Epithelial Stem Cells: Turning over New Leaves

Cell

Volumn 128, Issue 3, 2007, Pages 445-458

  Blanpain, Cédric ^a   Horsley, Valerie ^a   Fuchs, Elaine ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER; CELL ACTIVATION; CELL DIFFERENTIATION; CELL INTERACTION; CELL LINEAGE; CELL STRUCTURE; EPITHELIUM CELL; MESENCHYME; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; SYSTEMATIC REVIEW;

EID: 33846705750     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2007.01.014     Document Type: Review

References (105)

1. Andl T., Ahn K., Kairo A., Chu E.Y., Wine-Lee L., Reddy S.T., Croft N.J., Cebra-Thomas J.A., Metzger D., Chambon P., et al. Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development 131 (2004) 2257-2268
2. Andl T., Reddy S.T., Gaddapara T., and Millar S.E. WNT signals are required for the initiation of hair follicle development. Dev. Cell 2 (2002) 643-653
3. Artavanis-Tsakonas S., Rand M.D., and Lake R.J. Notch signaling: cell fate control and signal integration in development. Science 284 (1999) 770-776
4. Barker N., Huls G., Korinek V., and Clevers H. Restricted high level expression of Tcf-4 protein in intestinal and mammary gland epithelium. Am. J. Pathol. 154 (1999) 29-35
5. Barrandon Y., and Green H. Three clonal types of keratinocyte with different capacities for multiplication. Proc. Natl. Acad. Sci. USA 84 (1987) 2302-2306
6. Batlle E., Henderson J.T., Beghtel H., van den Born M.M., Sancho E., Huls G., Meeldijk J., Robertson J., van de Wetering M., Pawson T., and Clevers H. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 111 (2002) 251-263
7. Batlle E., Bacani J., Begthel H., Jonkheer S., Gregorieff A., van de Born M., Malats N., Sancho E., Boon E., Pawson T., et al. EphB receptor activity suppresses colorectal cancer progression. Nature 435 (2005) 1126-1130
8. Beachy P.A., Karhadkar S.S., and Berman D.M. Tissue repair and stem cell renewal in carcinogenesis. Nature 432 (2004) 324-331
9. Bickenbach, J.R. (1981). Identification and behavior of label-retaining cells in oral mucosa and skin. J. Dent. Res. 60 Spec No C, 1611-1620.
10. Birchmeier C., and Birchmeier W. Molecular aspects of mesenchymal-epithelial interactions. Annu. Rev. Cell Biol. 9 (1993) 511-540
11. Bjerknes M., and Cheng H. Clonal analysis of mouse intestinal epithelial progenitors. Gastroenterology 116 (1999) 7-14
12. Blanpain C., and Fuchs E. Epidermal stem cells of the skin. Annu. Rev. Cell Dev. Biol. 22 (2006) 339-373
13. Blanpain C., Lowry W.E., Geoghegan A., Polak L., and Fuchs E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118 (2004) 635-648
14. Blanpain C., Lowry W.E., Pasolli H.A., and Fuchs E. Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 20 (2006) 3022-3035
15. Botchkarev V.A., Botchkareva N.V., Nakamura M., Huber O., Funa K., Lauster R., Paus R., and Gilchrest B.A. Noggin is required for induction of the hair follicle growth phase in postnatal skin. FASEB J. 15 (2001) 2205-2214
16. Buono K.D., Robinson G.W., Martin C., Shi S., Stanley P., Tanigaki K., Honjo T., and Hennighausen L. The canonical Notch/RBP-J signaling pathway controls the balance of cell lineages in mammary epithelium during pregnancy. Dev. Biol. 293 (2006) 565-580
17. Chan E.F., Gat U., McNiff J.M., and Fuchs E. A common human skin tumour is caused by activating mutations in beta-catenin. Nat. Genet. 21 (1999) 410-413
18. Chu E.Y., Hens J., Andl T., Kairo A., Yamaguchi T.P., Brisken C., Glick A., Wysolmerski J.J., and Millar S.E. Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis. Development 131 (2004) 4819-4829
19. Claudinot S., Nicolas M., Oshima H., Rochat A., and Barrandon Y. Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc. Natl. Acad. Sci. USA 102 (2005) 14677-14682
20. Cotsarelis G., Cheng S.Z., Dong G., Sun T.T., and Lavker R.M. Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57 (1989) 201-209
21. Cotsarelis G., Sun T.T., and Lavker R.M. Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61 (1990) 1329-1337
22. Cunha G.R., Young P., Christov K., Guzman R., Nandi S., Talamantes F., and Thordarson G. Mammary phenotypic expression induced in epidermal cells by embryonic mammary mesenchyme. Acta Anat. (Basel) 152 (1995) 195-204
23. DasGupta R., and Fuchs E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126 (1999) 4557-4568
24. Dor Y., Brown J., Martinez O.I., and Melton D.A. Adult pancreatic beta-cells are formed by self-duplication rather than stem-cell differentiation. Nature 429 (2004) 41-46
25. Ferraris C., Chevalier G., Favier B., Jahoda C.A., and Dhouailly D. Adult corneal epithelium basal cells possess the capacity to activate epidermal, pilosebaceous and sweat gland genetic programs in response to embryonic dermal stimuli. Development 127 (2000) 5487-5495
26. Fre S., Huyghe M., Mourikis P., Robine S., Louvard D., and Artavanis-Tsakonas S. Notch signals control the fate of immature progenitor cells in the intestine. Nature 435 (2005) 964-968
27. Fuchs E., and Raghavan S. Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3 (2002) 199-209
28. Gat U., Dasgupta R., Degenstein L., and Fuchs E. De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell 95 (1998) 605-614
29. Ghazizadeh S., and Taichman L.B. Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin. EMBO J. 20 (2001) 1215-1222
30. Giancotti F.G., and Tarone G. Positional control of cell fate through joint integrin/receptor protein kinase signaling. Annu. Rev. Cell Dev. Biol. 19 (2003) 173-206
31. Giannakis M., Stappenbeck T.S., Mills J.C., Leip D.G., Lovett M., Clifton S.W., Ippolito J.E., Glasscock J.I., Arumugam M., Brent M.R., and Gordon J.I. Molecular properties of adult mouse gastric and intestinal epithelial progenitors in their niches. J. Biol. Chem. 281 (2006) 11292-11300
32. Haramis A.P., Begthel H., van den Born M., van Es J., Jonkheer S., Offerhaus G.J., and Clevers H. De novo crypt formation and juvenile polyposis on BMP inhibition in mouse intestine. Science 303 (2004) 1684-1686
33. Hardy M.H. The secret life of the hair follicle. Trends Genet. 8 (1992) 55-61
34. He X. Unwinding a path to nuclear beta-catenin. Cell 127 (2006) 139-155
35. He X.C., Zhang J., Tong W.G., Tawfik O., Ross J., Scoville D.H., Tian Q., Zeng X., He X., Wiedemann L.M., et al. BMP signaling inhibits intestinal stem cell self-renewal through suppression of Wnt-beta-catenin signaling. Nat. Genet. 36 (2004) 1117-1121
36. Hennighausen L., and Robinson G.W. Information networks in the mammary gland. Nat. Rev. Mol. Cell Biol. 6 (2005) 715-725
37. Holmberg J., Genander M., Halford M.M., Anneren C., Sondell M., Chumley M.J., Silvany R.E., Henkemeyer M., and Frisen J. EphB receptors coordinate migration and proliferation in the intestinal stem cell niche. Cell 125 (2006) 1151-1163
38. Horsley V., O'Carroll D., Tooze R., Ohinata Y., Saitou M., Obukhanych T., Nussenzweig M., Tarakhovsky A., and Fuchs E. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell 126 (2006) 597-609
39. Hu C., Dievart A., Lupien M., Calvo E., Tremblay G., and Jolicoeur P. Overexpression of activated murine Notch1 and Notch3 in transgenic mice blocks mammary gland development and induces mammary tumors. Am. J. Pathol. 168 (2006) 973-990
40. Huelsken J., Vogel R., Erdmann B., Cotsarelis G., and Birchmeier W. beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105 (2001) 533-545
41. Iso T., Kedes L., and Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J. Cell. Physiol. 194 (2003) 237-255
42. Ito M., Liu Y., Yang Z., Nguyen J., Liang F., Morris R.J., and Cotsarelis G. Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Nat. Med. 11 (2005) 1351-1354
43. Jensen J., Pedersen E.E., Galante P., Hald J., Heller R.S., Ishibashi M., Kageyama R., Guillemot F., Serup P., and Madsen O.D. Control of endodermal endocrine development by Hes-1. Nat. Genet. 24 (2000) 36-44
44. Jones P.H., and Watt F.M. 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
45. Kenyon K.R., and Tseng S.C. Limbal autograft transplantation for ocular surface disorders. Ophthalmology 96 (1989) 709-722
46. Kobielak K., Pasolli H.A., Alonso L., Polak L., and Fuchs E. Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. J. Cell Biol. 163 (2003) 609-623
47. Kolodka T.M., Garlick J.A., and Taichman L.B. Evidence for keratinocyte stem cells in vitro: long term engraftment and persistence of transgene expression from retrovirus-transduced keratinocytes. Proc. Natl. Acad. Sci. USA 95 (1998) 4356-4361
48. Kordon E.C., and Smith G.H. An entire functional mammary gland may comprise the progeny from a single cell. Development 125 (1998) 1921-1930
49. Korinek V., Barker N., Moerer P., van Donselaar E., Huls G., Peters P.J., and Clevers H. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19 (1998) 379-383
50. Levy V., Lindon C., Harfe B.D., and Morgan B.A. Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Dev. Cell 9 (2005) 855-861
51. Lo Celso C., Prowse D.M., and Watt F.M. 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 131 (2004) 1787-1799
52. Logan C.Y., and Nusse R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20 (2004) 781-810
53. Lowry W.E., Blanpain C., Nowak J.A., Guasch G., Lewis L., and Fuchs E. Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 19 (2005) 1596-1611
54. Mackenzie I.C. Retroviral transduction of murine epidermal stem cells demonstrates clonal units of epidermal structure. J. Invest. Dermatol. 109 (1997) 377-383
55. Madison B.B., Braunstein K., Kuizon E., Portman K., Qiao X.T., and Gumucio D.L. Epithelial hedgehog signals pattern the intestinal crypt-villus axis. Development 132 (2005) 279-289
56. Mavilio F., Pellegrini G., Ferrari S., Di Nunzio F., Di Iorio E., Recchia A., Maruggi G., Ferrari G., Provasi E., Bonini C., et al. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat. Med. 12 (2006) 1397-1402
57. Merrill B.J., Gat U., Dasgupta R., and Fuchs E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 15 (2001) 1688-1705
58. Moore K.A., and Lemischka I.R. Stem cells and their niches. Science 311 (2006) 1880-1885
59. Morris R.J., Liu Y., Marles L., Yang Z., Trempus C., Li S., Lin J.S., Sawicki J.A., and Cotsarelis G. Capturing and profiling adult hair follicle stem cells. Nat. Biotechnol. 22 (2004) 411-417
60. Nguyen H., Rendl M., and Fuchs E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 127 (2006) 171-183
61. Nicolas M., Wolfer A., Raj K., Kummer J.A., Mill P., van Noort M., Hui C.C., Clevers H., Dotto G.P., and Radtke F. Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33 (2003) 416-421
62. O'Connor N.E., Mulliken J.B., Banks-Schlegel S., Kehinde O., and Green H. Grafting of burns with cultured epithelium prepared from autologous epidermal cells. Lancet 1 (1981) 75-78
63. Oshima H., Rochat A., Kedzia C., Kobayashi K., and Barrandon Y. Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104 (2001) 233-245
64. Pan Y., Lin M.H., Tian X., Cheng H.T., Gridley T., Shen J., and Kopan R. gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev. Cell 7 (2004) 731-743
65. Pellegrini G., Traverso C.E., Franzi A.T., Zingirian M., Cancedda R., and De Luca M. Long-term restoration of damaged corneal surfaces with autologous cultivated corneal epithelium. Lancet 349 (1997) 990-993
66. Pellegrini G., Ranno R., Stracuzzi G., Bondanza S., Guerra L., Zambruno G., Micali G., and De Luca M. The control of epidermal stem cells (holoclones) in the treatment of massive full-thickness burns with autologous keratinocytes cultured on fibrin. Transplantation 68 (1999) 868-879
67. Pinto D., Gregorieff A., Begthel H., and Clevers H. Canonical Wnt signals are essential for homeostasis of the intestinal epithelium. Genes Dev. 17 (2003) 1709-1713
68. Ponder B.A., Schmidt G.H., Wilkinson M.M., Wood M.J., Monk M., and Reid A. Derivation of mouse intestinal crypts from single progenitor cells. Nature 313 (1985) 689-691
69. Potten C.S. The epidermal proliferative unit: the possible role of the central basal cell. Cell Tissue Kinet. 7 (1974) 77-88
70. Potten C.S., Owen G., and Booth D. Intestinal stem cells protect their genome by selective segregation of template DNA strands. J. Cell Sci. 115 (2002) 2381-2388
71. Radtke F., and Clevers H. Self-renewal and cancer of the gut: two sides of a coin. Science 307 (2005) 1904-1909
72. Rangarajan A., Talora C., Okuyama R., Nicolas M., Mammucari C., Oh H., Aster J.C., Krishna S., Metzger D., Chambon P., et al. Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J. 20 (2001) 3427-3436
73. Rendl M., Lewis L., and Fuchs E. Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biol. 3 (2005) e331 10.1371/journal.pbio.0030331
74. Reya T., and Clevers H. Wnt signalling in stem cells and cancer. Nature 434 (2005) 843-850
75. Rheinwald J.G., and Green H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6 (1975) 331-343
76. Richardson G.D., Arnott E.C., Whitehouse C.J., Lawrence C.M., Reynolds A.J., Hole N., and Jahoda C.A. Plasticity of rodent and human hair follicle dermal cells: implications for cell therapy and tissue engineering. J. Investig. Dermatol. Symp. Proc. 10 (2005) 180-183
77. Ro S., and Rannala B. A stop-EGFP transgenic mouse to detect clonal cell lineages generated by mutation. EMBO Rep. 5 (2004) 914-920
78. Ronfard V., Rives J.M., Neveux Y., Carsin H., and Barrandon Y. Long-term regeneration of human epidermis on third degree burns transplanted with autologous cultured epithelium grown on a fibrin matrix. Transplantation 70 (2000) 1588-1598
79. Sancho E., Batlle E., and Clevers H. Signaling pathways in intestinal development and cancer. Annu. Rev. Cell Dev. Biol. 20 (2004) 695-723
80. Schmidt G.H., Winton D.J., and Ponder B.A. Development of the pattern of cell renewal in the crypt-villus unit of chimaeric mouse small intestine. Development 103 (1988) 785-790
81. Schroder N., and Gossler A. Expression of Notch pathway components in fetal and adult mouse small intestine. Gene Expr. Patterns 2 (2002) 247-250
82. Searfoss G.H., Jordan W.H., Calligaro D.O., Galbreath E.J., Schirtzinger L.M., Berridge B.R., Gao H., Higgins M.A., May P.C., and Ryan T.P. Adipsin, a biomarker of gastrointestinal toxicity mediated by a functional gamma-secretase inhibitor. J. Biol. Chem. 278 (2003) 46107-46116
83. Shackleton M., Vaillant F., Simpson K.J., Stingl J., Smyth G.K., Asselin-Labat M.L., Wu L., Lindeman G.J., and Visvader J.E. Generation of a functional mammary gland from a single stem cell. Nature 439 (2006) 84-88
84. Shin K., Fogg V.C., and Margolis B. Tight junctions and cell polarity. Annu. Rev. Cell Dev. Biol. 22 (2006) 207-235
85. Silva-Vargas V., Lo Celso C., Giangreco A., Ofstad T., Prowse D.M., Braun K.M., and Watt F.M. 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 9 (2005) 121-131
86. Stanger B.Z., Datar R., Murtaugh L.C., and Melton D.A. Direct regulation of intestinal fate by Notch. Proc. Natl. Acad. Sci. USA 102 (2005) 12443-12448
87. Stingl J., Eirew P., Ricketson I., Shackleton M., Vaillant F., Choi D., Li H.I., and Eaves C.J. Purification and unique properties of mammary epithelial stem cells. Nature 439 (2006) 993-997
88. Sun T.T., and Lavker R.M. Corneal epithelial stem cells: past, present, and future. J. Investig. Dermatol. Symp. Proc. 9 (2004) 202-207
89. Suzuki K., Fukui H., Kayahara T., Sawada M., Seno H., Hiai H., Kageyama R., Okano H., and Chiba T. Hes1-deficient mice show precocious differentiation of Paneth cells in the small intestine. Biochem. Biophys. Res. Commun. 328 (2005) 348-352
90. Taub R. Liver regeneration: from myth to mechanism. Nat. Rev. Mol. Cell Biol. 5 (2004) 836-847
91. Taylor G., Lehrer M.S., Jensen P.J., Sun T.T., and Lavker R.M. Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102 (2000) 451-461
92. Teuliere J., Faraldo M.M., Deugnier M.A., Shtutman M., Ben-Ze'ev A., Thiery J.P., and Glukhova M.A. Targeted activation of beta-catenin signaling in basal mammary epithelial cells affects mammary development and leads to hyperplasia. Development 132 (2005) 267-277
93. Tsukamoto A.S., Grosschedl R., Guzman R.C., Parslow T., and Varmus H.E. Expression of the int-1 gene in transgenic mice is associated with mammary gland hyperplasia and adenocarcinomas in male and female mice. Cell 55 (1988) 619-625
94. Tumbar T., Guasch G., Greco V., Blanpain C., Lowry W.E., Rendl M., and Fuchs E. Defining the epithelial stem cell niche in skin. Science 303 (2004) 359-363
95. van de Wetering M., Sancho E., Verweij C., de Lau W., Oving I., Hurlstone A., van der Horn K., Batlle E., Coudreuse D., Haramis A.P., et al. The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111 (2002) 241-250
96. van den Brink G.R., Bleuming S.A., Hardwick J.C., Schepman B.L., Offerhaus G.J., Keller J.J., Nielsen C., Gaffield W., van Deventer S.J., Roberts D.J., and Peppelenbosch M.P. Indian Hedgehog is an antagonist of Wnt signaling in colonic epithelial cell differentiation. Nat. Genet. 36 (2004) 277-282
97. van Es J.H., Jay P., Gregorieff A., van Gijn M.E., Jonkheer S., Hatzis P., Thiele A., van den Born M., Begthel H., Brabletz T., et al. Wnt signalling induces maturation of Paneth cells in intestinal crypts. Nat. Cell Biol. 7 (2005) 381-386
98. van Es J.H., van Gijn M.E., Riccio O., van den Born M., Vooijs M., Begthel H., Cozijnsen M., Robine S., Winton D.J., Radtke F., and Clevers H. Notch/gamma-secretase inhibition turns proliferative cells in intestinal crypts and adenomas into goblet cells. Nature 435 (2005) 959-963
99. van Genderen C., Okamura R.M., Farinas I., Quo R.G., Parslow T.G., Bruhn L., and Grosschedl R. Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes Dev. 8 (1994) 2691-2703
100. Van Mater D., Kolligs F.T., Dlugosz A.A., and Fearon E.R. Transient activation of beta-catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17 (2003) 1219-1224
101. Vauclair S., Nicolas M., Barrandon Y., and Radtke F. Notch1 is essential for postnatal hair follicle development and homeostasis. Dev. Biol. 284 (2005) 184-193
102. Watt F.M. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21 (2002) 3919-3926
103. Yamamoto N., Tanigaki K., Han H., Hiai H., and Honjo T. Notch/RBP-J signaling regulates epidermis/hair fate determination of hair follicular stem cells. Curr. Biol. 13 (2003) 333-338
104. Yang Q., Bermingham N.A., Finegold M.J., and Zoghbi H.Y. Requirement of Math1 for secretory cell lineage commitment in the mouse intestine. Science 294 (2001) 2155-2158
105. Zeps N., Bentel J.M., Papadimitriou J.M., D'Antuono M.F., and Dawkins H.J. Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation 62 (1998) 221-226