Lrig1 Expression Defines a Distinct Multipotent Stem Cell Population in Mammalian Epidermis

Cell Stem Cell

Volumn 4, Issue 5, 2009, Pages 427-439

  Jensen, Kim B ^a   Collins, Charlotte A ^a   Nascimento, Elisabete ^a   Tan, David W ^a   Frye, Michaela ^a   Itami, Satoshi ^b   Watt, Fiona M ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

STEMCELL

Indexed keywords

BETA CATENIN; CELL PROTEIN; PROTEIN LRIG1; RETINOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL ISOLATION; CELL POPULATION; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS; FLOW CYTOMETRY; HAIR FOLLICLE; HOMEOSTASIS; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEBACEOUS GLAND; STEM CELL;

ANIMALS; BETA CATENIN; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; EPIDERMIS; HAIR FOLLICLE; MAMMALS; MEMBRANE GLYCOPROTEINS; MICE; MICE, TRANSGENIC; MULTIPOTENT STEM CELLS; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS C-MYC;

MAMMALIA;

EID: 65349166258     PISSN: 19345909     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stem.2009.04.014     Document Type: Article

References (47)

1. Arnold I., and Watt F.M. c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr. Biol. 11 (2001) 558-568
2. 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
3. Bleul C.C., Corbeaux T., Reuter A., Fisch P., Monting J.S., and Boehm T. Formation of a functional thymus initiated by a postnatal epithelial progenitor cell. Nature 441 (2006) 992-996
4. Braun K.M., Niemann C., Jensen U.B., Sundberg J.P., Silva-Vargas V., and Watt F.M. Manipulation of stem cell proliferation and lineage commitment: Visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130 (2003) 5241-5255
5. Chuong C.M. Regenerative biology: New hair from healing wounds. Nature 447 (2007) 265-266
6. Clayton E., Doupé D.P., Klein A.M., Winton D.J., Simons B.D., and Jones P.H. A single type of progenitor cell maintains normal epidermis. Nature 446 (2007) 185-189
7. Collins C.A., and Watt F.M. Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling. Dev. Biol. 324 (2008) 55-67
8. 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
9. Estrach S., Ambler C.A., Lo Celso C., Hozumi K., and Watt F.M. Jagged 1 is a beta-catenin target gene required for ectopic hair follicle formation in adult epidermis. Development 133 (2006) 4427-4438
10. Fuchs E., Tumbar T., and Guasch G. Socializing with the neighbors: Stem cells and their niche. Cell 116 (2004) 769-778
11. Gambardella L., and Barrandon Y. The multifaceted adult epidermal stem cell. Curr. Opin. Cell Biol. 15 (2003) 771-777
12. Gu L.H., and Coulombe P.A. Keratin expression provides novel insight into the morphogenesis and function of the companion layer in hair follicles. J. Invest. Dermatol. 127 (2007) 1061-1073
13. Gur G., Rubin C., Katz M., Amit I., Citri A., Nilsson J., Amariglio N., Henriksson R., Rechavi G., Hedman H., et al. LRIG1 restricts growth factor signaling by enhancing receptor ubiquitylation and degradation. EMBO J. 23 (2004) 3270-3281
14. He T.C., Sparks A.B., Rago C., Hermeking H., Zawel L., da Costa L.T., Morin P.J., Vogelstein B., and Kinzler K.W. Identification of c-MYC as a target of the APC pathway. Science 281 (1998) 1509-1512
15. Hong K.U., Reynolds S.D., Watkins S., Fuchs E., and Stripp B.R. Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am. J. Pathol. 164 (2004) 577-588
16. Horsley V., Aliprantis A.O., Polak L., Glimcher L.H., and Fuchs E. NFATc1 balances quiescence and proliferation of skin stem cells. Cell 132 (2008) 299-310
17. 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
18. Hsu S.Y., Kudo M., Chen T., Nakabayashi K., Bhalla A., van der Spek P.J., van Duin M., and Hsueh A.J. The three subfamilies of leucine-rich repeat-containing G protein-coupled receptors (LGR): Identification of LGR6 and LGR7 and the signaling mechanism for LGR7. Mol. Endocrinol. 14 (2000) 1257-1271
19. 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
20. Ito M., Yang Z., Andl T., Cui C., Kim N., Millar S.E., and Cotsarelis G. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447 (2007) 316-320
21. Jaks V., Barker N., Kasper M., van Es J.H., Snippert H.J., Clevers H., and Toftgard R. Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 40 (2008) 1291-1299
22. Jensen K.B., and Watt F.M. 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 (2006) 11958-11963
23. Jensen U.B., Yan X., Triel C., Woo S.H., Christensen R., and Owens D.M. A distinct population of clonogenic and multipotent murine follicular keratinocytes residing in the upper isthmus. J. Cell Sci. 121 (2008) 609-617
24. Jones P.H., Simons B.D., and Watt F.M. Sic transit gloria: Farewell to the epidermal transit amplifying cell?. Cell Stem Cell 1 (2007) 371-381
25. Kawamoto S., Niwa H., Tashiro F., Sano S., Kondoh G., Takeda J., Tabayashi K., and Miyazaki J. A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470 (2000) 263-268
26. Laederich M.B., Funes-Duran M., Yen L., Ingalla E., Wu X., Carraway III K.L., and Sweeney C. The leucine-rich repeat protein LRIG1 is a negative regulator of ErbB family receptor tyrosine kinases. J. Biol. Chem. 279 (2004) 47050-47056
27. Levy V., Lindon C., Zheng Y., Harfe B.D., and Morgan B.A. Epidermal stem cells arise from the hair follicle after wounding. FASEB J. 21 (2007) 1358-1366
28. Liu Y., Lyle S., Yang Z., and Cotsarelis G. Keratin 15 promoter targets putative epithelial stem cells in the hair follicle bulge. J. Invest. Dermatol. 121 (2003) 963-968
29. 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
30. Lo Celso C., Berta M.A., Braun K.M., Frye M., Lyle S., Zouboulis C.C., and Watt F.M. Characterization of bipotential epidermal progenitors derived from human sebaceous gland: Contrasting roles of c-Myc and beta-catenin. Stem Cells 26 (2008) 1241-1252
31. Lustig B., Jerchow B., Sachs M., Weiler S., Pietsch T., Karsten U., van de Wetering M., Clevers H., Schlag P.M., Birchmeier W., and Behrens J. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell. Biol. 22 (2002) 1184-1193
32. Lyle S., Christofidou-Solomidou M., Liu Y., Elder D.E., Albelda S., and Cotsarelis G. The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. J. Cell Sci. 111 (1998) 3179-3188
33. Majo F., Rochat A., Nicolas M., Jaoude G.A., and Barrandon Y. Oligopotent stem cells are distributed throughout the mammalian ocular surface. Nature 456 (2008) 250-254
34. Morrison S.J., and Spradling A.C. Stem cells and niches: Mechanisms that promote stem cell maintenance throughout life. Cell 132 (2008) 598-611
35. Nijhof J.G., Braun K.M., Giangreco A., van Pelt C., Kawamoto H., Boyd R.L., Willemze R., Mullenders L.H., Watt F.M., de Gruijl F.R., and van Ewijk W. The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development 133 (2006) 3027-3037
36. Nowak J.A., Polak L., Pasolli H.A., and Fuchs E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3 (2008) 33-43
37. Owens D.M., and Watt F.M. Contribution of stem cells and differentiated cells to epidermal tumours. Nat. Rev. Cancer 3 (2003) 444-451
38. 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
39. Soucek L., Whitfield J., Martins C.P., Finch A.J., Murphy D.J., Sodir N.M., Karnezis A.N., Swigart L.B., Nasi S., and Evan G.I. Modelling Myc inhibition as a cancer therapy. Nature 455 (2008) 679-683
40. Suzuki Y., Miura H., Tanemura A., Kobayashi K., Kondoh G., Sano S., Ozawa K., Inui S., Nakata A., Takagi T., et al. Targeted disruption of LIG-1 gene results in psoriasiform epidermal hyperplasia. FEBS Lett. 521 (2002) 67-71
41. Tani H., Morris R.J., and Kaur P. Enrichment for murine keratinocyte stem cells based on cell surface phenotype. Proc. Natl. Acad. Sci. USA 97 (2000) 10960-10965
42. Trempus C.S., Morris R.J., Bortner C.D., Cotsarelis G., Faircloth R.S., Reece J.M., and Tennant R.W. Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 120 (2003) 501-511
43. Vasioukhin V., Degenstein L., Wise B., and Fuchs E. The magical touch: Genome targeting in epidermal stem cells induced by tamoxifen application to mouse skin. Proc. Natl. Acad. Sci. USA 96 (1999) 8551-8556
44. Waikel R.L., Kawachi Y., Waikel P.A., Wang X.J., and Roop D.R. Deregulated expression of c-Myc depletes epidermal stem cells. Nat. Genet. 28 (2001) 165-168
45. Walzer C., Benathan M., and Frenk E. Thermolysin treatment: A new method for dermo-epidermal separation. J. Invest. Dermatol. 92 (1989) 78-81
46. Watt F.M. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J. 21 (2002) 3919-3926
47. Watt F.M., and Hogan B.L. Out of Eden: Stem cells and their niches. Science 287 (2000) 1427-1430