Abstract
Odontogenesis has only been closely scrutinized at the molecular level in the mouse, an animal with an extremely restricted dentition of only two types and one set. However, within osteichthyans many species display complex and extensive dentitions, which questions the extent to which information from the mouse is applicable to all osteichthyans. We present novel comparative molecular and morphological data in the rainbow trout (Oncorhynchus mykiss) that show that three genes, essential for murine odontogenesis, follow identical spatial-temporal expression. Thus, at all tooth bud sites, epithelial genes Pitx-2 and Shh initiate the odontogenic cascade, resulting in dental mesenchymal Bmp-4 expression, importantly, including the previously unknown formation of replacement teeth. Significantly, this spatial-temporal sequence is the same for marginal and lingual dentitions, but we find notable differences regarding the deployment of Pitx-2 in the developing pharyngeal dentition. This difference may be highly significant in relation to the theory that dentitions may have evolved from pharyngeal tooth sets in jawless fishes. We have provided the first data on operational genes in tooth development to show that the same signalling genes choreograph this evolutionary stable event in fishes since the osteichthyan divergence 420 Myr ago, with the identical spatial-temporal expression as in mammals.
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Selected References
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- Avaron Fabien, Thaëron-Antono Christelle, Beck Caroline W., Borday-Birraux Véronique, Géraudie Jacqueline, Casane Didier, Laurenti Patrick. Comparison of even-skipped related gene expression pattern in vertebrates shows an association between expression domain loss and modification of selective constraints on sequences. Evol Dev. 2003 Mar-Apr;5(2):145–156. doi: 10.1046/j.1525-142x.2003.03021.x. [DOI] [PubMed] [Google Scholar]
- Bei M., Maas R. FGFs and BMP4 induce both Msx1-independent and Msx1-dependent signaling pathways in early tooth development. Development. 1998 Nov;125(21):4325–4333. doi: 10.1242/dev.125.21.4325. [DOI] [PubMed] [Google Scholar]
- Dassule H. R., Lewis P., Bei M., Maas R., McMahon A. P. Sonic hedgehog regulates growth and morphogenesis of the tooth. Development. 2000 Nov;127(22):4775–4785. doi: 10.1242/dev.127.22.4775. [DOI] [PubMed] [Google Scholar]
- Gritli-Linde Amel, Bei Marianna, Maas Richard, Zhang Xiaoyan M., Linde Anders, McMahon Andrew P. Shh signaling within the dental epithelium is necessary for cell proliferation, growth and polarization. Development. 2002 Dec;129(23):5323–5337. doi: 10.1242/dev.00100. [DOI] [PubMed] [Google Scholar]
- Jernvall J., Thesleff I. Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev. 2000 Mar 15;92(1):19–29. doi: 10.1016/s0925-4773(99)00322-6. [DOI] [PubMed] [Google Scholar]
- Laurenti Patrick, Thaëron Christelle, Allizard Françoise, Huysseune Ann, Sire Jean-Yves. Cellular expression of eve1 suggests its requirement for the differentiation of the ameloblasts and for the initiation and morphogenesis of the first tooth in the zebrafish (Danio rerio). Dev Dyn. 2004 Aug;230(4):727–733. doi: 10.1002/dvdy.20080. [DOI] [PubMed] [Google Scholar]
- Mucchielli M. L., Mitsiadis T. A., Raffo S., Brunet J. F., Proust J. P., Goridis C. Mouse Otlx2/RIEG expression in the odontogenic epithelium precedes tooth initiation and requires mesenchyme-derived signals for its maintenance. Dev Biol. 1997 Sep 15;189(2):275–284. doi: 10.1006/dbio.1997.8672. [DOI] [PubMed] [Google Scholar]
- Peters H., Balling R. Teeth. Where and how to make them. Trends Genet. 1999 Feb;15(2):59–65. doi: 10.1016/s0168-9525(98)01662-x. [DOI] [PubMed] [Google Scholar]
- Smith Moya Meredith, Johanson Zerina. Separate evolutionary origins of teeth from evidence in fossil jawed vertebrates. Science. 2003 Feb 21;299(5610):1235–1236. doi: 10.1126/science.1079623. [DOI] [PubMed] [Google Scholar]
- Smith Moya Meredith. Vertebrate dentitions at the origin of jaws: when and how pattern evolved. Evol Dev. 2003 Jul-Aug;5(4):394–413. doi: 10.1046/j.1525-142x.2003.03047.x. [DOI] [PubMed] [Google Scholar]
- Thesleff I., Sharpe P. Signalling networks regulating dental development. Mech Dev. 1997 Oct;67(2):111–123. doi: 10.1016/s0925-4773(97)00115-9. [DOI] [PubMed] [Google Scholar]
- 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 Oct 8;75(1):45–58. [PubMed] [Google Scholar]
- Van der heyden C., Huysseune A., Sire J. Y. Development and fine structure of pharyngeal replacement teeth in juvenile zebrafish (Danio rerio) (Teleostei, Cyprinidae). Cell Tissue Res. 2000 Nov;302(2):205–219. doi: 10.1007/s004410000180. [DOI] [PubMed] [Google Scholar]
- Van der heyden C., Wautier K., Huysseune A. Tooth succession in the zebrafish (Danio rerio). Arch Oral Biol. 2001 Nov;46(11):1051–1058. doi: 10.1016/s0003-9969(01)00064-4. [DOI] [PubMed] [Google Scholar]
- Xu Q., Holder N., Patient R., Wilson S. W. Spatially regulated expression of three receptor tyrosine kinase genes during gastrulation in the zebrafish. Development. 1994 Feb;120(2):287–299. doi: 10.1242/dev.120.2.287. [DOI] [PubMed] [Google Scholar]
- Zhang Y., Zhang Z., Zhao X., Yu X., Hu Y., Geronimo B., Fromm S. H., Chen Y. P. A new function of BMP4: dual role for BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development. 2000 Apr;127(7):1431–1443. doi: 10.1242/dev.127.7.1431. [DOI] [PubMed] [Google Scholar]