Epidermal stem cell diversity and quiescence

EMBO Molecular Medicine

Volumn 1, Issue 5, 2009, Pages 260-267

  Watt, Fiona M ^a,b   Jensen, Kim B ^a  

^a University of Cambridge   (United Kingdom)

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

Author keywords

EGF receptor; Lrig1; Myc; NFATc1; P catenin

Indexed keywords

BETA CATENIN; EPIDERMAL GROWTH FACTOR RECEPTOR; MYC PROTEIN; TRANSCRIPTION FACTOR NFAT; WNT PROTEIN;

BASEMENT MEMBRANE; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; CELL JUNCTION; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; DIMERIZATION; EMBRYO CELL; EPIDERMAL STEM CELL; EPIDERMIS CELL; GENETIC MANIPULATION; GENETIC VARIABILITY; HAIR FOLLICLE; HAIR GROWTH; HOMEOSTASIS; HUMAN; INFUNDIBULUM; MESENCHYMAL STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SEBACEOUS GLAND; SIGNAL TRANSDUCTION; SKIN EPITHELIUM; STEM CELL; ANIMAL; ARTICLE; CYTOLOGY; EPIDERMIS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EPIDERMIS; HAIR FOLLICLE; HUMANS; MICE; SIGNAL TRANSDUCTION; STEM CELLS;

EID: 77449119710     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.200900033     Document Type: Review

References (81)

1. Alonso L, Fuchs E (2006) The hair cycle. J Cell Sci 119: 391-393
2. Andl T, Reddy ST, Gaddapara T, Millar SE (2002) WNT signals are required for the initiation of hair follicle development. DevCell 2: 643-653
3. Arnold I, Watt FM (2001) c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr Biol 11: 558-568
4. Ballaro C, Ceccarelli S,Tiveron C,Tatangelo L, Salvatore AM, Segatto O, Alema S (2005) Targeted expression of RALT in mouse skin inhibits epidermal growth factor receptor signalling and generates a Waved-like phenotype. EMBO Rep 6: 755-761
5. Barrandon Y, Green H (1987) Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci USA 84: 2302-2306
6. Blanpain C, Fuchs E (2009) Epidermal homeostasis: a balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 10: 207-217
7. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118: 635-648
8. Braun KM, Niemann C,Jensen UB, SundbergJP, Silva-Vargas V, Watt FM (2003) Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130: 5241-5255
9. Clayton E, Doupe DP, Klein AM, Winton DJ, Simons BD, Jones PH (2007) A single type of progenitor cell maintains normal epidermis. Nature 446: 185-189
10. Collins CA, Watt FM (2008) Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for β-catenin and Notch signalling. Dev Biol 324: 55-67
11. Cotsarelis G, Cheng SZ, Dong G, Sun TT, Lavker RM (1989) Existence of slow- cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57: 201-209
12. CotsarelisG, Sun TT, Lavker RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61: 1329-1337
13. Depreter MG, Blair NF, Gaskell TL, Nowell CS, Davern K, Pagliocca A, Stenhouse FH, Farley AM, Fraser A, Vrana J, et al(2008) Identification of Plet-1 as a specific marker of early thymic epithelial progenitor cells. Proc Natl Acad Sci USA 105: 961-966
14. Dor Y, Brown J, Martinez OI, Melton DA (2004) Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429: 41-46
15. Estrach S, Legg J, Watt FM (2007) Syntenin mediates Delta1-induced cohesiveness of epidermal stem cells in culture. J Cell Sci 120: 2944-2952
16. Ferby I, Reschke M, Kudlacek O, Knyazev P, Pante G, Amann K, Sommergruber W, Kraut N, Ullrich A, Fassler R, et al(2006) Mig6 is a negative regulator of EGF receptor-mediated skin morphogenesis and tumorformation. Nat Med 12: 568-573
17. Gafter-Gvili A, Sredni B, Gal R, Gafter U, Kalechman Y (2003) Cyclosporin A- induced hair growth in mice is associated with inhibition of calcineurin- dependent activation of NFAT in follicular keratinocytes. Am J Physiol Cell Physiol 284: C1593-C1603
18. Gafter-Gvili A, Kalechman Y, Sredni B, Gal R, Gafter U (2004) Cyclosporin A-induced hair growth in mice is associated with inhibition of hair follicle regression. Arch Dermatol Res 296: 265-269
19. Gat U, DasGupta R, Degenstein L, Fuchs E (1998) De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95: 605-614
20. Ghazizadeh S, Taichman LB (2001) Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin. EMBO J 20: 1215-1222
21. Ghazizadeh S, Taichman LB (2005) Organization of stem cells and their progeny in human epidermis. J Invest Dermatol 124: 367-372
22. Giangreco A, Arwert EN, Rosewell IR, Snyder J, Watt FM,Stripp BR (2009) Stem cells are dispensable for lung homeostasis but restore airways after injury. Proc Natl Acad Sci USA 106: 9286-9291
23. Guo L, Yu QC, Fuchs E (1993) Targeting expression of keratinocyte growth factor to keratinocytes elicits striking changes in epithelial differentiation in transgenic mice. EMBO J 12: 973-986
24. Gurdon JB (1988) A community effect in animal development. Nature 336: 772-774
25. Hall PA, Watt FM (1989) Stem cells: the generation and maintenance of cellular diversity. Development 106: 619-633
26. Hansen LA, Alexander N, Hogan ME, Sundberg JP, Dlugosz A, Threadgill DW, Magnuson T, Yuspa SH (1997) Genetically null mice reveal a central role for epidermal growth factor receptor in the differentiation of the hair follicle and normal hair development. Am J Pathol 150: 1959-1975
27. Horsley V, O'Carroll D, Tooze R, Ohinata Y, Saitou M, Obukhanych T, Nussenzweig M, Tarakhovsky A, Fuchs E (2006) Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126: 597-609
28. Horsley V, Aliprantis AO, Polak L, Glimcher LH, Fuchs E (2008) NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132: 299-310
29. Ito M, Liu Y, Yang Z, Nguyen J, Liang F, Morris RJ, CotsarelisG (2005) Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 11: 1351-1354
30. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, Cotsarelis G (2007) Wnt- dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447: 316-320
31. JaksV, BarkerN, KasperM,van EsJH,Snippert HJ,Clevers H,Toftgard R(2008) Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40: 1291-1299
32. Jensen KB, Watt FM (2006) Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc Natl Acad Sci USA 103, 11958-11963
33. Jensen UB, Lowell S, Watt FM (1999) The spatial relationship between stem cells and their progeny in the basal layer of human epidermis: a new view based on whole-mount labelling and lineage analysis. Development 126: 2409-2418
34. Jensen UB, Yan X, Triel C, Woo SH, Christensen R, Owens DM (2008) A distinct population of clonogenic and multipotent murine follicular keratinocytes in the upper isthmus. J Cell Sci 121: 609-617
35. Jensen KB, Collins CA, Nascimento E,Tan DW, Frye M, Itami S, Watt FM (2009) Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4: 427-439
36. Jones PH, Watt FM (1993) Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73: 713-724
37. Jones PH, Harper S, Watt FM (1995) Stem cell patterning and fate in human epidermis. Cell 80: 83-93 Jones PH, Simons BD, Watt FM (2007) Sic transit gloria: farewell to the epidermal transit amplifying cell? Cell Stem Cell 1: 371-381
38. Kobielak K, Stokes N, de la Cruz J, Polak L, Fuchs E (2007) Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proc Natl Acad Sci USA 104: 10063-10068
39. Langton AK, Herrick SE, Headon DJ (2008) An extended epidermal response heals cutaneous wounds in the absence of a hair follicle stem cell contribution. J Invest Dermatol 128: 1311-1318
40. Levy V, Lindon C, Harfe BD, Morgan BA (2005) Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell 9: 855-861
41. Levy V, Lindon C, Zheng Y, Harfe BD, Morgan BA (2007) Epidermal stem cells arise from the hair follicle after wounding. FASEB J 21: 1358-1366
42. Lin Y, Wong K, Calame K (1997) Repression of c-myc transcription by Blimp-1, an inducer of terminal B cell differentiation. Science 276: 596-599
43. Lo Celso C, Prowse DM, Watt FM (2004) 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 131: 1787-1799
44. Lo Celso C, Berta MA, Braun KM, Frye M, Lyle S, Zouboulis CC, Watt FM (2008) Characterization of bipotential epidermal progenitors derived from human sebaceous gland: contrasting roles of c-Myc and p-catenin. Stem Cells 26: 1241-1252
45. Lowell S, Jones P, Le Roux I, Dunne J, Watt FM (2000) Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr Biol 10: 491-500
46. Lowry WE, Blanpain C, NowakJA, Guasch G, Lewis L, Fuchs E (2005) Defining the impact ofβ-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 19, 1596-1611
47. Luetteke NC, Phillips HK, Qiu TH, Copeland NG, Earp HS, Jenkins NA, Lee DC (1994) The mouse waved-2 phenotype results from a point mutation in the EGF receptor tyrosine kinase. Genes Dev 8: 399-413
48. Lyle S, Christofidou-Solomidou M, Liu Y, Elder DE, Albelda S, Cotsarelis G (1998) The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J Cell Sci 111: 3179-3188
49. Magnúsdóttir E, Kalachikov S, Mizukoshi K, Savitsky D, Ishida-Yamamoto A, Panteleyev AA, Calame K (2007) Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc Natl Acad Sci USA 104: 14988-14993
50. Mammucari C, Tommasi di Vignano A, Shariv AA, Neilson J, Havrda MC, Roop DR, Botchkarev VA, Crabtree GR, Dotto GP (2005) Integration of Notch 1 and calcineurin/NFAT signalling pathways in keratinocyte growth and differentiation control. DevCell 8: 665-676
51. Miettinen PJ, Berger JE, Meneses J, Phung Y, Pedersen RA, Werb Z, Derynck R (1995) Epithelial immaturity and multiorgan failure in mice lacking epidermal growth factor receptor. Nature 376: 337-341
52. Morris RJ, Liu Y, Marles L, Yang Z, Trempus C, Li S, Lin JS, Sawicki JA, Cotsarelis G (2004) Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 22: 411-417
53. Narhi K, Jarvinen E, Birchmeier W, Taketo MM, Mikkola ML, Thesleff I (2008) Sustained epithelial beta-catenin activity induces precocious hair development but disrupts hair follicle down-growth and hair shaft formation. Development 135: 1019-1028
54. Niemann C, Watt FM (2002) Designer skin: lineage commitment in postnatal epidermis. Trends Cell Biol 12: 185-192
55. Nijhof JG, Braun KM, Giangreco A, Van Pelt C, Kawamoto H, Boyd RL, Willemze R, Mullenders LH, Watt FM, DeGruijl FR, etal(2006) The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 133: 3027-3037
56. Nowak JA, Polak L, Pasolli HA, Fuchs E (2008) Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3: 33-43
57. Ohyama M, Terunuma A, Tock CL, Radonovich MF, Pise-Masison CA, Hopping SB, Brady JN, Udey MC, Vogel JC (2006) Characterization and isolation of stem cell-enriched human hair follicle bulge cells. J Clin Invest 116: 249260
58. Oshima H, Rochat A, Kedzia C, Kobayashi K, Barrandon Y (2001) Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104: 233-245
59. Owens DM, Watt FM (2003) Contribution of stem cells and differentiated cells to epidermal tumours. Nat Rev Cancer 3: 444-451
60. Plikus MV, Mayer JA, de la Cruz D, Baker RE, Maini PK, Maxson R, Chuong CM (2008) Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451: 340-344
61. Potten CS, Morris RJ (1988) Epithelial stem cells in vivo. J Cell Sci Suppl 10: 4562
62. Rheinwald JG, Green H (1977) Epidermal growth factor and the multiplication of cultured human epidermal keratinocytes. Nature 265: 421-424
63. Richardson GD, Bazzi H, Fantauzzo KA, Waters JM, Crawford H, Hynd P, Christiano AM, Jahoda CA (2009) KGF and EGF signalling block hair follicle induction and promote interfollicular epidermal fate in developing mouse skin. Development 136: 2153-2164
64. Rochat A, Kobayashi K, Barrandon Y (1994) Location of stem cells of human hair follicles by clonal analysis. Cell 76: 1063-1073
65. Santini MP, Talora C, Seki T, Bolgan L, Dotto GP (2001) Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1). Expression in keratinocyte differentiation. Proc Natl Acad Sci USA 98: 9575-9580
66. Schneider MR, Werner S, Paus R, Wolf E (2008) Beyond wavy hairs: the epidermal growth factor receptor and its ligands in skin biology and pathology. Am J Pathol 173: 14-24
67. Sibilia M, Wagner EF (1995) Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269: 234-238
68. Sibilia M, Fleischmann A, Behrens A, Stingl L, Carroll J, Watt FM, SchlessingerJ, Wagner EF (2000) The EGF receptor provides an essential survival signal for SOS-dependent skin tumor development. Cell 102: 211-220
69. Sick S, Reinker S, Timmer J, Schlake T (2006) WNT and DKK determine hair follicle spacing through a reaction-diffusion mechanism. Science 314: 1447-1450
70. Silva-Vargas V, Lo Celso C, Giangreco A, Ofstad T, Prowse DM, Braun KM, Watt FM (2005) 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 9: 121-131
71. Soucek L, Whitfield J, Martins CP, Finch AJ, Murphy DJ, Sodir NM, Karnezis AN, Swigart LB, Nasi S, Evan GI (2008) Modelling Myc inhibition as a cancer therapy. Nature 455: 679-683
72. Suzuki K, Yamaguchi Y, Villacorte M, Mihara K, Akiyama M, Shimizu H, Taketo MM, Nakagata N, Tsukiyama T, Yamaguchi TP, et al(2009) Embryonic hair follicle fate change by augmented beta-catenin through Shh and Bmp signaling. Development 136: 367-372
73. Taylor G, Lehrer MS, Jensen PJ, Sun TT, Lavker RM (2000) Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102: 451-461
74. Threadgill DW, Dlugosz AA, Hansen LA, Tennenbaum T, Lichti U, Yee D, LaMantia C, Mourton T, Herrup K, Harris RC, et al(1995)Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269: 230-234
75. Trempus CS, Morris RJ, Bortner CD, Cotsarelis G, Faircloth RS, Reece JM, Tennant RW (2003) Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 120: 501-511
76. TumbarT, Guasch G, Greco V, Blanpain C, Lowry WE, Rendl M, Fuchs E (2004) Defining the epithelial stem cell niche in skin. Science 303: 359-363
77. Vassar R, Fuchs E (1991) Transgenic mice provide new insights into the role of TGF-alpha during epidermal development and differentiation. Genes Dev 5: 714-727
78. Watt FM, Lo Celso C, Silva-Vargas V (2006) Epidermal stem cells: an update. Curr Opin Genet Dev 16: 518-524
79. Watt FM, Frye M, Benitah SA (2008) MYC in mammalian epidermis: how can an oncogene stimulate differentiation? Nat Rev Cancer 8: 234-242
80. Zhang J, He XC, Tong WG, Johnson T, Wiedemann LM, Mishina Y, Feng JQ, Li L (2006) Bone morphogenetic protein signaling inhibits hair follicle anagen induction by restricting epithelial stem/progenitor cell activation and expansion. Stem Cells 24: 2826-2839
81. Zhang Y, Andl T, Yang SH, Teta M, Liu F, Seykora JT, Tobias JW, Piccolo S, Schmidt-Ullrich R, Nagy A, et al(2008) Activation of β-catenin signaling programs embryonic epidermis to hair follicle fate. Development 135: 2161-2172