The TFIID subunit TAF4 regulates keratinocyte proliferation and has cell-autonomous and non-cell-autonomous tumour suppressor activity in mouse epidermis

Development

Volumn 134, Issue 16, 2007, Pages 2947-2958

  Fadloun, Anas ^a   Kobi, Dominique ^a   Pointud, Jean Christophe ^a,c   Indra, Arup Kumar ^a,d   Teletin, Marius ^a   Bole Feysot, Christine ^a   Testoni, Barbara ^b   Mantovani, Roberto ^b   Metzger, Daniel ^a   Mengus, Gabrielle ^a   Davidson, Irwin ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

^d OREGON STATE UNIVERSITY   (United States)

Author keywords

Alopecia; EGF; Growth factors; Hair cycle; Homologous recombination; TPA; Wnt pathway

Indexed keywords

CRE RECOMBINASE; CYTOKERATIN 14; TAMOXIFEN; TATA BINDING PROTEIN ASSOCIATED FACTOR; TATA BINDING PROTEIN ASSOCIATED FACTOR 4; TRANSCRIPTION FACTOR IID; UNCLASSIFIED DRUG;

ALOPECIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EPIDERMIS; FEMALE; FETUS; GENE EXPRESSION; GENE INACTIVATION; GENE LOSS; HAIR FOLLICLE; HAIR GROWTH; HOMOLOGOUS RECOMBINATION; HYPERPLASIA; KERATINOCYTE; MALE; MOUSE; MUTANT; NEWBORN DEATH; NONHUMAN; PAPILLOMA; PRIORITY JOURNAL; SKIN CARCINOGENESIS; SKIN PERMEABILITY; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; EPIDERMIS; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HAIR; HYPERPLASIA; KERATINOCYTES; MALE; MICE; MICE, KNOCKOUT; NEVUS, PIGMENTED; PROTEIN SUBUNITS; SKIN NEOPLASMS; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION FACTOR TFIID; TRETINOIN; TUMOR SUPPRESSOR PROTEINS;

EID: 34548570094     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.005041     Document Type: Article

References (62)

1. Abe, Y., Matsumoto, S., Kito, K. and Ueda, N. (2000). Cloning and expression of a novel MAPKK-like protein kinase, lymphokine-activated killer T-cell-originated protein kinase, specifically expressed in the testis and activated lymphoid cells. J. Biol. Chem. 275, 21525-21531.
2. Brand, M., Yamamoto, K., Staub, A. and Tora, L. (1999). Identification of TATA-binding protein-free TAI'll-containing complex subunits suggests a role in nucleosome acetylation and signal transcluction. J. Biol. Chem. 274, 18285-18289.
3. Chapellier, B., Mark, M., Messaddeq, N., Calleja, C., Warot, X., Brocard, J., Gerard, C., Li, M., Metzger, D., Ghyselinck, N. B. et al. (2002). Physiological and retinoid-induced proliferations of epidermis basal keratinocytes are differently controlled. EMBO J. 21, 3402-3413.
4. Collins, C. S., Hong, J., Sapinoso, L., Zhou, Y., Liu, Z., Micklash, K., Schultz, P. G. and Hampton, G. M. (2006). A small interfering RNA screen for modulators of tumor cell motility identifies MAP4K4 as a promigratory kinase. Proc. Natl. Acad. Sci. USA 103, 3775-3780.
5. Dai, X. and Segre, J. A. (2004). Transcriptional control of epidermal specification and differentiation. Curr. Opin. Genet. Dev. 14, 485-491.
6. Falender, A. E., Freiman, R. N., Geles, K. G., Lo, K. C., Hwang, K., Lamb, D. J., Morris, P L., Tjian, R. and Richards, J. S. (2005). Maintenance of spermatogenesis requires TAF41b, a gonad-specific subunit of TFIID. Genes Dev. 19, 794-803.
7. Freiman, R. N., Albright S. R., Zheng, S., Sha, W. C., Hammer, R. E. and Tjian, R. (2001). Requirement of tissue-selective TBP-associated factor TAFII105 in ovarian development. Science 293, 2084-2087.
8. Frontini, M., Soutoglou, E., Argentini, M., Bole-Feysot, C., Jost, B., Scheer, E. and Tora, L. (2005). TAF91b (formerly TAF9L) is a bona fide TAF that has unique and overlapping roles with TAF9. Mol. Cell. Biol. 25, 4638-4649.
9. Fuchs, E. and Raghavan, S. (2002). Getting under the skin of epidermal morphogenesis. Nat. Rev. Genet. 3, 199-209.
10. Fuchs, E., Merrill, B. J., Jamora, C. and DasGupta, R. (2001). At the roots of a never-ending cycle. Dev. Cell. 1, 13-25.
11. Furuse, M., Hata, M., Furuse, K., Yoshida, Y., Haratake, A., Sugitani, Y., Noda, T., Kubo, A. and Tsukita, S. (2002). Claudin-based tight junctions are crucial for the mammalian epidermal barrier: a lesson f rom claudin-1-deficient mice. J. Cell Biol. 156, 1099-1111.
12. Futoryan, T. and Gilchrest, B. A. (1994). Retinoids and the skin. Nutr. Rev. 52, 299-310.
13. Gangloff, Y. G., Werten, S., Romier, C., Carre, L., Poch, O., Moras, D. and Davidson, I. (2000). The human THID components TAF(II)135 and TAF(II)20 and the yeast SAGA components ADA1 and TAF(II)68 heterodimerize to form histone-like pairs. Mol. Cell. Biol. 20, 340-351.
14. Grimmond, S., Larder, R., Van Hateren, N., Siggers, R, Hulsebos, T. J., Arkell, R. and Greenfield, A. (2000). Cloning, mapping, and expression analysis of a gene encoding a novel mammalian EGF-related protein (SCUBE1), Genomics 70, 74-81.
15. Grob, P, Cruse, M. J., Inouye, C., Peris, M., Penczek, P A., Tjian, R. and Nogales, E. (2006). Cryo-electron microscopy studies of human TFIID: conformational breathing in the integration of gene regulatory cues. Structure 14, 511-520.
16. Hardman, M. J., Sisi, R, Banbury, D. N. and Byrne, C. (1998). Patterned acquisition of skin barrier function during development. Development 125, 1541-1552.
17. Hocevar, B. A., Smine, A., Xu, X. X. and Howe, P. H. (2001). The adaptor molecule Disabled-2 links the transforming growth factor beta receptors to the Smad pathway. EMBO J. 20, 2789-2801.
18. Hocevar, B. A., Mou, F., Rennolds, J. L., Morris, S. M., Cooper, J. A. and Howe, P. H. (2003). Regulation of the Wnt signaling pathway by disabled-2 (Dab2). EMBO J. 22, 3084-3094.
19. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G. and Birchmeier, W. (2001). beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545.
20. Husain, Z., Pathak, M. A., Flotte, T. and Wick, M. M. (1991). Role of ultraviolet radiation in the induction of melanocytic tumors in hairless mice following 7, 12-dimethylbenz(a)anthracene application and ultraviolet irradiation. Cancer Res. 51, 4964-4970.
21. Indra, A. K., Warot, X., Brocard, J., Bornert, J. M., Xiao, J. H., Chambon, P. and Metzger, D. (1999). Temporal ly-control led site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen- inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res. 27, 4324-4327.
22. Indra, A. K., Mohan, W. S., 2nd, Frontini, M., Scheer, E., Messaddeci, N., Metzger, D. and Tora, L. (2005). TAF10 is required for the establishment of skin barrier function in foetal, but not in adult mouse epidermis. Dev. Biol. 285, 28-37.
23. Indra, A. K., Casteneda, E., Antal, M. C., Jiang, M., Messaddeq, N., Meng, X., Loehr, C. V., Gariglio, R, Kato, S., Wahli, W. et al. (2007). Malignant transformation of DMBAITPA-incluced papiliomas and nevi in the skin of mice selectively lacking RXR alpha in epidermal keratinocytes. J. Invest. Dermatol. 127, 1250-1260.
24. Jiang, T. X., Liu, Y. H., Widelitz, R. B., Kundu, R. K., Maxson, R. E. and Chuong, C. M. (1999). Epidermal clysplasia and abnormal hair follicles in transgenic mice overexpressing homeobox gene MSX-2. J. Invest. Dermatol. 113, 230-237.
25. Koster, M. I. and Roop, D. R. (2004). The role of p63 in development and differentiation of the epidermis. J. Dermatol. Sci. 34, 3-9.
26. Koster, M. I., Kim, S., Mills, A. A., DeMayo, F. J. and Roop, D. R. (2004). p63 is the molecular switch for initiation of an epithelial stratification program. Genes Dev. 18, 126-131.
27. Le Brigand, K., Russell, R., Moreilhon, C., Rouillard, J. M., Jost, B., Amiot, F., Magnone, V., Bole-Feysot, C., Rostagno, P., Virolle, V. et al. (2006). An open-access long oligonucleoticle microarray resource for analysis of the human and mouse transcriptomes. Nucleic Acids Res. 34, e87.
28. Leurent, C., Sanders, S. L., Demeny, M. A., Garbett, K. A., Ruhimann, C., Weil, P. A., Tora, L. and Schultz, P. (2004). Mapping key functional sites within yeast TFIID. EMBO J. 23, 719-727.
29. Li, M., Indra, A. K., Warot, X., Brocard, J., Messaddeq, N., Kato, S., Metzger, D. and Chambon, P. (2000). Skin abnormalities generated by temporally controlled RXRalpha mutations in mouse epidermis. Nature 407, 633-636,
30. Li, M., Chiba, H., Warot, X., Messaddeq, N., Gerard, C., Chambon, P. and Metzger, D. (2001). RXR-alpha ablation in skin keratinocytes results in alopecia and epidermal alterations. Development 128, 675-688.
31. Ma, L., Liu, J., Wu, T., Plikus, M., Jiang, T. X., Bi, Q., Liu, Y. H., 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.
32. Matangkasombut O., Auty, R. and Buratowski, S. (2004). Structure and function of the TAID complex. Adv. Protein Chem. 67, 67-92.
33. Mengus, G., May, M., Carre, L., Chambon, P. and Davidson, I. (1997). Human TAF(II)135 potentiates transcriptional activation by the AF-2s of the retinoic acid, vitamin D3, and thyroid hormone receptors in mammalian cells. Gene Dev 11, 1381-1395.
34. Mengus, G., Fadloun, A., Kobi, D., Thibault, C., Perletti, L., Michel, I. and Davidson, I. (2005). TAF4 inactivation in embryonic fibroblasts activates TGFbeta signalling and autocrine growth. EMBO J. 24, 2753-2767.
35. Park, J. H., Lin, M. L., Nishiclate, Y. Nakamura, Y. and Katagiri, T. (2006). PDZ-binding kinase/T-LAK cell-originated protein kinase, a putative cancer/testis antigen with an oncogenic activity in breast cancer. Cancer Res. 66, 9186-9195.
36. Reiner, A., Yekutieli, D. and Benjamini, Y. (2003). Identifying differentially expressed genes using false discovery rate controlling procedures. Bioinformatics 19, 368-375.
37. Reynolds, P. A., Smolen, G. A., Palmer, R. E., Sgroi, D., Yajnik, V., Gerald, W. L. and Haber, D. A. (2003). Identification of a DNA-binding site and transcriptional target for the EWS-WT1 (+KTS) oncoprotein. Genes Dev. 17, 2094-2107.
38. Richard, G. (2000). Connexins: a connection with the skin. Exp. Dermatol. 9, 77-96.
39. Rittie, L., Varani, J., Kang, S., Voorhees, J. J. and Fisher, G. J. (2006). Retinoid-induced epidermal hyperplasia is mediated by epidermal growth factor receptor activation via specific induction of its ligands heparin-binding EGF and amphiregulin in human skin in vivo. J. Invest. Dermatol. 126, 732-739.
40. Rochaix, R, Lacroix-Triki, M., Lamant, L., Pichereaux, C., Valmary. S., Puente, E., Al, Saati, T., Monsarrat, B., Susini, C., Buscall, L. et al. (2003). PNL2, a new monoclonal antibody directed against a fixative-resistant melanocyte antigen. Mod. Pathol. 16, 481-490.
41. Sanders, S. L. and Weil, P. A. (2000). Identification of two novel TAF subunits of the yeast saccharomyces cerevisiae TRID complex. J. Biol. Chem. 275, 13895-13900.
42. Satoh, K., Hata, M. and Yokota, H. (2002). A novel member of the leucine-rich repeat superfamily induced in rat astrocytes by beta-amyloid. Biochem. Biophys. Res. Commun. 290, 756-762.
43. Shi, Y. and Massague, J. (2003). Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell 113, 685-700.
44. Steinert, P. M. (2000). The complexity and redundancy of epithelial barrier function. J. Cell Biol. 151, F5-F8.
45. Stoll, S. W. and Elder, J. T. (1998). Retinoid regulation of heparin-binding EGF-like growth factor gene expression in human keratinocytes and skin. Exp. Dermatol. 7, 391-397.
46. Takebe, K., Oka, Y., Radisky, D., Tsuda, H., Tochigui, K., Koshicla, S., Kogo, K. and Hirai, Y. (2003). Epimorphin acts to induce hair follicle anagen in C57BL/6 mice. FASEB J. 17, 2037-2047.
47. Tanese, N., Saluja, D., Vassallo, M. F., Chen, J. L. and Admon, A. (1996). Molecular cloning and analysis of two subunits of the human TFIID complex: hTAFII130 and hTAFII100. Proc. Natl. Acad. Sci. USA 93, 13611-13616.
48. Thuault S., Gangloff, Y. G., Kirchner, J., Sanders, S., Werten, S., Romier, C., Weil, R A. and Davidson, I. (2002). Functional analysis of the TFIID-specific yeast TAF4 (yTAF(II)48) reveals an unexpected organization of its histone-fold domain. J. Biol. Chem. 277, 45510-45517.
49. Tong, X. and Coulombe, P. A. (2006). Keratin 17 modulates hair follicle cycling in a TNFalpha-dependent fashion. Genes Dev. 20, 1353-1364.
50. Tora, L. (2002). A unified nomenclature for TATA box binding protein (TBP)-associated factors (TAFs) involved in RNA polymerase II transcription. Genes Dev. 16, 673-675.
51. Trempus, C. S., Morris, R. J., Bortner, C. D., Cotsarelis, G., Fairdoth, R. S., Reece, J. M. and Tennant R. W. (2003). Enrichment for living murine keratinocytes from the hair follicle bulge with the cell surface marker CD34. J. Invest. Dermatol. 120, 501-511.
52. Van Mater, D., Kolligs, F. T., Dlugosz, A. A. and Fearon, E. R. (2003). Transient activation of beta-catenin signaling in cutaneous keratinocytes is sufficient to trigger the active growth phase of the hair cycle in mice. Genes Dev. 17, 1219-1224.
53. Walker, A. K., Rothman, J. H., Shi, Y. and Blackwell, T. K. (2001). Distinct requirements for C.elegans TAF(II)s in early embryonic transcription. EMBO J. 20, 5269-5279.
54. Wang, W. P., Widelitz, R. B., Jiang, T. X. and Chuong, C. M. (1999). Msx-2 and the regulation of organ size: epidermal thickness and hair length. J. Investig. Dermatol. Symp. Proc. 4, 278-281.
55. Wang, X. J. (2001). Role of TGFbeta signaling in skin carcinogenesis. Microsc. Res. Tech. 52, 420-429.
56. Wang, Z., Tseng, C. P., Pong, R. C., Chen, H., McConnell, J. D., Navone, N. and Hsieh, J. T. (2002). The mechanism of growth-inhibitory effect of DOC-2/DAB2 in prostate cancer. Characterization of a novel GTPase-activating protein associated with N-terminal domain of DOC-2/DA92. J. Biol. Chem. 277, 12622-12631.
57. Woodring, P. J., Hunter, T. and Wang, J. Y. (2003). Regulation of F-actin-dependent processes by the AbI family of tyrosine kinases. J. Cell Sci. 116, 2613-2626.
58. Xiao, J. H., Feng, X., Di, W., Peng, Z. H., U, L. A., Chambon, P. and Voorhees, J. J. (1999). Identification of heparin-binding EGF-like growth factor as a target in intercellular regulation of epidermal basal cell growth by suprabasal retinoic acid receptors. EMBO J. 18, 1539-1548.
59. Zeeuwen, P. L. (2004). Epidermal differentiation: the role of proteases and their inhibitors. Eur. J. Cell Biol. 83, 761-773.
60. Zhou, J. and Hsieh, J. T. (2001). The inhibitory role of DOC-2/ DAB2 in growth factor receptor-mediated signal cascade. DOC-2/ DAB2-mediated inhibition of ERK phosphorylation via binding to Grb2. J. Biol. Chem. 276, 27793-27798.
61. Zhou, T., Raman, M., Gao, Y., Earnest, S., Chen, Z., Machius, M., Cobb, M. H. and Goldsmith, E. J. (2004). Crystal structure of the TAO2 kinase domain: activation and specificity of a Ste20p MAP3K. Structure 12, 1891-1900.
62. Zouboulis, C. C. (2001). Retinoids - which dermatological indications will benefit in the near future? Skin Pharmacol. Appl. Skin Physiol. 14, 303-315.