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Role of Dlx-1 and Dlx-2 Genes in Patterning of the Murine Dentition

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Role of Dlx-1 and Dlx-2 Genes in Patterning of the Murine Dentition Development 124, 4811-4818 (1997) 4811 Printed in Great Britain © The Company of Biologists Limited 1997 DEV2208 Role of Dlx-1 and Dlx-2 genes in patterning of the murine dentition Bethan L. Thomas1,*, Abigail S. Tucker1,*, Mensheng Qiu2, Christine A. Ferguson1, Zoë Hardcastle1, John L. R. Rubenstein2 and Paul T. Sharpe1,† 1Department of Craniofacial Development, Guy’s Hospital, London, SE1 9RT, UK 2Nina Ireland Laboratory of Developmental Neurobiology, Center for Neurobiology and Psychiatry, Department of Psychiatry and Programs in Neuroscience and Developmental Biology, University of California at San Francisco, USA *Contributed equally to this work †Author for correspondence (e-mail: [email protected]) SUMMARY The molecular events of odontogenic induction are molar epithelium has lost its odontogenic potential. Using beginning to be elucidated, but until now nothing was molecular markers of branchial arch neural crest (Barx1) known about the molecular basis of the patterning of the and commitment to chondrogenic differentiation (Sox9), dentition. A role for Dlx-1 and Dlx-2 genes in patterning of we show that this population alters its fate from odonto- the dentition has been proposed with the genes envisaged genic to become chondrogenic. These results provide as participating in an ‘odontogenic homeobox gene code’ evidence that a subpopulation of cranial neural crest is by specifying molar development. This proposal was specified as odontogenic by Dlx-1 and Dlx-2 genes. Loss of based on the restricted expression of the genes in molar function of these genes results in reprogramming of this ectomesenchyme derived from cranial neural crest cells population of ectomesenchyme cells into chondrocytes. prior to tooth initiation. This is the first indication that the development of different Mice with targeted null mutations of both Dlx-1 and Dlx- shaped teeth at different positions in the jaws is determined 2 homeobox genes do not develop maxillary molar teeth but by independent genetic pathways. incisors and mandibular molars are normal. We have carried out heterologous recombinations between mutant and wild-type maxillary epithelium and mesenchyme and Key words: homeobox, Dlx, patterning, tooth development, neural show that the ectomesenchyme underlying the maxillary crest, mouse, dentition, odontogenic induction INTRODUCTION still no firm evidence confirming which tissue sets up the initial patterning signals (Lumsden, 1988; Kollar and Baird, Tooth development is known to occur through a series of rec- 1969; Miller, 1969). Thus, despite over 40 years of discus- iprocal epithelial-mesenchymal interactions. The initiation of sion, there is no experimental evidence to explain what deter- tooth development involves an interaction between epi- mines the precise site of tooth development or what type of thelium of the first arch and the underlying neural-crest- tooth will develop at that site. We describe here the first derived ectomesenchyme. Following initiation, the epithe- molecular data relating to patterning of the dentition, showing lium invaginates forming a tooth bud around which the that the development of maxillary molars requires the ectomesenchyme condenses. During these stages and subse- regional specification of a population of cranial neural crest quent stages many potentially regulative molecules are cells by the Dlx-1 and Dlx-2 homeobox genes. expressed. Key components of tooth initiation signalling Dlx-1 and Dlx-2 expression in neural-crest-derived mes- pathways have been shown to be Bmp-4, Lef1 and Msx-1 enchyme of the mandibular and maxillary processes is (Vainio et al., 1993; van Gederen et al., 1994; Satokata and restricted to proximal regions where molar teeth will develop. Maas, 1994). Targeted mutations of Lef1 or Msx-1 result in Dlx-2 is also expressed in the epithelium of the distal aspects the arrest of all tooth development at the bud stage. Despite of the first branchial arch at this stage, prior to the initiation of an increasing wealth of information regarding tooth initiation tooth development (Fig. 1). Dlx-1 and Dlx-2 are members of a from recombination and knock-out studies, no molecular family of genes orthologous to the Drosophila distal-less evidence has been reported that may contribute to an under- homeobox gene. These genes are located on the same chro- standing of odontogenic patterning. Recombination experi- mosome (chromosome 2 in mouse), separated by 10 kb and are ments have been carried out by many workers to attempt to transcribed in oppposite directions (Ozcelick et al., 1992; elucidate whether the patterning is regulated by the epithe- McGuiness et al., 1996). Interestingly, Dlx-5 and Dlx-6 have lium or the mesenchyme. It appears from this work that the been found on a different chromosome in a similar arrange- control of morphogenesis fluctuates between these two tissue ment (Simeone et al., 1994), suggesting an initial duplication layers at different stages of tooth development, but there is event, followed by a second, tandem duplication. Dlx-5 and 4812 B. L. Thomas and others MATERIALS AND METHODS Generation of mutant mice Targeted mutations in Dlx-1 or Dlx-2 and both Dlx-1 and Dlx-2 genes were produced as described (Qiu et al., 1997). Mutations in Dlx-1 or Dlx-2 were produced using targeting vectors which deleted exons two and three of Dlx-1 or exons two, three and part of exon one of Dlx- 2. These both resulted in complete removal of the homeobox following homologous recombination. Since Dlx-1 and Dlx-2 are separated by only 10 kb of intergenic sequence, targeted disruption to Fig. 1. Expression of Dlx-2. produce double mutants was carried out using a targeting vector with Digoxigenin-labelled whole-mount deletion of exons two and three of Dlx-1 and exons two, three and in situ hybridisation of E10.5 part of exon one of Dlx-2. JM-1 ES cells were electroporated, selected embryos showing Dlx-2 expression and characterised as described (Qiu et al., 1995). Genotyping of ES from the oral aspect in the maxilla cells and mouse tails was performed using Southern blots and PCR and frontonasal process (A) and assays. Primers for the PCR assays were 5′-AAGGCGGGGCAG- mandibular process (B). White CTCTGGAG-3′, 5′-AGGGAGACGGGCAGGAAGCG-3′ for Dlx-1, shading indicates the areas of which amplified a fragment in the third exon, and 5′-TCCGAAT- mesenchymal Dlx-2 expression. AGTGAACGGGAAGCCAAAG-3′, 5′CAGGGTGCTGCTCGGTG- GGTATCTG-3′ for Dlx-2, which amplified a fragment in the 3′ coding region. The PCR conditions were: 1 cycle 94°C; 35 cycles of 94°C 1 min, 65°C 1 min, 72°C 1 min and 1 cycle 72°C, 1 min for the Dlx-1 Dlx-6 are expressed in very similar domains to Dlx-1 and Dlx- primers and 1 cycle 94°C; 35 cycles of 94°C 1 minute, 58°C 1 minute, 2 in the mandibular division of the first branchial arch, but are 72°C 1.5 minutes and 1 cycle 72°C 1.5 minutes for the Dlx-2 primers. not expressed in the maxillary division (Qiu et al., 1997). Thus, For the PCR assay to genotype the double mutants, the same primers prior to the initiation of tooth development, Dlx-1, Dlx-2, Dlx- and conditions were used as for the Dlx-1 mutants. 5 and Dlx-6 are all expressed in the ectomesenchyme of the presumptive mandibular molar region, but only Dlx-1 and Dlx- Embryo preparation 2 are expressed in the ectomesenchyme of the presumptive Embryos were obtained from matings between Dlx-1/Dlx-2 hetero- maxillary molars. zygous mice. Day E0 was taken as midnight prior to finding a vaginal A mechanism for patterning of the dentition, based on plug. spatially restricted expression of homeobox genes in first branchial arch mesenchyme has previously been proposed Heterotypic recombinations (Sharpe, 1995; Thomas and Sharpe, 1997). This ‘odontogenic Recombinations were carried out at E12.5 and E13.5. Heterozygous homeobox code’ proposes Dlx-1 and Dlx-2 genes to be females and males were mated to give a 1 in 4 chance of a homo- involved specifically in patterning of molar tooth development. zygous mutant. At these stages, there is no obvious difference in gross Furthermore, the fact that Dlx-1 and Dlx-2 are the only Dlx morphology between the wild types and mutants. Since the fron- genes expressed in the presumptive maxillary molar mes- tonasal process was not included in the dissection, the epithelium used in the culture excluded all presumptive incisor epithelium. The molar enchyme, suggested that these genes would play a specific role region of the maxillas were dissected out in D-MEM as indicated in in maxillary molar development. Fig. 3A. The rest of the embryo was used for genotyping. Epithelium Targeted mutations in either Dlx-1 or Dlx-2 affect devel- was removed using Dispase in calcium- and magnesium-free PBS at opment of cranial neural-crest-derived skeletal elements 2 units per ml. The E12.5 maxillas were incubated for 12 minutes at derived from the proximal parts of the first and second 37°C, the E13.5 maxillas for 15 minutes at 37°C. After incubation the branchial arches but have no effect on tooth development maxillas were washed in D-MEM with 10% fetal calf serum (FCS) (Fig. 2A,B) (Qiu et al., 1995, 1997). Mice generated with and the epithelium was dissected off using fine tungsten needles. The mutations in both genes, however, have a profound tooth mesenchyme was placed on membrane filters supported by metal phenotype where new-born mice have no maxillary molars grids following the Trowel technique as modified by Saxén (Trowel, but all other teeth are present (Fig. 2C-L). Analysis of specific 1959; Saxén, 1966). It was important that the mesenchyme was orientated on the filter molecular markers of tooth development shows this tooth so that the oral surface faced upwards.
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