Polyclonal origin and hair induction ability of dermal papillae in neonatal and adult mouse back skin

Developmental Biology

Volumn 366, Issue 2, 2012, Pages 290-297

  Collins, Charlotte A ^a   Jensen, Kim B ^a   MacRae, Elizabeth J ^a   Mansfield, William ^a   Watt, Fiona M ^a,b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

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

Author keywords

Dermal stem cells; Fibroblasts; Hair follicles

Indexed keywords

WNT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL INTERACTION; CELL LINEAGE; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME RECONSTITUTION; FEMALE; FIBROBLAST; GAMMA IRRADIATION; HAIR FOLLICLE; HAIR GROWTH; KERATINOCYTE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; SKIN PAPILLA; TISSUE GROWTH;

MUS;

EID: 84861224873     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2012.03.016     Document Type: Article

References (36)

1. Biernaskie J., Paris M., Morozova O., Fagan B.M., Marra M., Pevny L., Miller F.D. SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell. Stem. Cell. 2009, 5:610-623.
2. Chi W.Y., Enshell-Seijffers D., Morgan B.A. De novo production of dermal papilla cells during the anagen phase of the hair cycle. J. Invest. Dermatol. 2010, 130:2664-2666.
3. Collins C.A., Kretzschmar K., Watt F.M. Reprogramming adult dermis to a neonatal state through epidermal activation of Β-catenin. Development 2011, 138:5189-5199.
4. Driskell R.R., Giangreco A., Jensen K.B., Mulder K.W., Watt F.M. Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 2009, 136(16):2815-2823.
5. Driskell R.R., Clavel C., Rendl M., Watt F.M. Hair follicle dermal papilla cells at a glance. J. Cell Sci. 2011, 124:1179-1182.
6. Driskell R.R., Juneja V.R., Connelly J.T., Kretzschmar K., Tan D.W.-M., Watt F.M. Clonal growth of dermal papilla cells in hydrogels reveals intrinsic differences between Sox2-positive and -negative cells in vitro and in vivo. J. Invest. Dermatol. 2012, 132:1084-1093.
7. Enshell-Seijffers D., Lindon C., Kashiwagi M., Morgan B.A. Β-catenin activity in the dermal papilla regulates morphogenesis and regeneration of hair. Dev. Cell. 2010, 18:633-642.
8. Fernandes K.J., McKenzie I.A., Mill P., Smith K.M., Akhavan M., Barnabé-Heider F., Biernaskie J., Junek A., Kobayashi N.R., Toma J.G., Kaplan D.R., Labosky P.A., Rafuse V., Hui C.C., Miller F.D. A dermal niche for multipotent adult skin-derived precursor cells. Nat. Cell Biol. 2004, 6:1082-1089.
9. Fuchs E. Skin stem cells: rising to the surface. J. Cell Biol. 2008, 180:273-284.
10. Gao J., DeRouen M.C., Chen C.H., Nguyen M., Nguyen N.T., Ido H., Harada K., Sekiguchi K., Morgan B.A., Miner J.H., Oro A.E., Marinkovich M.P. Laminin-511 is an epithelial message promoting dermal papilla development and function during early hair morphogenesis. Genes. Dev. 2008, 22:2111-2124.
11. Greco V., Chen T., Rendl M., Schober M., Pasolli H.A., Stokes N., Dela Cruz-Racelis J., Fuchs E. A two-step mechanism for stem cell activation during hair regeneration. Cell. Stem. Cell. 2008, 4:155-169.
12. Hamilton T.G., Klinghoffer R.A., Corrin P.D., Soriano P. Evolutionary divergence of Platelet-Derived Growth Factor alpha signaling mechanisms. Mol. Cell Biol. 2003, 23:4013-4025.
13. Horne K.A., Jahoda C.A. Restoration of hair growth by surgical implantation of follicular dermal sheath. Development 1992, 116:563-571.
14. Iida M., Ihara S., Matsuzaki T. Follicular epithelia and dermal papillae of mouse vibrissal follicles qualitatively change their hair-forming ability during anagen. Differentiation 2007, 75:371-381.
15. Ito M., Yang Z., Andl T., Cui C., Kim N., Millar S.E., Cotsarelis G. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007, 447:316-320.
16. Ito Y., Hamazaki T.S., Ohnuma K., Tamaki K., Asashima M., Okochi H. Isolation of murine hair-inducing cells using the cell surface marker prominin-1/CD133. J. Invest. Dermatol. 2007, 127:1052-1060.
17. Jahoda C.A., Horne K.A., Oliver R.F. Induction of hair growth by implantation of cultured dermal papilla cells. Nature 1984, 311:560-562.
18. Jahoda C.A., Oliver R.F. Vibrissa dermal papilla cell aggregative behaviour in vivo and in vitro. J. Embryol. Exp. Morphol. 1984, 79:211-224.
19. Jensen K.B., Driskell R.R., Watt F.M. Assaying proliferation and differentiation capacity of stem cells using disaggregated adult mouse epidermis. Nature Protocols 2010, 5:898-911.
20. Jinno H., Morozova O., Jones K.L., Biernaskie J.A., Paris M., Hosokawa R., Rudnicki M.A., Chai Y., Rossi F., Marra M.A., Miller F.D. Convergent genesis of an adult neural crest-like dermal stem cell from distinct developmental origins. Stem Cells. 2010, 28:2027-2040.
21. Karlsson L., Bondjers C., Betsholtz C. Roles for PDGF-A and sonic hedgehog in development of mesenchymal components of the hair follicle. Development 1999, 126:2611-2621.
22. Kondo M., Wagers A.J., Manz M.G., Prohaska S.S., Scherer D.C., Beilhack G.F., Shizuru J.A., Weissman I.L. Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu. Rev. Immunol. 2003, 21:759-806.
23. Lepper C., Fan C.M. Inducible lineage tracing of Pax7-descendant cells reveals embryonic origin of adult satellite cells. Genesis 2010, 48:424-436.
24. Lichti U., Anders J., Yuspa S.H. 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 2008, 3:799-810.
25. Lo Celso C., Prowse D.M., Watt F.M. Transient activation of Β-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 2004, 131:1787-1799.
26. McElwee K.J., Kissling S., Wenzel E., Huth A., Hoffmann R. Cultured peribulbar dermal sheath cells can induce hair follicle development and contribute to the dermal sheath and dermal papilla. J. Invest. Dermatol. 2003, 121:1267-1275.
27. Millar S.E. Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 2002, 118:216-225.
28. Olivera-Martinez I., Thélu J., Dhouailly D. Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. Int. J. Dev. Biol. 2004, 48:93-101.
29. Reynolds A.J., Jahoda C.A. Hair matrix germinative epidermal cells confer follicle-inducing capabilities on dermal sheath and high passage papilla cells. Development 1996, 122:3085-3094.
30. Silva-Vargas V., Lo Celso C., Giangreco A., Ofstad T., Prowse D.M., Braun K.M., Watt F.M. Β-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev. Cell. 2005, 9:121-131.
31. St-Jacques B., Dassule H.R., Karavanova I., Botchkarev V.A., Li J., Danielian P.S., McMahon J.A., Lewis P.M., Paus R., McMahon A.P. Sonic hedgehog signaling is essential for hair development. Curr. Biol. 1998, 8:1058-1068.
32. Tobin D.J., Gunin A., Magerl M., Handijski B., Paus R. Plasticity and cytokinetic dynamics of the hair follicle mesenchyme: implications for hair growth control. J. Invest. Dermatol. 2003, 120:895-904.
33. Toma J.G., Akhavan M., Fernandes K.J., Barnabé-Heider F., Sadikot A., Kaplan D.R., Miller F.D. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 2001, 3:778-784.
34. Yamao M., Inamatsu M., Ogawa Y., Toki H., Okada T., Toyoshima K.E., Yoshizato K. Contact between dermal papilla cells and dermal sheath cells enhances the ability of DPCs to induce hair growth. J. Invest. Dermatol. 2010, 130:2707-2718.
35. Yang C.C., Cotsarelis G. Review of hair follicle dermal cells. J. Dermatol. Sci. 2010, 57:2-11.
36. Zammit P. All muscle satellite cells are equal, but are some more equal than others?. J. Cell Sci. 2008, 121:2975-2982.