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Development, Vol 126, Issue 20 4557-4568, Copyright © 1999 by Company of Biologists

JOURNAL ARTICLES

Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation

R DasGupta and E Fuchs
Howard Hughes Medical Institute, Department of Molecular Genetics and Cell Biology and Committee on Developmental Biology, The University of Chicago, Chicago, IL 60637, USA.

LEF/TCF DNA-binding proteins act in concert with activated beta -catenin, the product of Wnt signaling, to transactivate downstream target genes. To probe the role of activated LEF/TCF transcription factor complexes in hair follicle morphogenesis and differentiation, we engineered mice harboring TOPGAL, a beta -galactosidase gene under the control of a LEF/TCF and beta -catenin inducible promoter. In mice, TOPGAL expression was directly stimulated by a stabilized form of beta -catenin, but was also dependent upon LEF1/TCF3 in skin. During embryogenesis, TOPGAL activation occurred transiently in a subset of LEF1-positive cells of pluripotent ectoderm and underlying mesenchyme. Downgrowth of initiated follicles proceeded in the absence of detectable TOPGAL expression, even though LEF1 was still expressed. While proliferative matrix cells expressed the highest levels of Lef1 mRNAs, LEF1 concentrated in the precursor cells to the hair shaft, where TOPGAL expression was co-induced with hair-specific keratin genes containing LEF/TCF-binding motifs. LEF1 and TOPGAL expression ceased during catagen and telogen, but reappeared at the start of the postnatal hair cycle, concomitant with precortex formation. In contrast to hair shaft precursor cells, postnatal outer root sheath expressed TCF3, but not TOPGAL. TCF3 was also expressed in the putative follicle stem cells, and while TOPGAL was generally silent in this compartment, it was stimulated at the start of the hair cycle in a fashion that appeared to be dependent upon stabilization of beta -catenin. Taken together, our findings demonstrate that LEF1/TCF3 is necessary but not sufficient for TOPGAL activation, revealing the existence of positive and negative regulators of these factors in the skin. Furthermore, our findings unveil the importance of activated LEF/TCF complexes at distinct times in hair development and cycling when changes in cell fate and differentiation commitments take place.
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PNAS, September 19, 2006; 103(38): 14134 - 14139.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
S. J. Hatsell and P. Cowin
Gli3-mediated repression of Hedgehog targets is required for normal mammary development
Development, September 15, 2006; 133(18): 3661 - 3670.
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 Proc. Natl. Acad. Sci. USAHome page
M. J. Nemeth, M. R. Kirby, and D. M. Bodine
Hmgb3 regulates the balance between hematopoietic stem cell self-renewal and differentiation
PNAS, September 12, 2006; 103(37): 13783 - 13788.
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T.-F. Li, D. Chen, Q. Wu, M. Chen, T.-j. Sheu, E. M. Schwarz, H. Drissi, M. Zuscik, and R. J. O'Keefe
Transforming Growth Factor-beta Stimulates Cyclin D1 Expression through Activation of beta-Catenin Signaling in Chondrocytes
J. Biol. Chem., July 28, 2006; 281(30): 21296 - 21304.
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N. Bhatia, S. Thiyagarajan, I. Elcheva, M. Saleem, A. Dlugosz, H. Mukhtar, and V. S. Spiegelman
Gli2 Is Targeted for Ubiquitination and Degradation by beta-TrCP Ubiquitin Ligase
J. Biol. Chem., July 14, 2006; 281(28): 19320 - 19326.
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H. Rhee, L. Polak, and E. Fuchs
Lhx2 maintains stem cell character in hair follicles.
Science, June 30, 2006; 312(5782): 1946 - 1949.
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 DevelopmentHome page
J. M. Veltmaat, F. Relaix, L. T. Le, K. Kratochwil, F. G. Sala, W. van Veelen, R. Rice, B. Spencer-Dene, A. A. Mailleux, D. P. Rice, et al.
Gli3-mediated somitic Fgf10 expression gradients are required for the induction and patterning of mammary epithelium along the embryonic axes
Development, June 15, 2006; 133(12): 2325 - 2335.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
M. Mukhopadhyay, M. Gorivodsky, S. Shtrom, A. Grinberg, C. Niehrs, M. I. Morasso, and H. Westphal
Dkk2 plays an essential role in the corneal fate of the ocular surface epithelium
Development, June 1, 2006; 133(11): 2149 - 2154.
[Abstract] [Full Text] [PDF]

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W. V. Cardoso and J. Lu
Regulation of early lung morphogenesis: questions, facts and controversies
Development, May 1, 2006; 133(9): 1611 - 1624.
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T. Okada, Y. Ishii, K. Masujin, A. Yasoshima, J. Matsuda, A. Ogura, H. Nakayama, T. Kunieda, and K. Doi
The Critical Roles of Serum/Glucocorticoid-Regulated Kinase 3 (SGK3) in the Hair Follicle Morphogenesis and Homeostasis: The Allelic Difference Provides Novel Insights into Hair Follicle Biology
Am. J. Pathol., April 1, 2006; 168(4): 1119 - 1133.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
T. Ohyama, O. A. Mohamed, M. M. Taketo, D. Dufort, and A. K. Groves
Wnt signals mediate a fate decision between otic placode and epidermis
Development, March 1, 2006; 133(5): 865 - 875.
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 Proc. Natl. Acad. Sci. USAHome page
G. M. J. Beaudoin III, J. M. Sisk, P. A. Coulombe, and C. C. Thompson
Hairless triggers reactivation of hair growth by promoting Wnt signaling
PNAS, October 11, 2005; 102(41): 14653 - 14658.
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 DevelopmentHome page
E. Legue and J.-F. Nicolas
Hair follicle renewal: organization of stem cells in the matrix and the role of stereotyped lineages and behaviors
Development, September 15, 2005; 132(18): 4143 - 4154.
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J. JIMENEZ, G. M. JANG, B. L. SEMLER, and M. L. WATERMAN
An internal ribosome entry site mediates translation of lymphoid enhancer factor-1
RNA, September 1, 2005; 11(9): 1385 - 1399.
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L. Alonso, H. Okada, H. A. Pasolli, A. Wakeham, A. I. You-Ten, T. W. Mak, and E. Fuchs
Sgk3 links growth factor signaling to maintenance of progenitor cells in the hair follicle
J. Cell Biol., August 15, 2005; 170(4): 559 - 570.
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M. M. Riccomagno, S. Takada, and D. J. Epstein
Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh
Genes & Dev., July 1, 2005; 19(13): 1612 - 1623.
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 Genes Dev.Home page
W. E. Lowry, C. Blanpain, J. A. Nowak, G. Guasch, L. Lewis, and E. Fuchs
Defining the impact of {beta}-catenin/Tcf transactivation on epithelial stem cells
Genes & Dev., July 1, 2005; 19(13): 1596 - 1611.
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M. Kleber, H.-Y. Lee, H. Wurdak, J. Buchstaller, M. M. Riccomagno, L. M. Ittner, U. Suter, D. J. Epstein, and L. Sommer
Neural crest stem cell maintenance by combinatorial Wnt and BMP signaling
J. Cell Biol., April 25, 2005; 169(2): 309 - 320.
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H.-M. I. Yu, B. Jerchow, T.-J. Sheu, B. Liu, F. Costantini, J. E. Puzas, W. Birchmeier, and W. Hsu
The role of Axin2 in calvarial morphogenesis and craniosynostosis
Development, April 15, 2005; 132(8): 1995 - 2005.
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 Mol. Cell. Biol.Home page
J. Teuliere, M. M. Faraldo, M. Shtutman, W. Birchmeier, J. Huelsken, J. P. Thiery, and M. A. Glukhova
{beta}-Catenin-Dependent and -Independent Effects of {Delta}N-Plakoglobin on Epidermal Growth and Differentiation
Mol. Cell. Biol., October 1, 2004; 24(19): 8649 - 8661.
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X. Guo, T. F. Day, X. Jiang, L. Garrett-Beal, L. Topol, and Y. Yang
Wnt/{beta}-catenin signaling is sufficient and necessary for synovial joint formation
Genes & Dev., October 1, 2004; 18(19): 2404 - 2417.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
E. Y. Chu, J. Hens, T. Andl, A. Kairo, T. P. Yamaguchi, C. Brisken, A. Glick, J. J. Wysolmerski, and S. E. Millar
Canonical WNT signaling promotes mammary placode development and is essential for initiation of mammary gland morphogenesis
Development, October 1, 2004; 131(19): 4819 - 4829.
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U. Guha, L. Mecklenburg, P. Cowin, L. Kan, W. M. O'Guin, D. D'Vizio, R. G. Pestell, R. Paus, and J. A. Kessler
Bone Morphogenetic Protein Signaling Regulates Postnatal Hair Follicle Differentiation and Cycling
Am. J. Pathol., September 1, 2004; 165(3): 729 - 740.
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 Mol. Biol. CellHome page
J. A. McCormick, Y. Feng, K. Dawson, M. J. Behne, B. Yu, J. Wang, A. W. Wyatt, G. Henke, F. Grahammer, T. M. Mauro, et al.
Targeted Disruption of the Protein Kinase SGK3/CISK Impairs Postnatal Hair Follicle Development
Mol. Biol. Cell, September 1, 2004; 15(9): 4278 - 4288.
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W. T. O'Brien, A. D. Harper, F. Jove, J. R. Woodgett, S. Maretto, S. Piccolo, and P. S. Klein
Glycogen Synthase Kinase-3{beta} Haploinsufficiency Mimics the Behavioral and Molecular Effects of Lithium
J. Neurosci., July 28, 2004; 24(30): 6791 - 6798.
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 Mol. Cell. Biol.Home page
R. Gugasyan, A. Voss, G. Varigos, T. Thomas, R. J. Grumont, P. Kaur, G. Grigoriadis, and S. Gerondakis
The Transcription Factors c-rel and RelA Control Epidermal Development and Homeostasis in Embryonic and Adult Skin via Distinct Mechanisms
Mol. Cell. Biol., July 1, 2004; 24(13): 5733 - 5745.
[Abstract] [Full Text] [PDF]


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