HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Boran, T. Articles by Peterkova, R. Search for Related Content PubMed PubMed Citation Articles by Boran, T. Articles by Peterkova, R.

Increased Apoptosis during Morphogenesis of the Lower Cheek Teeth in Tabby/EDA Mice

¹ Department of Teratology, Institute of Experimental Medicine, Academy of Sciences of the CR, Prague, Czech Republic; and
² INSERM U595, Faculté de Médecine, Université Louis Pasteur, Strasbourg, France;

^* corresponding author, repete{at}biomed.cas.cz

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
In wild-type (WT) mice, epithelial apoptosis is involved in reducing the embryonic tooth number and the mesial delimitation of the first molar. We investigated whether apoptosis could also be involved in the reduction of tooth number and the determination of anomalous tooth boundaries in tabby (Ta)/EDA mice. Using serial histological sections and computer-aided 3D reconstructions, we investigated epithelial apoptosis in the lower cheek dentition at embryonic days 14.5–17.5. In comparison with WT mice, apoptosis was increased mainly mesially in Ta dental epithelium from day 15.5. This apoptosis showed a similar mesio-distal extent in all 5 morphotypes (Ia,b,c and IIa,b) of Ta dentition and eliminated the first cheek tooth in morphotypes IIa,b. Apoptosis did not appear to play any causal role in positioning inter-dental gaps. Analysis of the present data suggests that the increased apoptosis in Ta mice is a consequence of impaired tooth development caused by a defect in segmentation of dental epithelium.

KEY WORDS: EDA • apoptosis • mice • tabby • tooth development

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
X-linked hypohidrotic ectodermal dysplasia (XLHED) is a typical genetic syndrome including defects of ectodermal derivatives such as hair, glands, and teeth. XLHED in humans is homologous to the tabby (Ta) syndrome (Grüneberg, 1971) in the mouse (Blecher, 1986; Ferguson et al., 1997; Srivastava et al., 1997).

XLHED results from a mutation in the EDA gene (Kere et al., 1996). The mutation leads to a deficiency in the transmembrane protein (Ferguson et al., 1997) ectodysplasin A (EDA) (Srivastava et al., 1997). EDA plays a role in ectodermal-mesenchymal interactions (Mikkola et al., 1999) and in the development of ectodermal derivatives (Srivastava et al., 2001). The EDA signaling leads to the activation of the NFB pathway (Kumar et al., 2001). This pathway determines whether cells undergo apoptosis, survive, or proliferate in response to TNF family members (Gaur and Aggarwal, 2003). Mice with suppressed NFB have strongly increased apoptosis in their developing hair follicles (Schmidt-Ullrich et al., 2001).

Tabby dentition exhibits inborn defects in tooth number, shape, and size (Grüneberg, 1966; Sofaer, 1969). The most variable is the mandibular cheek dentition (Grüneberg, 1966), which has been classified into 2 basic morphotypes, I and II, subdivided into 3 (Ia, Ib, Ic) and 2 (IIa, IIb) particular subtypes, respectively (Kristenova et al., 2002; Peterkova et al., 2002). The different morphotypes result from a defect in the segmentation of the dental epithelium along the mesio-distal jaw axis (Fig. 1).

View larger version (41K): [in this window] [in a new window]   Figure 1. Schematic representation of the pattern of the lower cheek tooth primordia in wild-type (WT) and tabby (Ta) mouse fetuses (according to Peterkova et al., 2002). M1, M2, and M3—the first, second, and third lower molar primordia in WT mice. T1, T2, and T3—the prospective first, second, and third functional teeth in the different subtypes of Ta morphotypes I (Ia, Ib, Ic) and II (IIa, IIb). Note the decreasing volume of the most mesial tooth primordium from subtypes Ia to IIb, which is associated with increasing volume of the subsequent tooth primordia and a mesial shift in tooth boundaries compared with WT mice. The abortive tooth primordium (dashed line) represents an abortive cap (**) in subtype IIa and an abortive bud (*) in subtype IIb. These abortive tooth primordia do not give rise to a functional tooth. The first functional tooth (T1) in morphotype II is, in reality, the second tooth primordium, which originates in the mesio-distal sequence during odontogenesis. Accordingly, the morphology of T1 in morphotype II is similar to that of T2 in morphotype I (Peterkova et al., 2002).

	MATERIALS & METHODS

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
Mice
All animals were generated from the inbred Ta line B6CBACa-A^w-J/A-Eda^Ta/0 (the Jackson Laboratory, Bar Harbor, ME, USA). Only Ta homozygous and hemizygous specimens were analyzed and compared with WT mice. The WT mice were generated by the inbreeding of WT brothers and sisters of mutant animals (Kristenova et al., 2002). All the animals’ treatment satisfied the requirements of the Institutional Review Board.

Harvesting and Staging of Specimens
The females were mated overnight. The midnight before the morning detection of the vaginal plug was considered as embryonic day (ED) 0.0. The offspring were harvested from ED 14.5 to ED 17.5 and fixed in Bouin-Hollande fluid (self-made). The embryos/fetuses of the same harvesting age were staged in more detail according to their wet body weight (Peterka et al., 2002). We harvested 88 Ta homo/hemizygous mice (15 at ED 14.5, 15 at ED 15.5, 24 at ED 16.5, and 34 at ED 17.5) and 40 WT controls (9 at ED 14.5, 19 at ED 15.5, 7 at ED 16.5, and 5 at ED 17.5).

Histology
For each harvesting stage, at least 1 specimen from each available weight class was processed histologically: 41 Ta homo/hemizygous mice (4 at ED 14.5, 8 at ED 15.5, 20 at ED 16.5, and 8 at ED 17.5) and 15 WT mice (3 at ED 14.5, 6 at ED 15.5, 2 at ED 16.5, and 4 at ED 17.5). Heads were embedded in paraffin, cut in a series of 5-µm frontal sections, and stained with alcian-blue-hematoxylin-eosin. In each lower jaw quadrant, a particular Ta morphotype (Ia, Ib, Ic, IIa, or IIb) of the lower cheek dentition was determined (Peterkova et al., 2002).

Apoptosis Assay
Apoptotic cells and bodies were identified in the dental epithelium on histological sections based on morphological criteria (Kerr et al., 1995; Tureckova et al., 1996).

3D Reconstructions
The histological series of Ta and WT embryos showing similar body weight at a specific ED (Miard et al., 1999) were considered for 3D analysis. At each ED 15.5, 16.5, and 17.5, a sextet of lower jaw quadrants was selected at random from jaw quadrants ranked according to particular dentition morphotype. This sextet was comprised of 1 WT specimen and 5 Ta specimens, one from each of the lower cheek dentition morphotypes, Ia, Ib, Ic, IIa, and IIb (Fig. 1). These 18 specimens were processed for 3D reconstruction as in our previous studies (Lesot et al., 1996).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
The tooth terminology used in this study was derived from previous papers (Kristenova et al., 2002; Peterkova et al., 2002) (Fig. 1).

ED 14.5
Apoptosis occurred in WT embryos in the mesial epithelial ridge (see below) and in the mesial part of M₁, which was at the early cap stage. Only sparse apoptosis was present in the Ta dental epithelium at ED 14.5, when the morphotypes could not yet be distinguished.

ED 15.5
In WT embryos, large numbers of apoptotic cells and bodies were located in the mesial epithelial ridge (the epithelial ridge extending mesially from the most mesial cheek tooth primordium) and in the primary enamel knot (pEK) of the M₁ (Figs. 2A, 3A). Apoptosis was only sparse in the remaining dental epithelium.

View larger version (70K): [in this window] [in a new window]   Figure 2. Apoptosis in 3D reconstructions of the dental epithelium in the cheek region of the mandible at ED 15.5, 16.5, and 17.5. Apoptosis presented by apoptotic cells and bodies (black dots) is increased in Ta mice. It is distributed mesio-distally to a similar extent in all Ta morphotypes, but it affects different structures according to the specific tooth pattern (compare with Fig. 1). The mesenchymal face of the dental and adjacent oral epithelium is shown from an aerial view in wild-type (WT) controls and in subtypes Ia and Ib of Ta dentition. The pictures have been unified to show the right-side dentition. WT and Ta specimens of similar weight (Peterka et al., 2002) were selected for comparison on each of the embryonic days. Consequently, inter- and intra-litter variability in the length of the dental epithelium was minimalized (also see Figs. 3, 4). Various stages of tooth development are represented: The WT mice show the cap stage of M1 at ED 15.5, the cap-bell transition of M1 and the late bud/early cap of M2 at ED 16.5, the bell of M1, and the late cap of M2 at ED 17.5. In Ta subtypes Ia and Ib, the cap stage of T1 and the late bud/early cap of T2 occurred at ED 15.5, the early bell of T1 and the cap of T2 at ED 16.5, and the bell of T1 and T2 and the bud of T3 at ED 17.5. "mer" = mesial epithelial ridge (the epithelial ridge extending mesially from the primordium of the most mesial cheek tooth). Arrow = apoptosis in the pEK.

View larger version (66K): [in this window] [in a new window]   Figure 3. Apoptosis in 3D reconstructions of the dental epithelium in the cheek region of the mandible at ED 15.5, 16.5, and 17.5. Apoptosis presented by apoptotic cells and bodies (black dots) is increased in Ta mice. It is distributed mesio-distally to a similar extent in all Ta morphotypes, but it affects different structures according to the specific tooth pattern (compare with Fig. 1). The mesenchymal face of the dental and adjacent oral epithelium is shown from an aerial view in subtypes Ic, IIa, and IIb of Ta dentition. The pictures have been unified to present the right-side dentition. Various stages of tooth development are shown in subtype Ic: the cap of T1 and the early cap of T2 at ED 15.5, the cap-bell transition stage of T1 and the cap of T2 at ED 16.5, and the bell of both T1 and T2 at ED 17.5. In morphotypes IIa and IIb, the T1 showed from early cap to well-formed cap stage at ED 15.5–16.5 and the bell stage at ED 17.5. The bud of T3 in morphotype Ic and T2 in morphotypes IIa and IIb were distinct at ED 17.5. The abortive cap (double arrowhead) and abortive bud (single arrowhead) represent the most mesial primodium in morphotype II. "mer" = mesial epithelial ridge (the epithelial ridge extending mesially from the primordium of the most mesial cheek tooth). Arrow = apoptosis in the pEK.

View larger version (75K): [in this window] [in a new window]   Figure 4. 3D reconstructions of the dental epithelium in the cheek region of the mandible at ED 15.5, 16.5, and 17.5. The mesenchymal face of the dental and adjacent oral epithelium is shown from a lingual (medial) view. The pictures have been unified to present the right-side dentition. Apoptotic cells and bodies are represented by black dots. The dashed circle indicates apoptosis between the B1 and B2 (G) or B2 and B3 (M) cusps. Such apoptosis was not found in Ta specimens, which can be explained by their different tooth and cusp patterns (Kristenova et al., 2002). Arrow = apoptosis in the pEK. Double arrowhead = the abortive cap. Single arrowhead = abortive bud. For further explanation, see Figs. 1–3.

Similar to the previous stage, the mesial apoptotic accumulation extended more distally in Ta than in WT mice. In morphotype I, this mesial apoptotic accumulation went through the stalk and adjacent part of the T₁ enamel organ into the buccal epithelial mound interconnecting T₁ and T₂, where it decreased in intensity (Figs. 2E, 2F, 3D, 4H–4J). In morphotype II, apoptosis was strongly concentrated in the mesial epithelial ridge and predominantly in the buccal part of the abortive first tooth primordium (Figs. 3E, 3F). In addition, apoptosis was observed in the pEKs of the T₂ cap in morphotype I (Figs. 2E, 3D) and of the T₁ cap in morphotype II (Figs. 3E, 3F).

ED 17.5
In WT fetuses, apoptosis persisted in the mesial epithelial ridge (Figs. 2G, 4M). In the mesial third of the M₁, apoptosis was strongly concentrated in the stalk of the enamel organ and adjacent stellate reticulum. Another concentration of apoptotic cells was in the distal part of the M₁, at the junction of the buccal side of the enamel organ proper and its stalk. This apoptotic area extended distally, including the buccal epithelial mound located between the M₁ and M₂ (Figs. 2G, 4M). Apoptotic bodies were also found in the rudimentary anlage of the replacing molar (Gaunt, 1966) and in a small area of the stellate reticulum adjacent to the outer dental epithelium at the buccal surface of the M₁ enamel organ, between the B2 and B3 cusp regions (Fig. 4M). Apoptosis was sparse in the poorly developed pEK of the M₂.

Similar to the mesial part of the M₁ in the WT fetuses, apoptosis accumulated in the stalk and adjacent enamel organ of the mesial part of the T₁ and T₂ in morphotype I and of the T₁ in morphotype II (Fig. 4). In the distal part of these teeth, apoptosis was concentrated only in the rudimentary anlage of the replacing molar, and in the stalk and at its transition to the buccal side of the tooth bell. The latter apoptotic area extended to the epithelial ridges projecting distally from the tooth. In morphotype II, the strong accumulation of apoptosis continued in front of the T₁ germ, including the remnants of the abortive mesial tooth primordium (Figs. 3H, 3I, 4Q, 4R).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
In normal mice, apoptosis concentrates in the mesial epithelial ridge, in the primary and secondary enamel knots, in the stalk of the tooth enamel organ, and in the rudimentary anlage of the replacing dentition (for review, see Peterkova et al., 2003). The present data in WT mice were in accord with this scheme.

The temporospatial pattern of apoptosis distribution in the cap and early bell stages of the M₁ in the WT mice was similar to data achieved by the same method in the ICR mice (Viriot et al., 1997). In addition, we found specific accumulations of apoptosis in the well-formed bell of M₁: A large apoptotic area was located in the mesial part of the M₁ bell giving rise to the L1 and B1 cusps (see below). Further, 2 small foci of apoptosis were found at the buccal surface of the enamel organ between the prospective cusps B1 and B2 at ED 16.5, and between B2 and B3 at ED 17.5; they appear to anticipate the prospective inter-cusp fissures. The apoptosis in the stalk and at its transition to the buccal side of the tooth bell might relate to the budding of the dental epithelium in the distal part of the molar.

Compared with WT mice, the apoptosis in Ta specimens was increased at specific loci of the dental epithelium. Apoptosis was more intensive mesially and extended more distally in the Ta specimens at ED 15.5 and 16.5. It also included the most mesial tooth primordium, which was larger in morphotype I and smaller in morphotype II (Figs. 2–4). At ED 17.5 in morphotype II, apoptosis continued to suppress the most mesial tooth entirely (abortive cap in IIa and epithelial bud in IIb). In contrast, apoptosis was silenced in morphotype I, where the mesial tooth primordium finally survived and gave rise to a functional T₁ (Fig. 1). The mesial apoptotic zone was similar in morphotypes I and II, and the cell death seemed to proceed there, to a certain degree, independently of tooth morphogenesis at ED 15.5 and 16.5. The difference in the fate of the most mesial tooth primordium (survival in morphotype I and extinction in morphotype II) correlated with the volume of the structures at the time that cell death began there.

The small mesial cheek tooth in Ta mice might have a developmental relationship to the mesial part of the first molar in normal mice, where a premolar vestige had been presumably incorporated during evolution (Peterkova, 1983; Lisi et al., 2001). Indeed, 3D reconstructions have documented a vestigial bud incorporated into the mesial part of the M₁ cap in normal mice (Viriot et al., 2000). The up-regulation of apoptosis in the mesial part of the M₁ bell in WT mice at ED 17.5 (Fig. 2G) suggests that the incorporated heterogenous dental epithelium (the assumed premolar vestige) has not yet been completely adopted by M₁ from an evolutionary aspect. In consequence, the mesial part of the first molar might represent a locus minoris resistentiae in mutant mice. There, a defect in incorporation of a vestigial premolar epithelium may occur in Ta specimens (Peterkova, 1983; Peterkova et al., 2002) and may explain the increased cell death in the mesial portion of the Ta dental epithelium in the lower cheek region (Figs. 2–4).

Similar to M₁ in WT mice, apoptosis concentrated in the mesial part of the tooth bell of T₂ in Ta morphotype I. This supports the hypothesis that the mesial part of T₂ also includes a heterogeneous component, corresponding to the distal part of M₁ in normal mice (Peterkova et al., 2002; compare with Fig. 1).

Apoptosis was sparse between the M₁ and M₂ at ED 15.5 and 16.5. In Ta specimens at similar developmental stages, apoptosis was present buccally in the epithelium interconnecting the first and second tooth primordia. However, this apoptosis occurred too late to play any causal role in positioning the anomalous inter-dental gap. Rather, it belonged to a continuous zone of apoptosis, extending from the mesial end of the dental lamina to the second cheek tooth anlage. The anomalously located inter-dental gaps more probably result from the lack of budding of the dental epithelium at appropriate places, to give rise to tooth caps there.

It has been reported that the number of apoptotic cells does not change in mutant tooth germs in downless embryos (Tucker et al., 2000), and that apoptosis is not increased in Ta molars at pre-natal day 14 (Koppinen et al., 2001). The mutation in the EDA gene does not seem to be the primary cause of the up-regulation of apoptosis we observed at specific loci of the dental epithelium in the Ta mice from ED 15.5. Analysis of the present data suggests that the increased apoptosis is a consequence of impaired development of the lower cheek teeth, caused by a defect in segmentation of dental epithelium in the mice bearing the EDA mutation.

	ACKNOWLEDGMENTS

 
We appreciate the technical assistance of Dr. M. Hovorakova, Mrs. P. Novakova, Ms. I. Ruzickova, and Mr. J. Fluck. We thank Mr. J. Dutt for critical reading of the manuscript. This study was supported by the Grant Agency of the CR (304/02/0408), Ministry of Education, Youth and Sports CR (project B-23.002), Academy of Sciences CR (project AV0Z 5039906), and by grant APS02005MSA from the French Network GIS-Rare Diseases (Project A02178MS). Travel costs were partially supported based on the agreement between INSERM (France) and the Academy of Sciences CR.

Received June 30, 2004; Last revision December 3, 2004; Accepted December 22, 2004

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS & METHODS RESULTS DISCUSSION REFERENCES

 
Blecher SR (1986). Anhidrosis and absence of sweat glands in mice hemizygous for the Tabby gene: supportive evidence for the hypothesis of homology between Tabby and human anhidrotic (hypohidrotic) ectodermal dysplasia (Christ-Siemens-Touraine syndrome). J Invest Dermatol 87:720–722.[ISI][Medline]

Ferguson BM, Brockdorff N, Formstone E, Nguyen T, Kronmiller JE, Zonana J (1997). Cloning of Tabby, the murine homolog of the human EDA gene: evidence for a membrane-associated protein with a short collagenous domain. Hum Mol Genet 6:1589–1594.[Abstract/Free Full Text]

Gaunt WA (1966). The disposition of the developing cheek teeth in the albino mouse. Acta Anat (Basel) 64:572–585.[ISI][Medline]

Gaur U, Aggarwal BB (2003). Regulation of proliferation, survival and apoptosis by members of the TNF superfamily. Biochem Pharmacol 66:1403–1408.[ISI][Medline]

Grüneberg H (1966). The molars of the tabby mouse, and a test for the ‘single-active X-chromosome’ hypothesis. J Embryol Exp Morphol 15:223–244.[ISI][Medline]

Grüneberg H (1971). The tabby syndrome in the mouse. Proc R Soc Lond B 179:139–156.[Medline]

Kere J, Srivastava AK, Montonen O, Zonana J, Thomas N, Ferguson B, et al. (1996). X-linked anhidrotic (hypohidrotic) ectodermal dysplasia is caused by mutation in a novel transmembrane protein. Nat Genet 13:409–416.[ISI][Medline]

Kerr JF, Gobe GC, Winterford CM, Harmon BV (1995). Anatomical methods in cell death. Methods Cell Biol 46:1–27.[ISI][Medline]

Koppinen P, Pispa J, Laurikkala J, Thesleff I, Mikkola ML (2001). Signaling and subcellular localization of the TNF receptor Edar. Exp Cell Res 269:180–192.[ISI][Medline]

Kristenova P, Peterka M, Lisi S, Gendrault JL, Lesot H, Peterkova R (2002). Different morphotypes of functional dentition in the lower molar region of tabby (EDA) mice. Orthod Craniofac Res 5:205–214.[Medline]

Kumar A, Eby MT, Sinha S, Jasmin A, Chaudhary PM (2001). The ectodermal dysplasia receptor activates the nuclear factor-kappaB, JNK and cell death pathways and binds to ectodysplasin A. J Biol Chem 276:2668–2677.[Abstract/Free Full Text]

Lesot H, Vonesch JL, Peterka M, Tureckova J, Peterkova R, Ruch JV (1996). Mouse molar morphogenesis revisited by three-dimensional reconstruction: II. Spatial distribution of mitoses and apoptosis in cap to bell staged first and second upper molar teeth. Int J Dev Biol 40:1017–1031.[ISI][Medline]

Lisi S, Peterkova R, Kristenova P, Vonesch J-L, Peterka M, Lesot H (2001). Crown morphology and pattern of odontoblast differentiation in lower molars of tabby mice. J Dent Res 80:1980–1983.[Abstract/Free Full Text]

Matalova E, Tucker AS, Sharpe PT (2004). Death in the life of a tooth. J Dent Res 83:11–16.[Abstract/Free Full Text]

Miard S, Peterkova R, Vonesch JL, Peterka M, Ruch JV, Lesot H (1999). Alterations in the incisor development in the Tabby mouse. Int J Dev Biol 43:517–529.[ISI][Medline]

Mikkola ML, Pispa J, Pekkanen M, Paulin L, Nieminen P, Kere J, et al. (1999). Ectodysplasin, a protein required for epithelial morphogenesis, is a novel TNF homologue and promotes cell-matrix adhesion. Mech Dev 88:133–146.[ISI][Medline]

Peterka M, Lesot H, Peterkova R (2002). Body weight in mouse embryos specifies staging of tooth development. Connect Tissue Res 43:186–190.[ISI][Medline]

Peterkova R (1983). Dental lamina develops even within the mouse diastema. J Craniofac Genet Dev Biol 3:133–142.[ISI][Medline]

Peterkova R, Kristenova P, Lesot H, Lisi S, Vonesch JL, Gendrault JL, et al. (2002). Different morphotypes of the tabby (EDA) dentition in the mouse mandible result from a defect in the mesio-distal segmentation of dental epithelium. Orthod Craniofac Res 5:215–226.[Medline]

Peterkova R, Peterka M, Lesot H (2003). The developing mouse dentition: a new tool for apoptosis study. Ann NY Acad Sci 1010:453–466.[Abstract/Free Full Text]

Schmidt-Ullrich R, Aebischer T, Hulsken J, Birchmeier W, Klemm U, Scheidereit C (2001). Requirement of NF-kappaB/Rel for the development of hair follicles and other epidermal appendices. Development 128:3843–3853.[Abstract/Free Full Text]

Sofaer JA (1969). Aspects of the tabby-crinkled-downless syndrome. Observations on the reaction to changes of genetic background. J Embryol Exp Morphol 22:207–227.[ISI][Medline]

Srivastava AK, Pispa J, Hartung AJ, Du Y, Ezer S, Jenks T, et al. (1997). The Tabby phenotype is caused by mutation in a mouse homologue of the EDA gene that reveals novel mouse and human exons and encodes a protein (ectodysplasin-A) with collagenous domains. Proc Natl Acad Sci USA 94:13069–13074.[Abstract/Free Full Text]

Srivastava AK, Durmowicz MC, Hartung AJ, Hudson J, Ouzts LV, Donovan DM, et al. (2001). Ectodysplasin-A1 is sufficient to rescue both hair growth and sweat glands in Tabby mice. Hum Mol Genet 26:2973–2981.

Tucker AS, Headon DJ, Schneider P, Ferguson BM, Overbeek P, Tschopp J, et al. (2000). Edar/Eda interactions regulate enamel knot formation in tooth morphogenesis. Development 127:4691–4700.[Abstract]

Tureckova J, Lesot H, Vonesch JL, Peterka M, Peterkova R, Ruch JV (1996). Apoptosis is involved in the disappearance of the diastemal dental primordia in mouse embryo. Int J Dev Biol 40:483–489.[ISI][Medline]

Viriot L, Peterkova R, Vonesch JL, Peterka M, Ruch JV, Lesot H (1997). Mouse molar morphogenesis revisited by three-dimensional reconstruction. III. Spatial distribution of mitoses and apoptoses up to bell-staged first lower molar teeth. Int J Dev Biol 41:679–690.[ISI][Medline]

Viriot L, Lesot H, Vonesch JL, Ruch JV, Peterka M, Peterkova R (2000). The presence of rudimentary odontogenic structures in the mouse embryonic mandible requires reinterpretation of developmental control of first lower molar histomorphogenesis. Int J Dev Biol 44:233–240.[ISI][Medline]

This Article Abstract Figures Only Full Text (PDF) Services Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via ISI Web of Science (1) Citing Articles via Google Scholar Google Scholar Articles by Boran, T. Articles by Peterkova, R. Search for Related Content PubMed PubMed Citation Articles by Boran, T. Articles by Peterkova, R.