Abstract
Mouse incisors are capable of continuously growing due to the renewal of dental epithelium stem cells and mesenchymal stem cells residing at the proximal ends. The transcription factor Sox9 plays important roles in maintaining the stem cells of hair follicles, retinal progenitor cells and neural crest stem cells. Whether Sox9 is involved during mouse incisor development is not reported yet. In this study, we examined the expression pattern of Sox9 during mouse incisor development by in situ hybridization and immunohistochemistry. Sox9 mRNA and protein showed similar expression pattern from embryonic day (E) 13.5 to postnatal (PN) day 10. At E13.5 and E14.5, Sox9 was strongly expressed in the dental epithelium. At E16.5, Sox9 started to be detected in the mesenchymal cells within the dental pulp, especially the dental pulp cells that adjacent to the labial cervical loop. Similarly with E14.5, Sox9 was strongly detected in the labial cervical loop, including the basal epithelium, the stellate reticulum and the outer enamel epithelium from E16.5 to PN10. The mesenchyme adjacent to the labial cervical loop also showed strong signal of Sox9. The spatiotemporal expression of Sox9 suggested its possible involvement during mouse incisor development.
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References
Cheung M, Briscoe J (2003) Neural crest development is regulated by the transcription factor Sox9. Development 130:5681–5693. doi:10.1242/dev.00808
Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci USA 108:6503–6508. doi:10.1073/pnas.1015449108
Fujimori S et al (2010) Wnt/beta-catenin signaling in the dental mesenchyme regulates incisor development by regulating Bmp4. Dev Biol 348:97–106
Furuyama K et al (2011) Continuous cell supply from a Sox9-expressing progenitor zone in adult liver, exocrine pancreas and intestine. Nat Genet 43:34–41. doi:10.1038/ng.722
Guo W et al (2012) Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148:1015–1028. doi:10.1016/j.cell.2012.02.008
Harada H, Ohshima H (2004) New perspectives on tooth development and the dental stem cell niche. Arch Histol Cytol 67:1–11
Harada H, Kettunen P, Jung HS, Mustonen T, Wang YA, Thesleff I (1999) Localization of putative stem cells in dental epithelium and their association with Notch and FGF signaling. J Cell Biol 147:105–120
Harada H et al (2002) FGF10 maintains stem cell compartment in developing mouse incisors. Development 129:1533–1541
Jernvall J, Thesleff I (2000) Reiterative signaling and patterning during mammalian tooth morphogenesis. Mech Dev 92:19–29
Juuri E et al (2012) Sox2+ stem cells contribute to all epithelial lineages of the tooth via Sfrp5+ progenitors. Dev Cell 23:317–328. doi:10.1016/j.devcel.2012.05.012
Li J et al (2011a) SMAD4-mediated WNT signaling controls the fate of cranial neural crest cells during tooth morphogenesis. Development 138:1977–1989. doi:10.1242/dev.061341
Li L, Kwon HJ, Harada H, Ohshima H, Cho SW, Jung HS (2011b) Expression patterns of ABCG2, Bmi-1, Oct-3/4, and Yap in the developing mouse incisor. Gene Expr Patterns 11:163–170
Lian M et al (2016) JAB1 accelerates odontogenic differentiation of dental pulp stem cells. J Mol Histol 47:317–324. doi:10.1007/s10735-016-9672-5
Mitsiadis TA, Barrandon O, Rochat A, Barrandon Y, De Bari C (2007) Stem cell niches in mammals. Exp Cell Res 313:3377–3385. doi:10.1016/j.yexcr.2007.07.027
Moore KA, Lemischka IR (2006) Stem cells and their niches. Science 311:1880–1885. doi:10.1126/science.1110542
Nowak JA, Polak L, Pasolli HA, Fuchs E (2008) Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3:33–43. doi:10.1016/j.stem.2008.05.009
Poche RA, Furuta Y, Chaboissier MC, Schedl A, Behringer RR (2008) Sox9 is expressed in mouse multipotent retinal progenitor cells and functions in Muller glial cell development. J Comp Neurol 510:237–250. doi:10.1002/cne.21746
Seidel K et al (2010) Hedgehog signaling regulates the generation of ameloblast progenitors in the continuously growing mouse incisor. Development 137:3753–3761. doi:10.1242/dev.056358
Shi L, Li L, Wang D, Li S, Chen Z, An Z (2016) Spatiotemporal expression of caveolin-1 and EMMPRIN during mouse tooth development. J Mol Histol 47:337–344. doi:10.1007/s10735-016-9675-2
Slavkin HC, Snead ML, Zeichner-David M, Jaskoll TF, Smith BT (1984) Concepts of epithelial-mesenchymal interactions during development: tooth and lung organogenesis. J Cell Biochem 26:117–125. doi:10.1002/jcb.240260207
Sun Z et al (2016) Sox2 and Lef-1 interact with Pitx2 to regulate incisor development and stem cell renewal. Development 143:4115–4126. doi:10.1242/dev.138883
Thesleff I (2003) Epithelial-mesenchymal signalling regulating tooth morphogenesis. J Cell Sci 116:1647–1648
Thesleff I, Vaahtokari A, Partanen AM (1995) Regulation of organogenesis. Common molecular mechanisms regulating the development of teeth and other organs. Int J Dev Biol 39:35–50
Wang XP et al (2007) An integrated gene regulatory network controls stem cell proliferation in teeth. PLoS Biol 5:e159. doi:10.1371/journal.pbio.0050159
Zhang L, Yuan G, Liu H, Lin H, Wan C, Chen Z (2012) Expression pattern of Sox2 during mouse tooth development. Gene Expr Patterns 12:273–281. doi:10.1016/j.gep.2012.07.001
Zhao H, Li S, Han D, Kaartinen V, Chai Y (2011) Alk5-mediated transforming growth factor beta signaling acts upstream of fibroblast growth factor 10 to regulate the proliferation and maintenance of dental epithelial stem cells. Mol Cell Biol 31:2079–2089. doi:10.1128/mcb.01439-10
Zhao H, Feng J, Seidel K, Shi S, Klein O, Sharpe P, Chai Y (2014) Secretion of shh by a neurovascular bundle niche supports mesenchymal stem cell homeostasis in the adult mouse incisor. Cell Stem Cell 14:160–173. doi:10.1016/j.stem.2013.12.013
Acknowledgements
This study was supported by grants from the National Natural Science Foundation of China (NSFC) (81400479); Open Research Fund Program of Hubei-MOST KLOS & KLOBM (2014-03); Startup Foundation of Binzhou Medical University (511504 BY2013KYQD32) to Dr. Li Zhang and Natural Science Foundation of Shandong Province (ZR2014HL051) to Dr. Zhi-cheng Yang.
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Yang, Zc., Li, D., Feng, S. et al. Spatial and temporal expression of Sox9 during murine incisor development. J Mol Hist 48, 321–327 (2017). https://doi.org/10.1007/s10735-017-9730-7
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DOI: https://doi.org/10.1007/s10735-017-9730-7