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Hair Follicle Dermal Papilla Cells at a Glance

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Hair Follicle Dermal Papilla Cells at a Glance Cell Science at a Glance 1179 Hair follicle dermal interactions during development and in embryonic epidermis, which is detectable at postnatal life (Blanpain and Fuchs, 2009; embryonic day 14.5 (E14.5) of mouse papilla cells at a glance Müller-Röver et al., 2001; Schmidt-Ullrich and development. Soon after, a local condensation Paus, 2005; Watt and Jensen, 2009). One (dermal condensate) of fibroblasts forms Ryan R. Driskell1, Carlos Clavel2, population of mesenchymal cells in the skin, beneath the placode. Reciprocal signalling Michael Rendl2,* and Fiona M. known as dermal papilla (DP) cells, is the focus between the condensate and the placode leads Watt1,3,* of intense interest because the DP not only to proliferation of the overlying epithelium and 1Laboratory for Epidermal Stem Cell Biology, regulates hair follicle development and growth, downward extension of the new follicle into Wellcome Trust Centre for Stem Cell Research, but is also thought to be a reservoir of multi- the dermis (Millar, 2002; Schneider et al., University of Cambridge, Cambridge CB2 1QR, UK potent stem cells. In this article and the 2009; Ohyama et al., 2010; Yang and 2Black Family Stem Cell Institute and Department of Developmental and Regenerative Biology, Mount accompanying poster we review the origins of Cotsarelis, 2010). After the initial downward Sinai School of Medicine, New York, NY 10029, USA the DP during skin development, and discuss DP growth, the epithelial cells envelope the dermal 3CRUK Cambridge Research Institute, Li Ka Shing Centre, Robinson Way, Cambridge CB2 0RE, UK heterogeneity and the changes in the DP that condensate, thereby forming the mature DP. *Authors for correspondence occur during the hair growth cycle. We also The DP then instructs the surrounding ([email protected]; fi[email protected]) consider the different cell lineages along which epithelial cells, now called matrix cells, to Journal of Cell Science 124, 1179-1182 DP cells can differentiate as well as potential proliferate, move upward and differentiate into © 2011. Published by The Company of Biologists Ltd clinical applications of DP cells. the multiple layers of the outgrowing hair shaft doi:10.1242/jcs.082446 and the channel surrounding the hair shaft, Developmental origins of dermal called the inner root sheath (Millar, 2002; Introduction papilla cells Schneider et al., 2009). Mammalian skin is a highly tractable tissue in The precursor of the hair follicle is a local Tissue recombination studies have shown that which to explore epithelial–mesenchymal thickening, also known as placode, of the mouse dermis contains the activity necessary to Journal of Cell Science (See poster insert) 1180 Journal of Cell Science 124 (8) induce hair follicle formation as early as E12.5, (Driskell et al., 2009). At this stage, all DP cells At the onset of anagen the DP activates stem before the dermal condensate has developed express CD133 (also known as PROM1) and cells in the secondary hair germ leading to new (Dhouailly, 1973; Song and Sawyer, 1996). alkaline phosphatase (Handjiski et al., 1994), downward growth of follicles. In the hairless Dermis from hair-forming regions of skin can but DP of zigzag hairs are SOX2-negative and mutant mouse, DP cells become stranded deep induce follicles in both hair- and non-hair- guard, awl and auchene follicles are SOX2- in the dermis during catagen and lose contact forming epithelium, whereas dermis from non- positive. When different DP populations are with the bulge; the follicles in these mice cannot hair-forming sites cannot support the formation sorted and used in skin reconstitution assays, undergo anagen and eventually degenerate of hair follicles. Several of the pathways that are SOX-positive DP cells are found to be necessary (Panteleyev et al., 1999). Interruption of - involved in reciprocal signalling between the for the formation of guard, awl or auchene catenin signalling in the DP results in reduced epithelial cells and DP of the developing follicle follicles (Driskell et al., 2009). By contrast, DP proliferation of cells at the base of the follicle, have been identified, with reciprocal Wnt expression of SOX is required for the formation which induces catagen and prevents anagen signalling emerging as one of the earliest and of zigzag hair follicles (James et al., 2003). This induction (Enshell-Seijffers et al., 2010). - most-important (Kishimoto et al., 2000; Millar, indicates different roles for two SRY catenin activity in the DP regulates a number of 2002; Schneider et al., 2009; Ohyama et al., transcription factors in specifying hair follicle other signalling pathways, including the FGF 2010; Yang and Cotsarelis, 2010). However, type during development. pathway, which mediate the inductive effects of relatively little is known about how dermal Gene expression profiling of DP cells isolated the DP on the hair follicle epithelium (Enshell- condensate and DP cells become hair-inducing from developing mouse skin has resulted in the Seijffers et al., 2010). Fgf7 and Fgf10 are specialised fibroblasts (Schneider et al., 2009; definition of a core DP ‘signature’ of 184 genes expressed in the DP and stimulate proliferation Ohyama et al., 2009; Yang and Cotsarelis, (Rendl et al., 2005), and in signatures that are of the adjacent epithelial cells of the hair follicle 2009). specific for SOX2-positive and -negative DP (Greco et al., 2009). Fibroblasts and, therefore, DP in different types (Driskell et al., 2009). These signatures Some DP markers, such as alkaline body sites have different embryonic origins are beginning to provide information about the phosphatase and cellular retinoic-acid-binding (Fernandes et al., 2004; Rendl et al., 2005; signalling pathways that control DP and hair protein 1 (CRABP1), are expressed throughout Ohtola et al., 2008; Wong et al., 2006; Jinno et follicle function, in particular the importance of the hair growth cycle (Collins and Watt, 2008). al., 2010). Head and facial fibroblasts are Wnt, bone morphogenetic protein (BMP) and Others, such as the serine protease Corin, are derived from the neural crest, whereas dorsal fibroblast growth factor (FGF) (Greco et al., upregulated during anagen (Enshell-Seijffers et and ventral trunk fibroblasts come from the 2009; Kishimoto et al., 2000; Rendl et al., 2008). al., 2008). In adult mouse skin Sox2 expression dermomyotome of somitic and lateral plate In addition, comparison of the properties of hair in the DP varies during the hair growth cycle and origin, respectively. Cell autonomous, site- follicles in different body sites reveals is only detectable during anagen (Biernaskie et specific homeobox (Hox) gene expression differences in the properties of their DP. One al., 2009). confers positional memory on fibroblasts from example, in human skin, is the observation that different body sites and has a role in specifying androgens stimulate hair follicle growth in the Potential therapeutic applications of the gene expression profile of the overlying face but cause follicle miniaturisation in DP cells in restoring hair growth epidermis (Rinn et al., 2008). the scalp. DP cells express androgen receptors Hair loss (alopecia) is a common and distressing Journal of Cell Science and 5a-OH-reductase – a key enzyme in problem for men and women, and there is Dermal papilla heterogeneity androgen metabolism – and DP from different therefore considerable interest in treatments that Mouse skin contains several distinct hair follicle body sites differ in their responsiveness to can prevent or reverse it. Harnessing the ability types that differ in length, thickness and the androgen (Rutberg et al., 2006). of the differentiated and highly specialised shape of the hair shaft, i.e. straight or kinked. In fibroblasts of the DP to induce neighbouring back skin, the most abundant follicles form The role of the DP in the hair growth epidermal cells to differentiate along the hair zigzag hairs, which have two kinks in the shaft, cycle follicle lineages is an attractive approach to whereas the hairs of other follicle types (guard, In postnatal life the hair follicles undergo treating alopecia. awl and auchene) have longer shafts that are cyclical growth. The resting phase is known as The hair-inductive ability of DP cells is not either straight or have a single kink (Schlake, telogen, the growth phase as anagen and the restricted to embryonic development, and DP 2007). Guard hairs develop during the first wave regression phase as catagen (Müller-Röver et cells from postnatal skin retain the ability to of hair follicle morphogenesis around E14.5; al., 2001; Schmidt-Ullrich and Paus, 2005; direct epithelial cells to form hair follicles awl and auchene hairs form in the second wave Ohyama et al., 2010; Yang and Cotsarelis, (Jahoda et al., 1984). Furthermore, formation of around E16.5; and zigzag hairs form during the 2010). During catagen, the epithelial cells at the new DP can be induced in adult skin by third wave, starting at E18.5 (Schlake, 2007). base of the follicle undergo apoptosis, but activating the Wnt pathway in the epidermis The DP of zigzag hairs are smaller than those of the DP remains intact and is pulled or migrates (Silva-Vargas et al., 2005). These observations the other follicle types (Elliott et al., 1999). upwards, until it comes to rest next to the stem suggest that it is possible to generate DP cells in Between E14.5 and E16.5, all developing DP cells of the hair follicle bulge. This situation order to treat hair loss. (that is, those associated with guard, awl or persists during telogen. In anagen, cells at the One obvious strategy is to expand DP cells in auchene follicles) express the transcription base of the follicle start to proliferate, which culture before transplantation. DP cells not only factor sex determining region Y-box 2 (Sox2), results in downward growth of the follicle and retain the ability to form DP following in vitro but SOX2 is undetectable in the DP of zigzag envelopment of the DP.
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