Role of canonical Wnt signaling/β-catenin via Dermo1 in cranial dermal cell development

Development

Volumn 137, Issue 23, 2010, Pages 3973-3984

  Tran, Thu H ^a   Jarrell, Andrew ^a   Zentner, Gabriel E ^a   Welsh, Adrienne ^a   Brownell, Isaac ^b   Scacheri, Peter C ^a   Atit, Radhika ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Cartilage; Cell fate; Cranial bone; Cranial dermis; Craniofacial; Mouse

Indexed keywords

BETA CATENIN; PROTEIN; PROTEIN DERMO1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CANONICAL ANALYSIS; CARTILAGE; CELL LINEAGE; CONTROLLED STUDY; INTRACELLULAR SIGNALING; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; SKIN CELL; STEM CELL; TRUNK;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX LEUCINE ZIPPER TRANSCRIPTION FACTORS; BETA CATENIN; BIOLOGICAL MARKERS; BODY PATTERNING; CARTILAGE; CELL DIFFERENTIATION; CELL LINEAGE; DERMIS; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; HOMEODOMAIN PROTEINS; MESODERM; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SKULL; SOX9 TRANSCRIPTION FACTOR; STEM CELLS; TWIST TRANSCRIPTION FACTOR; WNT PROTEINS;

EID: 78649859867     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.056473     Document Type: Article

References (75)

1. Abzhanov, A., Rodda, S. J., McMahon, A. P. and Tabin, C. J. (2007). Regulation of skeletogenic differentiation in cranial dermal bone. Development 134, 3133-3144.
2. Akiyama, H., Lyons, J. P., Mori-Akiyama, Y., Yang, X., Zhang, R., Zhang, Z., Deng, J. M., Taketo, M. M., Nakamura, T., Behringer, R. R. et al. (2004). Interactions between Sox9 and beta-catenin control chondrocyte differentiation. Genes Dev. 18, 1072-1087.
3. Atit, R., Sgaier, S. K., Mohamed, O. A., Taketo, M. M., Dufort, D., Joyner, A. L., Niswander, L. and Conlon, R. A. (2006). Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. Dev. Biol. 296, 164-176.
4. Baker, C. V., Bronner-Fraser, M., Le Douarin, N. M. and Teillet, M. A. (1997). Early- and late-migrating cranial neural crest cell populations have equivalent developmental potential in vivo. Development 124, 3077-3087.
5. Bayle, J., Fitch, J., Jacobsen, K., Kumar, R., Lafyatis, R. and Lemaire, R. (2008). Increased expression of Wnt2 and SFRP4 in Tsk mouse skin: role of Wnt signaling in altered dermal fibrillin deposition and systemic sclerosis. J. Invest. Dermatol. 128, 871-881.
6. Benko, S., Fantes, J. A., Amiel, J., Kleinjan, D. J., Thomas, S., Ramsay, J., Jamshidi, N., Essafi, A., Heaney, S., Gordon, C. T. et al. (2009). Highly conserved non-coding elements on either side of SOX9 associated with Pierre Robin sequence. Nat. Genet. 41, 359-364.
7. Bowley, E., O'Gorman, D. B. and Gan, B. S. (2007). β-Catenin signaling in fibroproliferative disease. J. Surg. Res. 138, 141-150.
8. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O. and Kemler, R. (2001). Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264. (Pubitemid 32409648)
9. Chai, Y., Ito, Y. and Han, J. (2003). TGF-beta signaling and its functional significance in regulating the fate of cranial neural crest cells. Crit. Rev. Oral Biol. Med. 14, 78-88.
10. 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.
11. Day, T. F., Guo, X., Garrett-Beal, L. and Yang, Y. (2005). Wnt/beta-catenin signaling in mesenchymal progenitors controls osteoblast and chondrocyte differentiation during vertebrate skeletogenesis. Dev. Cell. 8, 739-750.
12. Deckelbaum, R. A., Majithia, A., Booker, T., Henderson, J. E. and Loomis, C. A. (2006). The homeoprotein engrailed 1 has pleiotropic functions in calvarial intramembranous bone formation and remodeling. Development 133, 63-74.
13. Dorsky, R. I., Moon, R. T. and Raible, D. W. (1998). Control of neural crest cell fate by the Wnt signalling pathway. Nature 396, 370-373.
14. Eames, B. F. and Schneider, R. A. (2005). Quail-duck chimeras reveal spatiotemporal plasticity in molecular and histogenic programs of cranial feather development. Development 132, 1499-1509.
15. Fernandes, K. J., McKenzie, I. A., Mill, P., Smith, K. M., Akhavan, M., Barnabe-Heider, F., Biernaskie, J., Junek, A., Kobayashi, N. R., Toma, J. G. et al. (2004). A dermal niche for multipotent adult skin-derived precursor cells. Nat. Cell Biol. 6, 1082-1093.
16. Gavrieli, Y., Sherman, Y. and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
17. Giese, K., Amsterdam, A. and Grosschedl, R. (1991). DNA-binding properties of the HMG domain of the lymphoid-specific transcriptional regulator LEF-1. Genes Dev. 5, 2567-2578. (Pubitemid 21905940)
18. Goltz, R. W. (1992). Focal dermal hypoplasia syndrome. An update. Arch. Dermatol. 128, 1108-1111.
19. Gong, X. Q. and Li, L. (2002). Dermo-1, a multifunctional basic helix-loop-helix protein, represses MyoD transactivation via the HLH domain, MEF2 interaction, and chromatin deacetylation. J. Biol. Chem. 277, 12310-12317.
20. Grzeschik, K. H., Bornholdt, D., Oeffner, F., Konig, A., del Carmen Boente, M., Enders, H., Fritz, B., Hertl, M., Grasshoff, U., Hofling, K. et al. (2007). Deficiency of PORCN, a regulator of Wnt signaling, is associated with focal dermal hypoplasia. Nat. Genet. 39, 833-835.
21. Haegel, H., Larue, L., Ohsugi, M., Fedorov, L., Herrenknecht, K. and Kemler, R. (1995). Lack of beta-catenin affects mouse development at gastrulation. Development 121, 3529-3537.
22. Hallikas, O., Palin, K., Sinjushina, N., Rautiainen, R., Partanen, J., Ukkonen, E. and Taipale, J. (2006). Genome-wide prediction of mammalian enhancers based on analysis of transcription-factor binding affinity. Cell 124, 47-59.
23. Hanks, M., Wurst, W., Anson-Cartwright, L., Auerbach, A. B. and Joyner, A. L. (1995). Rescue of the En-1 mutant phenotype by replacement of En-1 with En-2. Science 269, 679-682.
24. Harada, N., Tamai, Y., Ishikawa, T., Sauer, B., Takaku, K., Oshima, M. and Taketo, M. M. (1999). Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942.
25. Hartmann, C. (2007). Skeletal development-Wnts are in control. Mol. Cells 24, 177-184.
26. Heintzman, N. D., Stuart, R. K., Hon, G., Fu, Y., Ching, C. W., Hawkins, R. D., Barrera, L. O., Van Calcar, S., Qu, C., Ching, K. A. et al. (2007). Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat. Genet. 39, 311-318.
27. Heintzman, N. D., Hon, G. C., Hawkins, R. D., Kheradpour, P., Stark, A., Harp, L. F., Ye, Z., Lee, L. K., Stuart, R. K., Ching, C. W. et al. (2009). Histone modifications at human enhancers reflect global cell-type-specific gene expression. Nature 459, 108-112.
28. Hill, T. P., Spater, D., Taketo, M. M., Birchmeier, W. and Hartmann, C. (2005). Canonical Wnt/beta-catenin signaling prevents osteoblasts from differentiating into chondrocytes. Dev. Cell 8, 727-738.
29. Iwatsuki, K., Liu, H. X., Gronder, A., Singer, M. A., Lane, T. F., Grosschedl, R., Mistretta, C. M. and Margolskee, R. F. (2007). Wnt signaling interacts with Shh to regulate taste papilla development.. Proc. Natl. Acad. Sci. USA 104, 2253-2258.
30. Jiang, X., Iseki, S., Maxson, R. E., Sucov, H. M. and Morriss-Kay, G. M. (2002). Tissue origins and interactions in the mammalian skull vault. Dev. Biol. 241, 106-116.
31. Joyner, A. L. and Zervas, M. (2006). Genetic inducible fate mapping in mouse: establishing genetic lineages and defining genetic neuroanatomy in the nervous system. Dev. Dyn. 235, 2376-2385.
32. Kanzler, B., Foreman, R. K., Labosky, P. A. and Mallo, M. (2000). BMP signaling is essential for development of skeletogenic and neurogenic cranial neural crest. Development 127, 1095-1104.
33. Kim, T. K., Hemberg, M., Gray, J. M., Costa, A. M., Bear, D. M., Wu, J., Harmin, D. A., Laptewicz, M., Barbara-Haley, K., Kuersten, S. et al. (2010). Widespread transcription at neuronal activity-regulated enhancers. Nature 465, 182-187.
34. Kimmel, R. A., Turnbull, D. H., Blanquet, V., Wurst, W., Loomis, C. A. and Joyner, A. L. (2000). Two lineage boundaries coordinate vertebrate apical ectodermal ridge formation. Genes Dev. 14, 1377-1389.
35. Lee, Y. S., Lee, H. H., Park, J., Yoo, E. J., Glackin, C. A., Choi, Y. I., Jeon, S. H., Seong, R. H., Park, S. D. and Kim, J. B. (2003). Twist2, a novel ADD1/SREBP1c interacting protein, represses the transcriptional activity of ADD1/SREBP1c. Nucleic Acids Res. 31, 7165-7174.
36. Lefebvre, V., Huang, W., Harley, V. R., Goodfellow, P. N. and de Crombrugghe, B. (1997). SOX9 is a potent activator of the chondrocyte-specific enhancer of the pro alpha1(II) collagen gene. Mol. Cell. Biol. 17, 2336-2346. (Pubitemid 27133320)
37. Lev, R. and Spicer, S. S. (1964). Specific staining of sulphate groups with alcian blue at low Ph. J. Histochem. Cytochem. 12, 309.
38. Li, L., Cserjesi, P. and Olson, E. N. (1995). Dermo-1: a novel twist-related bHLH protein expressed in the developing dermis. Dev. Biol. 172, 280-292.
39. Liu, F., Thirumangalathu, S., Gallant, N. M., Yang, S. H., Stoick-Cooper, C. L., Reddy, S. T., Andl, T., Taketo, M. M., Dlugosz, A. A., Moon, R. T. et al. (2007). Wnt-beta-catenin signaling initiates taste papilla development. Nat. Genet. 39, 106-112.
40. 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/beta-catenin signaling directs multiple stages of tooth morphogenesis. Dev. Biol. 313, 210-224.
41. Livak, K. J. and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408.
42. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
43. MacDonald, B. T., Tamai, K. and He, X. (2009). Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell 17, 9-26.
44. Mani, P., Jarrell, A., Myers, J. and Atit, R. (2009). Visualizing canonical Wnt signaling during mouse craniofacial development. Dev. Dyn. 239, 354-363.
45. Matise, M. P. and Joyner, A. L. (1997). Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17, 7805-7816.
46. McGee-Russell, S. M. (1958). Histochemical methods for calcium. J. Histochem. Cytochem. 6, 22-42.
47. Miller, J. R. (2002). The Wnts. Genome Biol. 3, REVIEWS3001.
48. Moon, R. T., Kohn, A. D., De Ferrari, G. V. and Kaykas, A. (2004). WNT and beta-catenin signalling: diseases and therapies. Nat. Rev. Genet. 5, 691-701.
49. Noden, D. M. and Trainor, P. A. (2005). Relations and interactions between cranial mesoderm and neural crest populations. J. Anat. 207, 575-601.
50. Ohtola, J., Myers, J., Akhtar-Zaidi, B., Zuzindlak, D., Sandesara, P., Yeh, K., Mackem, S. and Atit, R. (2008). beta-Catenin has sequential roles in the survival and specification of ventral dermis. Development 135, 2321-2329.
51. Palin, K., Taipale, J. and Ukkonen, E. (2006). Locating potential enhancer elements by comparative genomics using the EEL software. Nat. Protoc. 1, 368-374.
52. Raible, D. W. and Eisen, J. S. (1996). Regulative interactions in zebrafish neural crest. Development 122, 501-507.
53. Rodda, S. J. and McMahon, A. P. (2006). Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 133, 3231-3244.
54. Schnetz, M. P., Bartels, C. F., Shastri, K., Balasubramanian, D., Zentner, G. E., Balaji, R., Zhang, X., Song, L., Wang, Z., Laframboise, T. et al. (2009). Genomic distribution of CHD7 on chromatin tracks H3K4 methylation patterns. Genome Res. 19, 590-601.
55. Sengel, P. and Abbott, U. K. (1963). In vitro studies with the scaleless mutant. Interactions during feather and scale differentiation. J. Hered. 54, 255-262.
56. Seo, H. S. and Serra, R. (2009). Tgfbr2 is required for development of the skull vault. Dev. Biol. 334, 481-490.
57. Sgaier, S. K., Millet, S., Villanueva, M. P., Berenshteyn, F., Song, C. and Joyner, A. L. (2005). Morphogenetic and cellular movements that shape the mouse cerebellum; insights from genetic fate mapping. Neuron 45, 27-40.
58. Sgaier, S. K., Lao, Z., Villanueva, M. P., Berenshteyn, F., Stephen, D., Turnbull, R. K. and Joyner, A. L. (2007). Genetic subdivision of the tectum and cerebellum into functionally related regions based on differential sensitivity to engrailed proteins. Development 134, 2325-2335.
59. Shah, N. M., Marchionni, M. A., Isaacs, I., Stroobant, P. and Anderson, D. J. (1994). Glial growth factor restricts mammalian neural crest stem cells to a glial fate. Cell 77, 349-360.
60. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
61. Spater, D., Hill, T. P., O'Sullivan, R. J., Gruber, M., Conner, D. A. and Hartmann, C. (2006). Wnt9a signaling is required for joint integrity and regulation of Ihh during chondrogenesis. Development 133, 3039-3049.
62. ten Berge, D., Brugmann, S. A., Helms, J. A. and Nusse, R. (2008). Wnt and FGF signals interact to coordinate growth with cell fate specification during limb development. Development 135, 3247-3257.
63. Trainor, P. and Krumlauf, R. (2000). Plasticity in mouse neural crest cells reveals a new patterning role for cranial mesoderm. Nat. Cell Biol. 2, 96-102.
64. Tukel, T., Sosic, D., Al-Gazali, L. I., Erazo, M., Casasnovas, J., Franco, H. L., Richardson, J. A., Olson, E. N., Cadilla, C. L. and Desnick, R. J. (2010). Homozygous nonsense mutations in TWIST2 cause Setleis syndrome. Am. J. Hum. Genet. 87, 289-296.
65. van Beest, M., Dooijes, D., van De Wetering, M., Kjaerulff, S., Bonvin, A., Nielsen, O. and Clevers, H. (2000). Sequence-specific high mobility group box factors recognize 10-12-base pair minor groove motifs. J. Biol. Chem. 275, 27266-27273.
66. van de Wetering, M., Oosterwegel, M., Dooijes, D. and Clevers, H. (1991). Identification and cloning of TCF-1, a T lymphocyte-specific transcription factor containing a sequence-specific HMG box. EMBO J. 10, 123-132.
67. Wang, X., Reid Sutton, V., Omar Peraza-Llanes, J., Yu, Z., Rosetta, R., Kou, Y. C., Eble, T. N., Patel, A., Thaller, C., Fang, P. et al. (2007). Mutations in X-linked PORCN, a putative regulator of Wnt signaling, cause focal dermal hypoplasia. Nat. Genet. 39, 836-838.
68. 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.
69. Wodarz, A. and Nusse, R. (1998). Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14, 59-88.
70. Won, K. J., Chepelev, I., Ren, B. and Wang, W. (2008). Prediction of regulatory elements in mammalian genomes using chromatin signatures. BMC Bioinformatics 9, 547.
71. Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y. and Iseki, S. (2008). Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125, 797-808.
72. Yu, K., Xu, J., Liu, Z., Sosic, D., Shao, J., Olson, E. N., Towler, D. A. and Ornitz, D. M. (2003). Conditional inactivation of FGF receptor 2 reveals an essential role for FGF signaling in the regulation of osteoblast function and bone growth. Development 130, 3063-3074.
73. Zhang, Y., Andl, T., Yang, S. H., Teta, M., Liu, F., Seykora, J. T., Tobias, J. W., Piccolo, S., Schmidt-Ullrich, R., Nagy, A. et al. (2008). Activation of beta-catenin signaling programs embryonic epidermis to hair follicle fate. Development 135, 2161-2172.
74. Zhang, Y., Tomann, P., Andl, T., Gallant, N. M., Huelsken, J., Jerchow, B., Birchmeier, W., Paus, R., Piccolo, S., Mikkola, M. L. et al. (2009). Reciprocal requirements for EDA/EDAR/NF-kappaB and Wnt/beta-catenin signaling pathways in hair follicle induction. Dev. Cell 17, 49-61.
75. Zhao, Q., Eberspaecher, H., Lefebvre, V. and De Crombrugghe, B. (1997). Parallel expression of Sox9 and Col2a1 in cells undergoing chondrogenesis. Dev. Dyn. 209, 377-386.