Tooth Morphogenesis and Renewal
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This chapter describes the developmental anatomy and molecular regulation of tooth initiation, morphogenesis, and cell differentiation, as well as of tooth renewal and replacement. Tooth morphogenesis is guided by interactions between epithelial and mesenchymal tissues and progresses through distinct stages defined by morphological features of the dental epithelium. Tooth morphogenesis is regulated by interactions between cells, in particular reciprocal and sequential interactions between the mesenchyme and epithelium. Tooth renewal and replacement require the action of stem cells that are capable of self-renewal and production of new progeny upon inductive signals. The study of tooth replacement using nonmodel animals for continuous lifelong tooth replacement, and the ferret for mammalian replacement, is generating new information on the mechanisms of successional tooth formation and the characteristics of dental stem and progenitor cells. For successful tooth regeneration, more detailed understanding is required of the gene regulatory networks and cellular mechanisms guiding tooth development.Keywords:
Mesenchyme
Previous observations have shown that, during the initiation phase of odontogenesis, signals from mouse odontogenic epithelium can elicit teeth in non-odontogenic but neural crest–derived mesenchyme isolated from ectopic sites including chick mandibular mesenchyme. In the present study the formation of ectopic tooth buds and dental mesenchyme in chick mandibular mesenchyme was examined using heterospecific recombinations between E11 mouse odontogenic epithelium and stage 23 chick lateral mandibular mesenchyme. Both morphological criteria and chick-specific probes for Msx-1, Msx-2, and Bmp-4 mRNAs were used as markers for early dental mesenchyme. Our results demonstrated that interactions of mouse odontogenic epithelium with chick mandibular mesenchyme induce early changes in the chick mandibular mesenchyme including the appearance of a translucent zone, cell proliferation, and induction of expression of Msx-1, Msx-2, and Bmp-4, which have been shown to be associated with the formation of dental mesenchyme. In addition, tooth bud–like structures that resemble E13 tooth buds in vivo both morphologically and in their patterns of gene expression formed after 6 days in the heterospecific recombinations. The tooth bud–like structures consist of invaginated mouse mandibular epithelium and condensed chick mandibular mesenchyme expressing high levels of Msx-1 and Bmp-4, but undetectable levels of Msx-2. Unlike the induction of Msx-1, Msx-2, and Bmp-4 in the underlying mesenchyme, which is specific for signals derived from odontogenic epithelium, the induction of a translucent zone and cellular proliferation in the underlying mesenchyme may be related to the growth-promoting potential of embryonic epithelia and not be specific to signals derived from the odontogenic epithelium. Similar to mouse odontogenic epithelium, agarose beads soaked in recombinant BMP-4 induced a translucent zone, cellular proliferation, and expression of Msx-1, Msx-2, and Bmp-4 in chick mandibular mesenchyme after 24 hours. These observations together showed that avian mandibular mesenchyme has odontogenic potential that is expressed upon interactions with inductive signals from mouse odontogenic epithelium. Similar to odontogenesis in vivo, formation of dental mesenchyme in chick mandibular mesenchyme is mediated by the activation of Msx-1, Msx-2, and Bmp-4. Dev. Dyn. 1998;213:386–397. © 1998 Wiley-Liss, Inc.
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ABSTRACT The morphogenetic capacity of prechondrogenic mesenchyme from two developmentally distinct sources was investigated in high density micromass cultures. We confirmed an earlier report (Weiss & Moscona, 1958) that scleral mesenchyme formed cartilage sheets whilst limb bud mesenchyme formed distinct cartilage nodules. It was thus suggested by these authors that this morphogenesis was tissue type specific. However, by varying cell density at inoculation (which controls cell configuration) and by varying the relative amount of prechondrogenic mesenchyme present in cultures we found that dramatic changes in morphogenesis could be brought about. Viewed in these terms we suggest that cartilage morphogenesis in vitro is dependent on cell configuration and the presence of non-chondrogenic cell types and hence is not necessarily a function of an intrinsic morphogenetic potential of the constituent cells.
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Limb, somite, and neural crest mesenchyme from quail embryos were implanted orthotopically and heterotopically into chick hosts to ascertain the relative importance of the local environment on mesenchyme migration. It was found that mesenchyme behavior is strongly influenced by the environment. Normally non-migratory, limb mesenchyme is capable of spreading like sclerotome when placed in the somite region. A somite placed in the limb acquires an appearance typical of limb mesenchyme. Neural crest placed in the limb migrates only along the co-implanted neural tube or axons growing out from it. The orthotopic transplantations showed that quail mesenchyme behaves normally in chick embryos. Furthermore, it was observed in the orthotopic transplants that there was no intermingling of quail and chick cells even at the edge of the graft. This result indicates that cells within mesenchyme are normally not locomotory; rather, the mesenchyme "migrates" by spreading and expansion of the tissue as a unit in response to local influences.
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The prostate gland develops from the urogenital sinus as epithelial buds projecting into the surrounding mesenchyme. The role of the mesenchyme in this process was determined using sinuses from normal and androgen-insensitive Tfm mice which are deficient in androgen receptors. Epithelium and mesenchyme from both types of sinus were separated and recombined and the recombinants grown in organ culture in the presence of testosterone. Recombinants consisting of normal epithelium and normal mesenchyme developed epithelial buds projecting into the surrounding mesenchyme but no buds were formed in recombinants of epithelium and mesenchyme from mutant mice. In recombinants of epithelium from mutant mice with normal mesenchyme the epithelium developed prostatic buds and the number was similar to that found if normal epithelium was associated with normal mesenchyme. In contrast, normal epithelium combined with mesenchyme from mutant mice failed to form prostatic buds. The results suggested that the mesenchyme determines the development of prostatic buds and that the lack of inductive capacity of the mesenchyme from mutant mice may be due to a deficiency of mesenchymal androgen receptors.
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During development, the embryos and larvae of the starfish Asterina pectinifera possess a single type of mesenchyme cell. The aim of this study was to determine the patterns of behavior of mesenchyme cells during the formation of various organs. To this end, we used a monoclonal antibody (mesenchyme cell marker) to identify the distribution patterns and numbers of mesenchyme cells. Our results revealed the following: (i) mesenchyme cell behavior differs in the formation of different organs, showing temporal variations and an uneven pattern of distribution; and (ii) mesenchyme cells continue to be generated throughout development, and their numbers are tightly regulated in proportion to total cell numbers.
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Insoluble "biomatrix" of mesenchyme is a stimulator of mammary cell differentiation in vitro, but its effect in the morphogenesis is unknown. Fetal salivary mesenchyme induces intense local duct formation when implanted into adult mammary gland. We have therefore tested whether biomatrix prepared from fetal salivary mesenchyme retains this abillity to stimulate duct formation in vivo. Salivary mesenchyme isolated from mouse fetuses at 13.5-14.0 days of gestation, extracted sequentially with water and with 1 M NaCl, then digested with DNAse and RNAse was implanted into mammary glands of female mice and left for periods of 1-35 days. In approximately 40% of recipients, the local epithelium either formed cyst like structures, or else "spikes" of mammary epithelium penetrated the matrix forming a simplified ductwork inside it. Similar responses were elicited by salivary mesenchyme killed by freezing and also by biomatrix prepared from fetal mammary fat pad precursor tissue, mesenchyme of fetal lung, and fetal heart, liver, and brain. However when mesenchyme was either fixed with glutaraldehyde or sonicated and embedded in polymer blocks before implantation, no epithelial response was noted. These observations suggest that the biomatrix provides a passive scaffolding that contributes to morphogenesis of mammary ducts, is insufficient to support normal morphogenesis.
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The ultrastructure of a fetal mesenchymal hamartoma of the kidney shows undifferentiated mesenchymal cells, whose morphological characteristics conform to those of secondary mesenchyme. In contrast to primary mesenchyme or mesoblast, which may form epithelial structures, secondary mesenchyme is incapable of doing so. While Wilms' tumor may be considered a tumor of mesoblast, the fetal mesenchymal hamartoma is believed to originate from secondary mesenchyme or some of its more mature derivatives.
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