Keratinocyte stem cells: Friends and foes

Journal of Cellular Physiology

Volumn 225, Issue 2, 2010, Pages 310-315

  Pincelli, Carlo ^a   Marconi, Alessandra ^a  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT STEM CELL; APOPTOSIS; CELL DIFFERENTIATION; CELL FATE; CELL REGENERATION; EPIDERMIS; HAIR FOLLICLE; HUMAN; KERATINOCYTE; NONHUMAN; PRIORITY JOURNAL; SHORT SURVEY; SKIN CANCER; STEM CELL; ANIMAL; CYTOLOGY; PATHOLOGY; PHYSIOLOGY; SKIN TUMOR;

BIOLOGICAL PRODUCT;

ANIMALS; APOPTOSIS; BIOLOGICAL PRODUCTS; CELL DIFFERENTIATION; HUMANS; KERATINOCYTES; SKIN NEOPLASMS; STEM CELLS;

EID: 77956533697     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22275     Document Type: Short Survey

References (77)

1. Alonso L, Fuchs E. 2006. The hair cycle. J Cell Sci 119:391-393.
2. Barrandon Y, Green H. 1987. Three clonal types of keratinocyte with different capacities for multiplication. Proc Natl Acad Sci 84:2302-2306.
3. Blanpain C, Fuchs E. 2009. Epidermal homeostasis: A balancing act of stem cells in the skin. Nat Rev Mol Cell Biol 10:207-217.
4. 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.
5. Botchkarev VA, Yaar M, Peters EM, Raychaudhuri SP, Botchkareva NV, Marconi A, Raychaudhuri SK, Paus R, Pincelli C. 2006. Neurotrophins in skin biology and pathology. J Invest Dermatol 126:1719-1727.
6. Braun KM, Niemann C, Jensen UB, Sundberg JP, 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. (Pubitemid 37369682)
7. Chao DL, Eck JT, Brash DE, Maley CC, Luebeck EG. 2008. Preneoplastic lesion growth driven by the death of adjacent normal stem cells. Proc Natl Acad Sci USA 105:15034-15039.
8. Charruyer A, Barland CO, Yue L, Wessendorf HB, Lu Y, Lawrence HJ, Mancianti ML, Ghadially R. 2009. Transit-amplifying cell frequency and cell cycle kinetics are altered in aged epidermis. J Invest Dermatol 129:2574-2583.
9. Chiarugi P, Giannoni E. 2008. Anoikis: A necessary death program for anchorage-dependent cell. Biochem Pharmacol 76:1352-1364.
10. Clayton E, Doupé DP, Klein AM, Winton DJ, Simons BD, Jones PH. 2007. A single type of progenitor cell maintains normal epidermis. Nature 446:185-189. (Pubitemid 46398664)
11. Coolen NA, Verkerk M, Reijnen L, Vlig M, van den Bogaerdt AJ, Breetveld M, Gibbs S, Middelkoop E, Ulrich MM. 2007. Culture of keratinocytes for transplantation without the need of feeder layer cells. Cell Transplant 16:649-661. (Pubitemid 351448279)
12. Cotsarelis G. 2006. Gene expression profiling gets to the root of human hair follicle stem cells. J Clin Invest 116:19-22. (Pubitemid 43121784)
13. Dallaglio K, Palazzo E, Marconi A, Dumas M, Truzzi F, Lotti R, Bontè F, Pincelli C. 2009. Endogenous survivin modulates survival and proliferation in UVB-treated human keratinocytes. Exp Dermatol 18:464-471.
14. Espada J, Varela I, Flores I, Ugalde AP, Cadiñanos J, Pendás AM, Stewart CL, Tryggvason K, Blasco MA, Freije JM, López-Otín C. 2008. Nuclear envelope defects cause stem cell dysfunction in premature-aging mice. J Cell Biol 181:27-35. (Pubitemid 351519761)
15. 1 integrin mutation increases the conversion of benign to malignant skin tumors. Cancer Res 69:1334-1342.
16. Franssen ME, Zeeuwen PL, Vierwinden G, van de Kerkhof PC, Schalkwijk J, van Erp PE. 2005. Phenotypical and functional differences in germinative subpopulations derived from normal and psoriatic epidermis. J Invest Dermatol 124:373-383. (Pubitemid 40175885)
17. Fuchs E. 2009. Finding one's niche in the skin. Cell Stem Cell 4:499-502.
18. Fuchs E, Horsley V. 2008. More than one way to skin. Genes Dev 22:976-985.
19. 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.
20. Ghazizadeh S, Taichman LB. 2005. Organization of stem cells and their progeny in human epidermis. J Invest Dermatol 124:367-372.
21. Giangreco A, Qin M, Pintar JE, Watt FM. 2008. Epidermal stem cells are retained in vivo throughout skin aging. Aging Cell 7:250-259. (Pubitemid 351359657)
22. Grabe N, Neuber K. 2007. Simulating psoriasis by altering transit amplifying cells. Bioinformatics 23:1309-1312. (Pubitemid 47050511)
23. Harper LJ, Costea DE, Gammon L, Fazil B, Biddle A, Mackenzie IC. 2010. Normal and malignant epithelial cells with stem-like properties have an extended G2 cell cycle phase that is associated with apoptotic resistance. BMC Cancer 10:166.
24. 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. (Pubitemid 44163616)
25. Inoue K, Aoi N, Sato T, Yamauchi Y, Suga H, Eto H, Kato H, Araki J, Yoshimura K. 2009. Differential expression of stem-cell-associated markers in human hair follicle epithelial cells. Lab Invest 89:844-856.
26. Jaks V, Barker N, Kasper M, van Es JH, Snippert HJ, Clevers H, Toftgård R. 2008. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat Genet 40:1291-1299.
27. 6 integrin expression protects squamous cell carcinomas from anoikis. J Cell Biol 166:419-431.
28. 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.
29. Jensen UB, Yan X, Triel C, Woo SH, Christensen R, Owens DM. 2008. A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus. J Cell Sci 121:609-617.
30. 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.
31. 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.
32. Jones PH, Simons BD, Watt FM. 2007. Sic transit gloria: Farewell to the epidermal transit amplifying cell? Cell Stem Cell 1:371-381.
33. Kim DJ, Kataoka K, Sano S, Connolly K, Kiguchi K, DiGiovanni J. 2009a. Targeted disruption of Bcl-xL in mouse keratinocytes inhibits both UVB- and chemically induced skin carcinogenesis. Mol Carcinog 48:873-885.
34. Kim DJ, Kataoka K, Rao D, Kiguchi K, Cotsarelis G, Digiovanni J. 2009b. Targeted disruption of stat3 reveals a major role for follicular stem cells in skin tumor initiation. Cancer Res 69:7587-7594.
35. Klein AM, Brash DE, Jones PH, Simons BD. 2009. Stochastic fate of p53-mutant epidermal progenitor cells is tilted toward proliferation by UV B during preneoplasia. Proc Natl Acad Sci USA 107:270-275.
36. Legg J, Jensen UB, Broad S, Leigh I, Watt FM. 2003. Role of melanoma chondroitin sulphate proteoglycan in patterning stem cells in human interfollicular epidermis. Development 130:6049-6063. (Pubitemid 38008807)
37. Lena AM, Shalom-Feuerstein R, Rivetti di Val Cervo P, Aberdam D, Knight RA, Melino G, Candi E. 2008. miR-203 represses 'stemness' by repressing DeltaNp63. Cell Death Differ 15:1187-1195.
38. 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.
39. Li A, Simmons PJ, Kaur P. 1998. Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc Natl Acad Sci USA 95:3902-3907. (Pubitemid 28173226)
40. Liefer KM, Koster MI, Wang XJ, Yang A, McKeon F, Roop DR. 2000. Down-regulation of p63 is required for epidermal UV-B-induced apoptosis. Cancer Res 60:4016-4020. (Pubitemid 30636575)
41. Lindner G, Botchkarev VA, Botchkareva NV, Ling G, van der Veen C, Paus R. 1997. Analysis of apoptosis during hair follicle regression (catagen). Am J Pathol 151:1601-1617. (Pubitemid 27527923)
42. Lippens S, Denecker G, Ovaere P, Vandenabeele P, Declercq W. 2005. Death penalty for keratinocytes: Apoptosis versus cornification. Cell Death Differ 12:1497-1508.
43. Lo Muzio L, Staibano S, Pannone G, Mignogna MD, Mariggiò A, Salvatore G, Chieffi P, Tramontano D, De Rosa G, Altieri DC. 2001. Expression of the apoptosis inhibitor survivin in aggressive squamous cell carcinoma. Exp Mol Pathol 70:249-254.
44. 1B integrin isoform in caspase-8-dependent integrin-mediated keratinocyte death. J Invest Dermatol (in press).
45. Manohar A, Shome SG, Lamar J, Stirling L, Iyer V, Pumiglia K, DiPersio CM. 2004. α3β1 integrin promotes keratinocyte cell survival through activation of a MEK/ERK signaling pathway. J Cell Sci 117:4043-4054. (Pubitemid 39328293)
46. Marconi A, Terracina M, Fila C, Franchi J, Bonté F, Romagnoli G, Maurelli R, Failla CM, Dumas M, Pincelli C. 2003. Expression and function of neurotrophins and their receptors in cultured human keratinocytes. J Invest Dermatol 121:1515-1521. (Pubitemid 38005507)
47. Marconi A, Atzei P, Panza C, Fila C, Tiberio R, Truzzi F, Wachter T, Leverkus M, Pincelli C. 2004. FLICE/caspase-8 activation triggers anoikis induced by beta1-integrin blockade in human keratinocytes. J Cell Sci 117:5815-5823. (Pubitemid 40123948)
48. 1 integrin during anoikis. Stem Cells 25:149-155.
49. Medawar A, Virolle T, Rostagno P, de la Forest-Divonne S, Gambaro K, Rouleau M, Aberdam D. 2008. ΔNp63 is essential for epidermal commitment of embryonic stem cells. PLoS One 3:e3441.
50. Mita AC, Mita MM, Nawrocki ST, Giles FJ. 2008. Survivin: Key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res 14:5000-5005.
51. Mitra RS, Wrone-Smith T, Simonian P, Foreman KE, Nunez G, Nickoloff BJ. 1997. Apoptosis in keratinocytes is not dependent on induction of differentiation. Lab Invest 76:99-107. (Pubitemid 27058201)
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. (Pubitemid 38451371)
53. Muffler S, Stark HJ, Amoros M, Falkowska-Hansen B, Boehnke K, Bühring HJ, Marmé A, Bickenbach JR, Boukamp P. 2008.Astable niche supports long-term maintenance of human epidermal stem cells in organotypic cultures. Stem Cells 26:2506-2515.
54. Nijhof JG, Braun KM, Giangreco A, van Pelt C, Kawamoto H, Boyd RL, Willemze R, Mullenders LH, Watt FM, de Gruijl FR, van Ewijk W. 2006. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 133:3027-3037.
55. Pellegrini G, Ranno R, Stracuzzi G, Bondanza S, Guerra L, Zambruno G, Micali G, De Luca M. 1999. The control of epidermal stem cells (holoclones) in the treatment of massive full-thickness burns with autologous keratinocytes cultured on fibrin. Transplantation 68:868-879.
56. 1 integrin-mediated adhesion signalling is essential for epidermal progenitor cell expansion. PLoS One 4:e5488.
57. Qin JZ, Chaturvedi V, Denning MF, Bacon P, Panella J, Choubey D, Nickoloff BJ. 2002. Regulation of apoptosis by p53 in UV-irradiated human epidermis, psoriatic plaques and senescent keratinocytes. Oncogene 21:2991-3002. (Pubitemid 34522898)
58. Savoia P, Cremona O, Trusolino L, Pepino E, Marchisio PC. 1994. Integrins and basement membrane proteins in skin carcinomas. Pathol Res Pract 190:950-954. (Pubitemid 24370108)
59. Schneider MR, Schmidt-Ullrich R, Paus R. 2009. The hair follicle as a dynamic miniorgan. Curr Biol 19:R132-R142.
60. Senoo M, Pinto F, Crum CP, McKeon F. 2007. p63 is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129:523-536. (Pubitemid 46660965)
61. Snippert HJ, Haegebarth A, Kasper M, Jaks V, van Es JH, Barker N, van de Wetering M, van den Born M, Begthel H, Vries RG, Stange DE, Toftga° rd R, Clevers H. 2010. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science 327:1385-1389.
62. Sotiropoulou PA, Candi A, Blanpain C. 2008. The majority of multipotent epidermal stem cells do not protect their genome by asymmetrical chromosome segregation. Stem Cells 26:2964-2973.
63. Sotiropoulou PA, Candi A, Mascré G, De Clercq S, Youssef KK, Lapouge G, Dahl E, Semeraro C, Denecker G, Marine JC, Blanpain C. 2010. Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death. Nat Cell Biol 12:572-582.
64. Tiberio R, Marconi A, Fila C, Fumelli C, Pignatti M, Krajewski S, Giannetti A, Reed JC, Pincelli C. 2002. Keratinocytes enriched for stem cells are protected from anoikis via an integrin signaling pathway in a Bcl-2 dependent manner. FEBS Lett 524:139-144.
65. Tiede S, Koop N, Kloepper JE, Fässler R, Paus R. 2009. Nonviral in situ green fluorescent protein labeling and culture of primary, adult human hair follicle epithelial progenitor cells. Stem Cells 27:2793-2803.
66. Titeux M, Pendaries V, Zanta-Boussif MA, Décha A, Pironon N, Tonasso L, Mejia JE, Brice A, Danos O, Hovnanian A. 2010. SIN retroviral vectors expressing COL7A1 under human promoters for ex vivo gene therapy of recessive dystrophic epidermolysis bullosa. Mol Ther (in press).
67. 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.
68. Trempus CS, Dang H, Humble MM, Wei SJ, Gerdes MJ, Morris RJ, Bortner CD, Cotsarelis G, Tennant RW. 2007. Comprehensive microarray transcriptome profiling of CD34-enriched mouse keratinocyte stem cells. J Invest Dermatol 127:2904-2907.
69. Tudor D, Chaudry F, Harper L, Mackenzie IC. 2007. The in vitro behaviour and patterns of colony formation of murine epithelial stem cells. Cell Prolif 40:706-720. (Pubitemid 47421967)
70. Wang X, Pasolli HA, Williams T, Fuchs E. 2008. AP-2 factors act in concert with Notch to orchestrate terminal differentiation in skin epidermis. J Cell Biol 183:37-48.
71. Watt FM, Estrach S, Ambler CA. 2008. Epidermal Notch signalling: Differentiation, cancer and adhesion. Curr Opin Cell Biol 20:171-179.
72. Yi R, Poy MN, Stoffel M, Fuchs E. 2008. A skin microRNA promotes differentiation by repressing 'stemness'. Nature 452:225-229.
73. Youssef KK, Van Keymeulen A, Lapouge G, Beck B, Michaux C, Achouri Y, Sotiropoulou PA, Blanpain C. 2010. Identification of the cell lineage at the origin of basal cell carcinoma. Nat Cell Biol 12:299-305.
74. Yu H, Kumar SM, Kossenkov AV, Showe L, Xu X. 2010. Stem cells with neural crest characteristics derived from the bulge region of cultured human hair follicles. J Invest Dermatol 130:1227-1236.
75. Zhan Q, Signoretti S, Whitaker-Menezes D, Friedman TM, Korngold R, Murphy GF. 2007. Cytokeratin 15-positive basal epithelial cells targeted in graft-versus-host disease express a constitutive antiapoptotic phenotype. J Invest Dermatol 127:106-115. (Pubitemid 46005667)
76. Zhang W, Remenyik E, Zelterman D, Brash DE, Wikonkal NM. 2001. 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 USA 98:13948-13953. (Pubitemid 33116004)
77. Zhang W, Hanks AN, Boucher K, Florell SR, Allen SM, Alexander A, Brash DE, Grossman D. 2005. UVB-induced apoptosis drives clonal expansion during skin tumor development. Carcinogenesis 26:249-257. (Pubitemid 40207720)