Biochemistry of epidermal stem cells

Biochimica et Biophysica Acta - General Subjects

Volumn 1830, Issue 2, 2013, Pages 2427-2434

  Eckert, Richard L ^a,b   Adhikary, Gautam ^a   Balasubramanian, Sivaprakasam ^a   Rorke, Ellen A ^a   Vemuri, Mohan C ^c   Boucher, Shayne E ^c   Bickenbach, Jackie R ^d   Kerr, Candace ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MARYLAND GREENEBAUM CANCER CENTER   (United States)

^c Life Technologies Inc   (United States)

^d UNIVERSITY OF IOWA   (United States)

Author keywords

Epidermis; Hair follicle; Interfollicular stem cell; Keratinocyte; Stem cell

Indexed keywords

BETA CATENIN; CELL MARKER; EPIDERMAL GROWTH FACTOR RECEPTOR; EPITOPE; MICRORNA; MICRORNA 137; MICRORNA 15B; MICRORNA 182; MICRORNA 221; MICRORNA 222; NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

BASAL CELL CARCINOMA; CANCER GROWTH; CANCER INCIDENCE; CANCER STEM CELL; CELL DIFFERENTIATION; CELL POPULATION; CELL PROLIFERATION; EPIDERMAL STEM CELL; GENE MUTATION; HAIR FOLLICLE; HEMATOPOIETIC STEM CELL; HOMEOSTASIS; HUMAN; INTRACELLULAR SIGNALING; LIGAND BINDING; MELANOMA; MOLECULAR PATHOLOGY; NON MELANOMA SKIN CANCER; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SEBACEOUS GLAND; SQUAMOUS CELL CARCINOMA; STEM CELL; STEM CELL EXPANSION; STEM CELL NICHE; ULTRAVIOLET RADIATION; WNT SIGNALING PATHWAY;

EPIDERMIS; HUMANS; STEM CELLS;

EID: 84872500170     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.07.002     Document Type: Review

References (144)

1. D. Aberdam, E. Candi, R.A. Knight, and G. Melino miRNAs, 'stemness' and skin Trends Biochem. Sci. 33 2008 583 591
2. G. Adhikary, Y.C. Chew, E.A. Reece, and R.L. Eckert PKC-delta and -eta, MEKK-1, MEK-6, MEK-3, and p38-delta are essential mediators of the response of normal human epidermal keratinocytes to differentiating agents J. Invest. Dermatol. 130 2010 2017 2030
3. M. Al-Hajj, and M.F. Clarke Self-renewal and solid tumor stem cells Oncogene 23 2004 7274 7282
4. M. Al-Hajj, M.S. Wicha, A. Benito-Hernandez, S.J. Morrison, and M.F. Clarke Prospective identification of tumorigenic breast cancer cells Proc. Natl. Acad. Sci. U. S. A. 100 2003 3983 3988
5. H.N. Ananthaswamy, S.M. Loughlin, S.E. Ullrich, and M.L. Kripke Inhibition of UV-induced p53 mutations by sunscreens: implications for skin cancer prevention J. Investig. Dermatol. Symp. Proc. 3 1998 52 56
6. T. Andl, E.P. Murchison, F. Liu, Y. Zhang, M. Yunta-Gonzalez, J.W. Tobias, C.D. Andl, J.T. Seykora, G.J. Hannon, and S.E. Millar The miRNA-processing enzyme dicer is essential for the morphogenesis and maintenance of hair follicles Curr. Biol. 16 2006 1041 1049
7. D. Antonini, M.T. Russo, R.L. De, M. Gorrese, V.L. Del, and C. Missero Transcriptional repression of miR-34 family contributes to p63-mediated cell cycle progression in epidermal cells J. Invest. Dermatol. 130 2010 1249 1257
8. M. Athar, C. Li, X. Tang, S. Chi, X. Zhang, A.L. Kim, S.K. Tyring, L. Kopelovich, J. Hebert, E.H. Epstein Jr., D.R. Bickers, and J. Xie Inhibition of smoothened signaling prevents ultraviolet B-induced basal cell carcinomas through regulation of Fas expression and apoptosis Cancer Res. 64 2004 7545 7552
9. H. Backvall, A. Asplund, A. Gustafsson, A. Sivertsson, J. Lundeberg, and F. Ponten Genetic tumor archeology: microdissection and genetic heterogeneity in squamous and basal cell carcinoma Mutat. Res. 571 2005 65 79
10. E.V. Badiavas, M. Abedi, J. Butmarc, V. Falanga, and P. Quesenberry Participation of bone marrow derived cells in cutaneous wound healing J. Cell. Physiol. 196 2003 245 250
11. Y. Barrandon, and H. Green Three clonal types of keratinocyte with different capacities for multiplication Proc. Natl. Acad. Sci. U. S. A. 84 1987 2302 2306
12. M.A. Baxter, R.F. Wynn, S.N. Jowitt, J.E. Wraith, L.J. Fairbairn, and I. Bellantuono Study of telomere length reveals rapid aging of human marrow stromal cells following in vitro expansion Stem Cells 22 2004 675 682
13. L.T. Bemis, R. Chen, C.M. Amato, E.H. Classen, S.E. Robinson, D.G. Coffey, P.F. Erickson, Y.G. Shellman, and W.A. Robinson MicroRNA-137 targets microphthalmia-associated transcription factor in melanoma cell lines Cancer Res. 68 2008 1362 1368
14. S.A. Benitah Epidermal stem cells in skin homeostasis and cutaneous carcinomas Clin. Transl. Oncol. 9 2007 760 766
15. V. Bergoglio, F. Larcher, O. Chevallier-Lagente, A. Bernheim, O. Danos, A. Sarasin, M.D. Rio, and T. Magnaldo Safe selection of genetically manipulated human primary keratinocytes with very high growth potential using CD24 Mol. Ther. 15 2007 2186 2193
16. J.R. Bickenbach Identification and behavior of label-retaining cells in oral mucosa and skin J. Dent. Res. 60 Spec No C 1981 1611 1620
17. J.R. Bickenbach Isolation, characterization, and culture of epithelial stem cells Methods Mol. Biol. 289 2005 97 102
18. J.R. Bickenbach, and K.L. Grinnell Epidermal stem cells: interactions in developmental environments Differentiation 72 2004 371 380
19. J.R. Bickenbach, and K.A. Holbrook Label-retaining cells in human embryonic and fetal epidermis J. Invest. Dermatol. 88 1987 42 46
20. J.R. Bickenbach, J. McCutecheon, and I.C. Mackenzie Rate of loss of tritiated thymidine label in basal cells in mouse epithelial tissues Cell Tissue Kinet. 19 1986 325 333
21. J.R. Bickenbach, and M.M. Stern Plasticity of epidermal stem cells: survival in various environments Stem Cell Rev. 1 2005 71 77
22. C. Blanpain, W.E. Lowry, A. Geoghegan, L. Polak, and E. Fuchs Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche Cell 118 2004 635 648
23. K. Boehnke, B. Falkowska-Hansen, H.J. Stark, and P. Boukamp Stem cells of the human epidermis and their niche: composition and function in epidermal regeneration and carcinogenesis Carcinogenesis 2012 (Electronic publication ahead of print)
24. X. Borue, S. Lee, J. Grove, E.L. Herzog, R. Harris, T. Diflo, E. Glusac, K. Hyman, N.D. Theise, and D.S. Krause Bone marrow-derived cells contribute to epithelial engraftment during wound healing Am. J. Pathol. 165 2004 1767 1772
25. P. Boukamp Non-melanoma skin cancer: what drives tumor development and progression? Carcinogenesis 26 2005 1657 1667
26. P. Boukamp UV-induced skin cancer: similarities-variations J. Dtsch. Dermatol. Ges. 3 2005 493 503
27. S. Braig, D.W. Mueller, T. Rothhammer, and A.K. Bosserhoff MicroRNA miR-196a is a central regulator of HOX-B7 and BMP4 expression in malignant melanoma Cell. Mol. Life Sci. 67 2010 3535 3548
28. K.M. Braun, and F.M. Watt Epidermal label-retaining cells: background and recent applications J. Investig. Dermatol. Symp. Proc. 9 2004 196 201
29. M. Brittan, K.M. Braun, L.E. Reynolds, F.J. Conti, A.R. Reynolds, R. Poulsom, M.R. Alison, N.A. Wright, and K.M. Hodivala-Dilke Bone marrow cells engraft within the epidermis and proliferate in vivo with no evidence of cell fusion J. Pathol. 205 2005 1 13
30. J. Chen, H.E. Feilotter, G.C. Pare, X. Zhang, J.G. Pemberton, C. Garady, D. Lai, X. Yang, and V.A. Tron MicroRNA-193b represses cell proliferation and regulates cyclin D1 in melanoma Am. J. Pathol. 176 2010 2520 2529
31. Z. Chen, W.H. Evans, S.C. Pflugfelder, and D.Q. Li Gap junction protein connexin 43 serves as a negative marker for a stem cell-containing population of human limbal epithelial cells Stem Cells 24 2006 1265 1273
32. C. Cheung, C.K. Smith, J.O. Hoog, and S.A. Hotchkiss Expression and localization of human alcohol and aldehyde dehydrogenase enzymes in skin Biochem. Biophys. Res. Commun. 261 1999 100 107
33. T. Christoph, S. Muller-Rover, H. Audring, D.J. Tobin, B. Hermes, G. Cotsarelis, R. Ruckert, and R. Paus The human hair follicle immune system: cellular composition and immune privilege Br. J. Dermatol. 142 2000 862 873
34. E. Clayton, D.P. Doupe, A.M. Klein, D.J. Winton, B.D. Simons, and P.H. Jones A single type of progenitor cell maintains normal epidermis Nature 446 2007 185 189
35. W. Deng, Q. Han, L. Liao, C. Li, W. Ge, Z. Zhao, S. You, H. Deng, F. Murad, and R.C. Zhao Engrafted bone marrow-derived flk-(1 +) mesenchymal stem cells regenerate skin tissue Tissue Eng. 11 2005 110 119
36. R.L. Eckert, J.F. Crish, T. Efimova, S.R. Dashti, A. Deucher, F. Bone, G. Adhikary, G. Huang, R. Gopalakrishnan, and S. Balasubramanian Regulation of involucrin gene expression J. Invest. Dermatol. 123 2004 13 22
37. R.L. Eckert, J.F. Crish, and N.A. Robinson The epidermal keratinocyte as a model for the study of gene regulation and cell differentiation Physiol. Rev. 77 1997 397 424
38. R.L. Eckert, T. Efimova, S. Balasubramanian, J.F. Crish, F. Bone, and S. Dashti p38 mitogen-activated protein kinases on the body surface - a function for p38delta J. Invest. Dermatol. 120 2003 823 828
39. T. Efimova, A.M. Broome, and R.L. Eckert A regulatory role for p38 delta MAPK in keratinocyte differentiation. Evidence for p38 delta-ERK1/2 complex formation J. Biol. Chem. 278 2003 34277 34285
40. T. Efimova, A. Deucher, T. Kuroki, M. Ohba, and R.L. Eckert Novel protein kinase C isoforms regulate human keratinocyte differentiation by activating a p38 delta mitogen-activated protein kinase cascade that targets CCAAT/enhancer-binding protein alpha J. Biol. Chem. 277 2002 31753 31760
41. T. Efimova, P. LaCelle, J.F. Welter, and R.L. Eckert Regulation of human involucrin promoter activity by a protein kinase C, Ras, MEKK1, MEK3, p38/RK, AP1 signal transduction pathway J. Biol. Chem. 273 1998 24387 24395
42. C. Fathke, L. Wilson, J. Hutter, V. Kapoor, A. Smith, A. Hocking, and F. Isik Contribution of bone marrow-derived cells to skin: collagen deposition and wound repair Stem Cells 22 2004 812 822
43. A. Faurschou, and R. Gniadecki TNF-alpha stimulates Akt by a distinct aPKC-dependent pathway in premalignant keratinocytes Exp. Dermatol. 17 2008 992 997
44. F. Felicetti, M.C. Errico, L. Bottero, P. Segnalini, A. Stoppacciaro, M. Biffoni, N. Felli, G. Mattia, M. Petrini, M.P. Colombo, C. Peschle, and A. Care The promyelocytic leukemia zinc finger-microRNA-221/-222 pathway controls melanoma progression through multiple oncogenic mechanisms Cancer Res. 68 2008 2745 2754
45. N.O. Fortunel, J.A. Hatzfeld, P.A. Rosemary, C. Ferraris, M.N. Monier, V. Haydont, J. Longuet, B. Brethon, B. Lim, I. Castiel, R. Schmidt, and A. Hatzfeld Long-term expansion of human functional epidermal precursor cells: promotion of extensive amplification by low TGF-beta1 concentrations J. Cell Sci. 116 2003 4043 4052
46. E. Fuchs, and V. Horsley More than one way to skin Genes Dev. 22 2008 976 985
47. E. Fuchs, and J.A. Nowak Building epithelial tissues from skin stem cells Cold Spring Harb. Symp. Quant. Biol. 73 2008 333 350
48. L. Gambardella, and Y. Barrandon The multifaceted adult epidermal stem cell Curr. Opin. Cell Biol. 15 2003 771 777
49. A. Gandarillas Epidermal differentiation, apoptosis, and senescence: common pathways? Exp. Gerontol. 35 2000 53 62
50. A. Gandarillas, L.A. Goldsmith, S. Gschmeissner, I.M. Leigh, and F.M. Watt Evidence that apoptosis and terminal differentiation of epidermal keratinocytes are distinct processes Exp. Dermatol. 8 1999 71 79
51. M.J. Gerdes, and S.H. Yuspa The contribution of epidermal stem cells to skin cancer Stem Cell Rev. 1 2005 225 231
52. B.M. Gilfix, and R.L. Eckert Coordinate control by vitamin A of keratin gene expression in human keratinocytes J. Biol. Chem. 260 1985 14026 14029
53. C. Ginestier, M.H. Hur, E. Charafe-Jauffret, F. Monville, J. Dutcher, M. Brown, J. Jacquemier, P. Viens, C.G. Kleer, S. Liu, A. Schott, D. Hayes, D. Birnbaum, M.S. Wicha, and G. Dontu ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome Cell Stem Cell 1 2007 555 567
54. M. Glud, M. Rossing, C. Hother, L. Holst, N. Hastrup, F.C. Nielsen, R. Gniadecki, and K.T. Drzewiecki Downregulation of miR-125b in metastatic cutaneous malignant melanoma Melanoma Res. 20 2010 479 484
55. M. Grachtchouk, J. Pero, S.H. Yang, A.N. Ermilov, L.E. Michael, A. Wang, D. Wilbert, R.M. Patel, J. Ferris, J. Diener, M. Allen, S. Lim, L.J. Syu, M. Verhaegen, and A.A. Dlugosz Basal cell carcinomas in mice arise from hair follicle stem cells and multiple epithelial progenitor populations J. Clin. Invest. 121 2011 1768 1781
56. V. Greco, T. Chen, M. Rendl, M. Schober, H.A. Pasolli, N. Stokes, J. Dela Cruz-Racelis, and E. Fuchs A two-step mechanism for stem cell activation during hair regeneration Cell Stem Cell 4 2009 155 169
57. H. Green The keratinocyte as differentiated cell type Harvey Lect. 74 1980 101 139
58. K.L. Grinnell, and J.R. Bickenbach Skin keratinocytes pre-treated with embryonic stem cell-conditioned medium or BMP4 can be directed to an alternative cell lineage Cell Prolif. 40 2007 685 705
59. K.L. Grinnell, B. Yang, R.L. Eckert, and J.R. Bickenbach De-differentiation of mouse interfollicular keratinocytes by the embryonic transcription factor Oct-4 J. Invest. Dermatol. 40 2006 685 705
60. S. Gupta, and H. Mukhtar Chemoprevention of skin cancer: current status and future prospects Cancer Metastasis Rev. 21 2002 363 380
61. A. Gutierrez-Rivera, A. Pavon-Rodriguez, F. Jimenez-Acosta, E. Poblet, K.M. Braun, P. Cormenzana, J.P. Ciria, R. Larretxea, J.M. Cardenas, and A. Izeta Functional characterization of highly adherent CD34 + keratinocytes isolated from human skin Exp. Dermatol. 19 2010 685 688
62. R.G. Harris, E.L. Herzog, E.M. Bruscia, J.E. Grove, J.S. Van Arnam, and D.S. Krause Lack of a fusion requirement for development of bone marrow-derived epithelia Science 305 2004 90 93
63. V. Horsley, D. O'Carroll, R. Tooze, Y. Ohinata, M. Saitou, T. Obukhanych, M. Nussenzweig, A. Tarakhovsky, and E. Fuchs Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland Cell 126 2006 597 609
64. K. Inoue, N. Aoi, T. Sato, Y. Yamauchi, H. Suga, H. Eto, H. Kato, J. Araki, and K. Yoshimura Differential expression of stem-cell-associated markers in human hair follicle epithelial cells Lab. Invest. 89 2009 844 856
65. K.B. Jensen, C.A. Collins, E. Nascimento, D.W. Tan, M. Frye, S. Itami, and F.M. Watt Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis Cell Stem Cell 4 2009 427 439
66. K.B. Jensen, and F.M. Watt Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence Proc. Natl. Acad. Sci. U. S. A. 103 2006 11958 11963
67. U.B. Jensen, X. Yan, C. Triel, S.H. Woo, R. Christensen, and D.M. Owens A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus J. Cell Sci. 121 2008 609 617
68. P.H. Jones, B.D. Simons, and F.M. Watt Sic transit gloria: farewell to the epidermal transit amplifying cell? Cell Stem Cell 1 2007 371 381
69. P.H. Jones, and F.M. Watt Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression Cell 73 1993 713 724
70. T. Kangsamaksin, H.J. Park, C.S. Trempus, and R.J. Morris A perspective on murine keratinocyte stem cells as targets of chemically induced skin cancer Mol. Carcinog. 46 2007 579 584
71. J. Legg, U.B. Jensen, S. Broad, I. Leigh, and F.M. Watt Role of melanoma chondroitin sulphate proteoglycan in patterning stem cells in human interfollicular epidermis Development 130 2003 6049 6063
72. A.M. Lena, R. Shalom-Feuerstein, P. Rivetti di Val Cervo, D. Aberdam, R.A. Knight, G. Melino, and E. Candi miR-203 represses 'stemness' by repressing DeltaNp63 Cell Death Differ. 15 2008 1187 1195
73. V. Levy, C. Lindon, Y. Zheng, B.D. Harfe, and B.A. Morgan Epidermal stem cells arise from the hair follicle after wounding FASEB J. 21 2007 1358 1366
74. A. Li, P.J. Simmons, and P. Kaur Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype Proc. Natl. Acad. Sci. U. S. A. 95 1998 3902 3907
75. C. Li, S. Chi, and J. Xie Hedgehog signaling in skin cancers Cell. Signal. 23 2011 1235 1243
76. L. Li, M. Fukunaga-Kalabis, H. Yu, X. Xu, J. Kong, J.T. Lee, and M. Herlyn Human dermal stem cells differentiate into functional epidermal melanocytes J. Cell Sci. 123 2010 853 860
77. S. Lowell, P. Jones, I. Le Roux, J. Dunne, and F.M. Watt Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters Curr. Biol. 10 2000 491 500
78. W.E. Lowry, C. Blanpain, J.A. Nowak, G. Guasch, L. Lewis, and E. Fuchs Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells Genes Dev. 19 2005 1596 1611
79. S. Lyle, M. Christofidou-Solomidou, Y. Liu, D.E. Elder, S. Albelda, and G. Cotsarelis The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells J. Cell Sci. 111 Pt 21 1998 3179 3188
80. A. Marconi, K. Dallaglio, R. Lotti, C. Vaschieri, F. Truzzi, F. Fantini, and C. Pincelli Survivin identifies keratinocyte stem cells and is downregulated by anti-beta1 integrin during anoikis Stem Cells 25 2007 149 155
81. A.N. Mardaryev, M.I. Ahmed, N.V. Vlahov, M.Y. Fessing, J.H. Gill, A.A. Sharov, and N.V. Botchkareva Micro-RNA-31 controls hair cycle-associated changes in gene expression programs of the skin and hair follicle FASEB J. 24 2010 3869 3881
82. C. Margadant, R.A. Charafeddine, and A. Sonnenberg Unique and redundant functions of integrins in the epidermis FASEB J. 24 2010 4133 4152
83. M. Matic A subpopulation of human basal keratinocytes has a low/negative MHC class I expression Hum. Immunol. 66 2005 962 968
84. B.J. Merrill, U. Gat, R. DasGupta, and E. Fuchs Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin Genes Dev. 15 2001 1688 1705
85. M. Michel, N. Torok, M.J. Godbout, M. Lussier, P. Gaudreau, A. Royal, and L. Germain Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage J. Cell Sci. 109 Pt 5 1996 1017 1028
86. R.J. Morris, S.M. Fischer, and T.J. Slaga Evidence that the centrally and peripherally located cells in the murine epidermal proliferative unit are two distinct cell populations J. Invest. Dermatol. 84 1985 277 281
87. R.J. Morris, S.M. Fischer, and T.J. Slaga Evidence that a slowly cycling subpopulation of adult murine epidermal cells retains carcinogen Cancer Res. 46 1986 3061 3066
88. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, and G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nat. Biotechnol. 22 2004 411 417
89. R.J. Morris, K.A. Tryson, and K.Q. Wu Evidence that the epidermal targets of carcinogen action are found in the interfollicular epidermis of infundibulum as well as in the hair follicles Cancer Res. 60 2000 226 229
90. D.W. Mueller, and A.K. Bosserhoff MicroRNA miR-196a controls melanoma-associated genes by regulating HOX-C8 expression Int. J. Cancer 129 2011 1064 1074
91. S. Muffler, H.J. Stark, M. Amoros, B. Falkowska-Hansen, K. Boehnke, H.J. Buhring, A. Marme, J.R. Bickenbach, and P. Boukamp A stable niche supports long-term maintenance of human epidermal stem cells in organotypic cultures Stem Cells 26 2008 2506 2515
92. P. Myung, and M. Ito Dissecting the bulge in hair regeneration J. Clin. Invest. 122 2012 448 454
93. M.C. Myzak, and R.H. Dashwood Histone deacetylases as targets for dietary cancer preventive agents: lessons learned with butyrate, diallyl disulfide, and sulforaphane Curr. Drug Targets 7 2006 443 452
94. Z. Nemes, and P.M. Steinert Bricks and mortar of the epidermal barrier Exp. Mol. Med. 31 1999 5 19
95. C. Niemann, D.M. Owens, J. Hulsken, W. Birchmeier, and F.M. Watt Expression of DeltaNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours Development 129 2002 95 109
96. J.G. Nijhof, K.M. Braun, A. Giangreco, C. van Pelt, H. Kawamoto, R.L. Boyd, R. Willemze, L.H. Mullenders, F.M. Watt, F.R. de Gruijl, and W. van Ewijk The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells Development 133 2006 3027 3037
97. M. Ohyama Hair follicle bulge: a fascinating reservoir of epithelial stem cells J. Dermatol. Sci. 46 2007 81 89
98. M. Ohyama, A. Terunuma, C.L. Tock, M.F. Radonovich, C.A. Pise-Masison, S.B. Hopping, J.N. Brady, M.C. Udey, and J.C. Vogel Characterization and isolation of stem cell-enriched human hair follicle bulge cells J. Clin. Invest. 116 2006 249 260
99. M. Ohyama, J.C. Vogel, and M. Amagai Gene ontology analysis of human hair follicle bulge molecular signature J. Dermatol. Sci. 45 2007 147 150
100. G.K. Patel, C.L. Yee, A. Terunuma, W.G. Telford, N. Voong, S.H. Yuspa, and J.C. Vogel Identification and characterization of tumor-initiating cells in human primary cutaneous squamous cell carcinoma J. Invest. Dermatol. 132 2012 401 409
101. M.E. Prince, R. Sivanandan, A. Kaczorowski, G.T. Wolf, M.J. Kaplan, P. Dalerba, I.L. Weissman, M.F. Clarke, and L.E. Ailles Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc. Natl. Acad. Sci. U. S. A. 104 2007 973 978
102. T. Reya, and H. Clevers Wnt signalling in stem cells and cancer Nature 434 2005 843 850
103. I. Satzger, A. Mattern, U. Kuettler, D. Weinspach, B. Voelker, A. Kapp, and R. Gutzmer MicroRNA-15b represents an independent prognostic parameter and is correlated with tumor cell proliferation and apoptosis in malignant melanoma Int. J. Cancer 126 2010 2553 2562
104. R. Schmidt-Ullrich, and R. Paus Molecular principles of hair follicle induction and morphogenesis Bioessays 27 2005 247 261
105. M.R. Schneider, R. Schmidt-Ullrich, and R. Paus The hair follicle as a dynamic miniorgan Curr. Biol. 19 2009 R132 R142
106. M. Schober, and E. Fuchs Tumor-initiating stem cells of squamous cell carcinomas and their control by TGF-beta and integrin/focal adhesion kinase (FAK) signaling Proc. Natl. Acad. Sci. U. S. A. 108 2011 10544 10549
107. J. Schultz, P. Lorenz, G. Gross, S. Ibrahim, and M. Kunz MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth Cell Res. 18 2008 549 557
108. M.F. Segura, D. Hanniford, S. Menendez, L. Reavie, X. Zou, S. Alvarez-Diaz, J. Zakrzewski, E. Blochin, A. Rose, D. Bogunovic, D. Polsky, J. Wei, P. Lee, I. Belitskaya-Levy, N. Bhardwaj, I. Osman, and E. Hernando Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor Proc. Natl. Acad. Sci. U. S. A. 106 2009 1814 1819
109. K. Sellheyer Basal cell carcinoma: cell of origin, cancer stem cell hypothesis and stem cell markers Br. J. Dermatol. 164 2011 696 711
110. M. Senoo, F. Pinto, C.P. Crum, and F. McKeon p63 is essential for the proliferative potential of stem cells in stratified epithelia Cell 129 2007 523 536
111. A. Singh, H. Park, T. Kangsamaksin, A. Singh, N. Readio, and R.J. Morris Keratinocyte stem cells and the targets for nonmelanoma skin cancer Photochem. Photobiol. 2012 (Electronic publication ahead of print)
112. H.J. Snippert, A. Haegebarth, M. Kasper, V. Jaks, J.H. van Es, N. Barker, M. van de Wetering, M. van den Born, H. Begthel, R.G. Vries, D.E. Stange, R. Toftgard, and H. Clevers Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin Science 327 2010 1385 1389
113. E. Sonkoly, T. Wei, L.E. Pavez, H. Suzuki, M. Kato, H. Torma, M. Stahle, and A. Pivarcsi Protein kinase C-dependent upregulation of miR-203 induces the differentiation of human keratinocytes J. Invest. Dermatol. 130 2010 124 134
114. B. St-Jacques, H.R. Dassule, I. Karavanova, V.A. Botchkarev, J. Li, P.S. Danielian, J.A. McMahon, P.M. Lewis, R. Paus, and A.P. McMahon Sonic hedgehog signaling is essential for hair development Curr. Biol. 8 1998 1058 1068
115. X. Su, D. Chakravarti, M.S. Cho, L. Liu, Y.J. Gi, Y.L. Lin, M.L. Leung, A. El-Naggar, C.J. Creighton, M.B. Suraokar, I. Wistuba, and E.R. Flores TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs Nature 467 2010 986 990
116. K. Tanese, M. Fukuma, T. Yamada, T. Mori, T. Yoshikawa, W. Watanabe, A. Ishiko, M. Amagai, T. Nishikawa, and M. Sakamoto G-protein-coupled receptor GPR49 is up-regulated in basal cell carcinoma and promotes cell proliferation and tumor formation Am. J. Pathol. 173 2008 835 843
117. H. Tani, R.J. Morris, and P. Kaur Enrichment for murine keratinocyte stem cells based on cell surface phenotype Proc. Natl. Acad. Sci. U. S. A. 97 2000 10960 10965
118. C.S. Trempus, H. Dang, M.M. Humble, S.J. Wei, M.J. Gerdes, R.J. Morris, C.D. Bortner, G. Cotsarelis, and R.W. Tennant Comprehensive microarray transcriptome profiling of CD34-enriched mouse keratinocyte stem cells J. Invest. Dermatol. 127 2007 2904 2907
119. C.S. Trempus, R.J. Morris, C.D. Bortner, G. Cotsarelis, R.S. Faircloth, J.M. Reece, and R.W. Tennant Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34 J. Invest. Dermatol. 120 2003 501 511
120. D. Tsuruta, T. Hashimoto, K.J. Hamill, and J.C. Jones Hemidesmosomes and focal contact proteins: functions and cross-talk in keratinocytes, bullous diseases and wound healing J. Dermatol. Sci. 62 2011 1 7
121. H. Wan, M.G. Stone, C. Simpson, L.E. Reynolds, J.F. Marshall, I.R. Hart, K.M. Hodivala-Dilke, and R.A. Eady Desmosomal proteins, including desmoglein 3, serve as novel negative markers for epidermal stem cell-containing population of keratinocytes J. Cell Sci. 116 2003 4239 4248
122. H. Wan, M. Yuan, C. Simpson, K. Allen, F.N. Gavins, M.S. Ikram, S. Basu, N. Baksh, E.A. O'Toole, and I.R. Hart Stem/progenitor cell-like properties of desmoglein 3dim cells in primary and immortalized keratinocyte lines Stem Cells 25 2007 1286 1297
123. G.Y. Wang, J. Wang, M.L. Mancianti, and E.H. Epstein Jr. Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/-) mice Cancer Cell 19 2011 114 124
124. L.C. Wang, Z.Y. Liu, L. Gambardella, A. Delacour, R. Shapiro, J. Yang, I. Sizing, P. Rayhorn, E.A. Garber, C.D. Benjamin, K.P. Williams, F.R. Taylor, Y. Barrandon, L. Ling, and L.C. Burkly Regular articles: conditional disruption of hedgehog signaling pathway defines its critical role in hair development and regeneration J. Invest. Dermatol. 114 2000 901 908
125. F.M. Watt The stem cell compartment in human interfollicular epidermis J. Dermatol. Sci. 28 2002 173 180
126. F.M. Watt, S. Estrach, and C.A. Ambler Epidermal Notch signalling: differentiation, cancer and adhesion Curr. Opin. Cell Biol. 20 2008 171 179
127. F.M. Watt, and K.B. Jensen Epidermal stem cell diversity and quiescence EMBO Mol. Med. 1 2009 260 267
128. A. Webb, and P. Kaur Epidermal stem cells Front. Biosci. 11 2006 1031 1041
129. A. Webb, A. Li, and P. Kaur Location and phenotype of human adult keratinocyte stem cells of the skin Differentiation 72 2004 387 395
130. T. Wei, K. Orfanidis, N. Xu, P. Janson, M. Stahle, A. Pivarcsi, and E. Sonkoly The expression of microRNA-203 during human skin morphogenesis Exp. Dermatol. 19 2010 854 856
131. A.C. White, K. Tran, J. Khuu, C. Dang, Y. Cui, S.W. Binder, and W.E. Lowry Defining the origins of Ras/p53-mediated squamous cell carcinoma Proc. Natl. Acad. Sci. U. S. A. 108 2011 7425 7430
132. E. Wienholds, W.P. Kloosterman, E. Miska, E. Alvarez-Saavedra, E. Berezikov, E. De Bruijn, H.R. Horvitz, S. Kauppinen, and R.H. Plasterk MicroRNA expression in zebrafish embryonic development Science 309 2005 310 311
133. W.M. Woo, and A.E. Oro SnapShot: hair follicle stem cells Cell 146 2011 334
134. Y. Wu, L. Chen, P.G. Scott, and E.E. Tredget Mesenchymal stem cells enhance wound healing through differentiation and angiogenesis Stem Cells 25 2007 2648 2659
135. Y. Wu, R.C. Zhao, and E.E. Tredget Concise review: bone marrow-derived stem/progenitor cells in cutaneous repair and regeneration Stem Cells 28 2010 905 915
136. R. Yi, and E. Fuchs MicroRNA-mediated control in the skin Cell Death Differ. 17 2010 229 235
137. R. Yi, H.A. Pasolli, M. Landthaler, M. Hafner, T. Ojo, R. Sheridan, C. Sander, D. O'Carroll, M. Stoffel, T. Tuschl, and E. Fuchs DGCR8-dependent microRNA biogenesis is essential for skin development Proc. Natl. Acad. Sci. U. S. A. 106 2009 498 502
138. R. Yi, M.N. Poy, M. Stoffel, and E. Fuchs A skin microRNA promotes differentiation by repressing 'stemness' Nature 452 2008 225 229
139. K.K. Youssef, K.A. Van, G. Lapouge, B. Beck, C. Michaux, Y. Achouri, P.A. Sotiropoulou, and C. Blanpain Identification of the cell lineage at the origin of basal cell carcinoma Nat. Cell Biol. 12 2010 299 305
140. H. Yu, S.M. Kumar, A.V. Kossenkov, L. Showe, and X. Xu Stem cells with neural crest characteristics derived from the bulge region of cultured human hair follicles J. Invest. Dermatol. 130 2010 1227 1236
141. Y. Yu, A. Flint, E.L. Dvorin, and J. Bischoff AC133-2, a novel isoform of human AC133 stem cell antigen J. Biol. Chem. 277 2002 20711 20716
142. L. Zhang, N. Stokes, L. Polak, and E. Fuchs Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment Cell Stem Cell 8 2011 294 308
143. W. Zhang, E. Remenyik, D. Zelterman, D.E. Brash, and N.M. Wikonkal Escaping the stem cell compartment: sustained UVB exposure allows p53-mutant keratinocytes to colonize adjacent epidermal proliferating units without incurring additional mutations Proc. Natl. Acad. Sci. U. S. A. 98 2001 13948 13953
144. P. Zhou, C. Byrne, J. Jacobs, and E. Fuchs Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate Genes Dev. 9 1995 700 713