The non-canonical BMP and Wnt/β-catenin signaling pathways orchestrate early tooth development

Development (Cambridge)

Volumn 142, Issue 1, 2015, Pages 128-139

  Yuan, Guohua ^a,b   Yang, Guobin ^a,b   Zheng, Yuqian ^b,c   Zhu, Xiaojing ^d   Chen, Zhi ^a   Zhang, Zunyi ^d   Chen, Yiping ^b  

^a Wuhan University   (China)

^b Tulane University   (United States)

^c FUJIAN MEDICAL UNIVERSITY   (China)

^d HANGZHOU NORMAL UNIVERSITY   (China)

Author keywords

BMP; Development; Mouse; Noggin; Tooth; Wnt

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; NOGGIN; WNT PROTEIN; CARRIER PROTEIN; CRE RECOMBINASE; HOMEODOMAIN PROTEIN; INTEGRASE; MSX1 PROTEIN, MOUSE; NOGGIN PROTEIN; PROTEIN BINDING; PROTEIN KINASE INHIBITOR; SMAD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR PITX2; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; EMBRYO; HEK293 CELL LINE; HISTOLOGY; HUMAN; HUMAN CELL; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; ORGAN CULTURE; ORGANOGENESIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOOTH DEVELOPMENT; TRANSGENIC MOUSE; WESTERN BLOTTING; WNT SIGNALING PATHWAY; ANIMAL; BIOLOGICAL MODEL; CELL LINEAGE; CYTOLOGY; DOWN REGULATION; DRUG EFFECTS; EMBRYOLOGY; EPITHELIUM; MESODERM; METABOLISM; TOOTH; TOOTH GERM;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CARRIER PROTEINS; CELL LINEAGE; CELL PROLIFERATION; DOWN-REGULATION; EPITHELIUM; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; INTEGRASES; MESODERM; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MSX1 TRANSCRIPTION FACTOR; ODONTOGENESIS; PROTEIN BINDING; PROTEIN KINASE INHIBITORS; SMAD PROTEINS; TOOTH; TOOTH GERM; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; WNT SIGNALING PATHWAY;

EID: 84918549050     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.117887     Document Type: Article

References (69)

1. Andl, T., Ahn, K., Kairo, A., Chu, E. Y., Wine-Lee, L., Reddy, S. T., Croft, N. J., Cebra-Thomas, J. A., Metzger, D., Chambon, P. et al. (2004). Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131, 2257-2268.
2. Bai, X. M., Van der Schueren, B., Cassiman, J. J., Van den Berghe, H. and David, G. (1994). Differential expression of multiple cell-surface heparan sulfate proteoglycans during embryonic tooth development. J. Histochem. Cytochem. 42, 1043-1054.
3. Bayramov, A. V., Eroshkin, F. M., Martynova, N. Y., Ermakova, G. V., Solovieva, E. A. and Zaraisky, A. G. (2011). Novel functions of Nog proteins: inhibition of Activin/Nodal and Wnt signaling. Development 138, 5345-5356.
4. Bell, E., Muñoz-Sanjuán, I., Altmann, C. R., Vonica, A. and Brivanlou, A. H. (2003). Cell fate specification and competence by Coco, a maternal BMP, TGFbeta and Wnt inhibitor. Development 130, 1381-1389.
5. Briata, P., Ilengo, C., Corte, G., Moroni, C., Rosenfeld, M. G., Chen, C.-Y. and Gherzi, R. (2003). The Wnt/β-catenin→Pitx2 pathway controls the turnover of Pitx2 and other unstable mRNAs. Mol. Cell 12, 1201-1211.
6. Chai, Y., Mah, A., Crohin, C., Groff, S., Bringas, P., Jr, Le, T., Santo, V. and Slavkin, H. C. (1994). Specific transforming growth factor-beta subtypes regulate embryonic mouse Meckel’s cartilage and tooth development. Dev. Biol. 162, 85-103.
7. Chen, Y., Bei, M., Woo, I., Satokata, I. and Maas, R. (1996). Msx1 controls inductive signaling in mammalian tooth morphogenesis. Development 122, 3035-3044.
8. Chen, Y., Whetstone, H. C., Youn, A., Nadesan, P., Chow, E. C. Y., Lin, A. C. and Alman, B. A. (2007). Beta-catenin signaling pathway is crucial for bone morphogenetic protein 2 to induce new bone formation. J. Biol. Chem. 282, 526-533.
9. Chen, J., Lan, Y., Baek, J.-A., Gao, Y. and Jiang, R. (2009). Wnt/beta-catenin signaling plays an essential role in activation of odontogenic mesenchyme during early tooth development. Dev. Biol. 334, 174-185.
10. Chesnutt, C., Burrus, L. W., Brown, A. M. C. and Niswander, L. (2004). Coordinate regulation of neural tube patterning and proliferation by TGFbeta and WNT activity. Dev. Biol. 274, 334-347.
11. Cho, K.-W., Cho, S.-W., Lee, J.-M., Lee, M.-J., Gang, H.-S. and Jung, H.-S. (2008). Expression of phosphorylated forms of ERK, MEK, PTEN and PI3K in mouse oral development. Gene Expr. Patterns 8, 284-290.
12. Ferguson, C. A., Tucker, A. S., Christensen, L., Lau, A. L., Matzuk, M. M. and Sharpe, P. T. (1998). Activin is an essential early mesenchymal signal in tooth development that is required for patterning of the murine dentition. Genes Dev. 12, 2636-2649.
13. Goumans, M.-J., Valdimarsdottir, G., Itoh, S., Rosendahl, A., Sideras, P. and ten Dijke, P. (2002). Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 21, 1743-1753.
14. Goumans, M.-J., Valdimarsdottir, G., Itoh, S., Lebrin, F., Larsson, J., Mummery, C., Karlsson, S. and ten Dijke, P. (2003). Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFbeta/ALK5 signaling. Mol. Cell 12, 817-828.
15. Groppe, J., Greenwald, J., Wiater, E., Rodriguez-Leon, J., Economides, A. N., Kwiatkowski, W., Affolter, M., Vale, W. W., Izpisua Belmonte, J. C. and Choe, S. (2002). Structural basis of BMP signalling inhibition by the cystine knot protein Nog. Nature 420, 636-642.
16. He, F., Xiong, W., Wang, Y., Matsui, M., Yu, X., Chai, Y., Klingensmith, J. and Chen, Y. (2010). Modulation of BMP signaling by Nog is required for the maintenance of palatal epithelial integrity during palatogenesis. Dev. Biol. 347, 109-121.
17. Hu, B., Nadiri, A., Kuchler-Bopp, S., Perrin-Schmitt, F., Peters, H. and Lesot, H. (2006). Tissue engineering of tooth crown, root, and periodontium. Tissue Eng. 12, 2069-2075.
18. Hu, X., Wang, Y., He, F., Li, L., Zheng, Y., Zhang, Y. and Chen, Y. P. (2012). Nog is required for early development of murine upper incisors. J. Dent. Res. 91, 394-400.
19. Ille, F., Atanasoski, S., Falk, S., Ittner, L. M., Mürki, D., Büchmann-Møller, S., Wurdak, H., Suter, U., Taketo, M. M. and Sommer, L. (2007). Wnt/BMP signal integration regulates the balance between proliferation and differentiation of neuroepithelial cells in the dorsal spinal cord. Dev. Biol. 304, 394-408.
20. Ito, Y., Yeo, J. Y., Chytil, A., Han, J., Bringas, P., Jr, Nakajima, A., Shuler, C. F., Moses, H. L. and Chai, Y. (2003). Conditional inactivation of Tgfbr2 in cranial neural crest causes cleft palate and calvaria defects. Development 21, 5280-5296.
21. Jürvinen, E., Salazar-Ciudad, I., Birchmeier, W., Taketo, M. M., Jernvall, J. and Thesleff, I. (2006). Continuous tooth generation in mouse is induced by activated epithelial Wnt/beta-catenin signaling. Proc. Natl. Acad. Sci. USA 103, 18627-18632.
22. Jia, S., Zhou, J., Gao, Y., Baek, J.-A., Martin, J. F., Lan, Y. and Jiang, R. (2013). Roles of Bmp4 during tooth morphogenesis and sequential tooth formation. Development 140, 423-432.
23. Ke, J., Harikumar, K. G., Erice, C., Chen, C., Gu, X., Wang, L., Parker, N., Cheng, Z., Xu, W., Williams, B. O. et al. (2013). Structure and function of Norrin in assembly and activation of a frizzled 4-Lrp5/6 complex. Genes Dev. 27, 2305-2319.
24. Kioussi, C., Briata, P., Baek, S. H., Rose, D.W., Hamblet, N. S., Herman, T., Ohgi, K. A., Lin, C., Gleiberman, A., Wang, J. et al. (2002). Identification of a Wnt/Dvl/ beta-catenin→Pitx2 pathway mediating cell-type-specific proliferation during development. Cell 111, 673-685.
25. Korchynskyi, O. and ten Dijke, P. (2002). Identification and functional characterization of distinct critically important bone morphogenetic proteinspecific response elements in the Id1 promoter. J. Biol. Chem. 277, 4883-4891.
26. Lee, M. Y., Lim, H.W., Lee, S. H. and Han, H. J. (2009). Smad, PI3K/Akt, and Wntdependent signaling pathways are involved in BMP-4-induced ESC self-renewal. Stem Cells 27, 1858-1868.
27. Li, L., Lin, M., Wang, Y., Cserjesi, P., Chen, Z. and Chen, Y. (2011). BmprIa is required in mesenchymal tissue and has limited redundant function with BmprIb in tooth and palate development. Dev. Biol. 349, 451-461.
28. Lin, C. R., Kioussi, C., O’Connel, S., Briata, P., Szeto, D., Liu, F., Izpisúa-Belmonte, J. C. and Rosenfeld, M. G. (1999). Pitx2 regulates lung asymmetry, cardiac positioning and pituitary and tooth morphogenesis. Nature 401, 279-282.
29. Lintern, K. B., Guidato, S., Rowe, A., Saldanha, J. W. and Itasaki, N. (2009). Characterization of wise protein and its molecular mechanism to interact with both Wnt and BMP signals. J. Biol. Chem. 284, 23159-23168.
30. Liu, F. and Millar, S. E. (2010). Wnt/β-catenin signaling in oral tissue development and disease. J. Dent. Res. 89, 318-330.
31. Liu, W., Selever, J., Lu, M.-F. and Martin, J. F. (2003). Genetic dissection of Pitx2 in craniofacial development uncovers new functions in branchial arch morphogenesis, late aspects of tooth morphogenesis and cell migration. Development 130, 6375-6385.
32. Liu, W., Sun, X., Braut, A., Mishina, Y., Behringer, R. R., Mina, M. and Martin, J. F. (2005). Distinct functions for Bmp signaling in lip and palate fusion in mice. Development 132, 1453-1461.
33. Liu, Z., Tang, Y., Qiu, T., Cao, X. and Clemens, T. L. (2006). A dishevelled-1/ Smad1 interaction couples WNT and bone morphogenetic protein signaling pathways in uncommitted bone marrow stromal cells. J. Biol. Chem. 281, 17156-17163.
34. Liu, F., Chu, E.Y., Watt, B., Zhang, Y., Gallant, N.M., Andl, T., Yang, S.H., Lu, M.-M., Piccolo, S., Schmidt-Ullrich, R. et al. (2008). Wnt/β-catenin signaling directs multiple stages of tooth morphogenesis. Dev. Biol. 313, 210-224.
35. Liu, C., Gu, S., Sun, C., Ye, W., Song, Z., Zhang, Y. and Chen, Y. (2013). FGF signaling sustains the odontogenic fate of dental mesenchyme by suppressing β-catenin signaling. Development 140, 4375-4385.
36. Lohi, M., Tucker, A. S. and Sharpe, P. T. (2010). Expression of Axin2 indicates a role for canonical Wnt signaling in development of the crown and root during preand postnatal tooth development. Dev. Dyn. 239, 160-167.
37. Lustig, B., Jerchow, B., Sachs, M., Weiler, S., Pietsch, T., Karsten, U., van de Wetering, M., Clevers, H., Schlag, P. M., Birchmeier, W. et al. (2002). Negative feedback loop of Wnt signaling through upregulation of conductin/Axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22, 1184-1193.
38. Maretto, S., Cordenonsi, M., Dupont, S., Braghetta, P., Broccoli, V., Hassan, A. B., Volpin, D., Bressan, G. M. and Piccolo, S. (2003). Mapping Wnt/betacatenin signaling during mouse development and in colorectal tumors. Proc. Natl. Acad. Sci. USA 100, 3299-3304.
39. McMahon, J. A., Takada, S., Zimmerman, L. B., Fan, C.-M., Harland, R. M. and McMahon, A. P. (1998). Nog-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12, 1438-1452.
40. Monteiro, R. M., de Sousa Lopes, S. M. C., Bialecka, M., de Boer, S., Zwijsen, A. and Mummery, C. L. (2008). Real time monitoring of BMP Smads transcriptional activity during mouse development. Genesis 46, 335-346.
41. Moriguchi, M., Yamada, M., Miake, Y. and Yanagisawa, T. (2011). Immunolocalization of TAK1, TAB1, and p38 in the developing rat molar. Anat. Sci. Int. 86, 69-77.
42. Moustakas, A. and Heldin, C.-H. (2009). The regulation of TGFbeta signal transduction. Development 136, 3699-3714.
43. Mucchielli, M.-L., Mitsiadis, T. A., Raffo, S., Brunet, J.-F., Proust, J.-P. and Goridis, C. (1997). Mouse Otlx2/RIEG expression in the odontogenic epithelium precedes tooth initiation and requires mesenchyme-derived signals for its maintenance. Dev. Biol. 189, 275-284.
44. Nathan, E. and Tzahor, E. (2009). sFRPs: a declaration of (Wnt) independence. Nat. Cell Biol. 11, 13.
45. Pacheco, M. S., Reis, A. H., Aguiar, D. P., Lyons, K. M. and Abreu, J. G. (2008). Dynamic analysis of the expression of the TGFbeta/SMAD2 pathway and CCN2/ CTGF during early steps of tooth development. Cells Tissues Organs 187, 199-210.
46. Paine-Saunders, S, Viviano, B. L., Economides, A. N. and Saunders, S. (2002). Heparan sulfate proteoglycans retain Nog at the cell surface: a potential mechanism for shaping bone morphogenetic protein gradients. J. Biol. Chem. 277, 2089-2096.
47. Piccolo, S., Agius, E., Leyns, L., Bhattacharyya, S., Grunz, H., Bouwmeester, T. and De Robertis, E. M. (1999). The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710.
48. Porntaveetus, T., Otsuka-Tanaka, Y., Basson, M. A., Moon, A. M., Sharpe, P. T. and Ohazama, A. (2011). Expression of fibroblast growth factors (Fgfs) in murine tooth development. J. Anat. 218, 534-543.
49. Sarkar, L. and Sharpe, P. T. (1999). Expression of Wnt signalling pathway genes during tooth development. Mech. Dev. 85, 197-200.
50. Shtutman, M., Zhurinsky, J., Simcha, I., Albanese, C., D’Amico, M., Pestell, R. and Ben-Ze’ev, A. (1999). The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. USA 96, 5522-5527.
51. Sieber, C., Kopf, J., Hiepen, C. and Knaus, P. (2009). Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 20, 343-355.
52. Söderberg, O., Leuchowius, K.-J., Gullberg, M., Jarvius, M., Weibrecht, I., Larsson, L.-G. and Landegren, U. (2008). Characterizing proteins and their interactions in cells and tissues using the in situ proximity ligation assay. Methods 45, 227-232.
53. Soshnikova, N., Zechner, D., Huelsken, J., Mishina, Y., Behringer, R. R., Taketo, M. M., Crenshaw, E. B.III and Birchmeier, W. (2003). Genetic interaction between Wnt/beta-catenin and BMP receptor signaling during formation of the AER and the dorsal-ventral axis in the limb. Genes Dev. 17, 1963-1968. St.
54. Amand, T. R., Zhang, Y., Semina, E. V., Zhao, X., Hu, Y., Nguyen, L., Murray, J. C. and Chen, Y. (2000). Antagonistic signals between BMP4 and FGF8 define the expression of Pitx1 and Pitx2 in mouse tooth-forming anlage. Dev. Biol. 217, 323-332.
55. Tetsu, O. and McCormick, F. (1999). Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398, 422-426.
56. Tummers, M. and Thesleff, I. (2009). The importance of signal pathway modulation in all aspects of tooth development. J. Exp. Zool. B Mol. Dev. Evol. 312B, 309-319.
57. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I. (1993). Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
58. Wang, X.-P., O’Connell, D. J., Lund, J. J., Saadi, I., Kuraguchi, M., Turbe-Doan, A., Cavallesco, R., Kim, H., Park, P. J., Harada, H. et al. (2009). Apc inhibition of Wnt signaling regulates supernumerary tooth formation during embryogenesis and throughout adulthood. Development 136, 1939-1949.
59. Wang, Y., Li, L., Zheng, Y., Yuan, G., Yang, G., He, F. and Chen, Y. (2012). BMP activity is required for tooth development from the lamina to bud stage. J. Dent. Res. 91, 690-695.
60. Wang, Y., Zheng, Y., Chen, D. and Chen, Y. (2013). Enhanced BMP signaling prevents degeneration and leads to endochondral ossification of Meckel’s cartilage in mice. Dev. Biol. 381, 301-311.
61. Xiong, W., He, F., Morikawa, Y., Yu, X., Zhang, Z., Lan, Y., Jiang, R., Cserjesi, P. and Chen, Y. (2009). Hand2 is required in the epithelium for palatogenesis in mice. Dev. Biol. 330, 131-141.
62. Xu, X., Jeong, L., Han, J., Ito, Y., Bringas, P., Jr and Chai, Y. (2003). Developmental expression of Smad1-7 suggests critical function of TGF-beta/ BMP signaling in regulating epithelial-mesenchymal interaction during tooth morphogenesis. Int. J. Dev. Biol. 47, 31-39.
63. Xu, X., Han, J., Ito, Y., Bringas, P., Jr, Deng, C. and Chai, Y. (2008). Ectodermal Smad4 and p38 MAPK are functionally redundant in mediating TGF-β/BMP signaling during tooth and palate development. Dev. Cell 15, 322-329.
64. Yang, G., Yuan, G., Ye, W., Cho, K. W. Y. and Chen, Y. (2014). An atypical canonical BMP signaling pathway regulates msh homeobox 1 (Msx1) expression during odontogenesis. J. Biol. Chem. Published October 1, 2014 (Epub ahead of print).
65. Yi, S. E., Daluiski, A., Pederson, R., Rosen, V. and Lyons, K. M. (2000). The type I BMP receptor BMPRIB is required for chondrogenesis in the mouse limb. Development 127, 621-630.
66. Yu, P. B., Hong, C. C., Sachidanandan, C., Babitt, J. L., Deng, D. Y., Hoyng, S. A., Lin, H. Y., Bloch, K. D. and Peterson, R. T. (2008). Dorsomorphin inhibits BMP signals required for embryogenesis and iron metabolism. Nat. Chem. Biol. 4, 33-41.
67. Yuan, G. H., Zhang, L., Zhang, Y. D., Fan, M. W., Bian, Z. and Chen, Z. (2008). Mesenchyme is responsible for tooth suppression in the mouse lower diastema. J. Dent. Res. 87, 386-390.
68. Zhang, Y., Zhang, Z., Zhao, X., Yu, X., Hu, Y., Geronimo, B., Fromm, S. H. and Chen, Y. P. (2000). A new function of BMP4: dual role of BMP4 in regulation of Sonic hedgehog expression in the mouse tooth germ. Development 127, 1431-1443.
69. Zhu, X., Zhao, P., Liu, Y., Zhang, X., Fu, J., Ivy Yu, H.-M., Qiu, M., Chen, Y., Hsu, W. and Zhang, Z. (2013). Intra-epithelial requirement of canonical Wnt signaling for tooth development. J. Biol. Chem. 288, 12080-12089.