Dermal β-catenin activity in response to epidermal Wnt ligands is required for fibroblast proliferation and hair follicle initiation

Development

Volumn 139, Issue 8, 2012, Pages 1522-1533

  Chen, Demeng ^a   Jarrell, Andrew ^a   Guo, Canting ^a   Lang, Richard ^b   Atit, Radhika ^a  

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

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

catenin; Dermis; Fibroblasts; Hair follicle; Mouse embryo; Wnt

Indexed keywords

BETA CATENIN; WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; DERMIS; EMBRYO; EPIDERMIS; FIBROBLAST; HAIR FOLLICLE; HAIR GROWTH; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN; UPREGULATION;

ANIMALS; BETA CATENIN; CELL PROLIFERATION; CELL SURVIVAL; FIBROBLASTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR FOLLICLE; LIGANDS; MICE; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SKIN; STEM CELLS; TIME FACTORS; WNT PROTEINS;

MUS;

EID: 84863388324     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.076463     Document Type: Article

References (63)

1. Andl, T., Reddy, S. T., Gaddapara, T. and Millar, S. E. (2002). WNT signals are required for the initiation of hair follicle development. Dev. Cell 2, 643-653.
2. Ansel, J. C., Kaynard, A. H., Armstrong, C. A., Olerud, J., Bunnett, N. and Payan, D. (1996). Skin-nervous system interactions. J. Invest. Dermatol. 106, 198-204.
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. Banziger, C., Soldini, D., Schutt, C., Zipperlen, P., Hausmann, G. and Basler, K. (2006). Wntless, a conserved membrane protein dedicated to the secretion of Wnt proteins from signaling cells. Cell 125, 509-522.
5. Bartscherer, K., Pelte, N., Ingelfinger, D. and Boutros, M. (2006). Secretion of Wnt ligands requires Evi, a conserved transmembrane protein. Cell 125, 523-533.
6. 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.
7. Bazzi, H., Fantauzzo, K. A., Richardson, G. D., Jahoda, C. A. and Christiano, A. M. (2007). The Wnt inhibitor, Dickkopf 4, is induced by canonical Wnt signaling during ectodermal appendage morphogenesis. Dev. Biol. 305, 498-507.
8. Botchkarev, V. A., Botchkareva, N. V., Roth, W., Nakamura, M., Chen, L. H., Herzog, W., Lindner, G., McMahon, J. A., Peters, C., Lauster, R. et al. (1999). Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nat. Cell Biol. 1, 158-164.
9. Bowley, E., O'Gorman, D. B. and Gan, B. S. (2007). Beta-catenin signaling in fibroproliferative disease. J. Surg. Res. 138, 141-150.
10. 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 betacatenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264.
11. Carpenter, A. C., Rao, S., Wells, J. M., Campbell, K. and Lang, R. A. (2010). Generation of mice with a conditional null allele for Wntless. Genesis 48, 554-558.
12. Chang, C. H., Jiang, T. X., Lin, C. M., Burrus, L. W., Chuong, C. M. and Widelitz, R. (2004). Distinct Wnt members regulate the hierarchical morphogenesis of skin regions (spinal tract) and individual feathers. Mech. Dev. 121, 157-171.
13. Christiansen, J. H., Dennis, C. L., Wicking, C. A., Monkley, S. J., Wilkinson, D. G. and Wainwright, B. J. (1995). Murine Wnt-11 and Wnt-12 have temporally and spatially restricted expression patterns during embryonic development. Mech. Dev. 51, 341-350.
14. Collins, C. A., Kretzschmar, K. and Watt, F. M. (2011). Reprogramming adult dermis to a neonatal state through epidermal activation of beta-catenin. Development 138, 5189-5199.
15. Cui, C. Y., Kunisada, M., Piao, Y., Childress, V., Ko, M. S. and Schlessinger, D. (2010). Dkk4 and Eda regulate distinctive developmental mechanisms for subtypes of mouse hair. PLoS ONE 5, e10009.
16. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
17. Dassule, H. R., Lewis, P., Bei, M., Maas, R. and McMahon, A. P. (2000). Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785.
18. Detmar, M. (1996). Molecular regulation of angiogenesis in the skin. J. Invest. Dermatol. 106, 207-208.
19. Dhouailly, D., Olivera-Martinez, I., Fliniaux, I., Missier, S., Viallet, J. P. and Thelu, J. (2004). Skin field formation: morphogenetic events. Int. J. Dev. Biol. 48, 85-91.
20. Driskell, R. R., Giangreco, A., Jensen, K. B., Mulder, K. W. and Watt, F. M. (2009). Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 136, 2815-2823.
21. Enshell-Seijffers, D., Lindon, C., Kashiwagi, M. and Morgan, B. A. (2010). Beta-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev. Cell 18, 633-642.
22. Goodman, R. M., Thombre, S., Firtina, Z., Gray, D., Betts, D., Roebuck, J., Spana, E. P. and Selva, E. M. (2006). Sprinter: a novel transmembrane protein required for Wg secretion and signaling. Development 133, 4901-4911.
23. Grigoryan, T., Wend, P., Klaus, A. and Birchmeier, W. (2008). Deciphering the function of canonical Wnt signals in development and disease: conditional lossand gain-of-function mutations of beta-catenin in mice. Genes Dev. 22, 2308-2341.
24. 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.
25. 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.
26. Hardy, M. H. (1992). The secret life of the hair follicle. Trends Genet. 8, 55-61.
27. Headon, D. J. and Overbeek, P. A. (1999). Involvement of a novel Tnf receptor homologue in hair follicle induction. Nat. Genet. 22, 370-374.
28. Horne, K. A., Jahoda, C. A. and Oliver, R. F. (1986). Whisker growth induced by implantation of cultured vibrissa dermal papilla cells in the adult rat. J. Embryol. Exp. Morphol. 97, 111-124.
29. Hu, B., Lefort, K., Qiu, W., Nguyen, B. C., Rajaram, R. D., Castillo, E., He, F., Chen, Y., Angel, P., Brisken, C. et al. (2010). Control of hair follicle cell fate by underlying mesenchyme through a CSL-Wnt5a-FoxN1 regulatory axis. Genes Dev. 24, 1519-1532.
30. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. and Birchmeier, W. (2001). Beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545.
31. Jahoda, C. A., Horne, K. A. and Oliver, R. F. (1984). Induction of hair growth by implantation of cultured dermal papilla cells. Nature 311, 560-562.
32. Jahoda, C. A., Reynolds, A. J. and Oliver, R. F. (1993). Induction of hair growth in ear wounds by cultured dermal papilla cells. J. Invest. Dermatol. 101, 584-590.
33. Jho, E. H., Zhang, T., Domon, C., Joo, C. K., Freund, J. N. and Costantini, F. (2002). Wnt/beta-catenin/Tcf signaling induces the transcription of Axin2, a negative regulator of the signaling pathway. Mol. Cell. Biol. 22, 1172-1183.
34. Jiang, T. X., Jung, H. S., Widelitz, R. B. and Chuong, C. M. (1999). Selforganization of periodic patterns by dissociated feather mesenchymal cells and the regulation of size, number and spacing of primordia. Development 126, 4997-5009.
35. 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.
36. Kratochwil, K., Dull, M., Farinas, I., Galceran, J. and Grosschedl, R. (1996). Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10, 1382-1394.
37. 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.
38. Liu, H., Mohamed, O., Dufort, D. and Wallace, V. A. (2003). Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina. Dev. Dyn. 227, 323-334.
39. McGowan, K. M. and Coulombe, P. A. (1998). Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development. J. Cell Biol. 143, 469-486.
40. Millar, S. E. (2002). Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216-225.
41. Nguyen, M. T., Zhu, J., Nakamura, E., Bao, X. and Mackem, S. (2009). Tamoxifen-dependent, inducible Hoxb6CreERT recombinase function in lateral plate and limb mesoderm, CNS isthmic organizer, posterior trunk neural crest, hindgut, and tailbud. Dev. Dyn. 238, 467-474.
42. 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.
43. Olivera-Martinez, I., Thelu, J., Teillet, M. A. and Dhouailly, D. (2001). Dorsal dermis development depends on a signal from the dorsal neural tube, which can be substituted by Wnt-1. Mech. Dev. 100, 233-244.
44. Paus, R. and Cotsarelis, G. (1999). The biology of hair follicles. N. Engl. J. Med. 341, 491-497.
45. Paus, R., Muller-Rover, S., Van Der Veen, C., Maurer, M., Eichmuller, S., Ling, G., Hofmann, U., Foitzik, K., Mecklenburg, L. and Handjiski, B. (1999). A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J. Invest. Dermatol. 113, 523-532.
46. Reddy, S., Andl, T., Bagasra, A., Lu, M. M., Epstein, D. J., Morrisey, E. E. and Millar, S. E. (2001). Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis. Mech. Dev. 107, 69-82.
47. Reynolds, A. J. and Jahoda, C. A. (1991). Inductive properties of hair follicle cells. Ann. N. Y. Acad. Sci. 642, 226-242.
48. Rivera-Perez, J. A., Wakamiya, M. and Behringer, R. R. (1999). Goosecoid acts cell autonomously in mesenchyme-derived tissues during craniofacial development. Development 126, 3811-3821.
49. Rodriguez-Niedenfuhr, M., Prols, F. and Christ, B. (2003). Temporal and spatial protease nexin 1 expression during chick development. Gene Expr. Patterns 3, 611-614.
50. Schmidt-Ullrich, R. and Paus, R. (2005). Molecular principles of hair follicle induction and morphogenesis. BioEssays 27, 247-261.
51. Sengel, P. and Mauger, A. (1976). Peridermal cell patterning in the featherforming skin of the chick embryo. Dev. Biol. 51, 166-171.
52. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
53. St-Jacques, B., Dassule, H. R., Karavanova, I., Botchkarev, V. A., Li, J., Danielian, P. S., McMahon, J. A., Lewis, P. M., Paus, R. and McMahon, A. P. (1998). Sonic hedgehog signaling is essential for hair development. Curr. Biol. 8, 1058-1068.
54. Tran, T. H., Jarrell, A., Zentner, G. E., Welsh, A., Brownell, I., Scacheri, P. C. and Atit, R. (2010). Role of canonical Wnt signaling/ss-catenin via Dermo1 in cranial dermal cell development. Development 137, 3973-3984.
55. van Amerongen, R. and Nusse, R. (2009). Towards an integrated view of Wnt signaling in development. Development 136, 3205-3214.
56. Vidal, V. P., Chaboissier, M. C., Lutzkendorf, S., Cotsarelis, G., Mill, P., Hui, C. C., Ortonne, N., Ortonne, J. P. and Schedl, A. (2005). Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr. Biol. 15, 1340-1351.
57. Wagner, J., Schmidt, C., Nikowits, W., Jr and Christ, B. (2000). Compartmentalization of the somite and myogenesis in chick embryos are influenced by wnt expression. Dev. Biol. 228, 86-94.
58. 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 Xlinked PORCN, a putative regulator of Wnt signaling, cause focal dermal hypoplasia. Nat. Genet. 39, 836-838.
59. Werner, S. and Smola, H. (2001). Paracrine regulation of keratinocyte proliferation and differentiation. Trends Cell Biol. 11, 143-146.
60. Wilson, N., Hynd, P. I. and Powell, B. C. (1999). The role of BMP-2 and BMP-4 in follicle initiation and the murine hair cycle. Exp. Dermatol. 8, 367-368.
61. Yoshida, T., Vivatbutsiri, P., Morriss-Kay, G., Saga, Y. and Iseki, S. (2008). Cell lineage in mammalian craniofacial mesenchyme. Mech. Dev. 125, 797-808.
62. 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 betacatenin signaling programs embryonic epidermis to hair follicle fate. Development 135, 2161-2172.
63. 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.