Unveiling Hair Follicle Stem Cells

Stem Cell Reviews and Reports

Volumn 6, Issue 4, 2010, Pages 658-664

  Yang, Leilei ^a   Peng, Ruiyun ^a  

^a BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

Author keywords

BMP TGF signaling; Cell fate determination; Hair follicle stem cells; Maintenance; Self renewal; Wnt catenin signaling

Indexed keywords

BETA CATENIN; BONE MORPHOGENETIC PROTEIN; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

ANIMAL; CYTOLOGY; HAIR FOLLICLE; HUMAN; METABOLISM; REVIEW; STEM CELL;

ANIMALS; BETA CATENIN; BONE MORPHOGENETIC PROTEINS; HAIR FOLLICLE; HUMANS; STEM CELLS; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEINS;

MAMMALIA;

EID: 77957351756     PISSN: 15508943     EISSN: 15586804     Source Type: Journal    
DOI: 10.1007/s12015-010-9172-z     Document Type: Review

References (81)

1. Fuchs, E. (2007). Scratching the surface of skin development. Nature, 445(7130), 834-842.
2. Cotsarelis, G., Sun, T. T., & Lavker, R. M. (1990). Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell, 61(7), 1329-1337.
3. Lyle, S., Christofidou-Solomidou, M., Liu, Y., Elder, D. E., Albelda, S., & Cotsarelis, G. (1998). The C8/144B monoclonal antibody recognizes cytokeratin 15 and defines the location of human hair follicle stem cells. Journal of Cell Science, 111(Pt 21), 3179-3188.
4. Ito, M., Liu, Y., Yang, Z., et al. (2005). Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis. Natural Medicines, 11(12), 1351-1354.
5. Levy, V., Lindon, C., Harfe, B. D., & Morgan, B. A. (2005). Distinct stem cell populations regenerate the follicle and interfollicular epidermis. Developmental Cell, 9(6), 855-861.
6. Morris, R. J., & Potten, C. S. (1999). Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen. Journal of Investigative Dermatology, 112(4), 470-475.
7. Taylor, G., Lehrer, M. S., Jensen, P. J., Sun, T. T., & Lavker, R. M. (2000). Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell, 102(4), 451-461.
8. Rochat, A., Kobayashi, K., & Barrandon, Y. (1994). Location of stem cells of human hair follicles by clonal analysis. Cell, 76(6), 1063-1073.
9. Ghazizadeh, S., & Taichman, L. B. (2001). Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin. The EMBO Journal, 20(6), 1215-1222.
10. Braun, K. M., Niemann, C., Jensen, U. B., Sundberg, J. P., Silva-Vargas, V., & Watt, F. M. (2003). Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development, 130(21), 5241-5255.
11. Kobayashi, K., Rochat, A., & Barrandon, Y. (1993). Segregation of keratinocyte colony-forming cells in the bulge of the rat vibrissa. Proceedings of the National Academy of Sciences of the United States of America, 90(15), 7391-7395.
12. Morris, R. J., Liu, Y., Marles, L., et al. (2004). Capturing and profiling adult hair follicle stem cells. Nature Biotechnology, 22(4), 411-417.
13. Trempus, C. S., Morris, R. J., Bortner, C. D., et al. (2003). Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. Journal of Investigative Dermatology, 120(4), 501-511.
14. Cotsarelis, G. (2006). Epithelial stem cells: a folliculocentric view. Journal of Investigative Dermatology, 126(7), 1459-1468.
15. Ohyama, M., Terunuma, A., Tock, C. L., et al. (2006). Characterization and isolation of stem cell-enriched human hair follicle bulge cells. Journal of Clinical Investigation, 116(1), 249-260.
16. Cotsarelis, G. (2006). Gene expression profiling gets to the root of human hair follicle stem cells. Journal of Clinical Investigation, 116(1), 19-22.
17. Vidal, V. P., Chaboissier, M. C., Lutzkendorf, S., et al. (2005). Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Current Biology, 15(15), 1340-1351.
18. DasGupta, R., & Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development, 126(20), 4557-4568.
19. Rhee, H., Polak, L., & Fuchs, E. (2006). Lhx2 maintains stem cell character in hair follicles. Science, 312(5782), 1946-1949.
20. Jaks, V., Barker, N., Kasper, M., et al. (2008). Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nature Genetics, 40(11), 1291-1299.
21. Trempus, C. S., Morris, R. J., Ehinger, M., et al. (2007). CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Research, 67(9), 4173-4181.
22. Tumbar, T., Guasch, G., Greco, V., et al. (2004). Defining the epithelial stem cell niche in skin. Science, 303(5656), 359-363.
23. Roh, C., Tao, Q., Photopoulos, C., & Lyle, S. (2005). In vitro differences between keratinocyte stem cells and transit-amplifying cells of the human hair follicle. Journal of Investigative Dermatology, 125(6), 1099-1105.
24. Blanpain, C., & Fuchs, E. (2006). Epidermal stem cells of the skin. Annual Review of Cell and Developmental Biology, 22, 339-373.
25. Oshima, H., Rochat, A., Kedzia, C., Kobayashi, K., & Barrandon, Y. (2001). Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell, 104(2), 233-245.
26. Claudinot, S., Nicolas, M., Oshima, H., Rochat, A., & Barrandon, Y. (2005). Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proceedings of the National Academy of Sciences of the United States of America, 102(41), 14677-14682.
27. Blanpain, C., Lowry, W. E., 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(5), 635-648.
28. Amoh, Y., Li, L., Katsuoka, K., & Hoffman, R. M. (2009). Multipotent nestin-expressing hair follicle stem cells. The Journal of Dermatology, 36(1), 1-9.
29. Snippert, H. J., Haegebarth, A., Kasper, M., et al. Lgr6 marks stem cells in the hair follicle that generate all cell lineages of the skin. Science, 327(5971), 1385-1389.
30. Nijhof, J. G., Braun, K. M., Giangreco, A., et al. (2006). The cell-surface marker MTS24 identifies a novel population of follicular keratinocytes with characteristics of progenitor cells. Development, 133(15), 3027-3037.
31. Jensen, K. B., Collins, C. A., Nascimento, E., et al. (2009). Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell, 4(5), 427-439.
32. Sarin, K. Y., Cheung, P., Gilison, D., et al. (2005). Conditional telomerase induction causes proliferation of hair follicle stem cells. Nature, 436(7053), 1048-1052.
33. Flores, I., Cayuela, M. L., & Blasco, M. A. (2005). Effects of telomerase and telomere length on epidermal stem cell behavior. Science, 309(5738), 1253-1256.
34. Benitah, S. A., Frye, M., Glogauer, M., & Watt, F. M. (2005). Stem cell depletion through epidermal deletion of Rac1. Science, 309(5736), 933-935.
35. Wu, X., Quondamatteo, F., Lefever, T., et al. (2006). Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes & Development, 20(5), 571-585.
36. Tiede, S., & Paus, R. (2006). Lhx2-decisive role in epithelial stem cell maintenance, or just the "tip of the iceberg"? Bioessays, 28(12), 1157-1160.
37. Nowak, J. A., Polak, L., Pasolli, H. A., & Fuchs, E. (2008). Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell, 3(1), 33-43.
38. Cianferotti, L., Cox, M., Skorija, K., & Demay, M. B. (2007). Vitamin D receptor is essential for normal keratinocyte stem cell function. Proceedings of the National Academy of Sciences of the United States of America, 104(22), 9428-9433.
39. van Genderen, C., Okamura, R. M., Farinas, I., et al. (1994). Development of several organs that require inductive epithelial-mesenchymal interactions is impaired in LEF-1-deficient mice. Genes & Development, 8(22), 2691-2703.
40. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G., & Birchmeier, W. (2001). Beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell, 105(4), 533-545.
41. Andl, T., Reddy, S. T., Gaddapara, T., & Millar, S. E. (2002). WNT signals are required for the initiation of hair follicle development. Developmental Cell, 2(5), 643-653.
42. Zhang, Y., Andl, T., Yang, S. H., et al. (2008). Activation of beta-catenin signaling programs embryonic epidermis to hair follicle fate. Development, 135(12), 2161-2172.
43. Gat, U., DasGupta, R., Degenstein, L., & Fuchs, E. (1998). De Novo hair follicle morphogenesis and hair tumors in mice expressing a truncated beta-catenin in skin. Cell, 95(5), 605-614.
44. van Mater, D., Kolligs, F. T., Dlugosz, A. A., & Fearon, E. R. (2003). Transient activation of beta -catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes & Development, 17(10), 1219-1224.
45. Lo Celso, C., Prowse, D. M., & Watt, F. M. (2004). 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(8), 1787-1799.
46. Lowry, W. E., Blanpain, C., Nowak, J. A., Guasch, G., Lewis, L., & Fuchs, E. (2005). Defining the impact of beta-catenin/Tcf transactivation on epithelial stem cells. Genes & Development, 19(13), 1596-1611.
47. Ito, M., Yang, Z., Andl, T., et al. (2007). Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature, 447(7142), 316-320.
48. Merrill, B. J., Gat, U., DasGupta, R., & Fuchs, E. (2001). Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes & Development, 15(13), 1688-1705.
49. Malanchi, I., Peinado, H., Kassen, D., et al. (2008). Cutaneous cancer stem cell maintenance is dependent on beta-catenin signalling. Nature, 452(7187), 650-653.
50. Xia, J., Urabe, K., Moroi, Y., et al. (2006). Beta-Catenin mutation and its nuclear localization are confirmed to be frequent causes of Wnt signaling pathway activation in pilomatricomas. Journal of Dermatological Science, 41(1), 67-75.
51. Chan, E. F., Gat, U., McNiff, J. M., & Fuchs, E. (1999). A common human skin tumour is caused by activating mutations in beta-catenin. Nature Genetics, 21(4), 410-413.
52. Zhang, J., He, X. C., Tong, W. G., et al. (2006). Bone morphogenetic protein signaling inhibits hair follicle anagen induction by restricting epithelial stem/progenitor cell activation and expansion. Stem Cells, 24(12), 2826-2839.
53. Nguyen, H., Merrill, B. J., Polak, L., et al. (2009). Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nature Genetics, 41(10), 1068-1075.
54. Tetsu, O., & McCormick, F. (1999). Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature, 398(6726), 422-426.
55. Silva-Vargas, V., Lo Celso, C., Giangreco, A., et al. (2005). Beta-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Developmental Cell, 9(1), 121-131.
56. Beaudoin, G. M., 3rd, Sisk, J. M., Coulombe, P. A., & Thompson, C. C. (2005). Hairless triggers reactivation of hair growth by promoting Wnt signaling. Proceedings of the National Academy of Sciences of the United States of America, 102(41), 14653-14658.
57. Wei, G., Ku, S., Ma, G. K., et al. (2007). HIPK2 represses beta-catenin-mediated transcription, epidermal stem cell expansion, and skin tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America, 104(32), 13040-13045.
58. Botchkarev, V. A., Botchkareva, N. V., Roth, W., et al. (1999). Noggin is a mesenchymally derived stimulator of hair-follicle induction. Nature Cell Biology, 1(3), 158-164.
59. Kobielak, K., Pasolli, H. A., Alonso, L., Polak, L., & Fuchs, E. (2003). Defining BMP functions in the hair follicle by conditional ablation of BMP receptor IA. The Journal of Cell Biology, 163(3), 609-623.
60. Kulessa, H., Turk, G., & Hogan, B. L. (2000). Inhibition of Bmp signaling affects growth and differentiation in the anagen hair follicle. The EMBO Journal, 19(24), 6664-6674.
61. Andl, T., Ahn, K., Kairo, A., et al. (2004). Epithelial Bmpr1a regulates differentiation and proliferation in postnatal hair follicles and is essential for tooth development. Development, 131(10), 2257-2268.
62. Botchkarev, V. A. (2003). Bone morphogenetic proteins and their antagonists in skin and hair follicle biology. Journal of Investigative Dermatology, 120(1), 36-47.
63. Botchkarev, V. A., Botchkareva, N. V., Nakamura, M., et al. (2001). Noggin is required for induction of the hair follicle growth phase in postnatal skin. The FASEB Journal, 15(12), 2205-2214.
64. Sharov, A. A., Sharova, T. Y., Mardaryev, A. N., et al. (2006). Bone morphogenetic protein signaling regulates the size of hair follicles and modulates the expression of cell cycle-associated genes. Proceedings of the National Academy of Sciences of the United States of America, 103(48), 18166-18171.
65. Ming Kwan, K., Li, A. G., Wang, X. J., Wurst, W., & Behringer, R. R. (2004). Essential roles of BMPR-IA signaling in differentiation and growth of hair follicles and in skin tumorigenesis. Genesis, 39(1), 10-25.
66. Yang, L., Wang, L., & Yang, X. (2009). Disruption of Smad4 in mouse epidermis leads to depletion of follicle stem cells. Molecular Biology of the Cell, 20(3), 882-890.
67. Mou, C., Jackson, B., Schneider, P., Overbeek, P. A., & Headon, D. J. (2006). Generation of the primary hair follicle pattern. Proceedings of the National Academy of Sciences of the United States of America, 103(24), 9075-9080.
68. Plikus, M. V., Mayer, J. A., de la Cruz, D., et al. (2008). Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature, 451(7176), 340-344.
69. Greco, V., Chen, T., Rendl, M., et al. (2009). A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell, 4(2), 155-169.
70. Kobielak, K., Stokes, N., de la Cruz, J., Polak, L., & Fuchs, E. (2007). Loss of a quiescent niche but not follicle stem cells in the absence of bone morphogenetic protein signaling. Proceedings of the National Academy of Sciences of the United States of America, 104(24), 10063-10068.
71. Moore, K. A., & Lemischka, I. R. (2006). Stem cells and their niches. Science, 311(5769), 1880-1885.
72. Jamora, C., DasGupta, R., Kocieniewski, P., & Fuchs, E. (2003). Links between signal transduction, transcription and adhesion in epithelial bud development. Nature, 422(6929), 317-322.
73. Horsley, V., Aliprantis, A. O., Polak, L., Glimcher, L. H., & Fuchs, E. (2008). NFATc1 balances quiescence and proliferation of skin stem cells. Cell, 132(2), 299-310.
74. Shi, Y., & Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell, 113(6), 685-700.
75. Qiao, W., Li, A. G., Owens, P., Xu, X., Wang, X. J., & Deng, C. X. (2006). Hair follicle defects and squamous cell carcinoma formation in Smad4 conditional knockout mouse skin. Oncogene, 25(2), 207-217.
76. Yang, L., Mao, C., Teng, Y., et al. (2005). Targeted disruption of Smad4 in mouse epidermis results in failure of hair follicle cycling and formation of skin tumors. Cancer Research, 65(19), 8671-8678.
77. Foitzik, K., Lindner, G., Mueller-Roever, S., et al. (2000). Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. The FASEB Journal, 14(5), 752-760.
78. Frederick, J. P., Liberati, N. T., Waddell, D. S., Shi, Y., & Wang, X. F. (2004). Transforming growth factor beta-mediated transcriptional repression of c-myc is dependent on direct binding of Smad3 to a novel repressive Smad binding element. Molecular and Cellular Biology, 24(6), 2546-2559.
79. Arnold, I., & Watt, F. M. (2001). c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Current Biology, 11(8), 558-568.
80. Waikel, R. L., Kawachi, Y., Waikel, P. A., Wang, X. J., & Roop, D. R. (2001). Deregulated expression of c-Myc depletes epidermal stem cells. Nature Genetics, 28(2), 165-168.
81. Zanet, J., Pibre, S., Jacquet, C., Ramirez, A., de Alboran, I. M., & Gandarillas, A. (2005). Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. Journal of Cell Science, 118(Pt 8), 1693-1704.