Dentistry,
2 Dental Pharmacology, and
3 Pediatric Dentistry, Nagasaki University School of Dentistry, Nagasaki 852-8588, Japan;
4 CREST, KOKORO Biology Group, Laboratories of Intedgrated Biology, Graduated School of Frontier Biosciences, Osaka University, 1-3 Yamadaoka, Suita 565-0871, Japan;

*corresponding author, emiko{at}net.nagasaki-u.ac.jp


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cadherins are cell adhesion molecules that are critical for tissue development. In this report, we identified members of the cadherin family cadherin-related neuronal receptors (CNRs) 1 and 5 expressed in rat incisors by the differential display method. Quantitative RT-PCR revealed that CNR1 mRNA is expressed in the secretory stage but reduced in the early-maturation stage, while CNR5 mRNA is expressed in both these stages. In situ hybridization showed that strong expression of CNR1 is strong in the secretory stage, but reduced in the early phase and diminished in the late phase of the early-maturation stage. CNR5 mRNA is expressed almost at the same levels in the secretory and in the early phase of the early-maturation stages but is absent in the late phase of the early-maturation stage. Both CNR1 and 5 mRNA are continuously expressed in odontoblasts. Immunohistology showed that CNR proteins are expressed in the secretory and early-maturation stages of ameloblasts, but no protein expression at the late-maturation stage was observed. CNR proteins were continuously expressed in odontoblasts. We found that recombinant CNR1 binds dental epithelial and mesenchymal cells through N-terminal domain EC1 in vitro. These results suggest that CNR1 and CNR5 may play an important role in enamel and dentin formation, probably through cell-cell and/or cell-matrix interactions.

KEY WORDS: cadherin-related neuronal receptor • incisor • ameloblast • odontoblast


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The mammalian tooth has a specialized structure that develops through a series of reciprocal epithelial-mesenchymal interactions, ultimately resulting in the formation of the enamel, dentin, cementum, and pulp (Thesleff and Hurmerinta, 1981; Smith, 1998). Studies of these processes have identified transcription factors, growth factors, and extracellular matrix molecules that regulate tooth development (Ruch, 1995; Thesleff et al., 1995; Thesleff and Nieminen, 1996). Cadherins are cell adhesion molecules that mediate cell-cell and cell-matrix interactions during tooth formation. Classic cadherins, E-cadherin and P-cadherin, are expressed specifically in the early stage of dental epithelium but not in odontoblasts (Obara et al., 1998). It has been shown that cadherin-mediated cell adhesion is regulated by transcription factors Msx1 and Msx2 during amelogenesis (Lincecum et al., 1998). These results suggest that the classic cadherins play an important role in tooth morphogenesis through mediating cell-cell and/or cell-matrix interactions. However, the expression of E-cadherin and P-cadherin is restricted to the dental epithelium, and their expression levels are decreased in later development stages, suggesting that ameloblasts express other adhesion molecules at later stages that should play a role in cell-cell and cell-matrix interactions during amelogenesis.

Cadherin-related neuronal receptor (CNR) is a new member of the cadherin family and was shown to bind Fyn tyrosine kinase in the brain (Kohmura et al., 1998). CNR proteins consist of about 20 isoforms, which are derived from different genes. Each CNR contains six extracellular cadherin-like domains (EC) similar to cadherins but has a distinct cytoplasmic domain that interacts with Fyn. It has been shown that CNRs are expressed specifically in the brain and are localized to synaptic junctions. CNR family proteins bind to reelin (Senzaki et al., 1999), an extracellular glycoprotein that regulates layering and positioning of neurons (Ogawa et al., 1995; Frotscher, 1997). These findings suggest that CNRs play a role in specific neuronal connections, signal transduction at synaptic junctions, and neuronal differentiation through extracellular matrix interaction.

In this study, we identified partial cDNA segments for CNR1 and 5 by differential display from rat incisors. We demonstrated for the first time that CNR1 and 5 are expressed in the developing tooth in a stage-specific manner and bind dental epithelial and mesenchymal cells, suggesting that CNRs play an important role in odontogenesis.


   MATERIALS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Animals and Cell Culture
Wistar rats (from 4 to 25 wks old) and B6 mice (4 wks old) were obtained from Japan SLC (Shizuoka, Japan). Mandibular molars were dissected from post-natal day 3 (P3) mice, and dental epithelial and mesenchymal cells were prepared as described (Kukita et al., 1992; Den Besten et al., 1998). The cells were cultured on type I collagen (Nitta Geratin Co., Osaka, Japan) in keratinocyte-SFM for dental epithelial cells and D-MEM supplemented with 10% fetal bovine serum for dental mesenchymal cells (Invitrogen, Carslbad, CA, USA).

RNA Isolation and Differential Display
Total RNA was prepared from three different stages of rat enamel organs—secretory (S), early maturation (EM), and late maturation (LM) stages—with the use of TRIZOL (Invitrogen) (Miyazaki et al., 1998). The differential display method was performed as previously described (Liang and Pardee, 1992). We used two sets of primers—forward random primers and either reverse-mixture primers of oligo(dT)15A, oligo(dT)15G, and oligo(dT)15C, or reverse oligo(dT)20M13 forward primer—to ensure faithful RT-PCR. The PCR products were separated on 5% polyacrylamide gels and silver-stained by means of the Plus One DNA silver staining kit (Amersham Pharmacia Biotech, Buckinghamshire, UK). Bands of interest were excised, re-amplified, and cloned into the pBluescript SK II vector (Stratagene). Sequence analysis was performed in the ABI Prism 310 genetic analyzer (Applied Biosystems, Foster City, CA, USA). BLAST search protocols were used for sequence homology.

RT-PCR for CNRs
Total RNA was prepared from adult and P1 rats (Miyazaki et al., 1998). For detection of all CNR mRNA species, a primer set from a conserved region of CNR cDNAs was used. Reverse transcription was performed at 37°C for 90 min and PCR for 1 min at 95°C, 1 min at 60°C, and 1 min at 72°C for 25 cycles. PCR products were analyzed on 1.2% agarose gels. Quantitative real-time PCR for CNR1 and CNR5 was performed with specific primers with SYBR Green PCR Master Mix by TaqMan 7700 Sequencer Detection (Applied Biosystems) for 1 min at 95°C, 1 min at 60°C, and 1 min at 72°C for 40 cycles. (These primer sequences are shown in the Appendix, www.dentalresearch.org.).

In situ Hybridization
Tissues were fixed with 4% paraformaldehyde by cardiac perfusion. The maxilla was dissected, fixed, and decalcified with 10% EDTA. cDNA for rat CNR1 and CNR5 was obtained from rat enamel organ RNA by RT-PCR with the specific primers used for the Quantitative PCR analysis. Probes were prepared with a DIG-RNA Labeling Kit (Roche, Basel, Switzerland). In situ hybridization was performed as described by Nakase et al. (1994). Specificity of the probes was confirmed by Northern blot and/or in situ hybridization.

Immunohistochemical Staining
Sections were immunostained as described by Sakai et al. (1989), with an antibody (6-1B) against CNRs (Kohmura et al., 1998) and peroxidase-conjugated anti-mouse Igs (Biosource, Camarillo, CA, USA). Sections were visualized by means of a Histofine-AEC kit (Nitirei, Tokyo, Japan). Counterstaining for the nuclei was performed with methyl green.

Recombinant CNR1 and Cell Binding
cDNA for recombinant CNR1 proteins tagged with the Hisx6 or HA sequence was generated by PCR and cloned into pCEP4 (Invitrogen). Plasmids were transiently transfected into 293-EBNA cells, and fusion proteins were purified by affinity columns. FITC-conjugated recombinant CNR1 proteins were incubated with tooth germ cells for cell-binding assays. (Detailed protocols are shown in the Appendix, www.dentalresearch.org.)


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Molecular Cloning of CNR1 and CNR5 from Rat Incisors
To identify genes involved in tooth development, particularly amelogenesis, we applied the differential display method using RNA from the secretory, early-maturation, and late-maturation stages of rat enamel organ (Fig. 1AGo). With two different sets of primers in different gels, we identified 13 cDNA bands that showed preferential expression in the secretory and early-maturation stages, but not in the late stage. Sequencing of these bands revealed that they encode various proteins, including amelogenin, {alpha}1(I) collagen chain, fibulin-2, CNR1 and 5 (arrows in Figs. 1Ab and cGo), as well as est clones. Since expression of CNR1 and 5 has not been reported in the developing tooth, we further characterized these genes. Subsequently, we screened a rat incisor cDNA library and obtained larger coding sequences for CNR1 and CNR5. The C-terminal amino acid sequence was conserved in the CNR family among the rat, mouse, and human, with only two amino acid differences between the rat and mouse and four amino acid differences between the rat and human. The conserved C-terminal region contains four PXXP motifs, which are potential SH3 domain-binding sites (Fig. 1BGo).



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  		Figure 1. Isolation of CNRs by Differential Display Method. (A) (a) Schematic diagram of the differential display method using three different stages of ameloblasts: secretory (S), early-maturation (EM), and late-maturation (LM) stages. Panels (b) and (c) show differential displays with reverse primers oligo(dT)15A and oligo(dT)15G, respectively. Arrows represent CNR1 (b) and CNR5 (c) cDNA identified by band sequencing. (B) Schematic structures of cadherins and CNRs. Bold lines under CNRs represent conserved regions in the CNR family. S, signal peptide; EC, extracellular domain; TM, transmembrane domain; CP, cytoplasmic domain. A comparison of rat, mouse, and human C-terminal protein sequences is also shown. The nucleic acid and amino acid sequences for these clones were deposited in GenBank (accession number AB045585 for CNR1 and AB045586 for CNR5). (C) Tissue-specific expression of CNR mRNA in adult (upper) and P1 rats (lower) was analyzed by RT-PCR. Primers from the conserved regions were used. CNRs were expressed in the brain and incisor but not in other tissues. (D) mRNA expression was quantified by real-time PCR in three stages of ameloblasts. The relative percentage in each stage is shown in relation to the highest value as 100%. Statistical analysis was performed with the use of InStat3 software (GraphPad Software, San Diego, CA, USA). All results were expressed as mean ± SE, and P < 0.05 was used for significance. S, secretory stage; EM, early-maturation stage; LM, late-maturation stage.

 
Expression of CNR mRNA in Rat Incisors
We examined the expression of CNRs in adult and post-natal day 1 (P1) tissues by RT-PCR using common primers derived from the conserved regions, with which all mRNA species for CNR1 to 8 were detectable. CNR mRNAs were expressed in the brain and incisor of adult and P1 rats but not in other tissues examined (Fig. 1CGo). To confirm the RT-PCR products, we cloned the RT-PCR products from P1 incisor RNA into a plasmid vector, randomly picked about 30 clones, and sequenced their cDNA inserts. Sequence analysis revealed that the majority of CNR clones encoded either CNR1 or CNR5, and the remaining clones encoded all other previously identified CNR species and some unknown, potentially new, members of the CNR family. Real-time quantitative RT-PCR analysis showed that CNR1 mRNA was highly expressed in the secretory stage but not the early-maturation stage, while CNR5 mRNA expression was observed in both the secretory and early-maturation stages. The levels of both CNR1 and 5 mRNA were significantly reduced in the late-maturation stage (Fig. 1DGo). Amelogenin mRNA, an ameloblast-specific gene, was highly expressed in the secretory stage of ameloblasts, as expected (Fig. 1DGo). In situ hybridization revealed that CNR1 and 5 mRNA were expressed in the pre-secretory and secretory stages of ameloblasts in incisors (Fig. 2Go) and also in the early stages of the early-maturation stage but not in the late-maturation stage. Both mRNA were expressed continuously in odontoblasts.



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  		Figure 2. In situ hybridization of CNR1 and CNR5 mRNA in the rat incisor. (A) Whole stages of ameloblasts and odontoblasts. Arrows indicate the points of the signal that disappeared in ameloblasts. (B) Tissues were hybridized with CNR5 antisense (a,d,g,j), CNR1 antisense (b,e,h,k), and CNR5 sense cRNA probes (c,f,i,l). Bulbous portion of the odontogenic epithelium (a,b,c); secretory stage (d,e,f); early-maturation stage (g,h,i); and late-maturation stage (j,k,l). Magnification: x40. am, ameloblasts; od, odontoblasts. (C) High magnification of CNR5 mRNA expression. CNR5 antisense (a, c, e) and sense cRNA probes (b, d, f); secretory stage (a, b); early-maturation stage (c, d); and late-maturation stage (e, f). Magnification: x200. am, ameloblasts; pc, papillary cell layer. Scale bars: 50 µm (Bl); 20 µm (Cf).

 
Immunostaining of CNRs
We next analyzed CNR proteins by immunostaining using a monoclonal antibody that recognizes all CNR family proteins (Fig. 3Go). CNR proteins were stained in the pre-secretory, secretory, and early-maturation stages of ameloblasts but not in the late-maturation stage (Fig. 3Go). The signal was also detected in all stages of odontoblasts. CNRs were localized in dental epithelium and mesenchymal cells toward the epithelial-mesenchymal interface at the early stage (Fig. 3AaGo).



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  		Figure 3. Immunolocalization of CNRs in rat incisor (red). (A) A monoclonal antibody that reacts with all CNR isoforms was used. The bulbous portion of the odontogenic epithelium and mesenchyme (a), secretory stage (b), early-maturation stage (c), and late-maturation stage of ameloblasts (d). Magnification: x40. (B) High magnification of the early-maturation stage of ameloblasts and odontoblasts (a); second antibody only (b). Magnification: x200. am, ameloblasts; pc, papillary cell layer; od, odontoblasts; de, dentin. Scale bars: 50 µm (Ad); 20 µm (Bb).

 
Cell-binding Activity of Recombinant CNR1 Proteins
CNRs with a transmembrane domain (Kohmura et al., 1998) are localized on the cell surface and may mediate cell-cell interaction through EC domains, similar to cadherins. CNRs are also shown to bind reelin, a matrix protein in the brain, through the highly conserved EC1 domain (Senzaki et al., 1999). Hence, we speculated that CNR1 and 5 may mediate cell-cell or cell-matrix interactions in tooth development. To test cell binding, we purified recombinant CNR1 proteins containing various domains from 293 cells transfected with the expression vectors. Recombinant proteins containing EC1, EC1-His, EC1-2-His, and EC1-HA were able to bind both dental epithelial and mesenchymal cells, whereas proteins without the EC1 domain, S-His and {triangleup}EC1-His, failed to bind to these cells (Figs. 4AGo, 4BGo). To confirm the cell-binding activity of EC1-containing fusion proteins, we performed the competition assay using the two different tagged fusion proteins, EC1-HA and EC1-His. When the EC1-HA protein was used as a competitor in EC1-His-mediated cell-binding assays, EC1-HA inhibited cell binding of EC1-His in a dose-dependent manner (Fig. 4CGo). These results indicate that CNR1 binds specifically to both dental epithelial and mesenchymal cells through the EC1 domain.



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  		Figure 4. CNR1 binding to dental epithelial and mesenchymal cells. (A) Schematic structure of CNR1 and tagged CNR1 fusion proteins and their cell-binding activity. Recombinant proteins were incubated with cells, and bound proteins were analyzed by staining with anti-Hisx6 or anti-HA antibody, with FITC-conjugated secondary antibody. Activity of CNR binding to dental epithelial cells and mesenchymal cells is shown as + (positive-binding cells are more than 30%) or - (positive-binding cells are 0%). The percentage of positive-binding cells is calculated as 100 x [number of FITC-positive cells] / [number of Hochest-positive cells]. S, signal peptide; EC, extracellular domain; TM, transmembrane domain; CP, cytoplasmic domain; Hisx6, polyhistidine; HA, hemaglutinin. (B) Visualized image of EC1 binding to dental epithelial or mesenchymal cells. EC1-His was incubated with cells, and bound proteins were visualized by FITC-conjugated secondary antibody. Purple signal was Hochest staining for the cell nucleus. (C) Only recombinant protein containing EC1 (lane3) bound to the dental epithelial cells, not S-His or {triangleup}EC1-His (lanes 1 and 2). EC1-HA was used to compete with EC1-His for cell binding at equal (lane 4) or 10-fold concentrations (lane 5). Bound CNR1 proteins were detected by Western blotting with anti-His antibody (upper) and anti-HA antibody (lower).

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We identified cadherin family adhesion molecules CNR1 and CNR5 from incisor ameloblasts during incisor development. E-cadherin and P-cadherin are localized in the adherence junction of the enamel organ (Fausser et al., 1998; Obara et al., 1998) and are implicated in epithelial cell-cell and cell-matrix interactions during tooth formation. However, these cadherins are expressed in dental epithelium but not in dental mesenchyme. Moreover, the expression of these proteins is reduced in the later stage of dental epithelium development. We found that CNR1 and 5 are expressed by both ameloblasts and odontoblasts in the developing incisor. Their expression is also observed in polarized ameloblasts where E-cadherin and P-cadherin are not expressed, suggesting a distinct role of CNR1 and 5 in tooth development.

CNRs contain six extracellular domains similar to cadherins but have a distinct cytoplasmic domain. Since the cytoplasmic domain of CNR proteins specifically interacts with Fyn-tyrosine kinase, the presence of such a unique cytoplasmic domain of CNRs may have important functional implications (Sugino et al., 2000). The C-terminal region of CNRs contains four PXXP motifs, which are SH3 domain-binding sites and are lysine-rich. The amino acid sequence of this region is highly conserved, with two amino acid differences between the rat and mouse and four amino acid differences between the rat and human. The conserved region may play an important role in CNR-mediated signaling in ameloblasts through interaction with Fyn or other molecules containing the SH3 domain.

It is interesting to note that CNR proteins are localized toward the matrix side in ameloblasts and odontoblasts. Since the EC1 domain of CNR1 is the site responsible for cell binding, it may be important for the potential homophilic interaction between CNR1 and 5, similar to other cadherin family members. The CNRs could also bind to other cell-surface proteins in the dental epithelium and mesenchyme via the EC1 domain or bind to the extracellular matrix of dental tissues. Recently, it was reported that the N-terminal conserved region of CNRs bound reelin, a secreted glycoprotein in the matrix, which regulates layering and positioning of neurons (Ogawa et al., 1995; Frotscher, 1997; Senzaki et al., 1999). Reelin is also expressed by odontoblasts and dental epithelium (Ikeda and Terashima, 1997; Buchaille et al., 2000). Thus, reelin may be a candidate for a binding partner of CNR1 and 5 in tooth germ.


   ACKNOWLEDGMENTS
 
We thank Dr. Yoshihiko Yamada (NIDCR, NIH) for critically reading and Harry Grant for editing the manuscript.


   FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://www.dentalresearch.org.

Received November 16, 2000; Last revision July 24, 2002; Accepted October 7, 2002


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Buchaille R, Couble H, Magloire H, Bleicher F (2000). A subtractive PCR-based cDNA library from human odontoblast cells: identification of novel genes expressed in tooth forming cells. Matrix Biol 19:421–430.[ISI][Medline]

DenBesten PK, Mathews CH, Gao C, Li W (1998). Primary culture and characterization of enamel organ epithelial cells. Connect Tissue Res 38:3–8; discussion 35–41.[Medline]

Fausser JL, Schlepp O, Aberdam D, Meneguzzi G, Ruch JV, Lesot H (1998). Localization of antigens associated with adherens junctions, desmosomes, and hemidesmosomes during murine molar morphogenesis. Differentiation 63:1–11.[ISI][Medline]

Frotscher M (1997). Dual role of Cajal-Retzius cells and reelin in cortical development. Cell Tissue Res 290:315–322.[ISI][Medline]

Ikeda Y, Terashima T (1997). Expression of reelin, the gene responsible for the reeler mutation, in embryonic development and adulthood in the mouse. Dev Dyn 210:157–172.[ISI][Medline]

Kohmura N, Senzaki K, Hamada S, Kai N, Yasuda R, Watanabe M, et al. (1998). Diversity revealed by a novel family of cadherins expressed in neurons at a synaptic complex. Neuron 20:1137–1151.[ISI][Medline]

Kukita A, Harada H, Kukita T, Inai T, Matsuhashi S, Kurisu K. (1992). Primary and secondary culture of rat ameloblasts in serum-free medium. Connect Tissue Int 51:393–398.

Liang P, Pardee AB (1992). Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971.[Abstract/Free Full Text]

Lincecum JM, Fannon A, Song K, Wang Y, Sassoon DA (1998). Msh homeobox genes regulate cadherin-mediated cell adhesion and cell-cell sorting. J Cell Biochem 70:22–28.[ISI][Medline]

Miyazaki Y, Sakai H, Shibata Y, Shibata M, Mataki S, Kato Y (1998). Expression and localization of ferritin mRNA in ameloblasts of rat incisor. Arch Oral Biol 43:367–378.[ISI][Medline]

Nakase T, Takaoka K, Hirakawa K, Hirota S, Takemura T, Onoue H, et al. (1994). Alterations in the expression of osteonectin, osteopontin and osteocalcin mRNAs during the development of skeletal tissues in vivo. Bone Miner 26:109–122.[ISI][Medline]

Obara N, Suzuki Y, Nagai Y, Takeda M (1998). Expression of E- and P-cadherin during tooth morphogenesis and cytodifferentiation. Anat Embryol 197:469–475.[Medline]

Ogawa M, Miyata T, Nakajima K, Yagyu K, Seike M, Ikenaka K, et al. (1995). The reeler gene-associated antigen on Cajal-Retzius neurons is a crucial molecule for laminar organization of cortical neurons. Neuron 14:899–912.[ISI][Medline]

Ruch JV (1995). Tooth crown morphogenesis and cytodifferentiations: candid questions and critical comments. Connect Tissue Res 32:1–8.

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Senzaki K, Ogawa M, Yagi T (1999). Proteins of the CNR family are multiple receptors for Reelin. Cell 99:635–647.[ISI][Medline]

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Sugino H, Hamada S, Yasuda R, Tuji A, Matsuda Y, Fujita M, et al. (2000). Genomic organization of the family of CNR cadherin genes in mice and humans. Genomics 63:75–87.[ISI][Medline]

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