Epidermal stem cells: an update on their potential in regenerative medicine

Bibliography

• Aasen T, Raya A, Barrero MJ, et al. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008;26(11):1276-84
   PubMed Web of Science ®Google Scholar
• Cotsarelis G, Sun TT, Lavker RM. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 1990;61(7):1329-37
   PubMed Web of Science ®Google Scholar
• Tumbar T, Guasch G, Greco V, et al. Defining the epithelial stem cell niche in skin. Science 2004;303(5656):359-63
   PubMed Web of Science ®Google Scholar
• Mackenzie IC. Retroviral transduction of murine epidermal stem cells demonstrates clonal units of epidermal structure. J Invest Dermatol 1997;109(3):377-83
   PubMed Web of Science ®Google Scholar
• Ito M, Yang Z, Andl T, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007;447(7142):316-20
   PubMed Web of Science ®Google Scholar
• Kaur P. Interfollicular epidermal stem cells: identification, challenges, potential. J Invest Dermatol 2006;126(7):1450-8
   PubMed Web of Science ®Google Scholar
• Jones PH, Watt FM. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 1993;73(4):713-24
   PubMed Web of Science ®Google Scholar
• Horsley V, O'Carroll D, Tooze R, et al. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 2006;126(3):597-609
   PubMed Web of Science ®Google Scholar
• Jensen UB, Yan X, Triel C, et al. A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus. J Cell Sci 2008;121(Pt 5):609-17
   PubMed Web of Science ®Google Scholar
• Morris RJ, Liu Y, Marles L, et al. Capturing and profiling adult hair follicle stem cells. Nat Biotechnol 2004;22(4):411-17
   PubMed Web of Science ®Google Scholar
• Ito M, Liu Y, Yang Z, et al. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat Med 2005;11(12):1351-4
   PubMed Web of Science ®Google Scholar
• Silva-Vargas V, Lo Celso C, Giangreco A, et al. Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev Cell 2005;9(1):121-31
   PubMed Web of Science ®Google Scholar
• Nguyen H, Merrill BJ, Polak L, et al. Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat Genet 2009;41(10):1068-75
   PubMed Web of Science ®Google Scholar
• Oshima H, Rochat A, Kedzia C, et al. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 2001;104(2):233-45
   PubMed Web of Science ®Google Scholar
• Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche. Cell 2004;116(6):769-78
   PubMed Web of Science ®Google Scholar
• Cotsarelis G. Epithelial stem cells: a folliculocentric view. J Invest Dermatol 2006;126(7):1459-68
   PubMed Web of Science ®Google Scholar
• Trempus CS, Morris RJ, Bortner CD, et al. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J Invest Dermatol 2003;120(4):501-11
   PubMed Web of Science ®Google Scholar
• Blanpain C, Lowry WE, Geoghegan A, et al. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 2004;118(5):635-48
   PubMed Web of Science ®Google Scholar
• Tani H, Morris RJ, Kaur P. Enrichment for murine keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci USA 2000;97(20):10960-5
   PubMed Web of Science ®Google Scholar
• Jaks V, Barker N, Kasper M, et al. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 2008;40(11):1291-9
   PubMed Web of Science ®Google Scholar
• Levy V, Lindon C, Harfe BD, Morgan BA. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev Cell 2005;9(6):855-61
   PubMed Web of Science ®Google Scholar
• Levy V, Lindon C, Zheng Y, et al. Epidermal stem cells arise from the hair follicle after wounding. FASEB J 2007;21(7):1358-66
   PubMed Web of Science ®Google Scholar
• Nowak JA, Polak L, Pasolli HA, Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 2008;3(1):33-43
   PubMed Web of Science ®Google Scholar
• Petersson M, Brylka H, Kraus A, et al. TCF/lef1 activity controls establishment of diverse stem and progenitor compartments in mouse epidermis. EMBO J 2011;30(15):3004-18
   PubMed Web of Science ®Google Scholar
• Nijhof JG, Braun KM, Giangreco A, et al. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 2006;133(15):3027-37
   PubMed Web of Science ®Google Scholar
• Snippert HJ, Haegebarth A, Kasper M, et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 2010;327(5971):1385-9
   PubMed Web of Science ®Google Scholar
• Jensen KB, Collins CA, Nascimento E, et al. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 2009;4(5):427-39
   PubMed Web of Science ®Google Scholar
• Brownell I, Guevara E, Bai CB, et al. Nerve-derived sonic hedgehog defines a niche for hair follicle stem cells capable of becoming epidermal stem cells. Cell Stem Cell 2011;8(5):552-65
   PubMed Web of Science ®Google Scholar
• Yu H, Fang D, Kumar SM, et al. Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 2006;168(6):1879-88
   PubMed Web of Science ®Google Scholar
• Uchugonova A, Duong J, Zhang N, et al. The bulge area is the origin of nestin-expressing pluripotent stem cells of the hair follicle. J Cell Biochem 2011;112(8):2046-50
   PubMed Web of Science ®Google Scholar
• Mothe AJ, Zahir T, Santaguida C, et al. Neural stem/progenitor cells from the adult human spinal cord are multipotent and self-renewing and differentiate after transplantation. PLoS One 2011;6(11):e27079
   PubMed Web of Science ®Google Scholar
• Kadam SS, Bhonde RR. Islet neogenesis from the constitutively nestin expressing human umbilical cord matrix derived mesenchymal stem cells. Islets 2010;2(2):112-20
   PubMed Web of Science ®Google Scholar
• Zulewski H, Abraham EJ, Gerlach MJ, et al. Multipotential nestin-positive stem cells isolated from adult pancreatic islets differentiate ex vivo into pancreatic endocrine, exocrine, and hepatic phenotypes. Diabetes 2001;50(3):521-33
   PubMed Web of Science ®Google Scholar
• Amoh Y, Li L, Katsuoka K, et al. Multipotent nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc Natl Acad Sci USA 2005;102(15):5530-4
   PubMed Web of Science ®Google Scholar
• Amoh Y, Li L, Campillo R, et al. Implanted hair follicle stem cells form Schwann cells that support repair of severed peripheral nerves. Proc Natl Acad Sci USA 2005;102(49):17734-8
   PubMed Web of Science ®Google Scholar
• Amoh Y, Katsuoka K, Hoffman RM. The advantages of hair follicle pluripotent stem cells over embryonic stem cells and induced pluripotent stem cells for regenerative medicine. J Dermatol Sci 2010;60(3):131-7
   PubMed Web of Science ®Google Scholar
• Clark RA, Yamanaka K, Bai M, et al. Human skin cells support thymus-independent T cell development. J Clin Invest 2005;115(11):3239-49
   PubMed Web of Science ®Google Scholar
• Liang L, Bickenbach JR. Somatic epidermal stem cells can produce multiple cell lineages during development. Stem Cells 2002;20(1):21-31
   PubMed Web of Science ®Google Scholar
• Li J, Greco V, Guasch G, et al. Mice cloned from skin cells. Proc Natl Acad Sci USA 2007;104(8):2738-43
   PubMed Web of Science ®Google Scholar
• Bull JJ, Muller-Rover S, Patel SV, et al. Contrasting localization of c-Myc with other Myc superfamily transcription factors in the human hair follicle and during the hair growth cycle. J Invest Dermatol 2001;116(4):617-22
   PubMed Web of Science ®Google Scholar
• Barajon I, Rumio C, Donetti E, et al. Pattern of expression of c-Myc, Max and Bin1 in human anagen hair follicles. Br J Dermatol 2001;144(6):1193-203
   PubMed Web of Science ®Google Scholar
• Gandarillas A, Watt FM. c-Myc promotes differentiation of human epidermal stem cells. Genes Dev 1997;11(21):2869-82
   PubMed Web of Science ®Google Scholar
• Gebhardt A, Frye M, Herold S, et al. Myc regulates keratinocyte adhesion and differentiation via complex formation with Miz1. J Cell Biol 2006;172(1):139-49
   PubMed Web of Science ®Google Scholar
• Segre JA, Bauer C, Fuchs E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat Genet 1999;22(4):356-60
   PubMed Web of Science ®Google Scholar
• Aoi T, Yae K, Nakagawa M, et al. Generation of pluripotent stem cells from adult mouse liver and stomach cells. Science 2008;321(5889):699-702
   PubMed Web of Science ®Google Scholar
• Green H, Kehinde O, Thomas J. Growth of cultured human epidermal cells into multiple epithelia suitable for grafting. Proc Natl Acad Sci USA 1979;76(11):5665-8
   PubMed Web of Science ®Google Scholar
• Rheinwald JG, Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 1975;6(3):331-43
   PubMed Web of Science ®Google Scholar
• Matic M. A subpopulation of human basal keratinocytes has a low/negative MHC class I expression. Hum Immunol 2005;66(9):962-8
   PubMed Web of Science ®Google Scholar
• Christoph T, Muller-Rover S, Audring H, et al. The human hair follicle immune system: cellular composition and immune privilege. Br J Dermatol 2000;142(5):862-73
   PubMed Web of Science ®Google Scholar
• Mavilio F, Pellegrini G, Ferrari S, et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat Med 2006;12(12):1397-402
   PubMed Web of Science ®Google Scholar
• Novak A, Shtrichman R, Germanguz I, et al. Enhanced reprogramming and cardiac differentiation of human keratinocytes derived from plucked hair follicles, using a single excisable lentivirus. Cell Reprogram 2010;12(6):665-78
   PubMed Web of Science ®Google Scholar
• Amoh Y, Aki R, Hamada Y, et al. Nestin-positive hair follicle pluripotent stem cells can promote regeneration of impinged peripheral nerve injury. J Dermatol 2012;39(1):33-8
   PubMed Web of Science ®Google Scholar
• Aden N, Nuttall A, Shiwen X, et al. Epithelial cells promote fibroblast activation via IL-1alpha in systemic sclerosis. J Invest Dermatol 2010;130(9):2191-200
   PubMed Web of Science ®Google Scholar
• Jiao C, Bronner S, Mercer KL, et al. Epidermal cells accelerate the restoration of the blood flow in diabetic ischemic limbs. J Cell Sci 2004;117(Pt 7):1055-63
   PubMed Web of Science ®Google Scholar
• Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007;131(5):861-72
   PubMed Web of Science ®Google Scholar
• Hanna J, Markoulaki S, Schorderet P, et al. Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 2008;133(2):250-64
   PubMed Web of Science ®Google Scholar
• Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007;318(5858):1917-20
   PubMed Web of Science ®Google Scholar
• Hochedlinger K, Plath K. Epigenetic reprogramming and induced pluripotency. Development 2009;136(4):509-23
   PubMed Web of Science ®Google Scholar
• Zhou Q, Brown J, Kanarek A, et al. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 2008;455(7213):627-32
   PubMed Web of Science ®Google Scholar
• Forsberg M, Carlen M, Meletis K, et al. Efficient reprogramming of adult neural stem cells to monocytes by ectopic expression of a single gene. Proc Natl Acad Sci USA 2010;107(33):14657-61
   PubMed Web of Science ®Google Scholar
• Ieda M, Fu JD, Delgado-Olguin P, et al. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 2010;142(3):375-86
   PubMed Web of Science ®Google Scholar
• Takeuchi JK, Bruneau BG. Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 2009;459(7247):708-11
   PubMed Web of Science ®Google Scholar
• Caiazzo M, Dell'Anno MT, Dvoretskova E, et al. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011;476(7359):224-7
   PubMed Web of Science ®Google Scholar
• Pfisterer U, Kirkeby A, Torper O, et al. Direct conversion of human fibroblasts to dopaminergic neurons. Proc Natl Acad Sci USA 2011;108(25):10343-8
   PubMed Web of Science ®Google Scholar
• Li SC, Jin Y, Loudon WG, et al. Increase developmental plasticity of human keratinocytes with gene suppression. Proc Natl Acad Sci USA 2011;108(31):12793-8
   PubMed Web of Science ®Google Scholar
• Vierbuchen T, Wernig M. Direct lineage conversions: unnatural but useful? Nat Biotechnol 2011;29(10):892-907
   PubMed Web of Science ®Google Scholar
• Davidson EH. Emerging properties of animal gene regulatory networks. Nature 2010;468(7326):911-20
   PubMed Web of Science ®Google Scholar
• Mauda-Havakuk M, Litichever N, Chernichovski E, et al. Ectopic PDX-1 expression directly reprograms human keratinocytes along pancreatic insulin-producing cells fate. PLoS One 2011;6(10):e26298
   Google Scholar
• Han W, Chen M, Li M, et al. Acclimatized induction reveals the multipotency of adult human undifferentiated keratinocytes. Cell Reprogram 2010;12(3):283-94
   PubMed Web of Science ®Google Scholar
• da Silva-Diz V, Sole-Sanchez S, Valdes-Gutierrez A, et al. Progeny of Lgr5-expressing hair follicle stem cell contributes to papillomavirus-induced tumor development in epidermis. Oncogene 2012; doi: 10.1038/onc.2012.375
   PubMed Web of Science ®Google Scholar
• Kasper M, Jaks V, Are A, et al. Wounding enhances epidermal tumorigenesis by recruiting hair follicle keratinocytes. Proc Natl Acad Sci USA 2011;108(10):4099-104
   PubMed Web of Science ®Google Scholar
• Youssef KK, Van Keymeulen A, Lapouge G, et al. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 2010;12(3):299-305
   PubMed Web of Science ®Google Scholar
• Wong SY, Reiter JF. Wounding mobilizes hair follicle stem cells to form tumors. Proc Natl Acad Sci USA 2011;108(10):4093-8
   PubMed Web of Science ®Google Scholar
• Vidal VP, Chaboissier MC, Lutzkendorf S, et al. Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr Biol 2005;15(15):1340-51
   PubMed Web of Science ®Google Scholar
• Vidal VP, Ortonne N, Schedl A. SOX9 expression is a general marker of basal cell carcinoma and adnexal-related neoplasms. J Cutan Pathol 2008;35(4):373-9
   PubMed Web of Science ®Google Scholar
• Schlegelmilch K, Mohseni M, Kirak O, et al. Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011;144(5):782-95
   PubMed Web of Science ®Google Scholar
• Chan EF, Gat U, McNiff JM, Fuchs E. A common human skin tumour is caused by activating mutations in beta-catenin. Nat Genet 1999;21(4):410-13
   PubMed Web of Science ®Google Scholar
• Takeda H, Lyle S, Lazar AJ, et al. Human sebaceous tumors harbor inactivating mutations in LEF1. Nat Med 2006;12(4):395-7
   PubMed Web of Science ®Google Scholar
• Lo Celso C, Prowse DM, Watt FM. Transient activation of beta-catenin signalling in adult mouse epidermis is sufficient to induce new hair follicles but continuous activation is required to maintain hair follicle tumours. Development 2004;131(8):1787-99
   PubMed Web of Science ®Google Scholar
• Niemann C, Owens DM, Schettina P, Watt FM. Dual role of inactivating Lef1 mutations in epidermis: tumor promotion and specification of tumor type. Cancer Res 2007;67(7):2916-21
   PubMed Web of Science ®Google Scholar
• Malanchi I, Peinado H, Kassen D, et al. Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature 2008;452(7187):650-3
   PubMed Web of Science ®Google Scholar
• Arwert EN, Hoste E, Watt FM. Epithelial stem cells, wound healing and cancer. Nat Rev Cancer 2012;12(3):170-80
   PubMed Web of Science ®Google Scholar
• Baker CM, Verstuyf A, Jensen KB, Watt FM. Differential sensitivity of epidermal cell subpopulations to beta-catenin-induced ectopic hair follicle formation. Dev Biol 2010;343(1-2):40-50
   PubMed Web of Science ®Google Scholar
• Lowry WE, Blanpain C, Nowak JA, et al. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev 2005;19(13):1596-611
   PubMed Web of Science ®Google Scholar
• Silva-Vargas V, Lo Celso C, Giangreco A, et al. Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev Cell 2005;9(1):121-31
   PubMed Web of Science ®Google Scholar
• Hutchin ME, Kariapper MS, Grachtchouk M, et al. Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle. Genes Dev 2005;19(2):214-23
   PubMed Web of Science ®Google Scholar
• Oro AE, Higgins KM, Hu Z, et al. Basal cell carcinomas in mice overexpressing sonic hedgehog. Science 1997;276(5313):817-21
   PubMed Web of Science ®Google Scholar
• Xie J, Murone M, Luoh SM, et al. Activating Smoothened mutations in sporadic basal-cell carcinoma. Nature 1998;391(6662):90-2
   PubMed Web of Science ®Google Scholar
• Gailani MR, Stahle-Backdahl M, Leffell DJ, et al. The role of the human homologue of Drosophila patched in sporadic basal cell carcinomas. Nat Genet 1996;14(1):78-81
   PubMed Web of Science ®Google Scholar
• Hahn H, Wicking C, Zaphiropoulous PG, et al. Mutations of the human homolog of Drosophila patched in the nevoid basal cell carcinoma syndrome. Cell 1996;85(6):841-51
   PubMed Web of Science ®Google Scholar
• Dahmane N, Lee J, Robins P, et al. Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours. Nature 1997;389(6653):876-81
   PubMed Web of Science ®Google Scholar
• Unden AB, Zaphiropoulos PG, Bruce K, et al. Human patched (PTCH) mRNA is overexpressed consistently in tumor cells of both familial and sporadic basal cell carcinoma. Cancer Res 1997;57(12):2336-40
   PubMed Web of Science ®Google Scholar
• Grachtchouk M, Mo R, Yu S, et al. Basal cell carcinomas in mice overexpressing Gli2 in skin. Nat Genet 2000;24(3):216-17
   PubMed Web of Science ®Google Scholar
• Nilsson M, Unden AB, Krause D, et al. Induction of basal cell carcinomas and trichoepitheliomas in mice overexpressing GLI-1. Proc Natl Acad Sci USA 2000;97(7):3438-43
   PubMed Web of Science ®Google Scholar
• Sheng H, Goich S, Wang A, et al. Dissecting the oncogenic potential of Gli2: deletion of an NH(2)-terminal fragment alters skin tumor phenotype. Cancer Res 2002;62(18):5308-16
   PubMed Web of Science ®Google Scholar
• Wang GY, Wang J, Mancianti ML, Epstein EH Jr. Basal cell carcinomas arise from hair follicle stem cells in Ptch1(+/-) mice. Cancer Cell 2011;19(1):114-24
   PubMed Web of Science ®Google Scholar
• Natoli G. Maintaining cell identity through global control of genomic organization. Immunity 2010;33(1):12-24
   PubMed Web of Science ®Google Scholar
• Yan X, Owens DM. The skin: a home to multiple classes of epithelial progenitor cells. Stem Cell Rev 2008;4(2):113-18
   PubMed Web of Science ®Google Scholar