Redefining the structure of the hair follicle by 3D clonal analysis

Development (Cambridge)

Volumn 139, Issue 20, 2012, Pages 3741-3751

  Sequeira, Inês ^a,b   Nicolas, Jean François ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

Companion layer; Germinative layer; Hair follicle; Lgr5; Lower proximal cup; Mouse; Outer root sheath

Indexed keywords

AFIMOXIFENE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL TYPE; ELECTRON MICROSCOPY; HAIR FOLLICLE; HAIR GROWTH; HAIR ROOT; HISTOLOGY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MORPHOGENESIS; MOUSE; NONHUMAN; OUTER ROOT SHEATH; PRIORITY JOURNAL; SKIN; THREE DIMENSIONAL IMAGING;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; HAIR FOLLICLE; IMAGING, THREE-DIMENSIONAL; MICE; RECEPTORS, G-PROTEIN-COUPLED;

MUS;

EID: 84866510066     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.081091     Document Type: Article

References (47)

1. Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J. et al. (2007). Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 449, 1003-1007.
2. Blanpain, C. and Fuchs, E. (2006). Epidermal stem cells of the skin. Annu. Rev. Cell Dev. Biol. 22, 339-373.
3. Claudinot, S., Nicolas, J.-F., Oshima, H., Rochat, A. and Barrandon, Y. (2005). Long-term renewal of hair follicles from clonogenic multipotent stem cells. Proc. Natl. Acad. Sci. USA 102, 14677-14682.
4. Coulombe, P. A., Kopan, R. and Fuchs, E. (1989). Expression of keratin K14 in the epidermis and hair follicle: insights into complex programs of differentiation. J. Cell Biol. 109, 2295-2312.
5. Feil, R., Brocard, J., Mascrez, B., LeMeur, M., Metzger, D. and Chambon, P. (1996). Ligand-activated site-specific recombination in mice. Proc. Natl. Acad. Sci. USA 93, 10887-10890.
6. Fuchs, E. and Horsley, V. (2008). More than one way to skin... Genes Dev. 22, 976-985.
7. Fuchs, E., Merrill, B. J., Jamora, C. and DasGupta, R. (2001). At the roots of a never-ending cycle. Dev. Cell 1, 13-25.
8. Ghazizadeh, S. and Taichman, L. (2001). Multiple classes of stem cells in cutaneous epithelium: a lineage analysis of adult mouse skin. EMBO J. 20, 1215-1222.
9. Greco, V., Chen, T., Rendl, M., Schober, M., Pasolli, H. A., Stokes, N., Dela Cruz-Racelis, J. and Fuchs, E. (2009). A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155-169.
10. Gu, L. H. and Coulombe, P. A. (2007). Keratin expression provides novel insight into the morphogenesis and function of the companion layer in hair follicles. J. Invest. Dermatol. 127, 1061-1073.
11. Hanakawa, Y., Li, H., Lin, C., Stanley, J. R. and Cotsarelis, G. (2004). Desmogleins 1 and 3 in the companion layer anchor mouse anagen hair to the follicle. J. Invest. Dermatol. 123, 817-822.
12. Hardy, M. (1992). The secret life of the hair follicle. Trends Genet. 8, 55-61.
13. Hebert, J. M., Rosenquist, T., Gotz, J. and Martin, G. R. (1994). FGF5 as a regulator of the hair growth cycle: evidence from targeted and spontaneous mutations. Cell 78, 1017-1025.
14. Hsu, Y.-C., Pasolli, H. A. and Fuchs, E. (2011). Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144, 92-105.
15. Ito, M. (1986). The innermost cell layer of the outer root sheath in anagen hair follicle: light and electron microscopic study. Arch. Dermatol. Res. 279, 112-119.
16. Ito, M. (1988). Electron microscopic study on cell differentiation in anagen hair follicles in mice. J. Invest. Dermatol. 90, 65-72.
17. Ito, M. (1989). Biologic roles of the innermost cell layer of the outer root sheath in human anagen hair follicle: further electron microscopic study. Arch. Dermatol. Res. 281, 254-259.
18. Ito, M., Tazawa, T., Shimizu, N., Ito, K., Katsuumi, K., Sato, Y. and Hashimoto, K. (1986). Cell differentiation in human anagen hair and hair follicles studied with anti-hair keratin monoclonal antibodies. J. Invest. Dermatol. 86, 563-569.
19. Jaks, V., Barker, N., Kasper, M., Van Es, J. H., Snippert, H. J., Clevers, H. and Toftgard, R. (2008). Lgr5 marks cycling, yet long-lived, hair follicle stem cells. Nat. Genet. 40, 1291-1299.
20. Kopan, R., Lee, J., Lin, M.-H., Syder, A. J., Kesterson, J., Crutchfield, N., Li, C. R., Wu, W., Books, J. and Gordon, J. I. (2002). Genetic mosaic analysis indicates that the bulb region of coat hair follicles contains a resident population of several active multipotent epithelial lineage progenitors. Dev. Biol. 242, 44-57.
21. Langbein, L. and Schweizer, J. (2005). Keratins of the human hair follicle. Int. Rev. Cytol. 243, 1-78.
22. Langbein, L., Rogers, M. A., Praetzel-Wunder, S., Helmke, B., Schirmacher, P. and Schweizer, J. (2006). K25 (K25irs1), K26 (K25irs2), K27 (K25irs3), and K28 (K25irs4) represent the type I inner root sheath keratins of the human hair follicle. J. Invest. Dermatol. 126, 2377-2386.
23. Legué, E. and Nicolas, J.-F. (2005). Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors. Development 132, 4143-4154.
24. Legué, E., Sequeira, I. and Nicolas, J.-F. (2010). Hair follicle renewal: authentic morphogenesis that depends on a complex progression of stem cell lineages. Development 137, 569-577.
25. Legué, E., Sequeira, I. and Nicolas, J.-F. (2012). Hair follicle stem cells. In Stem Cells and Cancer Stem Cells: Therapeutic Applications in Disease and Injury, Vol. 3 (ed. M. A. Hayat), pp. 35-47. New York: Springer.
26. Metzger, D. and Chambon, P. (2001). Site- and time-specific gene targeting in the mouse. Methods 24, 71-80.
27. Millar, S. (2002). Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216-225.
28. Müller-Röver, S., Handjiski, B., van der Veen, C., Eichmüller, S., Foitzik, K., McKay, I. A., Stenn, K. S. and Paus, R. (2001). A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J. Invest. Dermatol. 117, 3-15.
29. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. and Luo, L. (2007). A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605.
30. Nowak, J. A., Polak, L., Pasolli, H. A. and Fuchs, E. (2008). Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3, 33-43.
31. Orwin, D. F. (1971). Cell differentiation in the lower outer sheath of the Romney wool follicle: a companion cell layer. Aust. J. Biol. Sci. 24, 989-999.
32. Oshima, H., Rochat, A., Kedzia, C., Kobayashi, K. and Barrandon, Y. (2001). Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104, 233-245.
33. Ota, Y., Saitoh, Y., Suzuki, S., Ozawa, K., Kawano, M. and Imamura, T. (2002). Fibroblast growth factor 5 inhibits hair growth by blocking dermal papilla cell activation. Biochem. Biophys. Res. Commun. 290, 169-176.
34. Panteleyev, A., Jahoda, C. A. B. and Christiano, A. M. (2001). Hair follicle predetermination. J. Cell Sci. 114, 3419-3431.
35. Petit, A.-C. and Nicolas, J.-F. (2009). Large-scale clonal analysis reveals unexpected complexity in surface ectoderm morphogenesis. PLoS ONE 4, e4353.
36. Pinkus, H., Iwasaki, T. and Mishima, Y. (1981). Outer root sheath keratinization in anagen and catagen of the mammalian hair follicle. A seventh distinct type of keratinization in the hair follicle: trichilemmal keratinization. J. Anat. 133, 19-35.
37. Poblet, E., Jimenez, F., de Cabo, C., Prieto-Martin, A. and Sánchez-Prieto, R. (2005). The calcium-binding protein calretinin is a marker of the companion cell layer of the human hair follicle. Br. J. Dermatol. 152, 1316-1320.
38. Rochat, A., Kobayashi, K. and Barrandon, Y. (1994). Location of stem cells of human hair follicles by clonal analysis. Cell 76, 1063-1073.
39. Rogers, G. E. (1964). Isolation and properties of inner sheath cells of hair follicles. Exp. Cell Res. 33, 264-276.
40. Rothnagel, J. A. and Roop, D. R. (1995). Hair follicle companion layer: reacquainting an old friend. J. Invest. Dermatol. 104, 42S-43S.
41. Soriano, P. (1999). Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21, 70-71.
42. Stenn, K. S. and Paus, R. (2001). Controls of hair follicle cycling. Physiol. Rev. 81, 449-494.
43. Taylor, G., Lehrer, M. S., Jensen, P. J., Sun, T.-T. and Lavker, R. M. (2000). Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102, 451-461.
44. Vidal, V. P. I., Chaboissier, M.-C., Lützkendorf, S., Cotsarelis, G., Mill, P., Hui, C.-C., Ortonne, N., Ortonne, J.-P. and Schedl, A. (2005). Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment. Curr. Biol. 15, 1340-1351.
45. Wang, Z., Wong, P., Langbein, L., Schweizer, J. and Coulombe, P. A. (2003). Type II epithelial keratin 6hf (K6hf) is expressed in the companion layer, matrix, and medulla in anagen-stage hair follicles. J. Invest. Dermatol. 121, 1276-1282.
46. Winter, H., Langbein, L., Praetzel, S., Jacobs, M., Rogers, M. A., Leigh, I. M., Tidman, N. and Schweizer, J. (1998). A novel human type II cytokeratin, K6hf, specifically expressed in the companion layer of the hair follicle. J. Invest. Dermatol. 111, 955-962.
47. Zhang, Y. V., Cheong, J., Ciapurin, N., Mcdermitt, D. J. and Tumbar, T. (2009). Distinct self-renewal and differentiation phases in the niche of infrequently dividing hair follicle stem cells. Cell Stem Cell 5, 267-278.