The disintegrin/metalloproteinase Adam10 is essential for epidermal integrity and Notch-mediated signaling

Development

Volumn 138, Issue 3, 2011, Pages 495-505

  Weber, Silvio ^a   Niessen, Michaela T ^b   Prox, Johannes ^a   Lüllmann Rauch, Renate ^a   Schmitz, Annika ^b   Schwanbeck, Ralf ^a   Blobel, Carl P ^c   Jorissen, Ellen ^d,e   De Strooper, Bart ^d,e   Niessen, Carien M ^b   Saftig, Paul ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d UNIVERSITY OF LEUVEN   (Belgium)

^e DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

Author keywords

Adam10; Epidermis; Mouse; Notch; Shedding; Skin

Indexed keywords

ADAM10 ENDOPEPTIDASE; NOTCH RECEPTOR; THYMIC STROMAL LYMPHOPOIETIN;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; EPIDERMIS; HAIR LOSS; KERATINOCYTE; LETHALITY; MORPHOGENESIS; MOUSE; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; SEBACEOUS GLAND; SIGNAL TRANSDUCTION; SKIN; THYMUS ATROPHY; UPREGULATION; VIBRISSA;

ADAM PROTEINS; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; BLOTTING, WESTERN; CELL PROLIFERATION; CELLS, CULTURED; EPIDERMIS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MEMBRANE PROTEINS; MICE; MICE, MUTANT STRAINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MUS;

EID: 78751520783     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.055210     Document Type: Article

References (63)

1. 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.
2. Berechid, B. E., Kitzmann, M., Foltz, D. R., Roach, A. H., Seiffert, D., Thompson, L. A., Olson, R. E., Bernstein, A., Donoviel, D. B. and Nye, J. S. (2002). Identification and characterization of presenilin-independent Notch signaling. J. Biol. Chem. 277, 8154-8165.
3. Blanpain, C. and Fuchs, E. (2009). Epidermal homeostasis: a balancing act of stem cells in the skin. Nat. Rev. Mol. Cell Biol. 10, 207-217.
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. Bozkulak, E. C. and Weinmaster, G. (2009). Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling. Mol. Cell. Biol. 29, 5679-5695.
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. Brou, C., Logeat, F., Gupta, N., Bessia, C., LeBail, O., Doedens, J. R., Cumano, A., Roux, P., Black, R. A. and Israel, A. (2000). A novel proteolytic cleavage involved in Notch signaling: the role of the disintegrin- metalloprotease TACE. Mol. Cell 5, 207-216.
8. Curry, C. L., Reed, L. L., Nickoloff, B. J., Miele, L. and Foreman, K. E. (2006). Notch-independent regulation of Hes-1 expression by c-Jun N-terminal kinase signaling in human endothelial cells. Lab. Invest. 86, 842-852.
9. Dassule, H. R., Lewis, P., Bei, M., Maas, R. and McMahon, A. P. (2000). Sonic hedgehog regulates growth and morphogenesis of the tooth. Development 127, 4775-4785.
10. 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.
11. 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.
12. Demehri, S., Turkoz, A. and Kopan, R. (2009). Epidermal Notch1 loss promotes skin tumorigenesis by impacting the stromal microenvironment. Cancer Cell 16, 55-66.
13. Diamond, I., Owolabi, T., Marco, M., Lam, C. and Glick, A. (2000). Conditional gene expression in the epidermis of transgenic mice using the tetracyclineregulated transactivators tTA and rTA linked to the keratin 5 promoter. J. Invest. Dermatol. 115, 788-794.
14. Dittmer, A., Hohlfeld, K., Lutzkendorf, J., Muller, L. P. and Dittmer, J. (2009). Human mesenchymal stem cells induce E-cadherin degradation in breast carcinoma spheroids by activating ADAM10. Cell Mol. Life Sci. 66, 3053-3065.
15. Dumortier, A., Durham, A. D., Di Piazza, M., Vauclair, S., Koch, U., Ferrand, G., Ferrero, I., Demehri, S., Song, L. L., Farr, A. G. et al. (2010). Atopic dermatitis-like disease and associated lethal myeloproliferative disorder arise from loss of notch signaling in the murine skin. PLoS ONE 5, e9258.
16. Ehebauer, M., Hayward, P. and Martinez-Arias, A. (2006). Notch signaling pathway. Sci. STKE 2006, cm7.
17. Fuchs, E. (1996). The cytoskeleton and disease: genetic disorders of intermediate filaments. Annu. Rev. Genet. 30, 197-231.
18. Gareus, R., Huth, M., Breiden, B., Nenci, A., Rosch, N., Haase, I., Bloch, W., Sandhoff, K. and Pasparakis, M. (2007). Normal epidermal differentiation but impaired skin-barrier formation upon keratinocyte-restricted IKK1 ablation. Nat. Cell Biol. 9, 461-469.
19. Hafner, M., Wenk, J., Nenci, A., Pasparakis, M., Scharffetter-Kochanek, K., Smyth, N., Peters, T., Kess, D., Holtkotter, O., Shephard, P. et al. (2004). Keratin 14 Cre transgenic mice authenticate keratin 14 as an oocyte-expressed protein. Genesis 38, 176-181.
20. Hardman, M. J., Sisi, P., Banbury, D. N. and Byrne, C. (1998). Patterned acquisition of skin barrier function during development. Development 125, 1541-1552.
21. Hartmann, D., de Strooper, B., Serneels, L., Craessaerts, K., Herreman, A., Annaert, W., Umans, L., Lubke, T., Lena Illert, A., von Figura, K. et al. (2002). The disintegrin/metalloprotease ADAM 10 is essential for Notch signalling but not for alpha-secretase activity in fibroblasts. Hum. Mol. Genet. 11, 2615-2624.
22. Hasler, R., Begun, A., Freitag-Wolf, S., Kerick, M., Mah, N., Zvirbliene, A., Spehlmann, M. E., von Wurmb-Schwark, N., Kupcinskas, L., Rosenstiel, P. et al. (2009). Genetic control of global gene expression levels in the intestinal mucosa: a human twin study. Physiol. Genomics 38, 73-79.
23. Hennings, H., Michael, D., Cheng, C., Steinert, P., Holbrook, K. and Yuspa, S. H. (1980). Calcium regulation of growth and differentiation of mouse epidermal cells in culture. Cell 19, 245-254.
24. Ingram, W. J., McCue, K. I., Tran, T. H., Hallahan, A. R. and Wainwright, B. J. (2008). Sonic Hedgehog regulates Hes1 through a novel mechanism that is independent of canonical Notch pathway signalling. Oncogene 27, 1489-1500.
25. Johnson, E. N., Nanney, L. B., Virmani, J., Lawson, J. A. and Funk, C. D. (1999). Basal transepidermal water loss is increased in platelet-type 12-lipoxygenase deficient mice. J. Invest. Dermatol. 112, 861-865.
26. Jones, P. H. and Watt, F. M. (1993). Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73, 713-724.
27. Jorissen, E., Prox, J., Bernreuther, C., Weber, S., Schwanbeck, R., Serneels, L., Snellinx, A., Craessaerts, K., Thathiah, A., Tesseur, I. et al. (2010). The disintegrin/metalloproteinase ADAM10 is essential for the establishment of the brain cortex. J. Neurosci. 30, 4833-4844.
28. Kaur, P., Li, A., Redvers, R. and Bertoncello, I. (2004). Keratinocyte stem cell assays: an evolving science. J. Investig. Dermatol. Symp. Proc. 9, 238-247.
29. Koster, M. I. and Roop, D. R. (2004). Genetic pathways required for epidermal morphogenesis. Eur. J. Cell Biol. 83, 625-629.
30. Koster, M. I. and Roop, D. R. (2007). Mechanisms regulating epithelial stratification. Annu. Rev. Cell Dev. Biol. 23, 93-113.
31. Kuraguchi, M., Wang, X. P., Bronson, R. T., Rothenberg, R., Ohene-Baah, N. Y., Lund, J. J., Kucherlapati, M., Maas, R. L. and Kucherlapati, R. (2006). Adenomatous polyposis coli (APC) is required for normal development of skin and thymus. PLoS Genet. 2, e146.
32. Lamar, E., Deblandre, G., Wettstein, D., Gawantka, V., Pollet, N., Niehrs, C. and Kintner, C. (2001). Nrarp is a novel intracellular component of the Notch signaling pathway. Genes Dev. 15, 1885-1899.
33. Lee, S. B., Schramme, A., Doberstein, K., Dummer, R., Abdel-Bakky, M. S., Keller, S., Altevogt, P., Oh, S. T., Reichrath, J., Oxmann, D. et al. (2010). ADAM10 is upregulated in melanoma metastasis compared with primary melanoma. J. Invest. Dermatol. 130, 763-773.
34. Lin, M. H. and Kopan, R. (2003). Long-range, nonautonomous effects of activated Notch1 on tissue homeostasis in the nail. Dev. Biol. 263, 343-359.
35. Lin, M. H., Leimeister, C., Gessler, M. and Kopan, R. (2000). Activation of the Notch pathway in the hair cortex leads to aberrant differentiation of the adjacent hair-shaft layers. Development 127, 2421-2432.
36. Mao, C. and Obeid, L. M. (2008). Ceramidases: regulators of cellular responses mediated by ceramide, sphingosine, and sphingosine-1-phosphate. Biochim. Biophys. Acta 1781, 424-434.
37. Maretzky, T., Scholz, F., Koten, B., Proksch, E., Saftig, P. and Reiss, K. (2008). ADAM10-mediated E-cadherin release is regulated by proinflammatory cytokines and modulates keratinocyte cohesion in eczematous dermatitis. J. Invest. Dermatol. 128, 1737-1746.
38. Miyazaki, M., Man, W. C. and Ntambi, J. M. (2001). Targeted disruption of stearoyl-CoA desaturase1 gene in mice causes atrophy of sebaceous and meibomian glands and depletion of wax esters in the eyelid. J. Nutr. 131, 2260-2268.
39. 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.
40. Moulson, C. L., Martin, D. R., Lugus, J. J., Schaffer, J. E., Lind, A. C. and Miner, J. H. (2003). Cloning of wrinkle-free, a previously uncharacterized mouse mutation, reveals crucial roles for fatty acid transport protein 4 in skin and hair development. Proc. Natl. Acad. Sci. USA 100, 5274-5279.
41. Mumm, J. S. and Kopan, R. (2000). Notch signaling: from the outside in. Dev. Biol. 228, 151-165.
42. Mumm, J. S., Schroeter, E. H., Saxena, M. T., Griesemer, A., Tian, X., Pan, D. J., Ray, W. J. and Kopan, R. (2000). A ligand-induced extracellular cleavage regulates gamma-secretase-like proteolytic activation of Notch1. Mol. Cell 5, 197-206.
43. 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-kappaB and PPARgamma. Cell Death Differ. 9, 842-855.
44. 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.
45. Oh, S. T., Schramme, A., Stark, A., Tilgen, W., Gutwein, P. and Reichrath, J. (2008). Overexpression of ADAM 10 and ADAM 12 in lesional psoriatic skin. Br. J. Dermatol. 158, 1371-1373.
46. Okochi, M., Fukumori, A., Jiang, J., Itoh, N., Kimura, R., Steiner, H., Haass, C., Tagami, S. and Takeda, M. (2006). Secretion of the Notch-1 Abeta-like peptide during Notch signaling. J. Biol. Chem. 281, 7890-7898.
47. Okuyama, R., Tagami, H. and Aiba, S. (2008). Notch signaling: its role in epidermal homeostasis and in the pathogenesis of skin diseases. J. Dermatol. Sci. 49, 187-194.
48. Oshima, H., Rochat, A., Kedzia, C., Kobayashi, K. and Barrandon, Y. (2001). Morphogenesis and renewal of hair follicles from adult multipotent stem cells. Cell 104, 233-245.
49. 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.
50. Proweller, A., Tu, L., Lepore, J. J., Cheng, L., Lu, M. M., Seykora, J., Millar, S. E., Pear, W. S. and Parmacek, M. S. (2006). Impaired notch signaling promotes de novo squamous cell carcinoma formation. Cancer Res. 66, 7438-7444.
51. Rangarajan, A., Talora, C., Okuyama, R., Nicolas, M., Mammucari, C., Oh, H., Aster, J. C., Krishna, S., Metzger, D., Chambon, P. et al. (2001). Notch signaling is a direct determinant of keratinocyte growth arrest and entry into differentiation. EMBO J. 20, 3427-3436.
52. Rodewald, H. R. (2008). Thymus organogenesis. Annu. Rev. Immunol. 26, 355-388.
53. Segre, J. A. (2006). Epidermal barrier formation and recovery in skin disorders. J. Clin. Invest. 116, 1150-1158.
54. Tavazoie, S., Hughes, J. D., Campbell, M. J., Cho, R. J., Church, G. M. (1999). Systematic determination of genetic network architecture. Nat. Genet. 22, 281-285.
55. Taylor, G., Lehrer, M. S., Jensen, P. J., Sun, T. T. and Lavker, R. M. (2000). Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102, 451-461.
56. Thelu, J., Rossio, P. and Favier, B. (2002). Notch signalling is linked to epidermal cell differentiation level in basal cell carcinoma, psoriasis and wound healing. BMC Dermatol. 2, 7.
57. Tunggal, J. A., Helfrich, I., Schmitz, A., Schwarz, H., Gunzel, D., Fromm, M., Kemler, R., Krieg, T. and Niessen, C. M. (2005). E-cadherin is essential for in vivo epidermal barrier function by regulating tight junctions. EMBO J. 24, 1146-1156.
58. Uyttendaele, H., Panteleyev, A. A., de Berker, D., Tobin, D. T. and Christiano, A. M. (2004). Activation of Notch1 in the hair follicle leads to cell-fate switch and Mohawk alopecia. Differentiation 72, 396-409.
59. Vauclair, S., Nicolas, M., Barrandon, Y. and Radtke, F. (2005). Notch1 is essential for postnatal hair follicle development and homeostasis. Dev. Biol. 284, 184-193.
60. Vauclair, S., Majo, F., Durham, A. D., Ghyselinck, N. B., Barrandon, Y. and Radtke, F. (2007). Corneal epithelial cell fate is maintained during repair by Notch1 signaling via the regulation of vitamin A metabolism. Dev. Cell 13, 242-253.
61. Watt, F. M., Estrach, S. and Ambler, C. A. (2008). Epidermal Notch signalling: differentiation, cancer and adhesion. Curr. Opin. Cell Biol. 20, 171-179.
62. Yamamoto, N., Tanigaki, K., Han, H., Hiai, H. and Honjo, T. (2003). Notch/RBPJ signaling regulates epidermis/hair fate determination of hair follicular stem cells. Curr. Biol. 13, 333-338.
63. Zhang, P., Yang, Y., Nolo, R., Zweidler-McKay, P. A. and Hughes, D. P. (2010). Regulation of NOTCH signaling by reciprocal inhibition of HES1 and Deltex 1 and its role in osteosarcoma invasiveness. Oncogene 29, 2916-2926.