MYC in mammalian epidermis: how can an oncogene stimulate differentiation? (original) (raw)
Fuchs, E. Scratching the surface of skin development. Nature445, 834–842 (2007). ArticleCAS Google Scholar
Owens, D. M. & Watt, F. M. Contribution of stem cells and differentiated cells to epidermal tumours. Nature Rev. Cancer3, 444–451 (2003). ArticleCAS Google Scholar
Watt, F. M., Lo Celso, C. & Silva-Vargas, V. Epidermal stem cells: an update. Curr. Opin. Genet. Dev.16, 518–524 (2006). ArticleCAS Google Scholar
Jones, P. H., Simons, B. D. & Watt, F. M. Sic transit Gloria. Farewell to the epidermal transit amplifying cell? Cell Stem Cell1, 371–381 (2007). ArticleCAS Google Scholar
Boukamp, P. Non-melanoma skin cancer: what drives tumor development and progression? Carcinogenesis26, 1657–1667 (2005). ArticleCAS Google Scholar
Bull, J. J. et al. Contrasting localization of c-Myc with other Myc superfamily transcription factors in the human hair follicle and during the hair growth cycle. J. Invest. Dermatol.116, 617–622 (2001). ArticleCAS Google Scholar
Gandarillas, A. & Watt, F. M. Changes in expression of members of the fos and jun families and myc network during terminal differentiation of human keratinocytes. Oncogene11, 1403–1407 (1995). CASPubMed Google Scholar
Honma, M., Benitah, S. A. & Watt, F. M. Role of LIM kinases in normal and psoriatic human epidermis. Mol. Biol. Cell17, 1888–1896 (2006). ArticleCAS Google Scholar
Barajon, I. et al. Pattern of expression of c-Myc, Max and Bin1 in human anagen hair follicles. Br. J. Dermatol.144, 1193–1203 (2001). ArticleCAS Google Scholar
Garte, S. J. The c-myc oncogene in tumor progression. Crit. Rev. Oncog.4, 435–449 (1993). CASPubMed Google Scholar
Littlewood, T. D., Hancock, D. C., Danielian, P. S., Parker, M. G. & Evan, G. I. A modified oestrogen receptor ligand-binding domain as an improved switch for the regulation of heterologous proteins. Nucleic Acids Res.23, 1686–1690 (1995). ArticleCAS Google Scholar
Coffey, R. J. Jr. et al. Selective inhibition of growth-related gene expression in murine keratinocytes by transforming growth factor beta. Mol. Cell. Biol.8, 3088–3093 (1988). ArticleCAS Google Scholar
Jensen, K. B. & Watt, F. M. Single-cell expression profiling of human epidermal stem and transit-amplifying cells: Lrig1 is a regulator of stem cell quiescence. Proc. Natl Acad. Sci. USA103, 11958–11963 (2006). ArticleCAS Google Scholar
Frye, M. & Watt, F. M. The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr. Biol.16, 971–981 (2006). ArticleCAS Google Scholar
Alexandrow, M. G., Kawabata, M., Aakre, M. & Moses, H. L. Overexpression of the c-Myc oncoprotein blocks the growth-inhibitory response but is required for the mitogenic effects of transforming growth factor β1. Proc. Natl Acad. Sci. USA92, 3239–3243 (1995). ArticleCAS Google Scholar
Hashiro, M., Matsumoto, K., Okumura, H., Hashimoto, K. & Yoshikawa, K. Growth inhibition of human keratinocytes by antisense c-myc oligomer is not coupled to induction of differentiation. Biochem. Biophys. Res. Comm.174, 287–292 (1991). ArticleCAS Google Scholar
Gandarillas, A. & Watt, F. M. c-Myc promotes differentiation of human epidermal stem cells. Genes Dev.11, 2869–2882 (1997). ArticleCAS Google Scholar
Smith, D. P., Bath, M. L., Metcalf, D., Harris, A. W. & Cory, S. Myc levels govern hematopoietic tumor type and latency in transgenic mice. Blood108, 653–661 (2006). ArticleCAS Google Scholar
Gebhardt, A. et al. Myc regulates keratinocyte adhesion and differentiation via complex formation with Miz1. J. Cell Biol.172, 139–149 (2006). ArticleCAS Google Scholar
Gandarillas, A., Goldsmith, L. A., Gschmeissner, S., Leigh, I. M. & Watt, F. M. Evidence that apoptosis and terminal differentiation of epidermal keratinocytes are distinct processes. Exp. Dermatol.8, 71–79 (1999). ArticleCAS Google Scholar
Pelengaris, S., Littlewood, T., Khan, M., Elia, G. & Evan, G. Reversible activation of c-Myc in skin: induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol. Cell3, 565–577 (1999). ArticleCAS Google Scholar
Wanzel, M., Herold, S. & Eilers, M. Transcriptional repression by Myc. Trends Cell Biol.13, 146–150 (2003). ArticleCAS Google Scholar
Knies-Bamforth, U. E., Fox, S. B., Poulsom, R., Evan, G. I. & Harris, A. L. c-Myc interacts with hypoxia to induce angiogenesis in vivo by a vascular endothelial growth factor-dependent mechanism. Cancer Res.64, 6563–6567 (2004). ArticleCAS Google Scholar
Flores, I., Evan, G. & Blasco, M. A. Genetic analysis of myc and telomerase interactions in vivo. Mol. Cell. Biol.26, 6130–6138 (2006). ArticleCAS Google Scholar
Flores, I., Murphy, D. J., Swigart, L. B., Knies, U. & Evan, G. I. Defining the temporal requirements for Myc in the progression and maintenance of skin neoplasia. Oncogene23, 5923–5930 (2004). ArticleCAS Google Scholar
Bull, J. J. et al. Ectopic expression of c-Myc in the skin affects the hair growth cycle and causes an enlargement of the sebaceous gland. Br. J. Dermatol.152, 1125–1123 (2005). ArticleCAS Google Scholar
Waikel, R. L., Wang, X. J. & Roop, D. R. Targeted expression of c-Myc in the epidermis alters normal proliferation, differentiation and UV-B induced apoptosis. Oncogene18, 4870–4878 (1999). ArticleCAS Google Scholar
Arnold, I. & Watt, F. M. c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr. Biol.11, 558–568 (2001). ArticleCAS Google Scholar
Waikel, R. L., Kawachi, Y., Waikel, P. A., Wang, X. J. & Roop, D. R. Deregulated expression of c-Myc depletes epidermal stem cells. Nature Genet.28, 165–168 (2001). ArticleCAS Google Scholar
Koster, M. I., Huntzinger, K. A. & Roop, D. R. Epidermal differentiation: transgenic/knockout mouse models reveal genes involved in stem cell fate decisions and commitment to differentiation. J. Investig. Dermatol. Symp. Proc.7, 41–45 (2002). ArticleCAS Google Scholar
Braun, K. M. et al. Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development130, 5241–5255 (2003). ArticleCAS Google Scholar
Frye, M., Gardner, C., Li, E. R., Arnold, I. & Watt, F. M. Evidence that Myc activation depletes the epidermal stem cell compartment by modulating adhesive interactions with the local microenvironment. Development130, 2793–2780 (2003). ArticleCAS Google Scholar
Rounbehler, R. J., Schneider-Broussard, R., Conti, C. J. & Johnson, D. G. Myc lacks E2F1′s ability to suppress skin carcinogenesis. Oncogene20, 5341–5349 (2001). ArticleCAS Google Scholar
Soucek, L., Nasi, S. & Evan, G. I. Omomyc expression in skin prevents Myc-induced papillomatosis. Cell Death Differ.11, 1038–1045 (2004). ArticleCAS Google Scholar
Gebhardt, A. et al. Miz1 is required for hair follicle structure and hair morphogenesis. J. Cell Sci.120, 2586–2593 (2007). ArticleCAS Google Scholar
Wu, S. et al. Myc represses differentiation-induced p21CIP1 expression via Miz-1-dependent interaction with the p21 core promoter. Oncogene22, 351–360 (2003). ArticleCAS Google Scholar
Zanet, J. et al. Endogenous Myc controls mammalian epidermal cell size, hyperproliferation, endoreplication and stem cell amplification. J. Cell Sci.118, 1693–1704 (2005). ArticleCAS Google Scholar
Oskarsson, T. et al. Skin epidermis lacking the c-Myc gene is resistant to Ras-driven tumorigenesis but can reacquire sensitivity upon additional loss of the p21Cip1 gene. Genes Dev.20, 2024–2029 (2006). ArticleCAS Google Scholar
Mill, P. et al. Shh controls epithelial proliferation via independent pathways that converge on N-Myc. Dev. Cell9, 293–303 (2005). ArticleCAS Google Scholar
Silva-Vargas, V. et al. β-catenin and Hedgehog signal strength can specify number and location of hair follicles in adult epidermis without recruitment of bulge stem cells. Dev. Cell9, 121–131 (2005). ArticleCAS Google Scholar
Watt, F. M. Role of integrins in regulating epidermal adhesion, growth and differentiation. EMBO J.21, 3919–3926 (2002). ArticleCAS Google Scholar
Benitah, S. A., Frye, M., Glogauer, M. & Watt, F. M. Stem cell depletion through epidermal deletion of Rac1. Science309, 933–935 (2005). Article Google Scholar
Huang, Z., Traugh, J. A. & Bishop, J. M. Negative control of the Myc protein by the stress-responsive kinase Pak2. Mol. Cell. Biol.24, 1582–1594 (2004). ArticleCAS Google Scholar
Benitah, S. A. & Watt, F. M. Epidermal deletion of Rac1 causes stem cell depletion, irrespective of whether deletion occurs during embryogenesis or adulthood. J. Invest. Dermatol.127, 1555–1557 (2007). ArticleCAS Google Scholar
Chrostek, A. et al. Rac1 is crucial for hair follicle integrity but is not essential for maintenance of the epidermis. Mol. Cell. Biol.26, 6957–6970 (2006). ArticleCAS Google Scholar
Castilho, R. M. et al. Requirement of Rac1 distinguishes follicular from interfollicular epithelial stem cells. Oncogene26, 5078–5085 (2007). ArticleCAS Google Scholar
Murphy, M. J., Wilson, A. & Trumpp, A. More than just proliferation: Myc function in stem cells. Trends Cell Biol.15, 128–137 (2005). ArticleCAS Google Scholar
Cowling, V. H. & Cole, M. D. E-cadherin repression contributes to c-Myc-induced epithelial cell transformation. Oncogene26, 3582–3586 (2007). ArticleCAS Google Scholar
Sumi, T., Tsuneyoshi, N., Nakatsuji, N. & Suemori, H. Apoptosis and differentiation of human embryonic stem cells induced by sustained activation of c-Myc. Oncogene26, 5564–5576 (2007). ArticleCAS Google Scholar
Wilson, A. et al. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev.18, 2747–2763 (2004). ArticleCAS Google Scholar
Amati, B., Frank, S. R., Donjerkovic, D. & Taubert, S. Function of the c-Myc oncoprotein in chromatin remodeling and transcription. Biochim. Biophys. Acta1471, M135–M145 (2001). CASPubMed Google Scholar
Frank, S. R. et al. MYC recruits the TIP60 histone acetyltransferase complex to chromatin. EMBO Rep.4, 575–580 (2003). ArticleCAS Google Scholar
Knoepfler, P. S. et al. Myc influences global chromatin structure. EMBO J.25, 2723–2734 (2006). ArticleCAS Google Scholar
Frye, M., Fisher, A. G. & Watt, F. M. Epidermal stem cells are defined by global histone modifications that are altered by Myc-induced differentiation. PLoS ONE2, e763 (2007). Article Google Scholar
Secombe, J., Li, L., Carlos, L. & Eisenman, R. N. The Trithorax group protein Lid is a trimethyl histone H3K4 demethylase required for dMyc-induced cell growth. Genes Dev.21, 537–551 (2007). ArticleCAS Google Scholar
Markova, N. G., Karaman-Jurukovska, N., Pinkas-Sarafova, A., Marekov, L. N. & Simon, M. Inhibition of histone deacetylation promotes abnormal epidermal differentiation and specifically suppresses the expression of the late differentiation marker profilaggrin. J. Invest. Dermatol.127, 1126–1139 (2007). ArticleCAS Google Scholar
Takahashi, K. & Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell126, 663–676 (2006). ArticleCAS Google Scholar
Wernig, M. et al. In vitro reprogramming of fibroblasts into a pluripotent ES-cell-like state. Nature448, 318–324 (2007). ArticleCAS Google Scholar
Nakagawa, M. et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nature Biotechnol. (in the press).
Dai, X., Schonbaum, C., Degenstein, L., Bai, W., Mahowald, A. & Fuchs, E. The ovo gene required for cuticle formation and oogenesis in flies is involved in hair formation and spermatogenesis in mice. Genes Dev.12, 3452–3463 (1998). ArticleCAS Google Scholar
Nair, M. et al. Ovol1 regulates the growth arrest of embryonic epidermal progenitor cells and represses c-myc transcription. J. Cell Biol.173, 253–264 (2006). ArticleCAS Google Scholar
Gomis, R. R. et al. FoxO-Smad synexpression group in human keratinocytes. Proc. Natl Acad. Sci. USA103, 12747–12752 (2006). ArticleCAS Google Scholar
Kallies, A. & Nutt, S. L. Terminal differentiation of lymphocytes depends on Blimp-1. Curr. Opin. Immunol.19, 156–162 (2007). ArticleCAS Google Scholar
Horsley, V. et al. Blimp1 defines a progenitor population that governs cellular input to the sebaceous gland. Cell126, 597–609 (2006). ArticleCAS Google Scholar
Magnúsdóttir, E. et al. Epidermal terminal differentiation depends on B lymphocyte-induced maturation protein-1. Proc. Natl Acad. Sci. USA104, 14988–14993 (2007). Article Google Scholar
van de Wetering, M. et al. The β-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell111, 241–250 (2002). ArticleCAS Google Scholar
Niemann, C., Owens, D. M., Hülsken, J., Birchmeier, W. & Watt, F. M. Expression of ΔNLef1 in mouse epidermis results in differentiation of hair follicles into squamous epidermal cysts and formation of skin tumours. Development129, 95–109 (2002). CASPubMed Google Scholar
Niemann, C., Owens, D. M., Schettina, P. & Watt, F. M. Dual role of inactivating Lef1 mutations in epidermis: tumor promotion and specification of tumor type. Cancer Res.67, 2916–2921 (2007). ArticleCAS Google Scholar
Williamson, L. et al. Pemphigus vulgaris identifies plakoglobin as key suppressor of c-Myc in the skin. EMBO J.25, 3298–3309 (2006). ArticleCAS Google Scholar
Gallant P. Control of transcription by Pontin and Reptin. Trends Cell Biol.17, 187–192 (2007). ArticleCAS Google Scholar
Etard, C., Gradl, D., Kunz, M. & Wedlich, D. Pontin and Reptin regulate cell proliferation in early Xenopus embryos in collaboration with c-Myc and Miz-1. Mech. Dev.122, 545–556 (2005). ArticleCAS Google Scholar
Senoo-Matsuda, N. & Johnston, L. A. Soluble factors mediate competitive and cooperative interactions between cells expressing different levels of Drosophila Myc. Proc. Natl Acad. Sci. USA104, 18543–18548 (2007). ArticleCAS Google Scholar
Evans, R. D. et al. A tumor-associated β1 integrin mutation that abrogates epithelial differentiation control. J. Cell Biol.160, 589–596 (2003). ArticleCAS Google Scholar
Zahir, N. et al. Autocrine laminin-5 ligates α6β4 integrin and activates RAC and NFκB to mediate anchorage-independent survival of mammary tumors. J. Cell Biol.163, 1397–1407 (2003). ArticleCAS Google Scholar
Brenner, C. et al. Myc represses transcription through recruitment of DNA methyltransferase corepressor. EMBO J.24, 336–346 (2005). ArticleCAS Google Scholar
Satou, A., Taira, T., Iguchi-Ariga, S. M. & Ariga, H. A novel transrepression pathway of c-Myc. Recruitment of a transcriptional corepressor complex to c-Myc by MM-1, a c-Myc-binding protein. J. Biol. Chem.276, 46562–46567 (2001). ArticleCAS Google Scholar