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Journal of Dental Research
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Localization of Nerve Cells in the Developing Rat Tooth

K. Luukko

Programme of Developmental Biology

K. Sainio

Programme of Developmental Biology

H. Sariola

Programme of Developmental Biology

M. Saarma

Neurobiology, Institute of Biotechnology, Biocentre 1A, P.O. Box 56 (Viikinkaari 9), FIN-00014 University of Helsinki and Institute of Dentistry, P.O. Box 41 (Mannerheimintie 172), FIN-00014 University of Helsinki, Helsinki, Finland

I. Thesleff

Programme of Developmental Biology

Earlier studies have shown that mammalian tooth formation can take place in the absence of peripheral nerve fibers. This has been taken to indicate that neurons are not needed for mammalian tooth development. However, our recent localization of peripherin, which is a neuronal cell marker, has suggested that neuronal cell bodies may be associated with developing teeth. In this study, we have analyzed in vivo and in vitro the presence of neuronal cells in developing rat tooth germs. When E14 and E16 rat first molars (thickening of presumptive dental epithelium and bud-stage tooth germ, respectively) were cultured in vitro, peripheral trigeminal axons degenerated. However, with antibodies against peripherin and L1 neural cell adhesion protein, we detected neuronal cell bodies and their axons in the explants. Next, the expression of neurofilament light-chain (NF-L) mRNAs was studied by in situ hybridization of embryonic E12 first branchial arches and tooth germs from initiation to completion of crown morphogenesis (E13, five-day post-natal teeth). NF-L transcripts were first seen at the bud stage (E15) next to the dental epithelium at the buccal side of the tooth germ. At the cap stage (E18), NF-L mRNAs were located under the oral epithelium at some distance from dental epithelium. These expression patterns correlate to the previous localization of peripherin-positive cells and suggest that NF-L expression also revealed neuronal cells. Taken together, these results demonstrate that, in addition to projections of peripheral neurons, neuronal cells are associated with the developing teeth. Hence, it is possible that neuronal cells may participate in the regulation of mammalian tooth formation.

Key Words: Neuronal cells • peripherin • neurofilaments • L1 neural cell adhesion molecule • organogenesis.

REFERENCES

  • Atkinson ME, Mohamed SS (1983). A histochemical study of the cholinergic and adrenergic innervation of the developing teeth and oral tissues in the mouse. Arch Oral Biol 28:353-357.[Medline] [Order article via Infotrieve]
  • Bernick S. (1959). Innervation of the developing molar teeth of rats. Anat Rec 133:91-103,
  • Bhatnagar M., Cintra A., Tinner B., Agnati LF, Kerezoudis N., Edwall L., et al. (1995), Neurotensin-like immunoreactivity in odontoblasts and their processes in rat maxillary molar teeth and the effect of pulpotomy. Regul Peptides 58:141-147. [Medline] [Order article via Infotrieve]
  • Garden MJ, Trojanowski JQ, Schlaepfer WW, Lee VM (1987). Two-stage expression of neurofilament polypeptides during rat neurogenesis with early establishment of adult phosphorylation patterns. J Neurosci 7:3489-3504.[Abstract]
  • Cassin C., Capurcan A. (1979). Buccal organogenesis in Pleurodeles waltlii Michah (urodele amphibian). Study by intrablastocelic transplantation and in vitro culture. J Biol Buccale 7:61-76.[Medline] [Order article via Infotrieve]
  • Christensen K. (1940). Sympathetic nerve fibers in the alveolar nerves and of the dental pulp. J Dent Res 19:227-242.
  • Christensen LR, Janas MS, Møllgård K., Kjær I. ( 1993). An immunocytochemical study of the innervation of developing human fetal teeth using protein gene product 9.5 (PGP 9.5). Arch Oral Biol 38:1113-1120.
  • Escurat M., Djabali K., Gumpel M., Cros F., Portier MM (1990). Differential expression of two neuronal intermediate filament proteins, peripherin and the low-molecule-mass neurofilament protein (NF-L) during the development of the rat. J Neurosci 10:764-784.[Abstract]
  • Fliegner KH, Kaplan MP, Wood TL, Pintar JE, Liem RK ( 1994). Expression of the gene for the neuronal intermediate filament protein-alpha-internexin coincides with the onset of neuronal differentiation in the developing rat nervous system. J Comp Neurol 342:161-173.[CrossRef][Medline] [Order article via Infotrieve]
  • Fristad I., Heyeraas KJ, Kvinnsland I. (1994). Nerve fibers and cells immunoreactive to neurochemical markers in developing rat molars and supporting tissues. Arch Oral Biol 39:633-646.[CrossRef][Medline] [Order article via Infotrieve]
  • Glasstone (1967). Development of teeth in tissue culture. J Dent Res 46:858-861.
  • Gorham JD, Baker H., Kegler D., Ziff EB ( 1990). The expression of the neuronal intermediate filament protein peripherin in the rat embryo. Dev Brain Res 57:235-248.[Medline] [Order article via Infotrieve]
  • Hall BK ( 1988). Patterning of connective tissues in the head: discussion report. Development 103(Suppl):171-174.[Abstract]
  • Imai H., Osumi-Yamashita N., Ninomiya Y., Eto K. (1996). Contribution of early-emigrating midbrain neural crest cells to the dental mesenchyme of mandibular molar teeth in rat embryos. Dev Biol 176:151-165.[CrossRef][Medline] [Order article via Infotrieve]
  • Jackson P., Thompson RJ (1981). The demonstration of new human brain-specific proteins by high resolution two dimensional polyacrylamide gel electrophoresis. J Neurol Sci 49:429-438.[CrossRef][Medline] [Order article via Infotrieve]
  • Johnsen DC (1985). Innervation of teeth: qualitative, quantitative, and developmental assessment. J Dent Res 64(Spec Iss):555-563.
  • Julien JP, Ramachandran K., Grosveld F. (1985). Cloning of cDNA encoding the smallest neurofilament protein from the rat. Biochem Biophys Acta 825:398-404.[Medline] [Order article via Infotrieve]
  • Julien JP, Meyer D., Flavell D., Hurst J., Grosveld F. (1986). Cloning and developmental expression of the murine neurofilament gene family. Brain Res 387:243-250.[Medline] [Order article via Infotrieve]
  • Karanth SS, Springall DR, Kuhn DM, Levene MM, Polak JM (1991). An immunocytochemical study of cutaneous innervation and the distribution of neuropeptides and protein gene product 9.5 in man and commonly employed laboratory animals. Am J Anat 191:369-383.[CrossRef][Medline] [Order article via Infotrieve]
  • Kollar EJ, Lumsden AG (1979). Tooth morphogenesis: the role of the innervation during induction and pattern formation. J Biol Buccale 7:49-60.[Medline] [Order article via Infotrieve]
  • Liem R. ( 1993). Molecular biology of neuronal intermediate filaments. Curr Opin Cell Biol 5:12-16.[CrossRef][Medline] [Order article via Infotrieve]
  • Lumsden Ags (1982). The developing innervation of the lower jaw and its relation to the formation of tooth germs in mouse. In: Teeth; form, function and evolution. Kurten B, editor. New York: Columbia University Press, pp. 32-43.
  • Lumsden Ags (1984). Tooth morphogenesis: contributions of the cranial neural crest in mammals. In: Tooth morphogenesis and differentiation. Belcourt AB, Ruch JV, editors. Paris: INSERM, pp. 29-40.
  • Lumsden Ags (1988). Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 103:155-169.[Abstract/Free Full Text]
  • Lumsden Ags, Buchanan Jag (1986). An experimental study of timing and topography of early tooth development in the mouse embryo with an analysis of the role of innervation. Arch Oral Biol 31:301-311.[CrossRef][Medline] [Order article via Infotrieve]
  • Luukko K. (1997). Immunohistochemical localization of nerve fibres during development of embryonic rat molar using peripherin and protein gene project 9.5 antibodies. Arch Oral Biol (in press).
  • Luukko K., Moshnyakov M., Sainio K., Saarma M., Sariola H., Thesleff I. (1996). Expression of neurotrophin receptors during rat tooth development is developmentally regulated, independent from innervation and suggests functions in regulation of morphogenesis and innervation. Dev Dyn 206:87-99.[CrossRef][Medline] [Order article via Infotrieve]
  • MacKenzie A., Ferguson MW, Sharpe PT (1992). Expression patterns of the homeobox gene Hox-8 in the mouse embryo suggest a role in specifying tooth initiation and shape. Development 115:403-420.[Abstract]
  • Matthews B., Robinson PP (1980). The course of post-ganglionic sympathetic fibres distributed with the trigeminal nerve in the cat. J Physiol 303:391-401.[Abstract/Free Full Text]
  • Mohamed SS, Atkinson ME (1983). A histological study of the innervation of developing mouse teeth. J Anat 136:735-749.[Medline] [Order article via Infotrieve]
  • Nolte C., Martini R. (1992). Immunocytochemical localization of the L1 and N-CAM cell adhesion molecules and their shared carbohydrate epitope L2/HNK-1 in the developing and differentiated gustatory papillae of the mouse tongue. J Neurocytol 21:19-33.[CrossRef][Medline] [Order article via Infotrieve]
  • Pearson AA (1977). The early innervation of the developing deciduous teeth. J Anat 123:563-577.[Medline] [Order article via Infotrieve]
  • Portier MM, de Nechaud B., Gros F. ( 1984). Peripherin, a new member of the intermediate filament protein family. Dev Neurosci 6:335-344.
  • Probstmeier R., Martini R., Tacke R., Schachner M. (1990). Expression of the adhesion molecules L1, N-CAM and Jl/tenascin during development of the murine small intestine. Differentiation 44:42-55.[CrossRef][Medline] [Order article via Infotrieve]
  • Rathjen F., Schachner M. (1984). Immunocytological and biochemical characterization of a new neuronal call surface component (L1 antigen) which is involved in cell adhesion. EMBO J 3:1-10.[Medline] [Order article via Infotrieve]
  • Ruch JV ( 1995). Tooth crown morphogenesis and cytodifferentiations: candid questions and critical comments. Connect Tissue Res 32:1-8.[Medline] [Order article via Infotrieve]
  • Ruch JV, Lesot H., Begue-Kirn C. (1995). Odontoblast differentiation. Int J Dev Biol 39:51-68.[Medline] [Order article via Infotrieve]
  • Sainio K., Nonclercq D., Saarma M., Palgi J., Saxen L., Sariola H. (1994). Neuronal characteristics in embryonic renal stroma. Int J Dev Biol 38:77-84.[Medline] [Order article via Infotrieve]
  • Selman S (1946). Some experiments on the determination of the larval teeth in Ambystoma mexicanum. Odontol Tidsk 54:1-128. Sharpe PT (1995). Homeobox genes and orofacial development. Connect Tissue Res 32:17-25.
  • Shaw G., Weber K. (1982). Differential expression of neurofilament triplet proteins in brain development. Nature 298:277-279.[CrossRef][Medline] [Order article via Infotrieve]
  • Sonderegger P., Rathjen FG (1992). Regulation of axonal growth in the vertebrate nervous system by interactions between glycoproteins belonging to two subgroups of the immunoglobulin superfamily. J Cell Biol 119:1387-1394.[Free Full Text]
  • Thesleff I. (1976). Differentiation of odontogenic tissues in organ culture. Scand J Dent Res 84:353-356.[Medline] [Order article via Infotrieve]
  • Thesleff I., Vaahtokari A., Partanen AM (1995). Regulation of organogenesis. Common molecular mechanisms regulating the development of the teeth and other organs. Int J Dev Biol 39:35-50.[Medline] [Order article via Infotrieve]
  • Tsuzuki H., Kitamura H. (1991). Immunohistochemical analysis of pulpal innervation in developing rat molars. Arch Oral Biol 36:139-146.[Medline] [Order article via Infotrieve]
  • Tuisku F., Hildebrand C. (1994). Evidence for a neural influence on tooth germ generation in a polyphyodont species. Dev Biol 165:1-9.[Medline] [Order article via Infotrieve]
  • Wassermann F. (1939). The innervation of the teeth. J Am Dent Assoc 26:1097-1109.
  • Watterson RL (1965). Structure and mitotic behaviour of the early neural tube. In Organogenesis. DeHaan RL, Ursprung H, editors. New York: Holt, Rinehart and Winston, pp. 129-160.
  • Weatherford HL (1939). The innervation of the teeth in the albino rat with some observations on the finer structure of the dental pulp. Anat Rec 74:329-347.
  • Weil M., Itin A., Keshet E. (1995). A role for mesenchyme-derived tachykinins in tooth and mammary gland morphogenesis. Development 121:2419-2428.[Abstract]

Journal of Dental Research, Vol. 76, No. 7, 1350-1356 (1997)
DOI: 10.1177/00220345970760070401


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