P63 control of desmosome gene expression and adhesion is compromised in AEC syndrome

Human Molecular Genetics

Volumn 22, Issue 3, 2013, Pages 531-543

  Ferone, Giustina ^a,h   Mollo, Maria Rosaria ^b   Thomason, Helen A ^c,i   Antonini, Dario ^b   Zhou, Huiqing ^d,e   Ambrosio, Raffaele ^a   De rosa, Laura ^b,j   Salvatore, Domenico ^f   Getsios, Spiro ^g   van Bokhoven, Hans ^d   Dixon, Jill ^c   Missero, Caterina ^a,b  

^a IRCCS SDN   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

^d RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^f UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^g NORTHWESTERN UNIVERSITY   (United States)

^h NETHERLANDS CANCER INSTITUTE   (Netherlands)

ⁱ UNIVERSITY OF MANCHESTER   (United Kingdom)

^j UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; DESMOCOLLIN; DESMOGLEIN 1; DESMOPLAKIN; P CADHERIN; PROTEIN P63; RNA; UVOMORULIN;

AEC SYNDROME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL ISOLATION; CELL JUNCTION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DESMOSOME; DISEASE ASSOCIATION; DISEASE SEVERITY; DOWN REGULATION; ELECTRON MICROSCOPY; EPIDERMIS; EPIDERMIS CELL; INHIBITION KINETICS; KERATINOCYTE; MECHANICAL STRESS; MISSENSE MUTATION; MOUSE; MUTATIONAL ANALYSIS; NEWBORN; NONHUMAN; PHENOTYPE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; SKIN FRAGILITY; TRANSACTIVATION; UPREGULATION; WILD TYPE;

ANIMALS; CELL ADHESION; CELLS, CULTURED; CHROMATIN IMMUNOPRECIPITATION; CLEFT LIP; CLEFT PALATE; CLONING, MOLECULAR; DESMOSOMES; ECTODERMAL DYSPLASIA; EPIDERMIS; EPITHELIUM; EYE ABNORMALITIES; EYELIDS; FEMALE; GENE EXPRESSION REGULATION; HUMANS; KERATINOCYTES; LUCIFERASES; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SKIN;

EID: 84872422284     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds464     Document Type: Article

References (77)

1. Fuchs, E. and Raghavan, S. (2002) Getting under the skin of epidermal morphogenesis. Nat. Rev., 3, 199-209.
2. Koster, M.I., Dai, D., Marinari, B., Sano, Y., Costanzo, A., Karin, M. and Roop, D.R. (2007) p63 induces key target genes required for epidermal morphogenesis. Proc. Natl Acad. Sci. U S A, 104, 3255-3260.
3. 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.
4. 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.
5. 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.
6. 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.
7. Truong, A.B., Kretz, M., Ridky, T.W., Kimmel, R. and Khavari, P.A. (2006) p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes Dev., 20, 3185-3197.
8. 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.
9. Nguyen, B.C., Lefort, K., Mandinova, A., Antonini, D., Devgan, V., Della Gatta, G., Koster, M.I., Zhang, Z., Wang, J., di Vignano, A.T. et al. (2006) Cross-regulation between Notch and p63 in keratinocyte commitment to differentiation. Genes Dev., 20, 1028-1042.
10. Carroll, D.K., Carroll, J.S., Leong, C.O., Cheng, F., Brown, M., Mills, A.A., Brugge, J.S. and Ellisen, L.W. (2006) p63 regulates an adhesion programme and cell survival in epithelial cells. Nat. Cell Biol., 8, 551-561.
11. Yang, A., Kaghad, M., Wang, Y., Gillett, E., Fleming, M.D., Dotsch, V., Andrews, N.C., Caput, D. and McKeon, F. (1998) p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol. Cell, 2, 305-316.
12. Della Gatta, G., Bansal, M., Ambesi-Impiombato, A., Antonini, D., Missero, C. and di Bernardo, D. (2008) Direct targets of the TRP63 transcription factor revealed by a combination of gene expression profiling and reverse engineering. Genome Res., 18, 939-948.
13. Koster, M.I. (2010) p63 in skin development and ectodermal dysplasias. J. Invest. Dermatol., 130, 2352-2358.
14. LeBoeuf, M., Terrell, A., Trivedi, S., Sinha, S., Epstein, J.A., Olson, E.N., Morrisey, E.E. and Millar, S.E. (2010) Hdac1 and Hdac2 act redundantly to control p63 and p53 functions in epidermal progenitor cells. Dev. Cell, 19, 807-818.
15. Romano, R.A., Smalley, K., Magraw, C., Serna, V.A., Kurita, T., Raghavan, S. and Sinha, S. (2012) DeltaNp63 knockout mice reveal its indispensable role as a master regulator of epithelial development and differentiation. Development, 139, 772-782.
16. Rinne, T., Hamel, B., van Bokhoven, H. and Brunner, H.G. (2006) Pattern of p63 mutations and their phenotypes-update. Am. J. Med. Genet. A, 140, 1396-1406.
17. Dishop, M.K., Bree, A.F. and Hicks, M.J. (2009) Pathologic changes of skin and hair in ankyloblepharon-ectodermal defects-cleft lip/palate (AEC) syndrome. Am. J. Med. Genet. A, 149A, 1935-1941.
18. McGrath, J.A., Duijf, P.H., Doetsch, V., Irvine, A.D., de Waal, R., Vanmolkot, K.R., Wessagowit, V., Kelly, A., Atherton, D.J., Griffiths, W.A. et al. (2001) Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum. Mol. Genet., 10, 221-229.
19. Julapalli, M.R., Scher, R.K., Sybert, V.P., Siegfried, E.C. and Bree, A.F. (2009) Dermatologic findings of ankyloblepharon-ectodermal defects-cleft lip/palate (AEC) syndrome. Am. J. Med. Genet. A, 149A, 1900-1906.
20. Siegfried, E., Bree, A., Fete, M. and Sybert, V.P. (2005) Skin erosions and wound healing in ankyloblepharon-ectodermal defect-cleft lip and/or palate. Arch. Dermatol., 141, 1591-1594.
21. Michels, C., Buchta, T., Bloch, W., Krieg, T. and Niessen, C.M. (2009) Classical cadherins regulate desmosome formation. J. Invest. Dermatol., 129, 2072-2075.
22. Simpson, C.L., Patel, D.M. and Green, K.J. (2011) Deconstructing the skin: cytoarchitectural determinants of epidermal morphogenesis. Nat. Rev., 12, 565-580.
23. Arnemann, J., Sullivan, K.H., Magee, A.I., King, I.A. and Buxton, R.S. (1993) Stratification-related expression of isoforms of the desmosomal cadherins in human epidermis. J. Cell Sci., 104(Pt 3), 741-750.
24. Chidgey, M.A., Yue, K.K., Gould, S., Byrne, C. and Garrod, D.R. (1997) Changing pattern of desmocollin 3 expression accompanies epidermal organisation during skin development. Dev. Dyn., 210, 315-327.
25. Desai, B.V., Harmon, R.M. and Green, K.J. (2009) Desmosomes at a glance. J. Cell Sci., 122, 4401-4407.
26. King, I.A., Tabiowo, A., Purkis, P., Leigh, I. and Magee, A.I. (1993) Expression of distinct desmocollin isoforms in human epidermis. J. Invest. Dermatol., 100, 373-379.
27. Shimizu, H., Masunaga, T., Ishiko, A., Kikuchi, A., Hashimoto, T. and Nishikawa, T. (1995) Pemphigus vulgaris and pemphigus foliaceus sera show an inversely graded binding pattern to extracellular regions of desmosomes in different layers of human epidermis. J. Invest. Dermatol., 105, 153-159.
28. Amagai, M. and Stanley, J.R. (2012) Desmoglein as a target in skin disease and beyond. J. Invest. Dermatol., 132, 776-784.
29. Petrof, G., Mellerio, J.E. and McGrath, J.A. (2012) Desmosomal genodermatoses. Br. J. Dermatol., 166, 36-45.
30. McGrath, J.A., McMillan, J.R., Shemanko, C.S., Runswick, S.K., Leigh, I.M., Lane, E.B., Garrod, D.R. and Eady, R.A. (1997) Mutations in the plakophilin 1 gene result in ectodermal dysplasia/skin fragility syndrome. Nat. Genet., 17, 240-244.
31. Pigors, M., Kiritsi, D., Krumpelmann, S., Wagner, N., He, Y., Podda, M., Kohlhase, J., Hausser, I., Bruckner-Tuderman, L. and Has, C. (2011) Lack of plakoglobin leads to lethal congenital epidermolysis bullosa: a novel clinico-genetic entity. Hum. Mol. Genet., 20, 1811-1819.
32. Whittock, N.V., Smith, F.J., Wan, H., Mallipeddi, R., Griffiths, W.A., Dopping-Hepenstal, P., Ashton, G.H., Eady, R.A., McLean, W.H. and McGrath, J.A. (2002) Frameshift mutation in the V2 domain of human keratin 1 results in striate palmoplantar keratoderma. J. Invest. Dermatol., 118, 838-844.
33. Jonkman, M.F., Pasmooij, A.M., Pasmans, S.G., van den Berg, M.P., Ter Horst, H.J., Timmer, A. and Pas, H.H. (2005) Loss of desmoplakin tail causes lethal acantholytic epidermolysis bullosa. Am. J. Hum. Genet., 77, 653-660.
34. Norgett, E.E., Hatsell, S.J., Carvajal-Huerta, L., Cabezas, J.C., Common, J., Purkis, P.E., Whittock, N., Leigh, I.M., Stevens, H.P. and Kelsell, D.P. (2000) Recessive mutation in desmoplakin disrupts desmoplakinintermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum. Mol. Genet., 9, 2761-2766.
35. Rickman, L., Simrak, D., Stevens, H.P., Hunt, D.M., King, I.A., Bryant, S.P., Eady, R.A., Leigh, I.M., Arnemann, J., Magee, A.I. et al. (1999) N-terminal deletion in a desmosomal cadherin causes the autosomal dominant skin disease striate palmoplantar keratoderma. Hum. Mol. Genet., 8, 971-976.
36. Chen, J., Den, Z. and Koch, P.J. (2008) Loss of desmocollin 3 in mice leads to epidermal blistering. J. Cell Sci., 121, 2844-2849.
37. Koch, P.J., Mahoney, M.G., Ishikawa, H., Pulkkinen, L., Uitto, J., Shultz, L., Murphy, G.F., Whitaker-Menezes, D. and Stanley, J.R. (1997) Targeted disruption of the pemphigus vulgaris antigen (desmoglein 3) gene in mice causes loss of keratinocyte cell adhesion with a phenotype similar to pemphigus vulgaris. J. Cell Biol., 137, 1091-1102.
38. Vasioukhin, V., Bowers, E., Bauer, C., Degenstein, L. and Fuchs, E. (2001) Desmoplakin is essential in epidermal sheet formation. Nat. Cell Biol., 3, 1076-1085.
39. Allen, E., Yu, Q.C. and Fuchs, E. (1996) Mice expressing a mutant desmosomal cadherin exhibit abnormalities in desmosomes, proliferation, and epidermal differentiation. J. Cell Biol., 133, 1367-1382.
40. Chidgey, M., Brakebusch, C., Gustafsson, E., Cruchley, A., Hail, C., Kirk, S., Merritt, A., North, A., Tselepis, C., Hewitt, J. et al. (2001) Mice lacking desmocollin 1 show epidermal fragility accompanied by barrier defects and abnormal differentiation. J. Cell Biol., 155, 821-832.
41. Gaudry, C.A., Palka, H.L., Dusek, R.L., Huen, A.C., Khandekar, M.J., Hudson, L.G. and Green, K.J. (2001) Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. J. Biol. Chem., 276, 24871-24880.
42. Klessner, J.L., Desai, B.V., Amargo, E.V., Getsios, S. and Green, K.J. (2009) EGFR and ADAMs cooperate to regulate shedding and endocytic trafficking of the desmosomal cadherin desmoglein 2. Mol. Biol. Cell, 20, 328-337.
43. Lorch, J.H., Klessner, J., Park, J.K., Getsios, S., Wu, Y.L., Stack, M.S. and Green, K.J. (2004) Epidermal growth factor receptor inhibition promotes desmosome assembly and strengthens intercellular adhesion in squamous cell carcinoma cells. J. Biol. Chem., 279, 37191-37200.
44. Yin, T., Getsios, S., Caldelari, R., Godsel, L.M., Kowalczyk, A.P., Muller, E.J. and Green, K.J. (2005) Mechanisms of plakoglobin-dependent adhesion: desmosome-specific functions in assembly and regulation by epidermal growth factor receptor. J. Biol. Chem., 280, 40355-40363.
45. Ferone, G., Thomason, H.A., Antonini, D., De Rosa, L., Hu, B., Gemei, M., Zhou, H., Ambrosio, R., Rice, D.P., Acampora, D. et al. (2012) Mutant p63 causes defective expansion of ectodermal progenitor cells and impaired FGF signalling in AEC syndrome. EMBO Mol. Med., 4, 192-205.
46. Clements, S.E., Techanukul, T., Lai-Cheong, J.E., Mee, J.B., South, A.P., Pourreyron, C., Burrows, N.P., Mellerio, J.E. and McGrath, J.A. (2012) Mutations in AEC syndrome skin reveal a role for p63 in basement membrane adhesion, skin barrier integrity and hair follicle biology. Br. J. Dermatol., 167, 134-144.
47. Ihrie, R.A., Marques, M.R., Nguyen, B.T., Horner, J.S., Papazoglu, C., Bronson, R.T., Mills, A.A. and Attardi, L.D. (2005) Perp is a p63-regulated gene essential for epithelial integrity. Cell, 120, 843-856.
48. Shimomura, Y., Wajid, M., Shapiro, L. and Christiano, A.M. (2008) P-cadherin is a p63 target gene with a crucial role in the developing human limb bud and hair follicle. Development, 135, 743-753.
49. Koster, M.I., Marinari, B., Payne, A.S., Kantaputra, P.N., Costanzo, A. and Roop, D.R. (2009) DeltaNp63 knockdown mice: a mouse model for AEC syndrome. Am. J. Med. Genet. A, 149A, 1942-1947.
50. Lopardo, T., Lo Iacono, N.,Marinari, B., Giustizieri,M.L., Cyr, D.G.,Merlo, G., Crosti, F., Costanzo, A. and Guerrini, L. (2008) Claudin-1 is a p63 target gene with a crucial role in epithelial development. PLoS ONE, 3, e2715.
51. Marinari, B., Ballaro, C., Koster, M.I., Giustizieri, M.L., Moretti, F., Crosti, F., Papoutsaki, M., Karin, M., Alema, S., Chimenti, S. et al. (2009) IKKalpha is a p63 transcriptional target involved in the pathogenesis of ectodermal dysplasias. J. Invest. Dermatol., 129, 60-69.
52. Ingraham, C.R., Kinoshita, A., Kondo, S., Yang, B., Sajan, S., Trout, K.J., Malik, M.I., Dunnwald, M., Goudy, S.L., Lovett, M. et al. (2006) Abnormal skin, limb and craniofacial morphogenesis in mice deficient for interferon regulatory factor 6 (Irf6). Nat. Genet., 38, 1335-1340.
53. Richardson, R.J., Dixon, J., Malhotra, S., Hardman, M.J., Knowles, L., Boot-Handford, R.P., Shore, P., Whitmarsh, A. and Dixon, M.J. (2006) Irf6 is a key determinant of the keratinocyte proliferation-differentiation switch. Nat. Genet, 38, 1329-1334.
54. Moretti, F., Marinari, B., Lo Iacono, N., Botti, E., Giunta, A., Spallone, G., Garaffo, G., Vernersson-Lindahl, E., Merlo, G., Mills, A.A. et al. (2010) A regulatory feedback loop involving p63 and IRF6 links the pathogenesis of 2 genetically different human ectodermal dysplasias. J. Clin. Invest., 120, 1570-1577.
55. Thomason, H.A., Zhou, H., Kouwenhoven, E.N., Dotto, G.P., Restivo, G., Nguyen, B.C., Little, H., Dixon, M.J., van Bokhoven, H. and Dixon, J. (2010) Cooperation between the transcription factors p63 and IRF6 is essential to prevent cleft palate in mice. J. Clin. Invest., 120, 1561-1569.
56. Restivo, G., Nguyen, B.C., Dziunycz, P., Ristorcelli, E., Ryan, R.J., Ozuysal, O.Y., Di Piazza, M., Radtke, F., Dixon, M.J., Hofbauer, G.F. et al. (2011) IRF6 is a mediator of Notch pro-differentiation and tumour suppressive function in keratinocytes. EMBO J., 30, 4571-4585.
57. Kouwenhoven, E.N., van Heeringen, S.J., Tena, J.J., Oti, M., Dutilh, B.E., Alonso, M.E., de la Calle-Mustienes, E., Smeenk, L., Rinne, T., Parsaulian, L. et al. (2010) Genome-wide profiling of p63 DNA-binding sites identifies an element that regulates gene expression during limb development in the 7q21 SHFM1 locus. PLoS Genet., 6, e1001065.
58. Sabo, P.J., Kuehn, M.S., Thurman, R., Johnson, B.E., Johnson, E.M., Cao, H., Yu, M., Rosenzweig, E., Goldy, J., Haydock, A. et al. (2006) Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays. Nat. Methods, 3, 511-518.
59. Bernstein, B.E., Kamal, M., Lindblad-Toh, K., Bekiranov, S., Bailey, D.K., Huebert, D.J., McMahon, S., Karlsson, E.K., Kulbokas, E.J. III, Gingeras, T.R. et al. (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell, 120, 169-181.
60. Getsios, S., Simpson, C.L., Kojima, S., Harmon, R., Sheu, L.J., Dusek, R.L., Cornwell, M. and Green, K.J. (2009) Desmoglein 1-dependent suppression of EGFR signaling promotes epidermal differentiation and morphogenesis. J. Cell Biol., 185, 1243-1258.
61. Barbieri, C.E., Barton, C.E. and Pietenpol, J.A. (2003) Delta Np63 alpha expression is regulated by the phosphoinositide 3-kinase pathway. J. Biol. Chem., 278, 51408-51414.
62. Payne, A.S., Yan, A.C., Ilyas, E., Li, W., Seykora, J.T., Young, T.L., Pawel, B.R., Honig, P.J., Camacho, J., Imaizumi, S. et al. (2005) Two novel TP63 mutations associated with the ankyloblepharon, ectodermal defects, and cleft lip and palate syndrome: a skin fragility phenotype. Arch. Dermatol., 141, 1567-1573.
63. Ioannides, D., Hytiroglou, P., Phelps, R.G. and Bystryn, J.C. (1991) Regional variation in the expression of pemphigus foliaceus, pemphigus erythematosus, and pemphigus vulgaris antigens in human skin. J. Invest. Dermatol., 96, 159-161.
64. McKoy, G., Protonotarios, N., Crosby, A., Tsatsopoulou, A., Anastasakis, A., Coonar, A., Norman, M., Baboonian, C., Jeffery, S. and McKenna, W.J. (2000) Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet, 355, 2119-2124.
65. Kurata, S., Okuyama, T., Osada, M., Watanabe, T., Tomimori, Y., Sato, S., Iwai, A., Tsuji, T., Ikawa, Y. and Katoh, I. (2004) p51/p63 Controls subunit alpha3 of the major epidermis integrin anchoring the stem cells to the niche. J. Biol. Chem., 279, 50069-50077.
66. Osada, M., Nagakawa, Y., Park, H.L., Yamashita, K., Wu, G., Kim, M.S., Fomenkov, A., Trink, B. and Sidransky, D. (2005) p63-specific activation of the BPAG-1e promoter. J. Invest. Dermatol., 125, 52-60.
67. Ihrie, R.A., Bronson, R.T. and Attardi, L.D. (2006) Adult mice lacking the p53/p63 target gene Perp are not predisposed to spontaneous tumorigenesis but display features of ectodermal dysplasia syndromes. Cell Death Differ., 13, 1614-1618.
68. Beaudry, V.G., Pathak, N., Koster, M.I. and Attardi, L.D. (2009) Differential PERP regulation by TP63 mutants provides insight into AEC pathogenesis. Am. J. Med. Genet. A, 149A, 1952-1957.
69. Smith, C., Zhu, K., Merritt, A., Picton, R., Youngs, D., Garrod, D. and Chidgey, M. (2004) Regulation of desmocollin gene expression in the epidermis: CCAAT/enhancer-binding proteins modulate early and late events in keratinocyte differentiation. Biochem. J., 380, 757-765.
70. Wilanowski, T., Caddy, J., Ting, S.B., Hislop, N.R., Cerruti, L., Auden, A., Zhao, L.L., Asquith, S., Ellis, S., Sinclair, R. et al. (2008) Perturbed desmosomal cadherin expression in grainy head-like 1-null mice. EMBO J., 27, 886-897.
71. Botti, E., Spallone, G., Moretti, F., Marinari, B., Pinetti, V., Galanti, S., De Meo, P.D., De Nicola, F., Ganci, F., Castrignano, T. et al. (2011) Developmental factor IRF6 exhibits tumor suppressor activity in squamous cell carcinomas. Proc. Natl Acad. Sci. U S A, 108, 13710-13715.
72. Kolev, V., Mandinova, A., Guinea-Viniegra, J., Hu, B., Lefort, K., Lambertini, C., Neel, V., Dummer, R., Wagner, E.F. and Dotto, G.P. (2008) EGFR signalling as a negative regulator of Notch1 gene transcription and function in proliferating keratinocytes and cancer. Nat. Cell Biol., 10, 902-911.
73. De Rosa, L., Antonini, D., Ferone, G., Russo, M.T., Yu, P.B., Han, R. and Missero, C. (2009) p63 Suppresses non-epidermal lineage markers in a bone morphogenetic protein-dependent manner via repression of Smad7. J. Biol. Chem., 284, 30574-30582.
74. Rinne, T., Clements, S.E., Lamme, E., Duijf, P.H., Bolat, E., Meijer, R., Scheffer, H., Rosser, E., Tan, T.Y., McGrath, J.A. et al. (2008) A novel translation re-initiation mechanism for the p63 gene revealed by amino-terminal truncating mutations in Rapp-Hodgkin/Hay-Wells-like syndromes. Hum. Mol. Genet., 17, 1968-1977.
75. Antonini, D., Dentice, M., Mahtani, P., De Rosa, L., Della Gatta, G., Mandinova, A., Salvatore, D., Stupka, E. and Missero, C. (2008) Tprg, a gene predominantly expressed in skin, is a direct target of the transcription factor p63. J. Invest. Dermatol., 128, 1676-1685.
76. Calautti, E., Cabodi, S., Stein, P.L., Hatzfeld, M., Kedersha, N. and Paolo Dotto, G. (1998) Tyrosine phosphorylation and src family kinases control keratinocyte cell-cell adhesion. J. Cell Biol., 141, 1449-1465.
77. Huen, A.C., Park, J.K., Godsel, L.M., Chen, X., Bannon, L.J., Amargo, E.V., Hudson, T.Y., Mongiu, A.K., Leigh, I.M., Kelsell, D.P. et al. (2002) Intermediate filament-membrane attachments function synergistically with actin-dependent contacts to regulate intercellular adhesive strength. J. Cell Biol., 159, 1005-1017.