Reprogramming adult dermis to a neonatal state through epidermal activation of β-catenin

Development

Volumn 138, Issue 23, 2011, Pages 5189-5199

  Collins, Charlotte A ^a   Kretzschmar, Kai ^a   Watt, Fiona M ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Dermis; Epidermis; Fibroblast; Mouse; Niche; Stem cell; Wnt

Indexed keywords

BETA CATENIN; COLLAGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL PROLIFERATION; CONTROLLED STUDY; DERMIS; DOWN REGULATION; EPIDERMIS CELL; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; HAIR FOLLICLE; HAIR GROWTH; MITOSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; SEBACEOUS GLAND; SIGNAL TRANSDUCTION; SKIN; SKIN FIBROBLAST; UPREGULATION;

AGE FACTORS; ANIMALS; BETA CATENIN; CELL PROLIFERATION; EXTRACELLULAR MATRIX; FIBROBLASTS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HISTOLOGICAL TECHNIQUES; IMAGE PROCESSING, COMPUTER-ASSISTED; IMMUNOHISTOCHEMISTRY; MICE; MICROSCOPY, CONFOCAL; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKIN;

EID: 80755184835     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.064592     Document Type: Article

References (42)

1. Baker, C. M., Verstuyf, A., Jensen, K. B. and Watt, F. M. (2010). Differential sensitivity of epidermal cell subpopulations to beta-catenin-induced ectopic hair follicle formation. Dev. Biol. 343, 40-50.
2. Bastide, P., Darido, C., Pannequin, J., Kist, R., Robine, S., Marty-Double, C., Bibeau, F., Scherer, G., Joubert, D., Hollande F. et al. (2007). Sox9 regulates cell proliferation and is required for Paneth cell differentiation in the intestinal epithelium. J. Cell Biol. 178, 635-648.
3. Biernaskie, J., Paris, M., Morozova, O., Fagan, M. B., Marra, M., Pevny, L. and Miller, F. D. (2009). SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell 5, 610-623.
4. Chan, E. F., Gat, U., McNiff, J. M. and Fuchs, E. (1999). A common human skin tumour is caused by activating mutations in b-catenin. Nat. Genet. 21, 410-413.
5. Chi, W. Y., Enshell-Seijffers, D. and Morgan, B. A. (2010). De novo production of dermal papilla cells during the anagen phase of the hair cycle. J. Invest. Dermatol. 130, 2664-2666.
6. Clevers, H. (2006). Wnt/b-catenin signaling in development and disease. Cell 127, 469-480.
7. Collins, C. A. and Watt, F. M. (2008). Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling. Dev. Biol. 324, 55-67.
8. 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.
9. Enshell-Seijffers, D., Lindon, C. and Morgan, B. A. (2008). The serine protease Corin is a novel modifier of the Agouti pathway. Development 135, 217-225.
10. 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.
11. Estrach, S., Ambler, C. A., Lo Celso, C., Hozumi, K. and Watt, F. M. (2006). Jagged 1 is a b-catenin target gene required for ectopic hair follicle formation in adult epidermis. Development 133, 4427-4438.
12. Fitzgerald, A. M. P., Kirkpatrick, J. J. R., Foo, I. T. H. and Naylor, I. L. (1996). Human skin histology as demonstrated using Herovici's stain: a guide for the improvement of dermal substitutes for use with cultured keratinocytes? Burns 22, 200-202.
13. Fliniaux, I., Viallet, J. P. and Dhouailly, D. (2004). Ventral vs. dorsal chick dermal progenitor specification. Int. J. Dev. Biol. 48, 103-106.
14. Fuchs, E. (2008). Skin stem cells: rising to the surface. J. Cell Biol. 180, 273-284.
15. Fuchs, E., Tumbar, T. and Guasch, G. (2004). Socializing with the neighbors: stem cells and their niche. Cell 116, 769-778.
16. Hamilton, T. G., Klinghoffer, R. A., Corrin, P. D. and Soriano, P. (2003). Evolutionary divergence of platelet-derived growth factor alpha signaling mechanisms. Mol. Cell. Biol. 23, 4013-4025.
17. Horne, K. A. and Jahoda, C. A. (1992). Restoration of hair growth by surgical implantation of follicular dermal sheath. Development 116, 563-571.
18. Ito, M., Yang, Z., Andl, T., Cui, C., Kim, N., Millar, S. E. and Cotsarelis, G. (2007). Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316-320.
19. Jensen, K. B., Collins, C. A., Nascimento, E., Tan, D. W., Frye, M., Itami, S. and Watt, F. M. (2009). Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 8, 427-439.
20. Kalluri, R. and Zeisberg, M. (2006). Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401.
21. Karlsson, L., Bondjers, C. and Betsholtz, C. (1999). Roles for PDGF-A and sonic hedgehog in development of mesenchymal components of the hair follicle. Development 126, 2611-2621.
22. Lichti, U., Anders, J. and Yuspa, S. H. (2008). Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat. Protoc. 3, 799-810.
23. Lo Celso, C., Prowse, D. M. and Watt, F. M. (2004). Transient activation of betacatenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 131, 1787-1799.
24. Mii, Y. and Taira, M. (2009). Secreted Frizzled-related proteins enhance the diffusion of Wnt ligands and expand their signalling range. Development 136, 4083-4088.
25. Millar, S. E. (2002). Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216-225.
26. Morris, R. J. and Potten, C. S. (1999). Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen. J. Invest. Dermatol. 112, 470-475.
27. Olivera-Martinez, I., Thélu, J. and Dhouailly, D. (2004). Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. Int. J. Dev. Biol. 48, 93-101.
28. Rendl, M., Lewis, L. and Fuchs, E. (2005). Molecular dissection of mesenchymalepithelial interactions in the hair follicle. PLoS Biol. 3, e331.
29. Rinn, J. L., Bondre, C., Gladstone, H. B., Brown, P. O. and Chang, H. Y. (2006). Anatomic demarcation by positional variation in fibroblast gene expression programs. PLoS Genet. 2, e119.
30. Romero, G., Sneddon, W. B., Yang, Y., Wheeler, D., Blair, H. C. and Friedman, P. A. (2010). Parathyroid hormone receptor directly interacts with dishevelled to regulate b-catenin signaling and osteoclastogenesis. J. Biol. Chem. 285, 14756-14763.
31. Sandulache, V. C., Parekh, A., Dohar, J. E. and Hebda, P. A. (2007). Fetal dermal fibroblasts retain a hyperactive migratory and contractile phenotype under 2-and 3-dimensional constraints compared to normal adult fibroblasts. Tissue Eng. 13, 2791-2801.
32. Schofield, R. (1978). The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells 4, 7-25.
33. Sick, S., Reinker, S., Timmer, J. and Schlake, T. (2006). WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314, 1447-1450.
34. Silva-Vargas, V., Lo Celso, C., Giangreco, A., Ofstad, T., Prowse, D. M., Braun, K. M. and Watt, F. M. (2005). Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev. Cell 9, 121-131.
35. Suceveanu, A. I., Suceveanu, A., Voinea, F., Mazilu, L., Mixici, F. and Adam, T. (2009). Introduction of cytogenetic tests in colorectal cancer screening. J. Gastrointestin. Liver Dis. 18, 33-38.
36. Takeda, H., Lyle, S., Lazar, A. J., Zouboulis, C. C., Smyth, I. and Watt, F. M. (2006). Human sebaceous tumors harbor inactivating mutations in LEF1. Nat. Med. 12, 395-397.
37. Van Mater, D., Kolligs, F. T., Dlugosz, A. A. and Fearon, E. R. (2003). Transient activation of beta-catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17, 1219-1224.
38. Vermeulen, L., De Sousa, E., Melo, F., van der Heijden, M., Cameron, K., de Jong, J. H., Borovski, T., Tuynman, J. B., Todaro, M., Merz, C. et al. (2010). Wnt activity defines colon cancer stem cells and is regulated by the microenvironment. Nat. Cell Biol. 12, 468-476.
39. Watt, F. M. and Driskell, R. R. (2010). The therapeutic potential of stem cells. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 155-163.
40. Werner, S., Krieg, T. and Smola, H. (2007). Keratinocyte-fibroblast interactions in wound healing. J. Invest. Dermatol. 127, 998-1008.
41. Yang, C. C. and Cotsarelis, G. (2010). Review of hair follicle dermal cells. J. Dermatol. Sci. 57, 2-11.
42. Zhao, Y., Zhou, T., Li, A., Yao, H., He, F., Wang, L. and Si, J. (2009). A potential role of collagens expression in distinguishing between premalignant and malignant lesions in stomach. Anat. Rec. (Hoboken) 292, 692-700.