Notch signaling represses p63 expression in the developing surface ectoderm

Development (Cambridge)

Volumn 140, Issue 18, 2013, Pages 3777-3786

  Tadeu, Ana Mafalda Baptista ^a   Horsley, Valerie ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Ectoderm; Keratinocyte specification; Notch signaling; p63

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; CYTOKERATIN 14; NOTCH RECEPTOR; PROTEIN P63; TRANSCRIPTION FACTOR CDX2;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOHISTOCHEMISTRY; KERATINOCYTE; MOUSE; MOUSE EMBRYO; NEUROECTODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ECTODERM; KERATINOCYTE SPECIFICATION; NOTCH SIGNALING; P63;

ANIMALS; BODY PATTERNING; CELL DIFFERENTIATION; ECTODERM; EMBRYONIC STEM CELLS; EPIDERMIS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; KERATIN-14; KERATINOCYTES; MICE; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TUMOR SUPPRESSOR PROTEINS;

EID: 84883236090     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.093948     Document Type: Article

References (59)

1. Aberdam, E., Barak, E., Rouleau, M., de LaForest, S., Berrih-Aknin, S., Suter, D. M., Krause, K.-H., Amit, M., Itskovitz-Eldor, J. and Aberdam, D. (2008). A pure population of ectodermal cells derived from human embryonic stem cells. Stem Cells 26, 440-444.
2. Bernando, A. S., Faial, T., Gardner, L., Niakan, K. K., Ortmann, D., Senner, C. E., Callery, E. M., Trotter, M. W., Hemberger, M., Smith J. C. et al. (2011). BRACHYURY and CDX2 mediate BMP-induced differentiation of human and mouse pluripotent stem cells into embryonic and extraembryonic lineages. Cell Stem Cell 9, 144-155.
3. Blanpain, C. and Fuchs, E. (2006). Epidermal stem cells of the skin. Annu. Rev. Cell Dev. Biol. 22, 339-373.
4. Blanpain, C., Lowry, W. E., Pasolli, H. A. and Fuchs, E. (2006). Canonical notch signaling functions as a commitment switch in the epidermal lineage. Genes Dev. 20, 3022-3035.
5. Bouras, T., Pal, B., Vaillant, F., Harburg, G., Asselin-Labat, M.-L., Oakes, S. R., Lindeman, G. J. and Visvader, J. E. (2008). Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 3, 429-441.
6. Byrne, C., Tainsky, M. and Fuchs, E. (1994). Programming gene expression in developing epidermis. Development 120, 2369-2383.
7. Candi, E., Schmidt, R. and Melino, G. (2005). The cornified envelope: a model of cell death in the skin. Nat. Rev. Mol. Cell Biol. 6, 328-340.
8. Chambers, S. M., Fasano, C. A., Papapetrou, E. P., Tomishima, M., Sadelain, M. and Studer, L. (2009). Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27, 275-280.
9. Coffman, C. R., Skoglund, P., Harris, W. A. and Kintner, C. R. (1993). Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73, 659-671.
10. Crum, C. P. and McKeon, F. D. (2010). p63 in epithelial survival, germ cell surveillance, and neoplasia. Annu. Rev. Pathol. 5, 349-371.
11. D'Amour, K. A., Agulnick, A. D., Eliazer, S., Kelly, O. G., Kroon, E. and Baetge, E. E. (2005). Efficient differentiation of human embryonic stem cells to definitive endoderm. Nat. Biotechnol. 23, 1534-1541.
12. Davidson, D. (1995). The function and evolution of Msx genes: pointers and paradoxes. Trends Genet. 11, 405-411.
13. Demehri, S. and Kopan, R. (2009). Notch signaling in bulge stem cells is not required for selection of hair follicle fate. Development 136, 891-896.
14. Donoviel, D. B., Hadjantonakis, A. K., Ikeda, M., Zheng, H., Hyslop, P. S. and Bernstein, A. (1999). Mice lacking both presenilin genes exhibit early embryonic patterning defects. Genes Dev. 13, 2801-2810.
15. Dovey, H. F., John, V., Anderson, J. P., Chen, L. Z., de Saint Andrieu, P., Fang, L. Y., Freedman, S. B., Folmer, B., Goldbach, E., Holsztynska, E. J. et al. (2001). Functional gamma-secretase inhibitors reduce beta-amyloid peptide levels in brain. J. Neurochem. 76, 173-181.
16. Festa, E., Fretz, J., Berry, R., Schmidt, B., Rodeheffer, M., Horowitz, M. and Horsley, V. (2011). Adipocyte lineage cells contribute to the skin stem cell niche to drive hair cycling. Cell 146, 761-771.
17. Fuchs, E. (2007). Scratching the surface of skin development. Nature 445, 834-842.
18. Han, S., Dziedzic, N., Gadue, P., Keller, G. M. and Gouon-Evans, V. (2011). An endothelial cell niche induces hepatic specification through dual repression of Wnt and Notch signaling. Stem Cells 29, 217-228.
19. Harvey, N. T., Hughes, J. N., Lonic, A., Yap, C., Long, C., Rathjen, P. D. and Rathjen, J. (2010). Response to BMP4 signalling during ES cell differentiation defines intermediates of the ectoderm lineage. J. Cell Sci. 123, 1796-1804.
20. Hayward, P., Kalmar, T. and Arias, A. M. (2008). Wnt/Notch signalling and information processing during development. Development 135, 411-424.
21. King, K. E. and Weinberg, W. C. (2007). p63: defining roles in morphogenesis, homeostasis, and neoplasia of the epidermis. Mol. Carcinog. 46, 716-724.
22. Kitamoto, T., Takahashi, K., Takimoto, H., Tomizuka, K., Hayasaka, M., Tabira, T. and Hanaoka, K. (2005). Functional redundancy of the Notch gene family during mouse embryogenesis: analysis of Notch gene expression in Notch3-deficient mice. Biochem. Biophys. Res. Commun. 331, 1154-1162.
23. Kopan, R. and Ilagan, M. X. G. (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
24. Koster, M. I. (2010). p63 in skin development and ectodermal dysplasias. J. Invest. Dermatol. 130, 2352-2358.
25. Koster, M. I. and Roop, D. R. (2004). p63 and epithelial appendage development. Differentiation 72, 364-370.
26. Koster, M. I. and Roop, D. R. (2007). Mechanisms regulating epithelial stratification. Annu. Rev. Cell Dev. Biol. 23, 93-113.
27. Krebs, L. T., Xue, Y., Norton, C. R., Shutter, J. R., Maguire, M., Sundberg, J. P., Gallahan, D., Closson, V., Kitajewski, J., Callahan, R. et al. (2000). Notch signaling is essential for vascular morphogenesis in mice. Genes Dev. 14, 1343-1352.
28. Lai, E. C. (2004). Notch signaling: control of cell communication and cell fate. Development 131, 965-973.
29. Laurikkala, J., Mikkola, M. L., James, M., Tummers, M., Mills, A. A. and Thesleff, I. (2006). p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation. Development 133, 1553-1563.
30. Lechler, T. and Fuchs, E. (2005). Asymmetric cell divisions promote stratification and differentiation of mammalian skin. Nature 437, 275-280.
31. Li, B., Kuriyama, S., Moreno, M. and Mayor, R. (2009). The posteriorizing gene Gbx2 is a direct target of Wnt signalling and the earliest factor in neural crest induction. Development 136, 3267-3278.
32. McGowan, K. M. and Coulombe, P. A. (1998). Onset of keratin 17 expression coincides with the definition of major epithelial lineages during skin development. J. Cell Biol. 143, 469-486.
33. Medawar, A., Virolle, T., Rostagno, P., de la Forest-Divonne, S., Gambaro, K., Rouleau, M. and Aberdam, D. (2008). DeltaNp63 is essential for epidermal commitment of embryonic stem cells. PLoS ONE 3, e3441.
34. Metallo, C. M., Ji, L., de Pablo, J. J. and Palecek, S. P. (2008). Retinoic acid and bone morphogenetic protein signaling synergize to efficiently direct epithelial differentiation of human embryonic stem cells. Stem Cells 26, 372-380.
35. Mills, A. A., Zheng, B., Wang, X. J., Vogel, H., Roop, D. R. and Bradley, A. (1999). p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708-713.
36. Mizutani, T., Taniguchi, Y., Aoki, T., Hashimoto, N. and Honjo, T. (2001). Conservation of the biochemical mechanisms of signal transduction among mammalian Notch family members. Proc. Natl. Acad. Sci. USA 98, 9026-9031.
37. Moriyama, M., Durham, A.-D., Moriyama, H., Hasegawa, K., Nishikawa, S.-I., Radtke, F. and Osawa, M. (2008). Multiple roles of Notch signaling in the regulation of epidermal development. Dev. Cell 14, 594-604.
38. Nagarajan, P., Romano, R.-A. and Sinha, S. (2008). Transcriptional control of the differentiation program of interfollicular epidermal keratinocytes. Crit. Rev. Eukaryot. Gene Expr. 18, 57-79.
39. Nguyen, B.-C., Lefort, K., Mandinova, A., Antonini, D., Devgan, V., Della Gatta, G., Koster, M. I., Zhang, Z., Wang, J., Tommasi di Vignano, A. et al. (2006). Cross-regulation between Notch and p63 in keratinocyte commitment to differentiation. Genes Dev. 20, 1028-1042.
40. Orford, R. L., Robinson, C., Haydon, J. M., Patient, R. K. and Guille, M. J. (1998). The maternal CCAAT box transcription factor which controls GATA-2 expression is novel and developmentally regulated and contains a doublestranded-RNA-binding subunit. Mol. Cell. Biol. 18, 5557-5566.
41. Pan, Y., Lin, M.-H., Tian, X., Cheng, H.-T., Gridley, T., Shen, J. and Kopan, R. (2004). gamma-secretase functions through Notch signaling to maintain skin appendages but is not required for their patterning or initial morphogenesis. Dev. Cell 7, 731-743.
42. Romano, R.-A., Birkaya, B. and Sinha, S. (2007). A functional enhancer of keratin14 is a direct transcriptional target of deltaNp63. J. Invest. Dermatol. 127, 1175-1186.
43. Romano, R.-A., Ortt, K., Birkaya, B., Smalley, K. and Sinha, S. (2009). An active role of the DeltaN isoform of p63 in regulating basal keratin genes K5 and K14 and directing epidermal cell fate. PLoS ONE 4, e5623.
44. Romano, R.-A., Smalley, K., Magraw, C., Serna, V. A., Kurita, T., Raghavan, S. and Sinha, S. (2012). ΔNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development 139, 772-782.
45. Sanalkumar, R., Dhanesh, S. B. and James, J. (2010). Non-canonical activation of Notch signaling/target genes in vertebrates. Cell. Mol. Life Sci. 67, 2957-2968.
46. Sanes, J. R., Rubenstein, J. L. and Nicolas, J. F. (1986). Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5, 3133-3142.
47. Saura, C. A., Choi, S.-Y., Beglopoulos, V., Malkani, S., Zhang, D., Shankaranarayana Rao, B. S., Chattarji, S., Kelleher, R. J., 3rd, Kandel, E. R., Duff, K. et al. (2004). Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42, 23-36.
48. Saxena, M. T., Schroeter, E. H., Mumm, J. S. and Kopan, R. (2001). Murine notch homologs (N1-4) undergo presenilin-dependent proteolysis. J. Biol. Chem. 276, 40268-40273.
49. Schlosser, G. and Ahrens, K. (2004). Molecular anatomy of placode development in Xenopus laevis. Dev. Biol. 271, 439-466.
50. Senoo, M., Pinto, F., Crum, C. P. and McKeon, F. (2007). p63 Is essential for the proliferative potential of stem cells in stratified epithelia. Cell 129, 523-536.
51. Shalom-Feuerstein, R., Lena, A. M., Zhou, H., De La Forest Divonne, S., Van Bokhoven, H., Candi, E., Melino, G. and Aberdam, D. (2011). ΔNp63 is an ectodermal gatekeeper of epidermal morphogenesis. Cell Death Differ. 18, 887-896.
52. Shih, I. M. and Kurman, R. J. (2004). p63 expression is useful in the distinction of epithelioid trophoblastic and placental site trophoblastic tumors by profiling trophoblastic subpopulations. Am. J. Surg. Pathol. 28, 1177-1183.
53. Truong, A. B. and Khavari, P. A. (2007). Control of keratinocyte proliferation and differentiation by p63. Cell Cycle 6, 295-299.
54. Tumbar, T., Guasch, G., Greco, V., Blanpain, C., Lowry, W. E., Rendl, M. and Fuchs, E. (2004). Defining the epithelial stem cell niche in skin. Science 303, 359-363.
55. Wilson, P. A. and Hemmati-Brivanlou, A. (1995). Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331-333.
56. Wilson, S. I., Rydström, A., Trimborn, T., Willert, K., Nusse, R., Jessell, T. M. and Edlund, T. (2001). The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature 411, 325-330.
57. Xu, R. H., Chen, X., Li, D. S., Li, R., Addicks, G. C., Glennon, C., Zwaka, T. P. and Thomson, J. A. (2002). BMP4 initiates human embryonic stem cell differentiation to trophoblast. Nat. Biotechnol. 20, 1261-1264.
58. Yang, A., Schweitzer, R., Sun, D., Kaghad, M., Walker, N., Bronson, R. T., Tabin, C., Sharpe, A., Caput, D., Crum, C. et al. (1999). p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714-718.
59. Yu, X., Zou, J., Ye, Z., Hammond, H., Chen, G., Tokunaga, A., Mali, P., Li, Y.-M., Civin, C., Gaiano, N. et al. (2008). Notch signaling activation in human embryonic stem cells is required for embryonic, but not trophoblastic, lineage commitment. Cell Stem Cell 2, 461-471.