In vivo transcriptional governance of hair follicle stem cells by canonical Wnt regulators (original) (raw)

• Clevers, H. & Nusse, R. Wnt–β-catenin signaling and disease. Cell 149, 1192–1205 (2012).
  Article CAS PubMed Google Scholar
• Willert, K. & Nusse, R. β-catenin: a key mediator of Wnt signaling. Curr. Opin. Genet. Dev. 8, 95–102 (1998).
  Article CAS PubMed Google Scholar
• Korinek, V. et al. Depletion of epithelial stem-cell compartments in the small intestine of mice lacking Tcf-4. Nat. Genet. 19, 379–383 (1998).
  Article CAS PubMed Google Scholar
• Sato, T. & Clevers, H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340, 1190–1194 (2013).
  Article CAS PubMed Google Scholar
• Willert, K. et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448–452 (2003).
  Article CAS PubMed Google Scholar
• Sato, N., Meijer, L., Skaltsounis, L., Greengard, P. & Brivanlou, A.H. Maintenance of pluripotency in human and mouse embryonic stem cells through activation of Wnt signaling by a pharmacological GSK-3-specific inhibitor. Nat. Med. 10, 55–63 (2004).
  Article CAS PubMed Google Scholar
• DasGupta, R. & Fuchs, E. Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557–4568 (1999).
  CAS PubMed Google Scholar
• Merrill, B. J., Gat, U., DasGupta, R. & Fuchs, E. Tcf3 and Lef1 regulate lineage differentiation of multipotent stem cells in skin. Genes Dev. 15, 1688–1705 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Wray, J. et al. Inhibition of glycogen synthase kinase-3 alleviates Tcf3 repression of the pluripotency network and increases embryonic stem cell resistance to differentiation. Nat. Cell Biol. 13, 838–845 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Lyashenko, N. et al. Differential requirement for the dual functions of β-catenin in embryonic stem cell self-renewal and germ layer formation. Nat. Cell Biol. 13, 753–761 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Yi, F., Pereira, L. & Merrill, B.J. Tcf3 functions as a steady-state limiter of transcriptional programs of mouse embryonic stem cell self-renewal. Stem Cells 26, 1951–1960 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Ten Berge, D. et al. Embryonic stem cells require Wnt proteins to prevent differentiation to epiblast stem cells. Nat. Cell Biol. 13, 1070–1075 (2011).
  Article CAS PubMed Google Scholar
• Shy, B. R. et al. Regulation of Tcf7l1 DNA binding and protein stability as principal mechanisms of Wnt–β-catenin signaling. Cell Rep. 4, 1–9 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Yi, F. et al. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat. Cell Biol. 13, 762–70 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Merrill, B. J. et al. Tcf3: a transcriptional regulator of axis induction in the early embryo. Development 131, 263–274 (2004).
  Article CAS PubMed Google Scholar
• Gat, U., DasGupta, R., Degenstein, L. & Fuchs, E. De novo hair follicle morphogenesis and hair tumors in mice expressing a truncated β-catenin in skin. Cell 95, 605–614 (1998).
  Article CAS PubMed Google Scholar
• Nguyen, H. et al. Tcf3 and Tcf4 are essential for long-term homeostasis of skin epithelia. Nat. Genet. 41, 1068–1075 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Nguyen, H., Rendl, M. & Fuchs, E. Tcf3 governs stem cell features and represses cell fate determination in skin. Cell 127, 171–183 (2006).
  Article CAS PubMed Google Scholar
• Wu, C.I. et al. Function of Wnt–β-catenin in counteracting Tcf3 repression through the Tcf3-β-catenin interaction. Development 139, 2118–2129 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Van de Wetering, M. et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell 111, 241–250 (2002).
  Article CAS PubMed Google Scholar
• Korinek, V. et al. Constitutive transcriptional activation by a β-catenin-Tcf complex in APC-/- colon carcinoma. Science 275, 1784–1787 (1997).
  Article CAS PubMed Google Scholar
• Angus-Hill, M. L., Elbert, K. M., Hidalgo, J. & Capecchi, M. R. T-cell factor 4 functions as a tumor suppressor whose disruption modulates colon cell proliferation and tumorigenesis. Proc. Natl Acad. Sci. USA 108, 4914–4919 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Tang, W. et al. A genome-wide RNAi screen for Wnt–β-catenin pathway components identifies unexpected roles for TCF transcription factors in cancer. Proc. Natl Acad. Sci. USA 105, 9697–9702 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Hoffman, J. A., Wu, C. I. & Merrill, B. J. Tcf7l1 prepares epiblast cells in the gastrulating mouse embryo for lineage specification. Development 140, 1665–1675 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Trompouki, E. et al. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 147, 577–589 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Verzi, M. P. et al. TCF4 and CDX2, major transcription factors for intestinal function, converge on the same cis-regulatory regions. Proc. Natl Acad. Sci. USA 107, 15157–15162 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Boj, S. F. et al. Diabetes risk gene and Wnt effector Tcf7l2/TCF4 controls hepatic response to perinatal and adult metabolic demand. Cell 151, 1595–1607 (2012).
  Article CAS PubMed Google Scholar
• Cole, M. F., Johnstone, S. E., Newman, J. J., Kagey, M. H. & Young, R. A. Tcf3 is an integral component of the core regulatory circuitry of embryonic stem cells. Genes Dev. 22, 746–755 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Cavallo, R. A. et al. Drosophila Tcf and Groucho interact to repress Wingless signalling activity. Nature 395, 604–608 (1998).
  Article CAS PubMed Google Scholar
• Brantjes, H., Roose, J., van De Wetering, M. & Clevers, H. All Tcf HMG box transcription factors interact with Groucho-related co-repressors. Nucleic Acids Res. 29, 1410–1419 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Hurlstone, A. & Clevers, H. T-cell factors: turn-ons and turn-offs. EMBO J. 21, 2303–2311 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, G. & Courey, A. J. Groucho/TLE family proteins and transcriptional repression. Gene 249, 1–16 (2000).
  Article CAS PubMed Google Scholar
• Liu, C. et al. Control of β-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108, 837–847 (2002).
  Article CAS PubMed Google Scholar
• Lo, M. C., Gay, F., Odom, R., Shi, Y. & Lin, R. Phosphorylation by the β-catenin/MAPK complex promotes 14-3-3-mediated nuclear export of TCF/POP-1 in signal-responsive cells in C. elegans . Cell 117, 95–106 (2004).
  Article CAS PubMed Google Scholar
• Hikasa, H. et al. Regulation of TCF3 by Wnt-dependent phosphorylation during vertebrate axis specification. Dev. Cell 19, 521–532 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Park, M. H. et al. Phosphorylation of β-catenin at serine 663 regulates its transcriptional activity. Biochem. Biophys. Res. Commun. 419, 543–549 (2012).
  Article CAS PubMed Google Scholar
• Blanpain, C. & Fuchs, E. Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10, 207–217 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Blanpain, C., Lowry, W. E., Geoghegan, A., Polak, L. & Fuchs, E. Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118, 635–648 (2004).
  Article CAS PubMed Google Scholar
• Millar, S. E. Molecular mechanisms regulating hair follicle development. J. Invest. Dermatol. 118, 216–225 (2002).
  Article CAS PubMed Google Scholar
• Schmidt-Ullrich, R. & Paus, R. Molecular principles of hair follicle induction and morphogenesis. Bioessays 27, 247–261 (2005).
  Article CAS PubMed Google Scholar
• Cotsarelis, G., Sun, T. T. & 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, 1329–1337 (1990).
  Article CAS PubMed Google Scholar
• Lustig, B. et al. Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors. Mol. Cell Biol. 22, 1184–1193 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Greco, V. et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell 4, 155–169 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lowry, W. E. et al. Defining the impact of β-catenin/Tcf transactivation on epithelial stem cells. Genes Dev. 19, 1596–1611 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Posthaus, H. et al. β-Catenin is not required for proliferation and differentiation of epidermal mouse keratinocytes. J. Cell Sci. 115, 4587–4595 (2002).
  Article CAS PubMed Google Scholar
• Hsu, Y. C., Pasolli, H. A. & Fuchs, E. Dynamics between stem cells, niche, and progeny in the hair follicle. Cell 144, 92–105 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, T. et al. An RNA interference screen uncovers a new molecule in stem cell self-renewal and long-term regeneration. Nature 485, 104–108 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zhou, P., Byrne, C., Jacobs, J. & Fuchs, E. Lymphoid enhancer factor 1 directs hair follicle patterning and epithelial cell fate. Genes Dev. 9, 700–713 (1995).
  Article CAS PubMed Google Scholar
• Lien, W. H. et al. Genome-wide maps of histone modifications unwind in vivo chromatin states of the hair follicle lineage. Cell Stem Cell 9, 219–232 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Landt, S. G. et al. ChIP-seq guidelines and practices of the ENCODE and modENCODE consortia. Genome Res. 22, 1813–1831 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
  Article PubMed PubMed Central Google Scholar
• Beronja, S., Livshits, G., Williams, S. & Fuchs, E. Rapid functional dissection of genetic networks via tissue-specific transduction and RNAi in mouse embryos. Nat. Med. 16, 821–827 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• Ito, M. et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature 447, 316–320 (2007).
  Article CAS PubMed Google Scholar
• Srinivas, S. et al. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1, 4 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Kaufman, C. K. et al. GATA-3: an unexpected regulator of cell lineage determination in skin. Genes Dev. 17, 2108–22 (2003).
  Article CAS PubMed PubMed Central Google Scholar
• Nowak, J. A., Polak, L., Pasolli, H. A. & Fuchs, E. Hair follicle stem cells are specified and function in early skin morphogenesis. Cell Stem Cell 3, 33–43 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
  Article PubMed PubMed Central Google Scholar
• Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Machanick, P. & Bailey, T. L. MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27, 1696–1697 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–555 (2010).
  Article CAS PubMed PubMed Central Google Scholar