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Mammalian Skin Cell Biology: at the Interface Between Laboratory and Clinic Fiona M

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Mammalian Skin Cell Biology: at the Interface Between Laboratory and Clinic Fiona M REVIEW environment, lubrication of the skin with lip- ids, and thermoregulation by hairs and sweat. Each function depends on nondividing, termi- nally differentiated keratinocytes that die and Mammalian skin cell biology: are shed from the body. These differentiated cells are replenished through a variety of stem cell pop- At the interface between ulations in different epidermal locations (Fig. 1) (6). Under steady-state conditions, each stem cell laboratory and clinic compartment produces a subset of differentiated epidermal cells, but when the cells are transplanted or the skin is damaged or otherwise manipulated Fiona M. Watt* experimentally, most stem cells can contribute to the full range of differentiated epidermal lineages. Mammalian skin research represents the convergence of three complementary disciplines: The epidermis is separated from the dermis by cell biology, mouse genetics, and dermatology. The skin provides a paradigm for current a basement membrane, an extracellular matrix research in cell adhesion, inflammation, and tissue stem cells. Here, I discuss recent (ECM) that is rich in type IV collagen and laminin. insights into the cell biology of skin. Single-cell analysis has revealed that human The main resident cell type of the dermis is the epidermal stem cells are heterogeneous and differentiate in response to multiple extrinsic fibroblast. The dermis is organized into three signals. Live-cell imaging, optogenetics, and cell ablation experiments show skin cells layers (Fig. 1). The layer closest to the epidermis to be remarkably dynamic. High-throughput, genome-wide approaches have yielded is the papillary layer, and beneath that lies the unprecedented insights into the circuitry that controls epidermal stem cell fate. Last, reticular layer. Fibroblast density is higher in integrative biological analysis of human skin disorders has revealed unexpected functions papillary dermis, and the reticular dermis is char- for elements of the skin that were previously considered purely structural. acterized by an abundance of fibrillar collagen. kin research has made spectacular pro- (5). The upper layer is an epithelium called the epi- The deepest dermal layer, historically termed the gress over the past 30 years (Box 1). In 1975, dermis, and the lower layer is a connective tissue hypodermis, is characterized by a thick layer of the ability to culture cells efficiently from called the dermis. The epidermis comprises a multi- white adipocytes. In addition to the three main biopsies of human epidermis, the outer layered epithelium, the interfollicular epidermis dermal layers, there are two other mesenchymal on August 3, 2015 S — covering of the skin, was reported (1). This (IFE), and associated (adnexal) structures hair fol- structures in the dermis that are important for quickly opened up opportunities to expand cell licles, sebaceous glands, and sweat glands. The skin function. These are the dermal papilla (DP), sheets for transplantation onto burn victims, distribution of adnexal structures differs in differ- a cluster of cells at the base of the hair follicle to characterize genes that are differentially ex- entbodysites,asdoesthethicknessoftheIFE. that control the hair follicle cycle, and the arrector pressed in different epidermal layers, and to ana- Keyfunctionsoftheepidermisaretheforma- pili muscle (APM), a smooth muscle that inserts lyze tissue assembly in cell culture (2). Cloning tion of a protective interface with the external into the basement membrane at a specific point the genes that encode epidermal keratins led to a second major advance: Gene promoters could drive transgene expression in specific layers of the skin and, subsequently, perform targeted www.sciencemag.org gene knockouts and lineage analysis in mice (3). Even with the power of the in vitro and in vivo laboratory-based approaches, skin research would not be in its current vibrant state had it not been for the major contributions of the dermatology community. Eminent clinicians in the early 1980s taught scientists the fundamentals of skin struc- tureandfunctionandcalledattentiontorareskin Downloaded from conditions, such as Epidermolysis bullosa, that atthetimewereofunknownetiology.Asaresult, themolecularbasisofmanyhumangeneticskin disorders was quickly determined and validated in mouse models, laying the foundation for on- going efforts to treat them by means of gene correction and other approaches (4). Here, I highlight recent advances in our un- derstanding of skin cell biology. A variety of tech- nologies are illuminating cellular heterogeneity, the extrinsic and intrinsic controls that regulate cell behavior and tissue architecture, and the sur- prising role of structural elements of the epider- misinregulatingskinfunction. Skin architecture Mammalian skin forms the outer covering of the Fig. 1. Mouse back skin. Markers of different epidermal stem cell populations (LGR6, LRIG1, PLET1, body and consists of two major layers (Fig. 1) GLI1, LGR5, and CD34) are shown. LGR6 and LRIG1 are expressed in the hair follicle isthmus, whereas CD34 and LGR5 are bulge markers. The three dermal layers (boxed) are the reticular dermis, papillary ’ King s College London Centre for Stem Cells and Regenerative dermis, and hypodermis/white adipose tissue. The dermal papilla and arrector pili muscle constitute two Medicine, 28th Floor, Tower Wing, Guy’sHospital,GreatMaze Pond, London SE1 9RT, UK. specialized populations of dermal mesenchymal cells. The hair is shown in the resting phase of the hair *Corresponding author. E-mail: [email protected] growth cycle. [Redrawn from (60).] SCIENCE sciencemag.org 21 NOVEMBER 2014 • VOL 346 ISSUE 6212 937 SKIN in the hair follicle and, on contrac- keratinocytes, single-cell global gene tion, causes the hair follicles to be- expression profiling has revealed come erect. cell-to-cell variation in the relative Although epidermal epithelial cells abundance of transcripts of two (keratinocytes) and dermal fibroblasts previously reported markers of hu- are the most abundant cell types in man epidermal stem cells: the Notch the skin, there are several other key ligand Delta-like 1 (DLL1) and the cell types that are either permanent epidermal growth factor receptor residents of the tissue or traffic through antagonist LRIG1 (26). Cells that theskin.Theseincludethecellsofthe express high levels of DLL1 also peripheral nervous system (7)and have elevated expression of genes blood vessels, melanocytes (8), and associated with endocytosis, integrin- cells of the innate and adaptive im- mediated adhesion, and receptor mune system (9). tyrosine kinase signaling, and there was some evidence that expres- Single-cell approaches sion of these genes is not inde- to skin cell biology pendently regulated (26). The two Cell behavior is regulated by a com- cell states may be reinforced by bination of intrinsic and extrinsic virtue of their influence on how mechanisms. Local extrinsic signals keratinocytes interact with the micro- areprovidedbythecellularmicro- environment. For example, one of environment, or niche, and include the genes up-regulated in cells with interactions with neighboring cells, high levels of DLL1 is caveolin-1, secreted factors, extracellular matrix Fig. 2. Reconstructing the epidermal stem cell niche at single-cell reso- which is known to couple b1integrin, (ECM) proteins, physical parameters lution. A single stem cell (green) is shown interacting with different compo- Notch1, and receptor tyrosine ki- such as tissue stiffness, and environ- nents of the microenvironment: the extracellular matrix supporting substrate nase signaling. The desmosomal mental conditions such as hypoxia adhesion, interactions with neighboring cells of the same or different type, cadherin Desmoglein-2 associates (10). The ability to isolate and cul- intercellular adhesion and signaling molecules that can be membrane-bound, with caveolin-1, an interaction that ture single stem cells from human or soluble factors. is believed to regulate prolifera- epidermis allows analysis of stem tion (27). cell–niche interactions at the single-cell level junction and different cytoskeletal elements (Fig. 2). One approach is to capture cells on ECM- within the epidermis. For example, cadherin- Cell behavior in the coated micropatterned islands and direct them mediated adhesions modulate forces transmit- context of the intact tissue to adopt specific shapes (11). Another is to seed ted to the ECM so that keratinocytes in a The way epidermal stem cells behave under steady- cells on hydrogels that differ in bulk stiffness or cohesive colony localize traction forces to the state conditions can be quite different from how on composite substrates containing gold nano- colony periphery (17) and the desmosomal pla- they behave after tissue damage or upon isolation particles that change the way that ECM proteins que protein desmoplakin regulates assembly and transplantation (6). This conclusion is based, are anchored to the substrate and thereby influ- and function of gap junctions (18). Understand- in part, on extensive lineage tracing of the prog- ence cell attachment (12). In both cases, activator ing the dynamics of these interactions has been enyofdifferentmouseepidermalstemcellpop- protein 1 (AP1) factors are activated to execute the facilitated by mathematical modeling, as in the ulations (Fig. 1). Most recently, lineage-tracing terminal differentiation program, but the signal case of the impact of actin and keratin filaments has also been performed
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