Angled Growth of the Dental Lamina Is Accompanied by Asymmetrical Expression of the WNT Pathway Receptor Frizzled 6

. 2017 ; 8 () : 29. [epub] 20170131

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid28197104

Frizzled 6 (FZD6) belongs to a family of proteins that serve as receptors in the WNT signaling pathway. FZD6 plays an important role in the establishment of planar cell polarity in many embryonic processes such as convergent extension during gastrulation, neural tube closure, or hair patterning. Based on its role during hair development, we hypothesized that FZD6 may have similar expression pattern and function in the dental lamina, which is also a distinct epithelial protrusion growing characteristically angled into the mesenchyme. Diphyodont minipig was selected as a model species because its dentition closely resemble human ones with successional generation of teeth initiated from the dental lamina. We revealed asymmetrical expression of FZD6 in the dental lamina of early as well as late stages during its regression with stronger expression located on the labial side of the dental lamina. During lamina regression, FZD6-positive cells were found in its superficial part and the signal coincided with the upregulation of molecules involved in epithelial-mesenchymal transition and increased migratory potential of epithelial cells. FZD6-expression was also turned on during differentiation of cells producing hard tissues, in which mature odontoblasts, ameloblasts, or surrounding osteoblasts were FZD6-positive. On the other hand, the tip of successional lamina and its lingual part, in which progenitor cells are located, exhibited FZD6-negativity. In conclusion, asymmetrical expression of FZD6 correlates with the growth directionality and side-specific morphological differences in the dental lamina of diphyodont species. Based on observed expression pattern, we propose that the dental lamina is other epithelial tissue, where planar cell polarity signaling is involved during its asymmetrical growth.

Zobrazit více v PubMed

Borello U., Buffa V., Sonnino C., Melchionna R., Vivarelli E., Cossu G. (1999). Differential expression of the Wnt putative receptors Frizzled during mouse somitogenesis. Mech. Dev. 89, 173–177. 10.1016/S0925-4773(99)00205-1 PubMed DOI

Buchtová M., Stembirek J., Glocová K., Matalová E., Tucker A. S. (2012). Early regression of the dental lamina underlies the development of diphyodont dentitions. J. Dent. Res. 91, 491–498. 10.1177/0022034512442896 PubMed DOI

Cai J., Mutoh N., Shin J. O., Tani-Ishii N., Ohshima H., Cho S. W., et al. . (2011). Wnt5a plays a crucial role in determining tooth size during murine tooth development. Cell Tissue Res. 345, 367–377. 10.1007/s00441-011-1224-4 PubMed DOI

Chang H., Smallwood P. M., Williams J., Nathans J. (2016). The spatio-temporal domains of Frizzled6 action in planar polarity control of hair follicle orientation. Dev. Biol. 409, 181–193. 10.1016/j.ydbio.2015.10.027 PubMed DOI PMC

Chien A. J., Conrad W. H., Moon R. T. (2009). A Wnt survival guide: from flies to human disease. J. Invest. Dermatol. 129, 1614–1627. 10.1038/jid.2008.445 PubMed DOI PMC

Cui C. Y., Klar J., Georgii-Heming P., Fröjmark A. S., Baig S. M., Schlessinger D., et al. . (2013). Frizzled6 deficiency disrupts the differentiation process of nail development. J. Invest. Dermatol. 133, 1990–1997. 10.1038/jid.2013.84 PubMed DOI PMC

Dijksterhuis J. P., Petersen J., Schulte G. (2016). WNT/Frizzled signalling: receptor-ligand selectivity with focus on FZD-G protein signalling and its physiological relevance: IUPHAR Review 3. Br. J. Pharmacol. 171, 1195–1209. 10.1111/bph.12364 PubMed DOI PMC

Du Y., Ling J., Wei X., Ning Y., Xie N., Gu H., et al. . (2012). Wnt/β-catenin signaling participates in cementoblast/osteoblast differentiation of dental follicle cells. Connect. Tissue Res. 53, 390–397. 10.3109/03008207.2012.668980 PubMed DOI

Fischer T., Guimera J., Wurst W., Prakash N. (2007). Distinct but redundant expression of the Frizzled Wnt receptor genes at signaling centers of the developing mouse brain. Neuroscience 147, 693–711. 10.1016/j.neuroscience.2007.04.060 PubMed DOI

Fröjmark A. S., Schuster J., Sobol M., Entesarian M., Kilander M. B., Gabrikova D., et al. . (2011). Mutations in Frizzled 6 cause isolated autosomal-recessive nail dysplasia. Am. J. Hum. Genet. 88, 852–860. 10.1016/j.ajhg.2011.05.013 PubMed DOI PMC

Gaete M., Tucker A. S. (2013). Organized emergence of multiple-generations of teeth in snakes is dysregulated by activation of Wnt/β-catenin signalling. PLoS ONE 8:e74484. 10.1371/journal.pone.0074484 PubMed DOI PMC

Grigoryan T., Wend P., Klaus A., Birchmeier W. (2008). Deciphering the function of canonical Wnt signals in development and disease: conditional loss- and gain-of-function mutations of β-catenin in mice. Genes Dev. 22, 2308–2341. 10.1101/gad.1686208 PubMed DOI PMC

Grumolato L., Liu G., Mong P., Mudbhary R., Biswas R., Arroyave R., et al. . (2010). Canonical and noncanonical Wnts use a common mechanism to activate completely unrelated coreceptors. Genes Dev. 24, 2517–2530. 10.1101/gad.1957710 PubMed DOI PMC

Gubb D., García-Bellido A. (1982). A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morphol. 68, 37–57. PubMed

Guo N., Hawkins C., Nathans J. (2004). Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. U.S.A. 101, 9277–9281. 10.1073/pnas.0402802101 PubMed DOI PMC

Handrigan G. R., Richman J. M. (2010). A network of Wnt, hedgehog and BMP signaling pathways regulates tooth replacement in snakes. Dev. Biol. 348, 130–141. 10.1016/j.ydbio.2010.09.003 PubMed DOI

Keller R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950–1954. 10.1126/science.1079478 PubMed DOI

Keller R., Davidson L., Edlund A., Elul T., Ezin M., Shook D., et al. . (2000). Mechanisms of convergence and extension by cell intercalation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 355, 897–922. 10.1098/rstb.2000.0626 PubMed DOI PMC

Kilian B., Mansukoski H., Barbosa F. C., Ulrich F., Tada M., Heisenberg C. P. (2003). The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev. 120, 467–476. 10.1016/S0925-4773(03)00004-2 PubMed DOI

Lin M., Li L., Liu C., Liu H., He F., Yan F., et al. . (2011). Wnt5a regulates growth, patterning, and odontoblast differentiation of developing mouse tooth. Dev. Dyn. 240, 432–440. 10.1002/dvdy.22550 PubMed DOI PMC

Liu G., Vijayakumar S., Grumolato L., Arroyave R., Qiao H., Akiri G., et al. . (2009). Canonical Wnts function as potent regulators of osteogenesis by human mesenchymal stem cells. J. Cell Biol. 185, 67–75. 10.1083/jcb.200810137 PubMed DOI PMC

Logan C. Y., Nusse R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781–810. 10.1146/annurev.cellbio.20.010403.113126 PubMed DOI

Mikels A. J., Nusse R. (2006). Purified Wnt5a protein activates or inhibits β-catenin-TCF signaling depending on receptor context. PLoS Biol. 4:e115. 10.1371/journal.pbio.0040115 PubMed DOI PMC

Millar S. E., Koyama E., Reddy S. T., Andl T., Gaddapara T., Piddington R., et al. . (2003). Over- and ectopic expression of Wnt3 causes progressive loss of ameloblasts in postnatal mouse incisor teeth. Connect. Tissue Res. 44(Suppl. 1), 124–129. 10.1080/03008200390152205 PubMed DOI

Mitsiadis T. A., Luder H. U. (2011). Genetic basis for tooth malformations: from mice to men and back again. Clin. Genet. 80, 319–329. 10.1111/j.1399-0004.2011.01762.x PubMed DOI

Moon R. T., Campbell R. M., Christian J. L., McGrew L. L., Shih J., Fraser S. (1993). Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119, 97–111. PubMed

Naz G., Pasternack S. M., Perrin C., Mattheisen M., Refke M., Khan S., et al. . (2012). FZD6 encoding the Wnt receptor frizzled 6 is mutated in autosomal-recessive nail dysplasia. Br. J. Dermatol. 166, 1088–1094. 10.1111/j.1365-2133.2011.10800.x PubMed DOI

Nemoto E., Sakisaka Y., Tsuchiya M., Tamura M., Nakamura T., Kanaya S., et al. . (2016). Wnt3a signaling induces murine dental follicle cells to differentiate into cementoblastic/osteoblastic cells via an osterix-dependent pathway. J. Periodont. Res. 51, 164–174. 10.1111/jre.12294 PubMed DOI

Nishikawa S., Kitamura H. (1985). Three-dimensional network of microtubules in secretory ameloblasts of rat incisors. Arch. Oral Biol. 30, 1–11. PubMed

Nishikawa S., Kitamura H. (1986). Localization of actin during differentiation of the ameloblast, its related epithelial cells and odontoblasts in the rat incisor using NBD-phallacidin. Differentiation 30, 237–243. PubMed

Oishi I., Suzuki H., Onishi N., Takada R., Kani S., Ohkawara B., et al. . (2003). The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 8, 645–654. 10.1046/j.1365-2443.2003.00662.x PubMed DOI

Peng L., Ren L. B., Dong G., Wang C. L., Xu P., Ye L., et al. . (2010). Wnt5a promotes differentiation of human dental papilla cells. Int. Endod. J. 43, 404–412. 10.1111/j.1365-2591.2010.01693.x PubMed DOI

Sakisaka Y., Tsuchiya M., Nakamura T., Tamura M., Shimauchi H., Nemoto E. (2015). Wnt5a attenuates Wnt3a-induced alkaline phosphatase expression in dental follicle cells. Exp. Cell Res. 336, 85–93. 10.1016/j.yexcr.2015.06.013 PubMed DOI

Sarkar L., Cobourne M., Naylor S., Smalley M., Dale T., Sharpe P. T. (2000). Wnt/Shh interactions regulate ectodermal boundary formation during mammalian tooth development. Proc. Natl. Acad. Sci. U.S.A. 97, 4520–4524. 10.1073/pnas.97.9.4520 PubMed DOI PMC

Sarkar L., Sharpe P. T. (1999). Expression of Wnt signalling pathway genes during tooth development. Mech. Dev. 85, 197–200. 10.1016/S0925-4773(99)00095-7 PubMed DOI

Schulte G., Bryja V. (2007). The Frizzled family of unconventional G-protein-coupled receptors. Trends Pharmacol Sci. 28, 518–525. 10.1016/j.tips.2007.09.001 PubMed DOI

Seifert J. R., Mlodzik M. (2007). Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8, 126–138. 10.1038/nrg2042 PubMed DOI

Simons M., Mlodzik M. (2008). Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42, 517–540. 10.1146/annurev.genet.42.110807.091432 PubMed DOI PMC

Thesleff I. (2003). Epithelial-mesenchymal signalling regulating tooth morphogenesis. J. Cell Sci. 116, 1647–1648. 10.1242/jcs.00410 PubMed DOI

Thesleff I., Vaahtokari A., Kettunen P., Aberg T. (1995). Epithelial-mesenchymal signaling during tooth development. Connect. Tissue Res. 32, 9–15. 10.3109/03008209509013700 PubMed DOI

Topol L., Jiang X., Choi H., Garrett-Beal L., Carolan P. J., Yang Y. (2003). Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent β-catenin degradation. J. Cell Biol. 162, 899–908. 10.1083/jcb.200303158 PubMed DOI PMC

Vinson C. R., Conover S., Adler P. N. (1989). A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338, 263–264. 10.1038/338263a0 PubMed DOI

Wang B., Li H., Liu Y., Lin X., Lin Y., Wang Y., et al. . (2014). Expression patterns of WNT/β-CATENIN signaling molecules during human tooth development. J. Mol. Histol. 45, 487–496. 10.1007/s10735-014-9572-5 PubMed DOI

Wang Y., Badea T., Nathans J. (2006). Order from disorder: self-organization in mammalian hair patterning. Proc. Natl. Acad. Sci. U.S.A. 103, 19800–19805. 10.1073/pnas.0609712104 PubMed DOI PMC

Wang Y., Chang H., Nathans J. (2010). When whorls collide: the development of hair patterns in frizzled 6 mutant mice. Development 137, 4091–4099. 10.1242/dev.057455 PubMed DOI PMC

Wang Y., Chang H., Rattner A., Nathans J. (2016). Frizzled receptors in development and disease. Curr. Top. Dev. Biol. 117, 113–139. 10.1016/bs.ctdb.2015.11.028 PubMed DOI PMC

Wang Y., Guo N., Nathans J. (2006). The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci. 26, 2147–2156. 10.1523/JNEUROSCI.4698-05.2005 PubMed DOI PMC

Wu P., Wu X., Jiang T. X., Elsey R. M., Temple B. L., Divers S. J., et al. . (2013). Specialized stem cell niche enables repetitive renewal of alligator teeth. Proc. Natl. Acad. Sci. U.S.A. 110, E2009–E2018. 10.1073/pnas.1213202110 PubMed DOI PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

The role of prickle proteins in vertebrate development and pathology

. 2024 May ; 479 (5) : 1199-1221. [epub] 20230626

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...