Adult epidermal Notch activity induces dermal accumulation of T cells and neural crest derivatives through upregulation of jagged 1

Development

Volumn 137, Issue 21, 2010, Pages 3569-3579

  Ambler, Carrie A ^a,b   Watt, Fiona M ^a,c  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Epidermis; Jagged 1; Mouse; Neural crest; Notch

Indexed keywords

CYTOKINE; GROWTH FACTOR; JAGGED1; NOTCH RECEPTOR; TAMOXIFEN; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLISTER; CARCINOGENESIS; CELL DIFFERENTIATION; CELL INFILTRATION; EPIDERMIS; EPITHELIAL MESENCHYMAL TRANSITION; GENE EXPRESSION; INHIBITION KINETICS; MELANOCYTE; MOUSE; NEURAL CREST; NONHUMAN; PERIPHERAL NERVE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SKIN; SKINFOLD; SMOOTH MUSCLE FIBER; STROMA CELL; T LYMPHOCYTE; TRANSGENE; UPREGULATION;

AGING; ANIMALS; CALCIUM-BINDING PROTEINS; CELL COUNT; CELL PROLIFERATION; DERMIS; EPIDERMIS; FEMALE; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; NEURAL CREST; ORGAN SIZE; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; UP-REGULATION;

EID: 78049333308     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.050310     Document Type: Article

References (74)

1. Aho, S. (2004). Soluble form of Jagged1: unique product of epithelial keratinocytes and a regulator of keratinocyte differentiation. J. Cell Biochem. 92, 1271-1281.
2. Ambler, C. A. and Watt, F. M. (2007). Expression of Notch pathway genes in mammalian epidermis and modulation by beta-catenin. Dev. Dyn. 236, 1595-1601.
3. Amoh, Y., Li, L., Katsuoka, K., Penman, S. and Hoffman, R. M. (2005). Multipotent Nestin-positive, keratin-negative hair-follicle bulge stem cells can form neurons. Proc. Natl. Acad. Sci. USA 102, 5530-5534.
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. (Pubitemid 44771736)
5. Botchkarev, V. A., Eichmuller, S., Johansson, O. and Paus, R. (1997). Hair cycle-dependent plasticity of skin and hair follicle innervation in normal murine skin. J. Comp. Neurol. 386, 379-395.
6. Braun, K. M., Niemann, C., Jensen, U. B., Sundberg, J. P., Silva-Vargas, V. and Watt, F. M. (2003). Manipulation of stem cell proliferation and lineage commitment: visualisation of label-retaining cells in wholemounts of mouse epidermis. Development 130, 5241-5255.
7. Brooker, R., Hozumi, K. and Lewis, J. (2006). Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133, 1277-1286.
8. Byrne, C. and Hardman, M. J. (2005). Whole-mount assays for gene induction and barrier formation in the developing epidermis. Methods Mol Biol. 289, 127-136.
9. Callahan, R. and Egan, S. E. (2004). Notch signaling in mammary development and oncogenesis. J. Mamm. Gland Biol. Neoplasia 9, 145-163.
10. Collins, C. A. and Watt, F. M. (2008). Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for β-catenin and Notch signalling. Dev. Biol. 324, 55-67.
11. Dalziel, K. L., Telfer, N. R., Wilson, C. L. and Dawber, R. P. (1990). Tufted folliculitis. A specific bacterial disease? Am. J. Dermatopathol. 12, 37-41.
12. Demehri, S., Liu, Z., Lee, J., Lin, M. H., Crosby, S. D., Roberts, C. J., Grigsby, P. W., Miner, J. H., Farr, A. G. and Kopan, R. (2008). Notch-deficient skin induces a lethal systemic B-lymphoproliferative disorder by secreting TSLP, a sentinel for epidermal integrity. PLoS Biol. 6, e123.
13. Demehri, S., Turkoz, A. and Kopan, R. (2009). Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 16, 55-66.
14. Driskell, R. R., Giangreco, A., Jensen, K. B., Mulder, K. W. and Watt, F. M. (2009). Sox2-positive dermal papilla cells specify hair follicle type in mammalian epidermis. Development 136, 2815-2823.
15. Duarte, M., Kolev, V., Kacer, D., Mouta-Bellum, C., Soldi, R., Graziani, I., Kirov, A., Friesel, R., Liaw, L., Small, D. et al. (2008). Novel cross-talk between three cardiovascular regulators: thrombin cleavage fragment of Jagged1 induces fibroblast growth factor 1 expression and release. Mol. Biol. Cell 19, 4863-4874.
16. Dunn, K. J., Williams, B. O., Li, Y. and Pavan, W. J. (2000). Neural crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development. Proc. Natl. Acad. Sci. USA 97, 10050-10055.
17. Estrach, S., Ambler, C. A., Lo Celso, C., Hozumi, K. and Watt, F. M. (2006). Jagged 1 is a beta-catenin target gene required for ectopic hair follicle formation in adult epidermis. Development 133, 4427-4438.
18. Estrach, S., Legg, J. and Watt, F. M. (2007). Syntenin mediates Delta1-induced cohesiveness of epidermal stem cells in culture. J. Cell Sci. 120, 2944-2952.
19. Estrach, S., Cordes, R., Hozumi, K., Gossler, A. and Watt, F. M. (2008). Role of the Notch ligand Delta1 in embryonic and adult mouse epidermis. J. Invest. Dermatol. 128, 825-832.
20. Fernandes, K. J., McKenzie, I. A., Mill, P., Smith, K. M., Akhavan, M., Barnabe-Heider, F., Biernaskie, J., Junek, A., Kobayashi, N. R., Toma, J. G. et al. (2004). A dermal niche for multipotent adult skin-derived precursor cells. Nat. Cell Biol. 6, 1082-1093.
21. Fuchs, E. and Horsley, V. (2008). More than one way to skin... Genes Dev. 22, 976-985.
22. Handjiski, B. K., Eichmuller, S., Hofmann, U., Czarnetzki, B. M. and Paus, R. (1994). Alkaline phosphatase activity and localization during the murine hair cycle. Br. J. Dermatol. 131, 303-310.
23. Hong, K. U., Reynolds, S. D., Watkins, S., Fuchs, E. and Stripp, B. R. (2004). Basal cells are a multipotent progenitor capable of renewing the bronchial epithelium. Am. J. Pathol. 164, 577-588.
24. Incorvaia, C., Frati, F., Verna, N., D'Alò, S., Motolese, A. and Pucci, S. (2008). Allergy and the skin. Clin. Exp. Immunol. 153, 27-29.
25. Jensen, K. B., Collins, C. A., Nascimento, E., Tan, D. W., Frye, M., Itami, S. and Watt, F. M. (2009). Lrig1 expression defines a distinct multipotent stem cell population in mammalian epidermis. Cell Stem Cell 4, 427-439.
26. Johnston, D. A., Dong, B. and Hughes, C. C. (2009). TNF induction of Jagged-1 in endothelial cells is NFκB-dependent. Gene 435, 36-44.
27. Kawamoto, S., Niwa, H., Tashiro, F., Sano, S., Kondoh, G., Takeda, J., Tabayashi, K. and Miyazaki, J. (2000). A novel reporter mouse strain that expresses enhanced green fluorescent protein upon Cre-mediated recombination. FEBS Lett. 470, 263-268.
28. Kawano, M., Komi-Kuramochi, A., Asada, M., Suzuki, M., Oki, J., Jiang, J. and Imamura, T. (2005). Comprehensive analysis of FGF and FGFR expression in skin: FGF18 is highly expressed in hair follicles and capable of inducing anagen from telogen stage hair follicles. J. Invest. Dermatol. 124, 877-885.
29. Kennard, S., Liu, H. and Lilly, B. (2008). Transforming growth factor-β (TGF- 1) down-regulates Notch3 in fibroblasts to promote smooth muscle gene expression. J. Biol. Chem. 283, 1324-1333.
30. Kishimoto, J., Burgeson, R. E. and Morgan, B. A. (2000). Wnt signaling maintains the hair-inducing activity of the dermal papilla. Genes Dev. 14, 1181-1185.
31. Kopan, R. and Ilagan, M. X. (2009). The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216-233.
32. Kruse, C., Bodo, E., Petschnik, A. E., Danner, S., Tiede, S. and Paus, R. (2006). Towards the development of a pragmatic technique for isolating and differentiating Nestin-positive cells from human scalp skin into neuronal and glial cell populations: generating neurons from human skin? Exp. Dermatol. 15, 794-800.
33. Lauria, G., Borgna, M., Morbin, M., Lombardi, R., Mazzoleni, G., Sghirlanzoni, A. and Pareyson, D. (2004). Tubule and neurofilament immunoreactivity in human hairy skin: markers for intraepidermal nerve fibers. Muscle Nerve 30, 310-316.
34. Le Douarin, N. M., Calloni, G. W. and Dupin, E. (2008). The stem cells of the neural crest. Cell Cycle 7, 1013-1019.
35. Lee, J., Basak, J. M., Demehri, S. and Kopan, R. (2007). Bi-compartmental communication contributes to the opposite proliferative behavior of Notch1-deficient hair follicle and epidermal keratinocytes. Development 134, 2795-2806. (Pubitemid 47305054)
36. Lefort, K., Mandinova, A., Ostano, P., Kolev, V., Calpini, V., Kolfschoten, I., Devgan, V., Lieb, J., Raffoul, W., Hohl, D. et al. (2007). Notch1 is a p53 target gene involved in human keratinocyte tumor suppression through negative regulation of ROCK1/2 and MRCKalpha kinases. Genes Dev. 21, 562-577.
37. Leong, K. G., Niessen, K., Kulic, I., Raouf, A., Eaves, C., Pollet, I. and Karsan, A. (2007). Jagged1-mediated Notch activation induces epithelial-to-mesenchymal transition through Slug-induced repression of E-cadherin. J. Exp. Med. 204, 2935-2948.
38. Li, L., Mignone, J., Yang, M., Matic, M., Penman, S., Enikolopov, G. and Hoffman, R. M. (2003). Nestin expression in hair follicle sheath progenitor cells. Proc. Natl. Acad. Sci. USA 100, 9958-9961.
39. Lo Celso, C., Prowse, D. M. and Watt, F. M. (2004). 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, 1787-1799.
40. López-Rovira, T., Silva-Vargas, V. and Watt, F. M. (2005). Different consequences of beta1 integrin deletion in neonatal and adult mouse epidermis reveal a context-dependent role of integrins in regulating proliferation, differentiation, and intercellular communication. J. Invest. Dermatol. 125, 1215-1227.
41. Lowell, S. and Watt, F. M. (2001). Delta regulates keratinocyte spreading and motility independently of differentiation. Mech. Dev. 107, 133-140.
42. Lowell, S., Jones, P., Le Roux, I., Dunne, J. and Watt, F. M. (2000). Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr. Biol. 10, 491-500.
43. McGowan, K. M. and Coulombe, P. A. (2000). Keratin 17 expression in the hard epithelial context of the hair and nail, and its relevance for the pachyonychia congenita phenotype. J. Invest. Dermatol. 114, 1101-1107.
44. Mei, L. and Xiong, W. C. (2008). Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat. Rev. Neurosci. 9, 437-452.
45. Moriyama, M., Durham, A. D., Moriyama, H., Hasegawa, K., Nishikawa, S., Radtke, F. and Osawa, M. (2008). Multiple roles of Notch signaling in the regulation of epidermal development. Dev. Cell 14, 594-604.
46. Nickoloff, B. J., Qin, J. Z., Chaturvedi, V., Denning, M. F., Bonish, B. and Miele, L. (2002). Jagged-1 mediated activation of notch signaling induces complete maturation of human keratinocytes through NF-κB and PPARγ. Cell Death Differ. 9, 842-855.
47. Nicolas, M., Wolfer, A., Raj, K., Kummer, J. A., Mill, P., van Noort, M., Hui, C. C., Clevers, H., Dotto, G. P. and Radtke, F. (2003). Notch1 functions as a tumor suppressor in mouse skin. Nat. Genet. 33, 416-421.
48. Niessen, K., Fu, Y., Chang, L., Hoodless, P. A., McFadden, D. and Karsan, A. (2008). Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell Biol. 182, 315-325.
49. Nikopoulos, G. N., Duarte, M., Kubu, C. J., Bellum, S., Friesel, R., Maciag, T., Prudovsky, I. and Verdi, J. M. (2007). Soluble Jagged1 attenuates lateral inhibition, allowing for the clonal expansion of neural crest stem cells. Stem Cells 25, 3133-3142.
50. Osipo, C., Golde, T. E., Osborne, B. A. and Miele, L. A. (2008). Off the beaten pathway: the complex cross talk between Notch and NF-kB. Lab. Invest. 88, 11-17.
51. 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.
52. Pla, P. and Larue, L. (2003). Involvement of endothelin receptors in normal and pathological development of neural crest cells. Int. J. Dev. Biol. 47, 315-325.
53. Powell, B. C., Passmore, E. A., Nesci, A. and Dunn, S. M. (1998). The Notch signalling pathway in hair growth. Mech. Dev. 78, 189-192.
54. Pranteda, G., Grimaldi, M., Palese, E., Di Napoli, A. and Bottoni, U. (2004). Tufted hair folliculitis: complete enduring response after treatment with rifampicin. J. Dermatolog. Treat. 15, 396-398.
55. Rendl, M., Lewis, L. and Fuchs, E. (2005). Molecular dissection of mesenchymal-epithelial interactions in the hair follicle. PLoS Biol. 3, e331.
56. Rendl, M., Polak, L. and Fuchs, E. (2008). BMP signaling in dermal papilla cells is required for their hair follicle-inductive properties. Genes Dev. 22, 543-557.
57. Ross, D. A. and Kadesch, T. (2004). Consequences of Notch-mediated induction of Jagged1. Exp. Cell Res. 296, 173-182.
58. Schneider, M. R., Schmidt-Ullrich, R. and Paus, R. (2009). The hair follicle as a dynamic miniorgan. Curr. Biol. 19, R132-R142.
59. Sechrist, J., Nieto, M. A., Zamanian, R. T. and Bronner-Fraser, M. (1995). Regulative response of the cranial neural tube after neural fold ablation: spatiotemporal nature of neural crest regeneration and up-regulation of Slug. Development 121, 4103-4115.
60. Shih, A. H. and Holland, E. C. (2006). Notch signaling enhances Nestin expression in gliomas. Neoplasia 8, 1072-1082.
61. Stemple, D. L. and Anderson, D. J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.
62. Tiede, S., Kloepper, J. E., Bodò, E., Tiwan, S., Kruse, C. and Paus, R. (2007). Hair follicle stem cells: walking the maze. Eur. J. Cell Biol. 86, 355-376.
63. Toma, J. G., Akhavan, M., Fernandes, K. J., Barnabe-Heider, F., Sadikot, A., Kaplan, D. R. and Miller, F. D. (2001). Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol. 3, 778-784.
64. Tong, A. K. and Baden, H. P. (1989). Tufted hair folliculitis. J. Am. Acad. Dermatol. 21, 1096-1099.
65. Tournoy, J., Bossuyt, X., Snellinx, A., Regent, M., Garmyn, M., Serneels, L., Saftig, P., Craessaerts, K., De Strooper, B. and Hartmann, D. (2004). Partial loss of presenilins causes seborrheic keratosis and autoimmune disease in mice. Hum. Mol. Genet. 13, 1321-1331.
66. Turner, F. E., Broad, S., Khanim, F. L., Jeanes, A., Talma, S., Hughes, S., Tselepis, C. and Hotchin, N. A. (2006). Slug regulates integrin expression and cell proliferation in human epidermal keratinocytes. J. Biol. Chem. 281, 21321-21331.
67. Urs, S., Roudabush, A., O'Neill, C. F., Pinz, I., Prudovsky, I., Kacer, D., Tang, Y., Liaw, L. and Small, D. (2008). Soluble forms of the Notch ligands Delta1 and Jagged1 promote in vivo tumorigenicity in NIH3T3 fibroblasts with distinct phenotypes. Am. J. Pathol. 173, 865-878.
68. Waters, J. M., Richardson, G. D. and Jahoda, C. A. (2007). Hair follicle stem cells. Semin. Cell Dev. Biol. 18, 245-254.
69. Watt, F. M., Lo Celso, C. and Silva-Vargas, V. (2006). Epidermal stem cells: an update. Curr. Opin. Genet. Dev. 16, 518-524.
70. Watt, F. M., Estrach, S. and Ambler, C. A. (2008). Epidermal Notch signalling: differentiation, cancer and adhesion. Curr. Opin. Cell Biol. 20, 171-179.
71. Wong, C. E., Paratore, C., Dours-Zimmermann, M. T., Rochat, A., Pietri, T., Suter, U., Zimmermann, D. R., Dufour, S., Thiery, J. P., Meijer, D. et al. (2006). Neural crest-derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J. Cell Biol. 175, 1005-1015.
72. Ya, J., Markman, M. W., Wagenaar, G. T., Blommaart, P. J., Moorman, A. F. and Lamers, W. H. (1997). Expression of the smooth-muscle proteins alpha-smooth-muscle actin and calponin, and of the intermediate filament protein desmin are parameters of cardiomyocyte maturation in the prenatal rat heart. Anat. Rec. 249, 495-505.
73. Zhang, J. C., Kim, S., Helmke, B. P., Yu, W. W., Du, K. L., Lu, M. M., Strobeck, M., Yu, Q. and Parmacek, M. S. (2001). Analysis of SM22alpha-deficient mice reveals unanticipated insights into smooth muscle cell differentiation and function. Mol. Cell. Biol. 21, 1336-1344.
74. Zhang, Y., Andl, T., Yang, S. H., Teta, M., Liu, F., Seykora, J. T., Tobias, J. W., Piccolo, S., Schmidt-Ullrich, R., Nagy, A. et al. (2008). Activation of beta-catenin signaling programs embryonic epidermis to hair follicle fate. Development 135, 2161-2172.