Scratching the surface of skin development

The epidermis and its appendages develop from a single layer of multipotent embryonic progenitor keratinocytes. Embryonic stem cells receive cues from their environment that instruct them to commit to a particular differentiation programme and generate a stratified epidermis, hair follicles or sebaceous glands. Exciting recent developments have focused on how adult skin epithelia maintain populations of stem cells for use in the natural cycles of hair follicle regeneration and for re-epithelialization in response to wounding.

[1]  M. Azim Surani,et al.  Blimp1 associates with Prmt5 and directs histone arginine methylation in mouse germ cells , 2006, Nature Cell Biology.

[2]  Yann Barrandon,et al.  Morphogenesis and Renewal of Hair Follicles from Adult Multipotent Stem Cells , 2001, Cell.

[3]  A. Margulis,et al.  E-cadherin loss promotes the initiation of squamous cell carcinoma invasion through modulation of integrin-mediated adhesion , 2006, Journal of Cell Science.

[4]  J. Segre,et al.  Transcriptional control of epidermal specification and differentiation. , 2004, Current opinion in genetics & development.

[5]  C. Kaufman,et al.  GATA-3: an unexpected regulator of cell lineage determination in skin. , 2003, Genes & development.

[6]  F. Watt,et al.  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 , 2004, Development.

[7]  F. Quondamatteo,et al.  Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. , 2006, Genes & development.

[8]  Yann Barrandon,et al.  Long-term renewal of hair follicles from clonogenic multipotent stem cells. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Higgins,et al.  Hair cycle regulation of Hedgehog signal reception. , 2003, Developmental biology.

[10]  W. Wurst,et al.  Essential roles of BMPR‐IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis , 2004, Genesis.

[11]  T. Sun,et al.  Label-retaining cells reside in the bulge area of pilosebaceous unit: Implications for follicular stem cells, hair cycle, and skin carcinogenesis , 1990, Cell.

[12]  Elaine Fuchs,et al.  Self-Renewal, Multipotency, and the Existence of Two Cell Populations within an Epithelial Stem Cell Niche , 2004, Cell.

[13]  R. Paus,et al.  Sonic hedgehog signaling is essential for hair development , 1998, Current Biology.

[14]  M. Justice,et al.  Gene defect in ectodermal dysplasia implicates a death domain adapter in development , 2001, Nature.

[15]  F. Watt,et al.  Stem Cell Depletion Through Epidermal Deletion of Rac1 , 2005, Science.

[16]  F. Watt,et al.  Role of integrins in regulating epidermal adhesion, growth and differentiation , 2002, The EMBO journal.

[17]  E. Fuchs,et al.  Defining the Epithelial Stem Cell Niche in Skin , 2004, Science.

[18]  C. Dickson,et al.  A crucial role for Fgfr2-IIIb signalling in epidermal development and hair follicle patterning , 2003, Development.

[19]  Sarah E. Millar,et al.  Characterization of Wnt gene expression in developing and postnatal hair follicles and identification of Wnt5a as a target of Sonic hedgehog in hair follicle morphogenesis , 2001, Mechanisms of Development.

[20]  R Paus,et al.  The biology of hair follicles. , 1999, The New England journal of medicine.

[21]  D. Dhouailly,et al.  Molecular mechanisms controlling dorsal dermis generation from the somitic dermomyotome. , 2004, The International journal of developmental biology.

[22]  M. H. Hardy,et al.  The secret life of the hair follicle. , 1992, Trends in genetics : TIG.

[23]  H. Merker,et al.  Development and morphology of the periderm of mouse embryos (days 9-12 of gestation). , 1988, Acta anatomica.

[24]  Howard Y. Chang,et al.  Anatomic Demarcation by Positional Variation in Fibroblast Gene Expression Programs , 2006, PLoS genetics.

[25]  Ian Smyth,et al.  Human sebaceous tumors harbor inactivating mutations in LEF1 , 2006, Nature Medicine.

[26]  A. Sonnenberg,et al.  Multiple Functions of the Integrin α6β4 in Epidermal Homeostasis and Tumorigenesis , 2006, Molecular and Cellular Biology.

[27]  E. Wagner,et al.  Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins , 2005, Nature.

[28]  Y. Barrandon,et al.  The transcriptional repressor CDP (Cutl1) is essential for epithelial cell differentiation of the lung and the hair follicle. , 2001, Genes & development.

[29]  E. Fuchs,et al.  Hyperproliferation and Defects in Epithelial Polarity upon Conditional Ablation of α-Catenin in Skin , 2001, Cell.

[30]  P. McCrea,et al.  A role for Kaiso–p120ctn complexes in cancer? , 2005, Nature Reviews Cancer.

[31]  J. Schweizer,et al.  Keratins of the human hair follicle. , 2005, International review of cytology.

[32]  M. Karin,et al.  IKKα controls formation of the epidermis independently of NF-κB , 2001, Nature.

[33]  E. Fuchs,et al.  Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA , 2003, The Journal of cell biology.

[34]  Hoang Nguyen,et al.  Tcf3 Governs Stem Cell Features and Represses Cell Fate Determination in Skin , 2006, Cell.

[35]  Raphael Kopan,et al.  gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. , 2004, Developmental cell.

[36]  L Wolpert,et al.  Local inhibitory action of BMPs and their relationships with activators in feather formation: implications for periodic patterning. , 1998, Developmental biology.

[37]  Gina A. Taylor,et al.  Involvement of Follicular Stem Cells in Forming Not Only the Follicle but Also the Epidermis , 2000, Cell.

[38]  R. Fässler,et al.  β 1 integrin function in vivo: Adhesion, migration and more , 2005, Cancer and Metastasis Reviews.

[39]  Hans Clevers,et al.  T‐cell factors: turn‐ons and turn‐offs , 2002, The EMBO journal.

[40]  C. Potten.  Cell replacement in epidermis (keratopoiesis) via discrete units of proliferation. , 1981, International review of cytology.

[41]  William J. Ray,et al.  A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain , 1999, Nature.

[42]  J. Nicolas,et al.  Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors , 2005, Development.

[43]  Pascal Schneider,et al.  Generation of the primary hair follicle pattern. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[44]  I. Smart.  VARIATION IN THE PLANE OF CELL CLEAVAGE DURING THE PROCESS OF STRATIFICATION IN THE MOUSE EPIDERMIS , 1970, The British journal of dermatology.

[45]  A. Christiano,et al.  Patterns of hairless (hr) gene expression in mouse hair follicle morphogenesis and cycling. , 2000, The American journal of pathology.

[46]  Christoph Peters,et al.  Noggin is a mesenchymally derived stimulator of hair-follicle induction , 1999, Nature Cell Biology.

[47]  Potten Cs.  Cell Replacement in Epidermis (Keratopoiesis) via Discrete Units of Proliferation , 1981 .

[48]  R. Paus,et al.  Molecular principles of hair follicle induction and morphogenesis , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[49]  A. Mitchell,et al.  Sex determination: ... and differentiation , 2002, Nature Reviews Molecular Cell Biology.

[50]  Elaine Fuchs,et al.  Epidermal stem cells of the skin. , 2006, Annual review of cell and developmental biology.

[51]  D. Davidson.  The mechanism of feather pattern development in the chick. II. Control of the sequence of pattern formation. , 1983, Journal of embryology and experimental morphology.

[52]  J. Zanet,et al.  Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification , 2005, Journal of Cell Science.

[53]  Jennifer Y. Zhang,et al.  NF-kappaB RelA opposes epidermal proliferation driven by TNFR1 and JNK. , 2004, Genes & development.

[54]  M. Capecchi,et al.  Hoxc13 mutant mice lack external hair. , 1998, Genes & development.

[55]  Yaping Liu,et al.  Capturing and profiling adult hair follicle stem cells , 2004, Nature Biotechnology.

[56]  Elaine Fuchs,et al.  Lhx2 Maintains Stem Cell Character in Hair Follicles , 2006, Science.

[57]  Fiona M Watt,et al.  c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny , 2001, Current Biology.

[58]  J. Garlick,et al.  Evidence for keratinocyte stem cells in vitro: long term engraftment and persistence of transgene expression from retrovirus-transduced keratinocytes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[59]  H. Vogel,et al.  p63 is a p53 homologue required for limb and epidermal morphogenesis , 1999, Nature.

[60]  J. Gordon,et al.  Genetic mosaic analysis indicates that the bulb region of coat hair follicles contains a resident population of several active multipotent epithelial lineage progenitors. , 2002, Developmental biology.

[61]  W. Birchmeier,et al.  β-Catenin Controls Hair Follicle Morphogenesis and Stem Cell Differentiation in the Skin , 2001, Cell.

[62]  Elaine Fuchs,et al.  Changes in keratin gene expression during terminal differentiation of the keratinocyte , 1980, Cell.

[63]  D. Roop,et al.  Deregulated expression of c-Myc depletes epidermal stem cells , 2001, Nature Genetics.

[64]  B. Morgan,et al.  Distinct stem cell populations regenerate the follicle and interfollicular epidermis. , 2005, Developmental cell.

[65]  C. Stern.  Neural induction: old problem, new findings, yet more questions , 2005, Development.

[66]  B. Morgan,et al.  beta-catenin signaling can initiate feather bud development. , 1999, Development.

[67]  W. Birchmeier,et al.  Expression of DeltaNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours. , 2002, Development.

[68]  A. Joyner,et al.  Beta-catenin activation is necessary and sufficient to specify the dorsal dermal fate in the mouse. , 2006, Developmental biology.

[69]  M. KolodkaT,et al.  in vitroでのケラチノサイト幹細胞の証拠 レトロウイルス導入ケラチノサイトの長期移植とトランス遺伝子発現持続 , 1998 .

[70]  Sarah E. Millar,et al.  Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development , 2004, Development.

[71]  E. Fuchs,et al.  Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. , 1999, Development.

[72]  E. Fuchs,et al.  Catenins: keeping cells from getting their signals crossed. , 2006, Developmental cell.

[73]  P. Coulombe,et al.  A keratin cytoskeletal protein regulates protein synthesis and epithelial cell growth , 2006, Nature.

[74]  X. Tong,et al.  Keratin 17 modulates hair follicle cycling in a TNFα-dependent fashion , 2006 .

[75]  K. Calame,et al.  BLIMP-1: trigger for differentiation of myeloid lineage , 2000, Nature Immunology.

[76]  Paul Tempst,et al.  The transcriptional repressor JHDM3A demethylates trimethyl histone H3 lysine 9 and lysine 36 , 2006, Nature.

[77]  S. Millar,et al.  WNT signals are required for the initiation of hair follicle development. , 2002, Developmental cell.

[78]  Elaine Fuchs,et al.  Canonical notch signaling functions as a commitment switch in the epidermal lineage. , 2006, Genes & development.

[79]  D. Davidson.  The mechanism of feather pattern development in the chick. 1. The time of determination of feather position. , 1983, Journal of embryology and experimental morphology.

[80]  I Fariñas,et al.  Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. , 1994, Genes & development.

[81]  Christopher P. Crum,et al.  p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development , 1999, Nature.

[82]  R. Atit,et al.  EGF signaling patterns the feather array by promoting the interbud fate. , 2003, Developmental cell.

[83]  P. Coulombe,et al.  Cytoplasmic intermediate filaments revealed as dynamic and multipurpose scaffolds , 2004, Nature Cell Biology.

[84]  M. Nussenzweig,et al.  Blimp1 Defines a Progenitor Population that Governs Cellular Input to the Sebaceous Gland , 2006, Cell.

[85]  Elaine Fuchs,et al.  Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. , 2005, Genes & development.

[86]  Desmond J. Tobin,et al.  NF-κB transmits Eda A1/EdaR signalling to activate Shh and cyclin D1 expression, and controls post-initiation hair placode down growth , 2006, Development.

[87]  H. Pasolli,et al.  p120-Catenin Mediates Inflammatory Responses in the Skin , 2006, Cell.

[88]  E. Fuchs,et al.  De Novo Hair Follicle Morphogenesis and Hair Tumors in Mice Expressing a Truncated β-Catenin in Skin , 1998, Cell.

[89]  E. Fuchs,et al.  A Role for αβ1 Integrins in Focal Adhesion Function and Polarized Cytoskeletal Dynamics , 2003 .

[90]  E. Fuchs,et al.  Links between signal transduction, transcription and adhesion in epithelial bud development , 2003, Nature.

[91]  G. Beaudoin,et al.  The hairless gene mutated in congenital hair loss disorders encodes a novel nuclear receptor corepressor. , 2001, Genes & development.

[92]  B. Morgan,et al.  BMPs mediate lateral inhibition at successive stages in feather tract development. , 1998, Development.

[93]  L. Taichman,et al.  Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin , 2001, The EMBO journal.

[94]  E. Fuchs,et al.  Links between α-catenin, NF-κB, and squamous cell carcinoma in skin , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[95]  Elaine Fuchs,et al.  Defining the impact of (cid:1) -catenin/Tcf transactivation on epithelial stem cells , 2005 .

[96]  Mark C Udey,et al.  Characterization and isolation of stem cell-enriched human hair follicle bulge cells. , 2005, The Journal of clinical investigation.

[97]  H Green,et al.  Cultured cells for the treatment of disease. , 1991, Scientific American.

[98]  E. Fuchs,et al.  Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. , 2001, Genes & development.

[99]  R Paus,et al.  A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. , 2001, The Journal of investigative dermatology.

[100]  Elaine Fuchs,et al.  A common human skin tumour is caused by activating mutations in β-catenin , 1999, Nature Genetics.

[101]  I. Mackenzie.  Relationship between Mitosis and the Ordered Structure of the Stratum Corneum in Mouse Epidermis , 1970, Nature.

[102]  Elaine Fuchs,et al.  Asymmetric cell divisions promote stratification and differentiation of mammalian skin , 2005, Nature.

[103]  E. Fearon,et al.  Transient activation of beta -catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. , 2003, Genes & development.