Sox9 is essential for outer root sheath differentiation and the formation of the hair stem cell compartment

Current Biology

Volumn 15, Issue 15, 2005, Pages 1340-1351

  Vidal, Valerie P I ^a   Chaboissier, Marie Christine ^a   Lützkendorf, Susanne ^f   Cotsarelis, George ^b   Mill, Pleasantine ^c   Hui, Chi Chung ^c   Ortonne, Nicolas ^d   Ortonne, Jean Paul ^e   Schedl, Andreas ^a  

^a CENTRE DE BIOCHIMIE   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^d HENRI MONDOR HOSPITAL   (France)

^e CENTRE HOSPITALIER UNIVERSITAIRE DE NICE   (France)

^f MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HIGH MOBILITY GROUP PROTEIN; SHH PROTEIN, MOUSE; SONIC HEDGEHOG PROTEIN; SOX-9 TRANSCRIPTION FACTOR; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR SOX9;

ALOPECIA; ANIMAL; ARTICLE; BASAL CELL CARCINOMA; COMPARATIVE STUDY; CYTOLOGY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; HAIR FOLLICLE; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; METABOLISM; MOUSE; PHYSIOLOGY; PRENATAL DEVELOPMENT; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; SKIN TUMOR; STEM CELL; TRANSGENIC MOUSE; ULTRASTRUCTURE;

ALOPECIA; ANIMALS; CARCINOMA, BASAL CELL; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; HAIR FOLLICLE; HEDGEHOG PROTEINS; HIGH MOBILITY GROUP PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MICE; MICE, TRANSGENIC; MICROSCOPY, ELECTRON, SCANNING; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; STEM CELLS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ERINACEIDAE; MAMMALIA;

EID: 23244443556     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2005.06.064     Document Type: Article

References (62)

1. E. Fuchs, B.J. Merrill, C. Jamora, and R. DasGupta At the roots of a never-ending cycle Dev Cell 1 2001 13 25
2. S.E. Millar Molecular mechanisms regulating hair follicle development J. Invest. Dermatol. 118 2002 216 225
3. R. Paus, and G. Cotsarelis The biology of hair follicles N. Engl. J. Med. 341 1999 491 497
4. K.S. Stenn, and R. Paus Controls of hair follicle cycling Physiol. Rev. 81 2001 449 494
5. G. Cotsarelis, T.T. Sun, and R.M. Lavker 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
6. R.J. Morris, Y. Liu, L. Marles, Z. Yang, C. Trempus, S. Li, J.S. Lin, J.A. Sawicki, and G. Cotsarelis Capturing and profiling adult hair follicle stem cells Nat. Biotechnol. 22 2004 411 417
7. R.J. Morris, and C.S. Potten Highly persistent label-retaining cells in the hair follicles of mice and their fate following induction of anagen J. Invest. Dermatol. 112 1999 470 475
8. L.C. Wang, Z.Y. Liu, L. Gambardella, A. Delacour, R. Shapiro, J. Yang, I. Sizing, P. Rayhorn, E.A. Garber, and C.D. Benjamin Regular articles: conditional disruption of hedgehog signaling pathway defines its critical role in hair development and regeneration J. Invest. Dermatol. 114 2000 901 908
9. N. Sato, P.L. Leopold, and R.G. Crystal Induction of the hair growth phase in postnatal mice by localized transient expression of Sonic hedgehog J. Clin. Invest. 104 1999 855 864
10. C. Lo Celso, D.M. Prowse, and F.M. Watt 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
11. D. Van Mater, F.T. Kolligs, A.A. Dlugosz, and E.R. Fearon 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
12. J. Huelsken, R. Vogel, B. Erdmann, G. Cotsarelis, and W. Birchmeier beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin Cell 105 2001 533 545
13. H. Oshima, A. Rochat, C. Kedzia, K. Kobayashi, and Y. Barrandon Morphogenesis and renewal of hair follicles from adult multipotent stem cells Cell 104 2001 233 245
14. G.E. Schepers, R.D. Teasdale, and P. Koopman Twenty pairs of sox: extent, homology, and nomenclature of the mouse and human sox transcription factor gene families Dev. Cell 3 2002 167 170
15. P. Sudbeck, M.L. Schmitz, P.A. Baeuerle, and G. Scherer Sex reversal by loss of the C-terminal transactivation domain of human SOX9 Nat. Genet. 13 1996 230 232
16. P. De Santa Barbara, N. Bonneaud, B. Boizet, M. Desclozeaux, B. Moniot, P. Sudbeck, G. Scherer, F. Poulat, and P. Berta Direct interaction of SRY-related protein SOX9 and steroidogenic factor 1 regulates transcription of the human anti-Mullerian hormone gene Mol. Cell. Biol. 18 1998 6653 6665
17. N.A. Arango, R. Lovell-Badge, and R.R. Behringer Targeted mutagenesis of the endogenous mouse Mis gene promoter: in vivo definition of genetic pathways of vertebrate sexual development Cell 99 1999 409 419
18. D.M. Bell, K.K. Leung, S.C. Wheatley, L.J. Ng, S. Zhou, K.W. Ling, M.H. Sham, P. Koopman, P.P. Tam, and K.S. Cheah SOX9 directly regulates the type-II collagen gene Nat. Genet. 16 1997 174 178
19. K. Ohe, E. Lalli, and P. Sassone-Corsi A direct role of SRY and SOX proteins in pre-mRNA splicing Proc. Natl. Acad. Sci. USA 99 2002 1146 1151
20. J.W. Foster, M.A. Dominguez Steglich, S. Guioli, G. Kowk, P.A. Weller, M. Stevanovic, J. Weissenbach, S. Mansour, I.D. Young, and P.N. Goodfellow Campomelic dysplasia and autosomal sex reversal caused by mutations in an SRY-related gene Nature 372 1994 525 530
21. T. Wagner, J. Wirth, J. Meyer, B. Zabel, M. Held, J. Zimmer, J. Pasantes, F.D. Bricarelli, J. Keutel, and E. Hustert Autosomal sex reversal and campomelic dysplasia are caused by mutations in and around the SRY-related gene SOX9 Cell 79 1994 1111 1120
22. C.S. Houston, J.M. Opitz, J.W. Spranger, R.I. Macpherson, M.H. Reed, E.F. Gilbert, J. Herrmann, and A. Schinzel The campomelic syndrome: review, report of 17 cases, and follow-up on the currently 17-year-old boy first reported by Maroteaux et al in 1971 Am. J. Med. Genet. 15 1983 3 28
23. W. Bi, J.M. Deng, Z. Zhang, R.R. Behringer, and B. de Crombrugghe Sox9 is required for cartilage formation Nat. Genet. 22 1999 85 89
24. W. Bi, W. Huang, D.J. Whitworth, J.M. Deng, Z. Zhang, R.R. Behringer, and B. de Crombrugghe Haploinsufficiency of Sox9 results in defective cartilage primordia and premature skeletal mineralization Proc. Natl. Acad. Sci. USA 98 2001 6698 6703
25. H. Akiyama, M.C. Chaboissier, J.F. Martin, A. Schedl, and B. de Crombrugghe The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 Genes Dev. 16 2002 2813 2828
26. M.C. Chaboissier, A. Kobayashi, V.I. Vidal, S. Lutzkendorf, H.J. van de Kant, M. Wegner, D.G. de Rooij, R.R. Behringer, and A. Schedl Functional analysis of Sox8 and Sox9 during sex determination in the mouse Development 131 2004 1891 1901
27. H. Akiyama, M.C. Chaboissier, R.R. Behringer, D.H. Rowitch, A. Schedl, J.A. Epstein, and B. de Crombrugghe Essential role of Sox9 in the pathway that controls formation of cardiac valves and septa Proc. Natl. Acad. Sci. USA 101 2004 6502 6507
28. C.C. Stolt, P. Lommes, E. Sock, M.C. Chaboissier, A. Schedl, and M. Wegner The Sox9 transcription factor determines glial fate choice in the developing spinal cord Genes Dev. 17 2003 1677 1689
29. M. Cheung, M.C. Chaboissier, A. Mynett, E. Hirst, A. Schedl, and J. Briscoe The transcriptional control of trunk neural crest induction, survival, and delamination Dev. Cell 8 2005 179 192
30. T. Tumbar, G. Guasch, V. Greco, C. Blanpain, W.E. Lowry, M. Rendl, and E. Fuchs Defining the epithelial stem cell niche in skin Science 303 2004 359 363
31. C.S. Trempus, R.J. Morris, C.D. Bortner, G. Cotsarelis, R.S. Faircloth, J.M. Reece, and R.W. Tennant Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34 J. Invest. Dermatol. 120 2003 501 511
32. C. Blanpain, W.E. Lowry, A. Geoghegan, L. Polak, and E. Fuchs Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche Cell 118 2004 635 648
33. I.S. Thorey, K. Muth, A.P. Russ, J. Otte, A. Reffelmann, and H. von Melchner Selective disruption of genes transiently induced in differentiating mouse embryonic stem cells by using gene trap mutagenesis and site-specific recombination Mol. Cell. Biol. 18 1998 3081 3088
34. J.P. Sundberg, and M.E. Hogan Hair types and subtypes in the laboratory mouse J.P. Sundberg Handbook of Mouse Mutations with Skin and Hair Abnormalities 1994 CRC Press London 57 68
35. A. Brancaccio, A. Minichiello, M. Grachtchouk, D. Antonini, H. Sheng, R. Parlato, N. Dathan, A.A. Dlugosz, and C. Missero Requirement of the forkhead gene Foxe1, a target of sonic hedgehog signaling, in hair follicle morphogenesis Hum. Mol. Genet. 13 2004 2595 2606
36. C.K. Kaufman, P. Zhou, H.A. Pasolli, M. Rendl, D. Bolotin, K.C. Lim, X. Dai, M.L. Alegre, and E. Fuchs GATA-3: an unexpected regulator of cell lineage determination in skin Genes Dev. 17 2003 2108 2122
37. C. Chiang, Y. Litingtung, E. Lee, K.E. Young, J.L. Corden, H. Westphal, and P.A. Beachy Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function Nature 383 1996 407 413
38. H. Sheng, S. Goich, A. Wang, M. Grachtchouk, L. Lowe, R. Mo, K. Lin, F.J. de Sauvage, H. Sasaki, and C.C. Hui Dissecting the oncogenic potential of Gli2: deletion of an NH(2)-terminal fragment alters skin tumor phenotype Cancer Res. 62 2002 5308 5316
39. M. Grachtchouk, R. Mo, S. Yu, X. Zhang, H. Sasaki, C.C. Hui, and A.A. Dlugosz Basal cell carcinomas in mice overexpressing Gli2 in skin Nat. Genet. 24 2000 216 217
40. A.E. Oro, K.M. Higgins, Z. Hu, J.M. Bonifas, E.H. Epstein Jr., and M.P. Scott Basal cell carcinomas in mice overexpressing sonic hedgehog Science 276 1997 817 821
41. P. Mill, R. Mo, H. Fu, M. Grachtchouk, P.C. Kim, A.A. Dlugosz, and C.C. Hui Sonic hedgehog-dependent activation of Gli2 is essential for embryonic hair follicle development Genes Dev. 17 2003 282 294
42. D. Pennisi, J. Gardner, D. Chambers, B. Hosking, J. Peters, G. Muscat, C. Abbott, and P. Koopman Mutations in Sox18 underlie cardiovascular and hair follicle defects in ragged mice Nat. Genet. 24 2000 434 437
43. D. Pennisi, J. Bowles, A. Nagy, G. Muscat, and P. Koopman Mice null for sox18 are viable and display a mild coat defect Mol. Cell. Biol. 20 2000 9331 9336
44. J. Roose, W. Korver, E. Oving, A. Wilson, G. Wagenaar, M. Markman, W. Lamers, and H. Clevers High expression of the HMG box factor sox-13 in arterial walls during embryonic development Nucleic Acids Res. 26 1998 469 476
45. D. Lang, M.M. Lu, L. Huang, K.A. Engleka, M. Zhang, E.Y. Chu, S. Lipner, A. Skoultchi, S.E. Millar, and J.A. Epstein Pax3 functions at a nodal point in melanocyte stem cell differentiation Nature 433 2005 884 887
46. B. St-Jacques, H.R. Dassule, I. Karavanova, V.A. Botchkarev, J. Li, P.S. Danielian, J.A. McMahon, P.M. Lewis, R. Paus, and A.P. McMahon Sonic hedgehog signaling is essential for hair development Curr. Biol. 8 1998 1058 1068
47. C. Chiang, R.Z. Swan, M. Grachtchouk, M. Bolinger, Y. Litingtung, E.K. Robertson, M.K. Cooper, W. Gaffield, H. Westphal, and P.A. Beachy Essential role for Sonic hedgehog during hair follicle morphogenesis Dev. Biol. 205 1999 1 9
48. L. Zeng, H. Kempf, L.C. Murtaugh, M.E. Sato, and A.B. Lassar Shh establishes an Nkx3.2/Sox9 autoregulatory loop that is maintained by BMP signals to induce somitic chondrogenesis Genes Dev. 16 2002 1990 2005
49. S. Tavella, R. Biticchi, A. Schito, E. Minina, D. Di Martino, A. Pagano, A. Vortkamp, W.A. Horton, R. Cancedda, and S. Garofalo Targeted expression of SHH affects chondrocyte differentiation, growth plate organization, and Sox9 expression J. Bone Miner. Res. 19 2004 1678 1688
50. B. St-Jacques, M. Hammerschmidt, and A.P. McMahon Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation Genes Dev. 13 1999 2072 2086
51. Niemann, C., Unden, A.B., Lyle, S., Zouboulis Ch, C., Toftgard, R., and Watt, F.M. (2003). Indian hedgehog and beta-catenin signaling: role in the sebaceous lineage of normal and neoplastic mammalian epidermis. Proc. Natl. Acad. Sci. USA Suppl. 100, 11873-11880
52. M.E. Hutchin, M.S. Kariapper, M. Grachtchouk, A. Wang, L. Wei, D. Cummings, J. Liu, L.E. Michael, A. Glick, and A.A. Dlugosz Sustained Hedgehog signaling is required for basal cell carcinoma proliferation and survival: conditional skin tumorigenesis recapitulates the hair growth cycle Genes Dev. 19 2005 214 223
53. N. Dahmane, J. Lee, P. Robins, P. Heller, and A. Ruiz i Altaba Activation of the transcription factor Gli1 and the Sonic hedgehog signalling pathway in skin tumours Nature 389 1997 876 881
54. P. Blache, M. van de Wetering, I. Duluc, C. Domon, P. Berta, J.N. Freund, H. Clevers, and P. Jay SOX9 is an intestine crypt transcription factor, is regulated by the Wnt pathway, and represses the CDX2 and MUC2 genes J. Cell Biol. 166 2004 37 47
55. C. Dong, D. Wilhelm, and P. Koopman Sox genes and cancer Cytogenet. Genome Res. 105 2004 442 447
56. J.K. Guo, A.L. Menke, M.C. Gubler, A.R. Clarke, D. Harrison, A. Hammes, N.D. Hastie, and A. Schedl WT1 is a key regulator of podocyte function: reduced expression levels cause crescentic glomerulonephritis and mesangial sclerosis Hum. Mol. Genet. 11 2002 651 659
57. Hammes, A., and Schedl, A. (2000). Generation of transgenic mice from plasmids, BACs and YACs. In Mouse Genetics and Transgenics: A Practical Approach, First Edition, I.J. Jackson and C.M. Abbott, eds. (New York: Oxford University Press), pp. 217-245.
58. H. Akiyama, M.C. Chaboissier, J.F. Martin, A. Schedl, and B. de Crombrugghe The transcription factor Sox9 has essential roles in successive steps of the chondrocyte differentiation pathway and is required for expression of Sox5 and Sox6 Genes Dev. 16 2002 2813 2828
59. Wilkinson, D.G. (1992). Whole mount in situ of vertebrate embryos. In In Situ Hybridization: A Practical Approach, D.G. Wilkinson, ed. (Oxford, UK: Oxford University Press), pp. 75-83.
60. S. Morais da Silva, A. Hacker, V. Harley, P. Goodfellow, A. Swain, and R. Lovell-Badge Sox9 expression during gonadal development implies a conserved role for the gene in testis differentiation in mammals and birds Nat. Genet. 14 1996 62 68
61. B. Lescher, B. Haenig, and A. Kispert sFRP-2 is a target of the Wnt-4 signaling pathway in the developing metanephric kidney Dev. Dyn. 213 1998 440 451
62. B. Hogan, R. Beddington, F. Costantini, and E. Lacy Manipulating The Mouse Embryo: A Laboratory Manual Second Edition 1994 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY