Banner Portal
Genes and tooth development: reviewing the structure and function of some key players.
Remote

Keywords

Tooth morphogenesis. Genes. Molecular signaling

How to Cite

1.
Caminaga RMS, Pasetto S, Silva ER da, Peres RCR. Genes and tooth development: reviewing the structure and function of some key players. Braz. J. Oral Sci. [Internet]. 2015 Nov. 12 [cited 2024 Apr. 26];2(7):339-47. Available from: https://periodicos.sbu.unicamp.br/ojs/index.php/bjos/article/view/8641715

Abstract

Similar to many other embryonic organs, the mammalian tooth development relies largely on epithelial-mesenchymal interactions. Tooth development may be divided in multiple stages, where the number, size and type of teeth are sequentially determined. Teeth are serially homologous structures, which allow the localization and quantification of the effects of specific gene mutations. Furthermore, it is also possible to determine the phase of odontogenesis affected by these conditions. These features make anomalies involving teeth an important system to understand the intricate molecular mechanisms that regulate developmental process. In this paper we review the structure and function of some key molecules that participate in tooth development.
https://doi.org/10.20396/bjos.v2i7.8641715
Remote

References

Kollar EJ, Baird GR. The influence of the dental papilla on the development of tooth shape in embryonic mouse tooth germs. J Embryol Exp Morphol 1969; 21: 131-48.

Kollar EJ, Baird GR. Tissue interactions in embryonic mouse tooth germs. J Embryol Exp Morphol 1970; 24: 159-86.

Thesleff I, Humerinta K. Tissue interactions in tooth development. Differentiation 1981; 18: 75-88.

Lumsden AGS. Spatial organization of the epithelium and the role of neural crest cells in the initiation of the mammalian tooth germ. Development 1988; 103: 155- 69.

Jahoda CA. Induction of follicle formatin and hair growth by vibrissa dermal papillae implanted into rat ear wounds: Vibrissa-type fibres are specified. Development 1992; 115: 1103-9.

Dassule HR, McMahon AP. Analysis of epithelialmesenchymal interactions in the initial morphogenesis of the mammalian tooth. Dev Biol 1998; 202: 215-27.

Jernvall J, Thesleff I. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 2000; 92: 19-29.

Maas R, Bei M. The genetic control of early tooth development. Crit Rev Oral Biol 1997; 8: 4-39.

Parr BA, McMahon AP. Wnt genes and vertebrate development. Curr Opin Genet Dev 1994; 4: 523-8.

Nieminen P, Pekkanen M, Åberg T, Thesleff I. A graphical www-database on gene expression in tooth. Eur J Oral Sci 1998; 1: 7-11.

McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ. A homologous protein-coding sequence in Drosophila homeotic genes and its conservation in other metazoans. Cell 1984; 37: 403-8.

Scott MP, Weiner AJ. Structural relationships among genes that control development: sequence homology between the Antennapedia, Ultrabithorax, and fushi tarazu loci of Drosophila. Proc Natl Acad Sci USA 1984; 81: 4115-9.

Davidson D. The function and evolution of Msx genes: pointers and paradoxes. Trends Genet 1995; 11: 405-11.

Manzanares M, Krumlauf R. Mammalian embryo: Hox genes. Enciclopedia of Life Sciences. 2001. Available from URL: http://www.els.net.

Vaahtokari A, Vainio S, Thesleff I. Associations between transforming growth factor b1 RNA expression and epithelial-mesenchymal interactions during tooth morphogenesis. Development 1991; 113: 985-94.

Satokata I, Maas R. Msx1 deficient mice exhibit cleft palate and abnormalities of craniofacial and tooth development. Nat Genet 1994; 6: 348-56.

Vastardis H, Karimbux N, Guthua SW, Seidman IG, Seidman CE. A human MSX1 homeodomain missense mutation causes selective tooth agenesis. Nat Genet 1996; 13: 417-21.

Scarel RM, Trevilatto PC, Di Hipólito Jr, O., Camargo LEA, Line, SRP. Absence of mutations in the homeodomain of the MSX1 gene in patients with hypodontia. Am J Med Genet 2000; 92: 346-9.

Jabs EW, Muller U, Li X, Ma L, Luo W, Haworth I et al. A mutation in the homeodomain of the MSX2 gene in a family affected with autosomal dominant craniosynostosis. Cell 1993; 75: 443-50.

Underhill DA. Genetic and biochemical diversity in the Pax gene family. Biochem Cell Biol 2000; 78: 629-38.

Chi N, Epstein JA. Getting your Pax straight: Pax proteins in development and disease. Trends Genet 2002; 18: 41-7.

Dietrich S, Gruss P. Undulated phenotypes suggests a role of Pax-1 for the development of vertebral and extravertebral structures. Dev Biol 1995; 167: 529-49.

Neubüser A, Peters H, Balling R, Martin GR. Antagonistic interactions between FGF and BMP signaling pathways: a mechanism for positioning the sites of tooth formation. Cell 1997; 90: 247-55.

Peters H, Neubüser A, Kratochwill K, Bailling R. Pax9 deficient mice lack pharyngeal pouch derivates and teeth, and exhibit craniofacial and limb abnormalities. Genes Dev 1998; 12: 2735-47.

Stockton DW, Das P, Goldenberg M, D´Souza RN, Patel PI. Mutation of PAX9 is associated with oligodontia. Nat Genet 2000; 24: 18-9.

Das P, Stockton DW, Bauer C, Shaffer LG, D´Souza RN, Wright JT et al. Haploinsufficiency of PAX9 is associated with autosomal dominant hypodontia. Hum Genet 2002; 110: 371-6.

Weiss K, Stock D, Zhao Z. Dynamic interactions and the evolutionary genetics of dental patterning. Crit Rev Oral Biol Med 1998; 9: 369-98.

Zhao Z, Stock D, Buchanan A, Weiss K. Expression of Dlx genes during the development of murine dentition. Dev Genes Evol 2000; 210: 270-5.

Price J, Bowden D, Wright J, Pettenati M, Hart TC. Identification of a mutation in DLX3 associated with tricodento-osseous (TDO) syndrome. Hum Mol Genet 1998; 7: 563-9.

Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA et al. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 1999; 126: 3831-46.

Giese K, Cox J, Grosschedl R. The HMG domain of lymphoid enhancer factor 1 bends DNA and facilitates assembly of functional nucleoprotein structures. Cell 1992; 69: 185-95.

Love JJ, Li X, Case DA, Grosschedl R, Wright PE. Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature 1995; 376: 791-5.

Giese K, Pagel J, Grosschedl R.. Functional analysis of DNA bending and unwinding by the high mobility group domain of LEF-1. Proc Natl Acad Sci 1997; 94: 12845-50.

van Genderen C, Okamura RM, Fariñas I, Quo R-G, Parslow TG, Bruhn L et al. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev 1994; 8: 2691-2703.

Travis A, Amsterdam A, Belanger C, Grosschedl R. LEF-1, a gene encoding a lymphoid-specific protein with an HMG domain, regulates T-cell receptor a enhancer function. Genes Dev 1991; 5: 880-94.

Waterman ML, Fischer WH, Jones KA. A thymus specific member of the HMG protein family regulates the human T-cell receptor Ca enhancer. Genes Dev 1991; 5: 656-69.

Oosterwegel M, van der Wetering M, Timmerman J, Kruisbeek A, Destree O, Meijlink F et al. Differentrial expression of the HMG box factors TCF-1 and LEF-1 during murine embryogenesis. Development 1993; 118: 439-48.

Zhou P, Byrne C, Jacobs J, Fuchs E. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev 1995; 9: 700-13.

Milatovich A, Travis A, Grosschedl R, Francke U. Gene for lymphoid enhancer-binding factor 1 (LEF-1) maped to human chromosome 4 (q23-q25) and mouse chromosome 3 near Egf. Genomics 1991; 11: 1040-8 40. Kratochwil K, Dull M, Farinas I, Galceran J, Grosschedl R. Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev 1996; 10: 1382-94.

Hammershmidt M, Brook A, McMahon AP. The world according to hedgehog. Trends Genet 1997; 13: 14-21.

Johnson RL, Tabin C. The long and short of hedgehog signaling. Cell 1995; 81: 313-6.

Zhang Y, Zhao X, Hu Y, St Amand T, Zhang M, Ramamurthy R, et al. Msx1 is required for the induction of Patched by Sonic Hedgehog in the mammalian tooth germ. Dev Dyn 1999; 215: 45-53.

Hooper JE, Scott MP. The Drosophila patched gene encodes a putative membrane protein required for segmental patterning. Cell 1989; 59: 751-65.

Thesleff I. Homeobox genes and growth factors in regulation of craniofacial and tooth morphogenesis. Acta Odontol Scand 1995; 53: 129-34.

Thesleff I. Genetic basis of the tooth development and dental defects. Acta Odontol Scand 2000; 58: 191-4.

Jernvall J, Kettunen P, Karavanova I, Martin LB, Thesleff I. Evidence for the role of the enamel knot as a control center in mammalian tooth cusp formation: Non-dividing cells express growth stimulating FGF-4 gene. Int J Dev Biol 1994; 38: 463-9.

Kettunen P, Thesleff I. Expression and function of FGFs 4, 8 and 9 suggest functional redundancy and repetitive use as epithelial signals during tooth development. Dev Dyn 1998; 211: 256-68.

Vaahtokari A, Aberg T, Thesleff I. Apoptosis in the developing tooth: association with an embryonic signaling center and suppression by EGF and FGF-4. Development 1996; 122: 121-6.

Thesleff I, Sharpe P. Signaling networks regulating dental development. Mech Dev 1997; 67: 111-23.

Thesleff I, Aberg T. Molecular regulation of tooth development. Bone 1999; 25: 123-125.

Grigoriou M, Tucker AS, Sharpe PT, Pachnis P. Expression and regulation of Lhx6 and Lhx7, a novel subfamily of LIM homeodomain encoding genes, suggests a role in mammalian head development. Development 1998; 125: 2063-74.

St Amand TR, Zhang Y, Semina E, Zhao X, Hu Y, Nguyen L, et al. Antagonistic signals between BMP4 and FGF8 define expression of Pitx1 and Pitx2 in mouse toothforming anlage. Dev Biol 2000; 217: 323-32.

. Mandler M, Neubüser A. FGF signaling is necessary for specification of the odontogenic mesenchyme. Dev Biol 2001; 240: 548-59.

Kettunen P, Laurikkala J, Itaranta P, Vainio S, Itoh N, Thesleff I. Associations of FGF-3 and FGF-10 with signaling networks regulating tooth morphogenesis. Dev Dyn 2000; 219: 322-32.

Jernvall J, Aberg T, Kettunen P, Keränen S, Thesleff I. The life history of an embryonic signaling center: BMP-4 induces p21 and is associated with apoptosis in the mouse tooth enamel knot. Development 1998; 125: 161-9.

Coin R, Lesot H, Vonesch JL, Haikel Y, Ruch JV. Aspects of cell proliferation kinetics of the inner dental epithelium during mouse molar and incisor morphogenesis: a reappraisal of the enamel knot area. Int J Dev Biol 1999; 43: 261-9.

Nexo E, Hollenberg MD, Figueroa A, Pratt RM. Detection of epidermal growth factor-urogastrone and its receptor during fetal mouse development. Proc Natl Acad Sci 1980; 77: 5 2782-5.

Partanem AM. Epidermal growth factor and transforming growth factor in the development of epithelialmesenchymal organ of the mouse. In: Hamilton MN. editor. Growth Factors and Development. New York: John Wiley; 1990. p. 31-53.

Carpenter G, Cohen S. Epidermal growth factor. Ann Rev Biochem 1979; 48: 193-216.

Kaplowitz PB, D´Ercole AJ, Underwood LE. Stimulation of embryonic mouse limb bud mesenchymal cell growth by peptide growth factors. J Cell Physiol 1982; 112: 353- 359.

Adamson ED. Developmental of epidermal growth factor receptor. In: Hamilton MN. editor. Growth Factors and Development. New York: John Wiley; 1990. p. 1-30.

Livneh E, Glaser L, Segal D, Schlessinger J, Shilo BZ. The Drosophila EGF receptor gene homolog conservation of both hormone binding and kinase domains. Cell 1985; 40: 599-607.

Kronmiller JE, Upholt WB, Kollar J. EGF antisense oligodeoxynucleotides block murine odontogenesis in vitro. Dev Biol 1991; 147: 485-8.

Kronmiller JE., Upholt WB, Kollar EJ. Effects of retinol on the temporal expression of transforming growth factoralpha mRNA in the embryonic mouse mandible. Arch Oral Biol 1993; 38: 185-8.

Kronmiller JE, Upholt WB, Kollar J. Expression of epidermal growth factor in RNA in the developing mouse mandibular process. Arch Oral Biol 1991; 36: 405-10.

Partanem AM, Thesleff I. Localization and quantification of 125I epidermal growth factor binding in mouse embryonic tooth and other embryonic tissue at different developmental stages. Dev Biol 1987; 120: 196-7, 68. Hsu S, Borke JL, Lewis JB, Singh B, Aiken AC, Huynh CT, et al. Transforming growth factor ²1 dysregulation in a human oral carcinoma tumour progression model. Cell Prolif 2002; 35: 183-92.

Shimo T, Wu C, Billings PC, Piddington R, Rosanbloom J, Pacifici M, et al. Expression, gene regulation, and roles of Fisp 12/CTGF in developing tooth germs. Dev Dyn 2002; 224: 267-78 Thesleff I, Vaahtokari A. The role of growth factors in determination of the odontoblastic cell lineage. Proc Finn Dent Soc 1992; 88: 357-68.

Makela TP, Alitalo R, Paulsson Y, Westermark B, Heldin CH, Alitalo K. Regulation of platelet-derived growth factor gene expression by transforming growth factor beta and phorbol ester in human leukemia cell lines. Molec Cell Biol 1987; 7: 3656-62.

Sutcliffe JE, Owens PDA. A light and scanning electron microscopic study of the development of enamel-free areas on the molar teeth of the rat. Archs Oral Biol 1980; 25: 263-8.

. Winnier G, Blessing M, Labosky PA, Hogan BLM. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995; 9: 2105-16.

Zhang H, Bradley A. Mice deficient for BMP-2 are nonviable and have defects in amnion/chorion and cardiac development. Development 1996; 122: 2977-86.

Sahlberg C, Reponen P, Tryggvason K, Thesleff I. Association between the expression of murine 72 kDa type IV collagenase by odontoblasts and basement membrane degradation during mouse tooth development. Arch Oral Biol 1992; 37: 1021-30.

Thesleff I, Barrach HJ, Foidart JM, Vaheri A, Pratt RM, Matin GR. Changes in the distribution of type IV collagen, laminin, proteoglycan and fibronectin during mouse tooth development. Dev Biol 1981; 81: 182-92.

Lesot H, Kubler MD, Fausser JL, Ruch JV. A 165 kDa membrane antigen mediating fibronectin-vinculin interactions is involved in murine odontoblast differentiation. Differentiation 1990; 44: 25-35.

Bernfield M, Sanderson RD. Syndecan, a morphogenetically regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Phil Trans R Soc (London) 1990; 327: 171-86.

Elenius K, Salmivirta M, Inki P, Mali M, Jalkanen M. Binding of human syndecan to extracellular matrix proteins. J Biol Chem 1990; 17: 837-43.

Salmivirta M, Elenius K, Vainio S, Hofer U, ChiquetEhrismann R, Thesleff I, et al. Syndecan from embryonic tooth mesenchyme binds tenascin. J Biol Chem 1991; 266: 7733-9.

Thesleff I, Jalkanen M, Vainio S, Berfield M. Cell surface proteoglycan expression correlates with epithelialmesenchymal interactions during tooth morphogenesis. Dev Biol 1988; 129: 565-72.

Saga Y, Yagi T, Ikawa Y, Sakakura T, Aizawa S. Mice develop normally without tenascin. Gene Dev 1992; 6: 1821-31.

Vainio S, Thesleff I. Sequential induction of syndecan, tenascin and cell proliferation associated with mesenchymal cell condensation during early tooth development. Differentiation 1992; 50: 97-105.

Rapraeger A. Transforming growth factor (Type b) promotes the addition of chondroitin sulfate chains to the cell surface proteoglycan (syndecan) of mouse mammary epithelia. J Cell Biol 1989; 109: 2509-18.

Kiefer MC, Stephans JC, Crawford K, Okino K, Barr PJ. Ligand affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. Proc Natl Acad Sci USA 1990; 87: 6985-9.

Rettig WJ, Erickson HP, Albino AP, Garin-Chesa P. Induction of human tenascin (neuronectin) by growth factors and cytokines: cell type-specific signals and signaling pathways. J Cell Sci 1994; 107: 487-97.

Sahlberg C, Aukhil I, Thesleff I. Tenascin-C in developing mouse teeth: expression of splice variants and stimulation by TGFb and FGF. Eur J Oral Sci 2001; 109: 114-24.

Rasmussen S, Rapraeger A. Altered structure of the hybrid cell surface proteoglycan of mammary epithelial cells in response to transforming growth factor-b. J Cell Biol 1988; 107: 1959-67.

Rizzino A, Kazakoff P, Ruff E, Kuszynski C, Nebelsick J.

Regulatory effects of cell density on the binding of transforming growth factor beta, epidermal growth factor, platelet-derived growth factor, and fibroblast growth factor.

Cancer Res 1988; 48: 4266-71 90. Roberts AB, Sporn MB, Assoian RK, Smith JM, Roche NS, Wakefield LM, et al. Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc Natl Acad Sci U S A 1986; 83: 4167-71.

Vainio S, Karavanova I, Jowett A, Thesleff I. Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 1993; 75: 45-58.

Bei M, Maas R. FGFs and BMP4 induce both Msx1- independent and Msx1-dependent signaling pathways in early tooth development. Development 1998; 125-4325- 33.

Tucker AS, Khamis A, Sharpe PT. Interactions between Bmp-4 and Msx-1 act to restrict gene expression to odontogenic mesenchyme. Dev Dyn 1998; 212: 533-9.

Chen YP, Bei M, Woo I, Satokata I, Maas R. Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 1996; 122: 3035-44.

Zhang Y, Zhang Z, Zhao X, Yu X, Hu Y, Geronimo B, et al.

A new function of BMP4: dual role for BMP4 in regulation of Sonic Hedgehog expression in the mouse tooth germ. Development 2000; 127: 1431-43.

Line SRP. Variation of tooth number in mammalian dentition: Connecting genetics, development, and evolution. Evolution and Development 2003; 5: 295-304.

The Brazilian Journal of Oral Sciences uses the Creative Commons license (CC), thus preserving the integrity of the articles in an open access environment.

Downloads

Download data is not yet available.