N-WASP is a novel regulator of hair-follicle cycling that controls antiproliferative TGFβ pathways

Journal of Cell Science

Volumn 123, Issue 1, 2010, Pages 128-140

  Lefever, Tine ^a,b   Pedersen, Esben ^a   Basse, Astrid ^a   Paus, Ralf ^c,d   Quondamatteo, Fabio ^e   Stanley, Alanna C ^e   Langbein, Lutz ^f   Wu, Xunwei ^a   Wehland, Jürgen ^g   Lommel, Silvia ^h   Brakebusch, Cord ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b GHENT UNIVERSITY   (Belgium)

^c UNIVERSITY OF LÜBECK   (Germany)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^h UNIVERSITY OF BONN   (Germany)

Author keywords

Hair cycling; Keratinocytes; N WASP

Indexed keywords

ALPHA6BETA4 INTEGRIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 2B; LORICRIN; MITOGEN ACTIVATED PROTEIN KINASE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; PROTEIN CDC42; TRANSCRIPTION FACTOR MSX2; TRANSFORMING GROWTH FACTOR BETA;

ALOPECIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; EPIDERMIS; GENE DELETION; HAIR FOLLICLE; KERATINOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SKIN EPITHELIUM; WOUND HEALING;

ALOPECIA; ANIMALS; CELL CYCLE; CELL PROLIFERATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P15; CYCLIN-DEPENDENT KINASE INHIBITOR P21; HAIR FOLLICLE; KERATINOCYTES; MICE; MICROFILAMENTS; MORPHOGENESIS; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA; WISKOTT-ALDRICH SYNDROME PROTEIN, NEURONAL;

MUS;

EID: 72449149288     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.053835     Document Type: Article

References (43)

1. Bierie, B. and Moses, H. L. (2006). Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat. Rev. Cancer 6, 506-520.
2. Chang, F. S., Stefan, C. J. and Blumer, K. J. (2003). A WASp homolog powers actin polymerization-dependent motility of endosomes in vivo. Curr. Biol. 13, 455-463.
3. Cho, Y. S., Bae, J. M., Chun, Y. S., Chung, J. H., Jeon, Y. K., Kim, I. S., Kim, M. S. and Park, J. W. (2008). HIF-1 alpha controls keratinocytes proliferation by up-regulating p21(WAF/Cip1). Biochim. Biophys. Acta. 1783, 323-333.
4. Chrostek, A., Wu, X., Quondamatteo, F., Hu, R., Sanecka, A., Niemann, C., Langbein, L., Haase, I. and Brakebusch, C. (2006). Rac1 is crucial for hair follicle integrity but is not essential for maintenance of the epidermis. Mol. Cell. Biol. 26, 6957-6970.
5. Co, C., Wong, D. T., Gierke, S., Chang, V. and Taunton, J. (2007). Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128, 901-913.
6. Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H. C. and Lempicki, R. A. (2003). DAVID: database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3.
7. Foitzik, K., Lindner, G., Mueller-Roever, S., Maurer, M., Botchkareva, N., Botchkarev, V., Handjiski, B., Metz, M., Hibino, T., Soma, T. et al. (2000). Control of murine hair follicle regression (catagen) by TGF-beta1 in vivo. FASEB J. 14, 752-760.
8. Fuchs, E. (2007). Scratching the surface of skin development. Nature 445, 834-842.
9. Guasch, G., Schober, M., Pasolli, H. A., Conn, E. B., Polak, L. and Fuchs, E. (2007). Loss of TGFbeta signaling destabilizes homeostasis and promotes squamous cell carcinomas in stratified epithelia. Cancer Cell 12, 313-327.
10. Hempel, N., How, T., Cooper, S. J., Green, T. R., Dong, M., Copland J. A., Wood, C. G. and Blobe, G. C. (2008). Expression of the type III TGF-beta receptor is negatively regulated by TGF-beta. Carcinogenesis 29, 905-912.
11. Innocenti, M., Gerboth, S., Rottner, K., Lai, F. P. L., Hertzog, M., Stradal, T. E. B., Frittoli, E., Didry, D., Polo, S., Disanza, A. et al. (2005). Abi1 regulates the activity of N-WASP and WAVE in distinct actin-based processes. Nat. Cell Biol. 7, 969-976.
12. Langbein, L. and Schweizer, J. (2005). Keratins of the human hair follicle. Int. Rev. Cytol. 243, 1-78.
13. Langbein, L., Rogers, M. A., Praetzel, S., Winter, H. and Schweizer, J. (2003). K6irs1, K6irs2, K6irs3, and K6irs4 represent the inner-root-sheath-specific type II epithelial keratins of the human hair follicle. J. Invest. Dermatol. 120, 512-522.
14. Le Roy, C. and Wrana J. L. (2005). Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell. Biol. 6, 112-126.
15. Li, A. G., Wang, D., Feng, X. and Wang, X. (2004). Latent TGFbeta1 overexpression in keratinocytes results in a severe psoriasis-like skin disorder. EMBO J. 23, 1770-1781.
16. Lommel, S., Benesch, S., Rottner, K., Franz, T., Wehland, J. and Kuhn, R. (2001). Actin pedestal formation by enteropathogenic Escherichia coli and intracellular motility of Shigella flexneri are abolished in N-WASP-defective cells. EMBO Rep. 2, 850-857.
17. Ma, L., Liu, J., Wu, T., Plikus, M., Jiang, T., Bi, Q., Liu, Y., Muller-Rover, S., Peters, H., Sundberg, J. P. et al. (2003). 'Cyclic alopecia' in Msx2 mutants: defects in hair cycling and hair shaft differentiation. Development 130, 379-389.
18. Mammucari, C., Tommasi di Vignano, A., Sharov, A. A., Neilson, J., Havrda, M. C., Roop, D. R., Botchkarev, V. A., Crabtree, G. R. and Dotto, G. P. (2005). Integration of Notch 1 and calcineurin/NFAT signaling pathways in keratinocyte growth and differentiation control. Dev. Cell 8, 665-676.
19. Millard, T. H., Sharp, S. J. and Machesky, L. M. (2004). Signalling to actin assembly via the WASP (Wiskott-Aldrich syndrome protein)-family proteins and the Arp2/3 complex. Biochem. J. 380, 1-17.
20. Mizutani, K., Miki, H., He, H., Maruta, H. and Takenawa, T. (2002). Essential role of neural Wiskott-Aldrich syndrome protein in podosome formation and degradation of extracellular matrix in src-transformed fibroblasts. Cancer Res. 62, 669-674.
21. Müller-Röver, S., Handjiski, B., van der Veen, C., Eichmüller, S., Foitzik, K., McKay, I. A., Stenn, K. S. and Paus, R. (2001). A comprehensive guide for the accurate classification of murine hair follicles in distinct hair cycle stages. J. Invest. Dermatol. 117, 3-15.
22. Niessen, C. M. (2007). Tight junctions/adherens junctions: basic structure and function. J. Invest. Dermatol. 127, 2525-2532.
23. Otani, T., Ichii, T., Aono, S. and Takeichi, M. (2006). Cdc42 GEF Tuba regulates the junctional configuration of simple epithelial cells. J. Cell Biol. 175, 135-146.
24. Pardali, K., Kowanetz, M., Heldin, C. and Moustakas, A. (2005). Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J. Cell Physiol. 204, 260-272.
25. Paus, R. and Foitzik K. (2004). In search of the "hair cycle clock": a guided tour. Differentiation 72, 489-511.
26. Paus, R., Müller-Röver, S., Van Der Veen, C., Maurer, M., Eichmuller, S., Ling, G., Hofmann, U., Foitzik, K., Mecklenburg, L. and Handjiski, L. B. (1999). A comprehensive guide for the recognition and classification of distinct stages of hair follicle morphogenesis. J. Invest. Dermatol. 113, 523-532.
27. Pinyol, R., Haeckel, A., Ritter, A., Qualmann, B. and Kessels, M. M. (2007). Regulation of N-WASP and the Arp2/3 complex by Abp1 controls neuronal morphology. PLoS ONE 2, e400.
28. Plikus, M. V., Mayer, J. A., de la Cruz, D., Baker, R. E., Maini, P. K., Maxson, R. and Chuong, C. (2008). Cyclic dermal BMP signalling regulates stem cell activation during hair regeneration. Nature 451, 340-344.
29. Pollard, T. D. and Borisy, G. G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112, 453-465.
30. Ramirez, A., Page, A., Gandarillas, A., Zanet, J., Pibre, S., Vidal, M., Tusell, L., Genesca, A., Whitaker, D. A. et al. (2004). A keratin K5Cre transgenic line appropriate for tissue-specific or generalized Cre-mediated recombination. Genesis 39, 52-57.
31. 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.
32. Reynisdóttir, I., Polyak, K., Iavarone, A. and Massagué, J. (1995). Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev. 9, 1831-1845.
33. Sellheyer, K., Bickenbach, J. R., Rothnagel, J. A., Bundman, D., Longley, M. A., Krieg, T., Roche, N. S., Roberts, A. B. and Roop, D. R. (1993). Inhibition of skin development by overexpression of transforming growth factor beta 1 in the epidermis of transgenic mice. Proc. Natl. Acad. Sci. USA 90, 5237-5241.
34. Snapper, S. B., Takeshima, F., Antón, I., Liu, C. H., Thomas, S. M., Nguyen, D., Dudley, D., Fraser, H., Purich, D., Lopez-Ilasaca, M. et al. (2001). N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3, 897-904.
35. Stenn, K. S. and Paus, R. (2001). Controls of hair follicle cycling. Physiol. Rev. 81, 449-494.
36. Ten Dijke, P., Goumans, M., Itoh, F. and Itoh, S. (2002). Regulation of cell proliferation by Smad proteins. J. Cell Physiol. 191, 1-16.
37. To, C., Kulkarni, S., Pawson, T., Honda, T., Gribble, G. W., Sporn, M. B., Wrana, J. L. and Di Guglielmo, G. M. (2008). The synthetic triterpenoid 2-cyano-3,12-dioxooleana-1,9-dien-28-oic acid-imidazolide alters transforming growth factor beta-dependent signaling and cell migration by affecting the cytoskeleton and the polarity complex. J. Biol. Chem. 283, 11700-11713.
38. Wang, X. J., Liefer, K. M., Tsai, S., O'Malley, B. W. and Roop, D. R. (1999). Development of gene-switch transgenic mice that inducibly express transforming growth factor beta1 in the epidermis. Proc. Natl. Acad. Sci. USA 96, 8483-8488.
39. Werner, S. and Grose, R. (2003). Regulation of wound healing by growth factors and cytokines. Physiol. Rev. 83, 835-870.
40. Wu, X., Yoo, Y., Okuhama, N. N., Tucker, P. W., Liu, G. and Guan, J. (2006a). Regulation of RNA-polymerase-II-dependent transcription by N-WASP and its nuclear-binding partners. Nat. Cell Biol. 8, 756-763.
41. Wu, X., Quondamatteo, F. and Brakebusch, C. (2006b). Cdc42 expression in keratinocytes is required for the maintenance of the basement membrane in skin. Matrix Biol. 25, 466-474.
42. Wu, X., Quondamatteo, F., Lefever, T., Czuchra, A., Meyer, H., Chrostek, A., Paus, R., Langbein, L. and Brakebusch, C. (2006c). Cdc42 controls progenitor cell differentiation and beta-catenin turnover in skin. Genes Dev. 20, 571-585.
43. Yarar, D., Waterman-Storer, C. M. and Schmid, S. L. (2007). SNX9 couples actin assembly to phosphoinositide signals and is required for membrane remodeling during endocytosis. Dev. Cell 13, 43-56.