Epidermal β-catenin activation remodels the dermis via paracrine signalling to distinct fibroblast lineages

Nature Communications

Volumn 7, Issue , 2016, Pages

  Lichtenberger, Beate M ^a,b   Mastrogiannaki, Maria ^a   Watt, Fiona M ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 5; SONIC HEDGEHOG PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; CTNNB1 PROTEIN, MOUSE; SHH PROTEIN, MOUSE; TGFB2 PROTEIN, MOUSE;

CELLS AND CELL COMPONENTS; GENE EXPRESSION; GENETIC ANALYSIS; HAIR; INHIBITOR; PROTEIN; SKIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CELL STIMULATION; CELL SUBPOPULATION; CONTROLLED STUDY; DERMIS; EPIDERMIS; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; GENE DELETION; GENE EXPRESSION; GENE INDUCTION; HAIR FOLLICLE; MALE; MOUSE; NEWBORN; NONHUMAN; NUCLEAR REPROGRAMMING; PARACRINE SIGNALING; SIGNAL TRANSDUCTION; WNT SIGNALING PATHWAY; ANIMAL; CYTOLOGY; FLOW CYTOMETRY; METABOLISM; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STEM CELL;

ERINACEIDAE;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; DERMIS; EPIDERMIS; EXTRACELLULAR MATRIX; FIBROBLASTS; FLOW CYTOMETRY; HAIR FOLLICLE; HEDGEHOG PROTEINS; MICE; PARACRINE COMMUNICATION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA2; WNT SIGNALING PATHWAY;

EID: 84957597219     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10537     Document Type: Article

References (52)

1. Clevers, H., Loh, K. M., Nusse, R. Stem cell signaling. An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control. Science 346, 1248012 (2014).
2. Lo Celso, C., Prowse, D. M., Watt, F. M. Transient activation of beta-catenin 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 (2004).
3. Watt, F. M. Mammalian skin cell biology: at the interface between laboratory and clinic. Science 346, 937-940 (2014).
4. Ito, M. et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316-320 (2007).
5. Silva-Vargas, V. et al. 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 (2005).
6. Collins, C. A., Kretzschmar, K., Watt, F. M. Reprogramming adult dermis to a neonatal state through epidermal activation of beta-catenin. Development 138, 5189-5199 (2011).
7. Driskell, R. R. et al. Distinct fibroblast lineages determine dermal architecture in skin development and repair. Nature 504, 277-281 (2013).
8. Holland, J. D., Klaus, A., Garratt, A. N., Birchmeier, W. Wnt signaling in stem and cancer stem cells. Curr. Opin. Cell Biol. 25, 254-264 (2013).
9. Kalluri, R., Zeisberg, M. Fibroblasts in cancer. Nat. Rev. Cancer 6, 392-401 (2006).
10. Le, N. H., Franken, P., Fodde, R. Tumour-stroma interactions in colorectal cancer: converging on beta-catenin activation and cancer stemness. Br. J. Cancer 98, 1886-1893 (2008).
11. Makino, T. et al. Basic fibroblast growth factor stimulates the proliferation of human dermal fibroblasts via the ERK1/2 and JNK pathways. Br. J. Dermatol. 162, 717-723 (2010).
12. Eto, H. et al. Therapeutic potential of fibroblast growth factor-2 for hypertrophic scars: upregulation of MMP-1 and HGF expression. Lab. Invest. 92, 214-223 (2012).
13. Chung, Y., Fu, E. Crosstalk between Shh and TGF-beta signaling in cyclosporine-enhanced cell proliferation in human gingival fibroblasts. PLoS ONE 8, e70128 (2013).
14. Zhou, D. et al. Sonic hedgehog is a novel tubule-derived growth factor for interstitial fibroblasts after kidney injury. J. Am. Soc. Nephrol. 25, 2187-2200 (2014).
15. Sgonc, R., Wick, G. Pro-and anti-fibrotic effects of TGF-beta in scleroderma. Rheumatology (Oxford) 47(Suppl 5): 55-57 (2008).
16. Tremblay, M. R. et al. Discovery of a potent and orally active hedgehog pathway antagonist (IPI-926). J. Med. Chem. 52, 4400-4418 (2009).
17. Smith-Mungo, L. I., Kagan, H. M. Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol. 16, 387-398 (1998).
18. Donati, G. et al. Epidermal Wnt/beta-catenin signaling regulates adipocyte differentiation via secretion of adipogenic factors. Proc. Natl Acad. Sci. USA 111, E1501-E1509 (2014).
19. Fitzgerald, A. M., Kirkpatrick, J. J., Foo, I. T., Naylor, I. L. Human skin histology as demonstrated by Herovici's stain: a guide for the improvement of dermal substitutes for use with cultured keratinocytes? Burns 22, 200-202 (1996).
20. Page, M. E., Lombard, P., Ng, F., Gottgens, B., Jensen, K. B. The epidermis comprises autonomous compartments maintained by distinct stem cell populations. Cell Stem Cell 13, 471-482 (2013).
21. Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140 (2010).
22. Arwert, E. N. et al. Upregulation of CD26 expression in epithelial cells and stromal cells during wound-induced skin tumour formation. Oncogene 31, 992-1000 (2011).
23. Gomez, C. et al. The interfollicular epidermis of adult mouse tail comprises two distinct cell lineages that are differentially regulated by Wnt, Edaradd, and Lrig1. Stem Cell Rep. 1, 19-27 (2013).
24. Kaushal, G. R. E. et al. Fate of prominin-1 expressing dermal papilla cells during homeostasis, wound healing and Wnt activation. J. Invest. Dermatol. 135, 2926-2934 (2015).
25. Athar, M., Tang, X., Lee, J. L., Kopelovich, L., Kim, A. L. Hedgehog signalling in skin development and cancer. Exp. Dermatol. 15, 667-677 (2006).
26. Long, F., Zhang, X. M., Karp, S., Yang, Y., McMahon, A. P. Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128, 5099-5108 (2001).
27. Sosic, D., Richardson, J. A., Yu, K., Ornitz, D. M., Olson, E. N. Twist regulates cytokine gene expression through a negative feedback loop that represses NF-kappaB activity. Cell 112, 169-180 (2003).
28. Rivers, L. E. et al. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat. Neurosci. 11, 1392-1401 (2008).
29. Massague, J. TGFbeta in cancer. Cell 134, 215-230 (2008).
30. Massague, J., Blain, S. W., Lo, R. S. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 103, 295-309 (2000).
31. Rinkevich, Y. et al. Skin fibrosis. Identification and isolation of a dermal lineage with intrinsic fibrogenic potential. Science 348, 2151 (2015).
32. Mao, J., Kim, B. M., Rajurkar, M., Shivdasani, R. A., McMahon, A. P. Hedgehog signaling controls mesenchymal growth in the developing mammalian digestive tract. Development 137, 1721-1729 (2010).
33. Fabian, S. L. et al. Hedgehog-Gli pathway activation during kidney fibrosis. Am. J. Pathol. 180, 1441-1453 (2012).
34. Chuang, P. T., McMahon, A. P. Vertebrate Hedgehog signalling modulated by induction of a Hedgehog-binding protein. Nature 397, 617-621 (1999).
35. Johnson, R. L., Tabin, C. The long and short of hedgehog signaling. Cell 81, 313-316 (1995).
36. Brownell, I., Guevara, E., Bai, C. B., Loomis, C. A., Joyner, A. L. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 8, 552-565 (2011).
37. Karlsson, L., Bondjers, C., Betsholtz, C. Roles for PDGF-A and sonic hedgehog in development of mesenchymal components of the hair follicle. Development 126, 2611-2621 (1999).
38. Sato, N., Leopold, P. L., Crystal, R. G. Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog. J. Clin. Invest. 104, 855-864 (1999).
39. Roberts, A. B. Molecular and cell biology of TGF-beta. Miner. Electrolyte Metab. 24, 111-119 (1998).
40. Akhmetshina, A. et al. Activation of canonical Wnt signalling is required for TGF-beta-mediated fibrosis. Nat. Commun. 3, 735 (2012).
41. Lakos, G. et al. Targeted disruption of TGF-beta/Smad3 signaling modulates skin fibrosis in a mouse model of scleroderma. Am. J. Pathol. 165, 203-217 (2004).
42. Kashpur, O., LaPointe, D., Ambady, S., Ryder, E. F., Dominko, T. FGF2-induced effects on transcriptome associated with regeneration competence in adult human fibroblasts. BMC Genomics 14, 656 (2013).
43. Hamburg-Shields, E., DiNuoscio, G. J., Mullin, N. K., Lafayatis, R., Atit, R. P. Sustained beta-catenin activity in dermal fibroblasts promotes fibrosis by up-regulating expression of extracellular matrix protein-coding genes. J. Pathol. 235, 686-697 (2014).
44. Ohtola, J. et al. beta-Catenin has sequential roles in the survival and specification of ventral dermis. Development 135, 2321-2329 (2008).
45. Beyer, C. et al. Beta-catenin is a central mediator of pro-fibrotic Wnt signaling in systemic sclerosis. Ann. Rheum. Dis. 71, 761-767 (2012).
46. Festa, E. et al. Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771 (2011).
47. Horn, A. et al. Hedgehog signaling controls fibroblast activation and tissue fibrosis in systemic sclerosis. Arthritis Rheum. 64, 2724-2733 (2012).
48. Yauch, R. L. et al. A paracrine requirement for hedgehog signalling in cancer. Nature 455, 406-410 (2008).
49. Ozdemir, B. C. et al. Depletion of carcinoma-associated fibroblasts and fibrosis induces immunosuppression and accelerates pancreas cancer with reduced survival. Cancer Cell 25, 719-734 (2014).
50. Rhim, A. D. et al. Stromal elements act to restrain, rather than support, pancreatic ductal adenocarcinoma. Cancer Cell 25, 735-747 (2014).
51. Robertson, E. J. et al. Blimp1 regulates development of the posterior forelimb, caudal pharyngeal arches, heart and sensory vibrissae in mice. Development 134, 4335-4345 (2007).
52. Hamilton, T. G., Klinghoffer, R. A., Corrin, P. D., Soriano, P. Evolutionary divergence of platelet-derived growth factor alpha receptor signaling mechanisms. Mol. Cell Biol. 23, 4013-4025 (2003).