Stem cells behind the barrier

International Journal of Molecular Sciences

Volumn 14, Issue 7, 2013, Pages 13670-13686

  Cangkrama, Michael ^a   Ting, Stephen B ^a   Darido, Charbel ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Asymmetric cell division; Barrier; Cancer; Differentiation; Epidermis; Epigenetic; MicroRNA; Proliferation; Stem cell; Transcription factor

Indexed keywords

HISTONE; MICRORNA; SMALL UNTRANSLATED RNA; TRANSCRIPTION FACTOR;

ANIMAL CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIDERMIS CELL; EPIGENETICS; EXOSOME; HISTONE MODIFICATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PROGENY; REVIEW; SKIN DISEASE; STEM CELL; STRATUM CORNEUM; ADULT; ADULT STEM CELL; ANIMAL; CELL DIVISION; CYTOLOGY; EPIDERMIS; HUMAN; METABOLISM; PHYSIOLOGY;

ADULT; ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIDERMIS; HUMANS; MICRORNAS;

EID: 84879922407     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms140713670     Document Type: Review

References (88)

1. Boehnke, K.; Falkowska-Hansen, B.; Stark, H.J.; Boukamp, P. Stem cells of the human epidermis and their niche: Composition and function in epidermal regeneration and carcinogenesis. Carcinogenesis 2012, 33, 1247-1258.
2. Moore, K.A.; Lemischka, I.R. Stem cells and their niches. Science 2006, 311, 1880-1885.
3. Lechler, T.; Fuchs, E. Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 2005, 437, 275-280.
4. Klein, A.M.; Doupé, D.P.; Jones, P.H.; Simons, B.D. Kinetics of cell division in epidermal maintenance. Phys. Rev. E 2007, 76, 021910.
5. Mascre, G.; Dekoninck, S.; Drogat, B.; Youssef, K.K.; Broheé, S.; Sotiropoulou, P.A.; Simons, B.D.; Blanpain, C. Distinct contribution of stem and progenitor cells to epidermal maintenance. Nature 2012, 489, 257-262.
6. Blanpain, C.; Horsley, V.; Fuchs, E. Epithelial stem cells: Turning over new leaves. Cell 2007, 128, 445-458.
7. Bickenbach, J.R. Identification and behavior of label-retaining cells in oral mucosa and skin. J. Dent. Res. 1981, 60, 1611-1620.
8. Tumbar, T.; Guasch, G.; Greco, V.; Blanpain, C.; Lowry, W.E.; Rendl, M.; Fuchs, E. Defining the epithelial stem cell niche in skin. Science 2004, 303, 359-363.
9. Jaks, V.; Barker, N.; Kasper, M.; van Es, J.H.; Snippert, H.J.; Clevers, H.; Toftgård, R. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 2008, 40, 1291-1299.
10. Morris, R.J.; Liu, Y.; Marles, L.; Yang, Z.; Trempus, C.; Li, S.; Lin, J.S.; Sawicki, J.A.; Cotsarelis, G. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 2004, 22, 411-417.
11. Trempus, C.S.; Morris, R.J.; Bortner, C.D.; Cotsarelis, G.; Faircloth, R.S.; Reece, J.M. Tennant RW. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 2003, 120, 501-511.
12. Blanpain, C.; Lowry, W.E.; Geoghegan, A.; Polak, L.; Fuchs, E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 2004, 118, 635-648.
13. Jones, P.H.; Harper, S.; Watt, F.M. Stem cell patterning and fate in human epidermis. Cell 1995, 80, 83-93.
14. Li, A.; Simmons, P.J.; Kaur, P. Identification and isolation of candidate human keratinocyte stem cells based on cell surface phenotype. Proc. Natl. Acad. Sci. USA 1998, 95, 3902-3907.
15. Wan, H.; Stone, M.G.; Simpson, C.; Reynolds, L.E.; Marshall, J.F.; Hart, I.R.; Hodivala-Dilke, K.M.; Eady, R.A. Desmosomal proteins, including desmoglein 3, serve as novel negative markers for epidermal stem cell-containing population of keratinocytes. J. Cell Sci. 2003, 116, 4239-4248.
16. Fortunel, N.O.; Hatzfeld, J.A.; Rosemary, P.A.; Ferraris, C.; Monier, M.N.; Haydont, V.; Longuet, J.; Brethon, B.; Lim, B.; Castiel, I.; et al. Long-term expansion of human functional epidermal precursor cells: Promotion of extensive amplification by low TGF-beta1 concentrations. J. Cell Sci. 2003, 116, 4043-4052.
17. Legg, J.; Jensen, U.B.; Broad, S.; Leigh, I.; Watt, F.M. Role of melanoma chondroitin sulphate proteoglycan in patterning stem cells in human interfollicular epidermis. Development 2003, 130, 6049-6063.
18. Niemann, C.; Watt, F.M. Designer skin: Lineage commitment in postnatal epidermis. Trends Cell Biol. 2002, 12, 185-192.
19. Watt, F.M.; Jensen, K.B. Epidermal stem cell diversity and quiescence. EMBO Mol. Med. 2009, 1, 260-267.
20. Ito, M.; Yang, Z.; Andl, T.; Cui, C.; Kim, N.; Millar, S.E.; Cotsarelis, G. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 2007, 447, 316-320.
21. Castilho, R.M.; Squarize, C.H.; Chodosh, L.A.; Williams, B.O.; Gutkind, J.S. mTOR mediates Wnt-induced epidermal stem cell exhaustion and aging. Cell Stem Cell 2009, 5, 279-289.
22. Li, L.; Clevers, H. Coexistence of quiescent and active adult stem cells in mammals. Science 2010, 327, 542-545.
23. Horsley, V.; Aliprantis, A.O.; Polak, L.; Glimcher, L.H.; Fuchs, E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell 2008, 132, 299-310.
24. Jensen, K.B.; Collins, C.A.; Nascimento, E.; Tan, D.W.; Frye, M.; Itami, S.; Watt, F.M. Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 2009, 4, 427-439.
25. Niessen, M.T.; Iden, S.; Niessen, C.M. The in vivo function of mammalian cell and tissue polarity regulators-How to shape and maintain the epidermal barrier. J. Cell Sci. 2012, 125, 3501-3510.
26. Caddy, J.; Wilanowski, T.; Darido, C.; Dworkin, S.; Ting, S.B.; Zhao, Q.; Rank, G.; Auden, A.; Srivastava, S.; Papenfuss, T.A.; et al. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev. Cell 2010, 19, 138-147.
27. Dworkin, S.; Jane, S.M.; Darido, C. The planar cell polarity pathway in vertebrate epidermal development, homeostasis and repair. Organogenesis 2011, 7, 202-208.
28. Poulson, N.D.; Lechler, T. Robust control of mitotic spindle orientation in the developing epidermis. J. Cell Biol. 2010, 191, 915-922.
29. Koster, M.I.; Dai, D.; Marinari, B.; Sano, Y.; Costanzo, A.; Karin, M.; Roop, D.R. p63 induces key target genes required for epidermal morphogenesis. Proc. Natl. Acad. Sci. USA 2007, 104, 3255-3260.
30. Truong, A.B.; Kretz, M.; Ridky, T.W.; Kimmel, R.; Khavari, P.A. p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes Dev. 2006, 20, 3185-3197.
31. Williams, S.E.; Beronja, S.; Pasolli, H.A.; Fuchs, E. Asymmetric cell divisions promote Notch-dependent epidermal differentiation. Nature 2011, 470, 353-358.
32. Koster, M.I.; Kim, S.; Huang, J.; Williams, T.; Roop, D.R. TAp63alpha induces AP-2gamma as an early event in epidermal morphogenesis. Dev. Biol. 2006, 289, 253-261.
33. Wang, X.; Pasolli, H.A.; Williams, T.; Fuchs, E. AP-2 factors act in concert with Notch to orchestrate terminal differentiation in skin epidermis. J. Cell Biol. 2008, 183, 37-48.
34. Demehri, S.; Turkoz, A.; Kopan, R. Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 2009, 16, 55-66.
35. Dumortier, A.; Durham, A.D.; Di Piazza, M.; Vauclair, S.; Koch, U.; Ferrand, G.; Ferrero, I.; Demehri, S.; Song, L.L.; Farr, A.G.; et al. Atopic dermatitis-like disease and associated lethal myeloproliferative disorder arise from loss of Notch signaling in the murine skin. PLoS One 2010, 5, e9258.
36. Mills, A.A.; Zheng, B.; Wang, X.J.; Vogel, H.; Roop, D.R.; Bradley, A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 1999, 398, 708-713.
37. Patel, S.; Xi, Z.F.; Seo, E.Y.; McGaughey, D.; Segre, J.A. Klf4 and corticosteroids activate an overlapping set of transcriptional targets to accelerate in utero epidermal barrier acquisition. Proc. Natl. Acad. Sci. USA 2006, 103, 18668-18673.
38. Segre, J.A.; Bauer, C.; Fuchs, E. Klf4 is a transcription factor required for establishing the barrier function of the skin. Nat. Genet 1999, 22, 356-360.
39. Teng, A.; Nair, M.; Wells, J.; Segre, J.A.; Dai, X. Strain-dependent perinatal lethality of Ovol1-deficient mice and identification of Ovol2 as a downstream target of Ovol1 in skin epidermis. Biochim. Biophys. Acta 2007, 1772, 89-95.
40. Lopez, R.G.; Garcia-Silva, S.; Moore, S.J.; Bereshchenko, O.; Martinez-Cruz, A.B.; Ermakova, O.; Kurz, E.; Paramio, J.M.; Nerlov, C. C/EBPalpha and beta couple interfollicular keratinocyte proliferation arrest to commitment and terminal differentiation. Nat. Cell Biol. 2009, 11, 1181-1190.
41. Magnusdottir, E.; Kalachikov, S.; Mizukoshi, K.; Savitsky, D.; Ishida-Yamamoto, A.; Panteleyev, A.A.; Calame, K. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl. Acad. Sci. USA 2007, 104, 14988-14993.
42. Zhang, H.; Pasolli, H.A.; Fuchs, E. Yes-associated protein (YAP) transcriptional coactivator functions in balancing growth and differentiation in skin. Proc. Natl. Acad. Sci. USA 2011, 108, 2270-2275.
43. Yu, Z.; Lin, K.K.; Bhandari, A.; Spencer, J.A.; Xu, X.; Wang, N.; Lu, Z.; Gill, G.N.; Roop, D.R.; Wertz, P.; et al. The Grainyhead-like epithelial transactivator Get-1/Grhl3 regulates epidermal terminal differentiation and interacts functionally with LMO4. Dev. Biol. 2006, 299, 122-136.
44. Senoo, M.; Pinto, F.; Crum, C.P.; McKeon, F. p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell 2007, 129, 523-536.
45. Gareus, R.; Huth, M.; Breiden, B.; Nenci, A.; Rösch, N.; Haase, I.; Bloch, W.; Sandhoff, K.; Pasparakis, M. Normal epidermal differentiation but impaired skin-barrier formation upon keratinocyte-restricted IKK1 ablation. Nat. Cell Biol. 2007, 9, 461-469.
46. Sen, G.L.; Boxer, L.D.; Webster, D.E.; Bussat, R.T.; Qu, K.; Zarnegar, B.J.; Johnston, D.; Siprashvili, Z.; Khavari, P.A. ZNF750 is a p63 target gene that induces KLF4 to drive terminal epidermal differentiation. Dev. Cell 2012, 22, 669-677.
47. Li, J.; Zheng, H.; Yu, F.; Yu, T.; Liu, C.; Huang, S.; Wang, T.C.; Ai, W. Deficiency of the Kruppel-like factor KLF4 correlates with increased cell proliferation and enhanced skin tumorigenesis. Carcinogenesis 2012, 33, 1239-1246.
48. Keyes, W.M.; Pecoraro, M.; Aranda, V.; Vernersson-Lindahl, E.; Li, W.; Vogel, H.; Guo, X.; Garcia, E. L.; Michurina, T.V.; Enikolopov, G.N.; et al. DeltaNp63alpha is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell 2011, 8, 164-176.
49. Nair, M.; Teng, A.; Bilanchone, V.; Agrawal, A.; Li, B.; Dai, X. Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J. Cell Biol. 2006, 173, 253-264.
50. Nascimento, E.M.; Cox, C.L.; MacArthur, S.; Hussain, S.; Trotter, M.; Blanco, S.; Suraj, M.; Nichols, J.; Kübler, B.; Benitah, S.A.; et al. The opposing transcriptional functions of Sin3a and c-Myc are required to maintain tissue homeostasis. Nat. Cell Biol. 2011, 13, 1395-1405.
51. Nerlov, C. The C/EBP family of transcription factors: A paradigm for interaction between gene expression and proliferation control. Trends Cell Biol. 2007, 17, 318-324.
52. Horsley, V.; O'Carroll, D.; Tooze, R.; Ohinata, Y.; Saitou, M.; Obukhanych, T.; Nussenzweig, M.; Tarakhovsky, A.; Fuchs, E. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 2006, 126, 597-609.
53. Sellheyer, K.; Krahl, D. Blimp-1: A marker of terminal differentiation but not of sebocytic progenitor cells. J. Cutan Pathol. 2010, 37, 362-370.
54. Schlegelmilch, K.; Mohseni, M.; Kirak, O.; Pruszak, J.; Vasioukhin, V.; Avruch, J.; Brummelkamp, T.R. Camargo FD Yap1 acts downstream of alpha-catenin to control epidermal proliferation. Cell 2011, 144, 782-795.
55. Lian, I.; Kim, J.; Okazawa, H.; Zhao, J.; Zhao, B.; Yu, J.; Chinnaiyan, A.; Israel, M.A.; Goldstein, L.S.; Abujarour, R.; et al. The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 2010, 24, 1106-1118.
56. Yi, R.; O'Carroll, D.; Pasolli, H.A.; Zhang, Z.; Dietrich, F.S.; Tarakhovsky, A.; Fuchs, E. Morphogenesis in skin is governed by discrete sets of differentially expressed microRNAs. Nat. Genet 2006, 38, 356-362.
57. Mistry, D.S.; Chen, Y.; Sen, G.L. Progenitor function in self-renewing human epidermis is maintained by the exosome. Cell Stem Cell 2012, 11, 127-135.
58. Auden, A.; Caddy, J.; Wilanowski, T.; Ting, S.B.; Cunningham, J.M.; Jane, S.M. Spatial and temporal expression of the Grainyhead-like transcription factor family during murine development. Gene Expr. Patterns 2006, 6, 964-970.
59. Ting, S.B.; Wilanowski, T.; Auden, A.; Hall, M.; Voss, A.K.; Thomas, T.; Parekh, V.; Cunningham, J.M.; Jane, S.M. Inositol-and folate-resistant neural tube defects in mice lacking the epithelial-specific factor Grhl-3. Nat. Med. 2003, 9, 1513-1519.
60. Ting, S.B.; Caddy, J.; Hislop, N.; Wilanowski, T.; Auden, A.; Zhao, L.L.; Ellis, S.; Kaur, P.; Uchida, Y.; Holleran, W.M.; et al. A homolog of Drosophila grainy head is essential for epidermal integrity in mice. Science 2005, 308, 411-413.
61. Darido, C.; Jane, S.M. Grhl3 and GEF19 in the front rho. Small GTPases 2010, 1, 104-107.
62. Hislop, N.R.; Caddy, J.; Ting, S.B.; Auden, A.; Vasudevan, S.; King, S.L.; Lindeman, G.J.; Visvader, J.E.; Cunningham, J.M.; Jane, S.M. Grhl3 and Lmo4 play coordinate roles in epidermal migration. Dev. Biol. 2008, 321, 263-272.
63. Darido, C.; Georgy, S.R.; Wilanowski, T.; Dworkin, S.; Auden, A.; Zhao, Q.; Rank, G.; Srivastava, S.; Finlay, M.J.; Papenfuss, A.T.; et al. Targeting of the tumor suppressor GRHL3 by a miR-21-dependent proto-oncogenic network results in PTEN loss and tumorigenesis. Cancer Cell 2011, 20, 635-648.
64. Zhang, L.; Stokes, N.; Polak, L.; Fuchs, E. Specific microRNAs are preferentially expressed by skin stem cells to balance self-renewal and early lineage commitment. Cell Stem Cell 2011, 8, 294-308.
65. Yi, R.; Poy, M.N.; Stoffel, M.; Fuchs, E. A skin microRNA promotes differentiation by repressing "stemness". Nature 2008, 452, 225-229.
66. Botchkarev, V.A.; Gdula, M.R.; Mardaryev, A.N.; Sharov, A.A.; Fessing, M.Y. Epigenetic regulation of gene expression in keratinocytes. J. Invest. Dermatol. 2012, 132, 2505-2521.
67. Frye, M.; Fisher, A.G.; Watt, F.M. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS One 2007, 2, e763.
68. Ezhkova, E.; Pasolli, H.A.; Parker, J.S.; Stokes, N.; Su, I.H.; Hannon, G. Tarakhovsky, A.; Fuchs, E. Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 2009, 136, 1122-1135.
69. Ezhkova, E.; Lien, W.H.; Stokes, N.; Pasolli, H.A.; Silva, J.M.; Fuchs, E. EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev. 2011, 25, 485-498.
70. Bao, X.; Tang, J.; Lopez-Pajares, V.; Tao, S.; Qu, K.; Crabtree, G.R.; Khavari, P.A. ACTL6a enforces the epidermal progenitor state by suppressing SWI/SNF-dependent induction of KLF4. Cell Stem Cell 2013, 12, 193-203.
71. Indra, A.K.; Dupé, V.; Bornert, J.M.; Messaddeq, N.; Yaniv, M.; Mark, M.; Chambon, P.; Metzger, D. Temporally controlled targeted somatic mutagenesis in embryonic surface ectoderm and fetal epidermal keratinocytes unveils two distinct developmental functions of BRG1 in limb morphogenesis and skin barrier formation. Development 2005, 132, 4533-4544.
72. Kashiwagi, M.; Morgan, B.A.; Georgopoulos, K. The chromatin remodeler Mi-2beta is required for establishment of the basal epidermis and normal differentiation of its progeny. Development 2007, 134, 1571-1582.
73. Darido, C.; Buchert, M.; Pannequin, J.; Bastide, P.; Zalzali, H.; Mantamadiotis, T.; Bourgaux, J.F.; Garambois, V.; Jay, P.; Blache, P.; et al. Defective claudin-7 regulation by Tcf-4 and Sox-9 disrupts the polarity and increases the tumorigenicity of colorectal cancer cells. Cancer Res. 2008, 68, 4258-4268.
74. Descargues, P.; Sil, A.K.; Karin, M. IKKalpha, a critical regulator of epidermal differentiation and a suppressor of skin cancer. EMBO J. 2008, 27, 2639-2647.
75. De Cid, R.; Riveira-Munoz, E.; Zeeuwen, P.L.; Robarge, J.; Liao, W.; Dannhauser, E.N.; Giardina, E.; Stuart, P.E.; Nair, R.; Helms, C.; et al. Deletion of the late cornified envelope LCE3B and LCE3C genes as a susceptibility factor for psoriasis. Nat. Genet. 2009, 41, 211-215.
76. Leech, S.N.; Moss, C. A current and online genodermatosis database. Br. J. Dermatol. 2007, 156, 1115-1148.
77. Nestle, F.O.; di Meglio, P.; Qin, J.Z.; Nickoloff, B.J. Skin immune sentinels in health and disease. Nat. Rev. Immunol. 2009, 9, 679-691.
78. Rogers, H.W.; Weinstock, M.A.; Harris, A.R.; Hinckley, M.R.; Feldman, S.R.; Fleischer, A.B.; Coldiron, B.M. Incidence estimate of nonmelanoma skin cancer in the United States, 2006. Arch. Dermatol. 2010, 146, 283-287.
79. Smith, C.H.; Barker, J.N. Psoriasis and its management. BMJ 2006, 333, 380-384.
80. Kangsamaksin, T.; Park, H.J.; Trempus, C.S.; Morris, R.J. A perspective on murine keratinocyte stem cells as targets of chemically induced skin cancer. Mol. Carcinog. 2007, 46, 579-584.
81. Jensen, K.B.; Jones, J.; Watt, F.M. A stem cell gene expression profile of human squamous cell carcinomas. Cancer Lett. 2008, 272, 23-31.
82. Morris, R.J.; Fischer, S.M.; Slaga, T.J. Evidence that the centrally and peripherally located cells in the murine epidermal proliferative unit are two distinct cell populations. J. Invest. Dermatol. 1985, 84, 277-281.
83. Morris, R.J.; Fischer, S.M.; Slaga, T.J. Evidence that a slowly cycling subpopulation of adult murine epidermal cells retains carcinogen. Cancer Res. 1986, 46, 3061-3066.
84. Youssef, K.K.; van Keymeulen, A.; Lapouge, G.; Beck, B.; Michaux, C.; Achouri, Y.; Sotiropoulou, P.A.; Blanpain, C. Identification of the cell lineage at the origin of basal cell carcinoma. Nat. Cell Biol. 2010, 12, 299-305.
85. Lapouge, G.; Youssef, K.K.; Vokaer, B.; Achouri, Y.; Michaux, C.; Sotiropoulou, P.A.; Blanpain, C. Identifying the cellular origin of squamous skin tumors. Proc. Natl. Acad. Sci. USA 2011, 108, 7431-7436.
86. Clayton, E.; Doupé, D.P.; Klein, A.M.; Winton, D.J.; Simons, B.D.; Jones, P.H. A single type of progenitor cell maintains normal epidermis. Nature 2007, 446, 185-189.
87. Ferraris, C.; Chaloin-Dufau, C.; Dhouailly, D. Transdifferentiation of embryonic and postnatal rabbit corneal epithelial cells. Differentiation 1994, 57, 89-96.
88. Neumuller, R.A.; Knoblich, J.A. Dividing cellular asymmetry: Asymmetric cell division and its implications for stem cells and cancer. Genes Dev. 2009, 23, 2675-2699.