Integrating Animal Models and In Vitro Tissue Models to Elucidate the Role of Desmosomal Proteins in Diseases

References

• Amagai M, Stanley JR (2012). Desmoglein as a target in skin disease and beyond. J Invest Dermatol. 132: 776–784.
   PubMed Web of Science ®Google Scholar
• Beaudry VG, Pathak N, Koster MI, Attardi LD (2009). Differential PERP regulation by TP63 mutants provides insight into AEC pathogenesis. Am J Med Genet A. 149A: 1952–1957.
   PubMed Web of Science ®Google Scholar
• Bellomaria A, Barbato G, Melino G, Paci M, Melino S (2010). Recognition of p63 by the E3 ligase ITCH: Effect of an ectodermal dysplasia mutant. Cell Cycle. 9: 3754–3763.
   Web of Science ®Google Scholar
• Bertola DR, Kim CA, Albano LM, Scheffer H, Meijer R, van Bokhoven H (2004). Molecular evidence that AEC syndrome and Rapp-Hodgkin syndrome are variable expression of a single genetic disorder. Clin Genet. 66: 79–80.
   PubMed Web of Science ®Google Scholar
• Bierkamp C, McLaughlin KJ, Schwarz H, Huber O, Kemler R (1996). Embryonic heart and skin defects in mice lacking plakoglobin. Dev Biol. 180: 780–785.
   PubMed Web of Science ®Google Scholar
• Browne G, Cipollone R, Lena AM, Serra V, Zhou H, van Bokhoven H, Dötsch V, Merico D, Mantovani R, Terrinoni A, Knight RA, Candi E, Melino G (2011). Differential altered stability and transcriptional activity of DeltaNp63 mutants in distinct ectodermal dysplasias. J Cell Sci. 124: 2200–2207.
   PubMed Web of Science ®Google Scholar
• Brunner HG, Hamel BCJ, van Bokhoven H (2002). The p63 gene in EEC and other syndromes. J Med Genet. 39: 377–381.
   PubMed Web of Science ®Google Scholar
• Buxton RS, Cowin P, Franke WW, Garrod DR, Green KJ, King IA, Koch PJ, Magee AI, Rees DA, Stanley JR (1993). Nomenclature of the desmosomal cadherins. J Cell Biol. 121: 481–483.
   PubMed Web of Science ®Google Scholar
• Chapman S, Liu X, Meyers C, Schlegel R, McBride AA (2010). Human keratinocytes are efficiently immortalized by a Rho kinase inhibitor. J Clin Invest. 120: 2619–2626.
   PubMed Web of Science ®Google Scholar
• Chen J, Den Z, Koch PJ (2008). Loss of desmocollin 3 in mice leads to epidermal blistering. J Cell Sci. 121: 2844–2849.
   PubMed Web of Science ®Google Scholar
• Chen J, O’Shea C, Fitzpatrick JE, Koster MI, Koch PJ. (2011). Loss of desmocollin 3 in skin tumor development and progression. Mol Carcinog. 51: 535–545.
   PubMed Web of Science ®Google Scholar
• Cheng X, Den Z, Koch PJ (2005). Desmosomal cell adhesion in mammalian development. Eur J Cell Biol. 84: 215–223.
   PubMed Web of Science ®Google Scholar
• Cheng X, Koch PJ. (2004). In vivo function of desmosomes. J Dermatol. 31: 171–187.
   PubMed Web of Science ®Google Scholar
• Chitaev NA, Leube RE, Troyanovsky RB, Eshkind LG, Franke WW, Troyanovsky SM (1996). The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J Cell Biol. 133: 359–369.
   PubMed Web of Science ®Google Scholar
• Chung J, Grant RI, Kaplan DR, Irwin MS (2011). Special AT-rich Binding Protein-2 (SATB2) Differentially Affects Disease-causing p63 Mutant Proteins. J Biol Chem. 286: 40671–40680.
   PubMed Web of Science ®Google Scholar
• Clements SE, Techanukul T, Holden ST, Mellerio JE, Dorkins H, Escande F, McGrath JA (2010). Rapp-Hodgkin and Hay-Wells ectodermal dysplasia syndromes represent a variable spectrum of the same genetic disorder. Br J Dermatol. 163: 624–629.
   PubMed Web of Science ®Google Scholar
• Clements SE, Techanukul T, Lai-Cheong JE, Mee JB, South AP, Pourreyron C, Burrows NP, Mellerio JE, McGrath JA (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.
   PubMed Web of Science ®Google Scholar
• Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F (2013). Multiplex genome engineering using CRISPR/Cas systems. Science. 339: 819–823.
   PubMed Web of Science ®Google Scholar
• Den Z, Cheng X, Merched-Sauvage M, Koch PJ (2006). Desmocollin 3 is required for pre-implantation development of the mouse embryo. J Cell Sci. 119: 482–489.
   PubMed Web of Science ®Google Scholar
• Di Costanzo A, Festa L, Duverger O, Vivo M, Guerrini L, La Mantia G, Morasso MI, Calabrò V (2009). Homeodomain protein Dlx3 induces phosphorylation-dependent p63 degradation. Cell Cycle. 8: 1185–1195.
   PubMed Web of Science ®Google Scholar
• Dianzani I, Garelli E, Gustavsson P, Carando A, Gustafsson B, Dahl N, Annerén G (2003). Rapp-Hodgkin and AEC syndromes due to a new frameshift mutation in the TP63 gene. J Med Genet. 40: e133.
   PubMedGoogle Scholar
• Ferone G, Mollo MR, Thomason HA, Antonini D, Zhou H, Ambrosio R, De Rosa L, Salvatore D, Getsios S, van Bokhoven H, Dixon J, Missero C (2013). p63 control of desmosome gene expression and adhesion is compromised in AEC syndrome. Hum Mol Genet. 22: 531–543.
   PubMed Web of Science ®Google Scholar
• Ferone G, Thomason HA, Antonini D, De Rosa L, Hu B, Gemei M, Zhou H, Ambrosio R, Rice DP, Acampora D, van Bokhoven H, Del Vecchio L, Koster MI, Tadini G, Spencer-Dene B, Dixon M, Dixon J, Missero C (2012). Mutant p63 causes defective expansion of ectodermal progenitor cells and impaired FGF signalling in AEC syndrome. EMBO Mol Med. 4: 192–205.
   PubMed Web of Science ®Google Scholar
• Fete M, van Bokhoven H, Clements SE, McKeon F, Roop DR, Koster MI, Missero C, Attardi LD, Lombillo VA, Ratovitski E, Julapalli M, Ruths D, Sybert VP, Siegfried EC, Bree AF (2009). International Research Symposium on Ankyloblepharon-Ectodermal Defects-Cleft Lip/Palate (AEC) syndrome. Am J Med Genet A. 149A: 1885–1893.
   PubMed Web of Science ®Google Scholar
• Gallicano GI, Bauer C, Fuchs E (2001). Rescuing desmoplakin function in extra-embryonic ectoderm reveals the importance of this protein in embryonic heart, neuroepithelium, skin and vasculature. Development. 128: 929–941.
   PubMed Web of Science ®Google Scholar
• Gallicano GI, Kouklis P, Bauer C, Yin M, Vasioukhin V, Degenstein L, Fuchs E (1998). Desmoplakin is required early in development for assembly of desmosomes and cytoskeletal linkage. J Cell Biol. 143: 2009–2022.
   PubMedGoogle Scholar
• Ganeshan R, Chen J, Koch PJ (2010). Mouse models for blistering skin disorders. Dermatol Res Pract. 2010: 584353.
   PubMedGoogle Scholar
• Green H, Rheinwald JG, Sun TT (1977). Properties of an epithelial cell type in culture: the epidermal keratinocyte and its dependence on products of the fibroblast. Prog Clin Biol Res. 17: 493–500.
   PubMedGoogle Scholar
• Hatano Y, Hashimoto T, Fukuda S, Ishikawa K, Goto M, Kai Y, Takeo N, Okamoto O, Fujiwara S (2012). Atypical pemphigus with exclusively anti-desmocollin 3-specific IgG antibodies. Eur J Dermatol. 22: 560–562.
   PubMed Web of Science ®Google Scholar
• Hockemeyer D, Soldner F, Beard C, Gao Q, Mitalipova M, DeKelver RC, Katibah GE, Amora R, Boydston EA, Zeitler B, Meng X, Miller JC, Zhang L, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2009). Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases. Nat Biotechnol. 27: 851–857.
   PubMed Web of Science ®Google Scholar
• Hockemeyer D, Wang H, Kiani S, Lai CS, Gao Q, Cassady JP, Cost GJ, Zhang L, Santiago Y, Miller JC, Zeitler B, Cherone JM, Meng X, Hinkley SJ, Rebar EJ, Gregory PD, Urnov FD, Jaenisch R (2011). Genetic engineering of human pluripotent cells using TALE nucleases. Nat Biotechnol. 29: 731–734.
   PubMed Web of Science ®Google Scholar
• Ihrie RA, Marques MR, Nguyen BT, Horner JS, Papazoglu C, Bronson RT, Mills AA, Attardi LD. (2005). Perp is a p63-regulated gene essential for epithelial integrity. Cell. 120: 843–856.
   PubMed Web of Science ®Google Scholar
• Itoh M, Kiuru M, Cairo MS, Christiano AM (2011). Generation of keratinocytes from normal and recessive dystrophic epidermolysis bullosa-induced pluripotent stem cells. Proc Natl Acad Sci U S A. 108: 8797–8802.
   PubMed Web of Science ®Google Scholar
• Julapalli MR, Scher RK, Sybert VP, Siegfried EC, Bree AF (2009). Dermatologic findings of ankyloblepharon-ectodermal defects-cleft lip/palate (AEC) syndrome. Am J Med Genet A. 149A: 1900–1906.
   PubMed Web of Science ®Google Scholar
• Koch PJ, Goldschmidt MD, Walsh MJ, Zimbelmann R, Franke WW (1991a). Complete amino acid sequence of the epidermal desmoglein precursor polypeptide and identification of a second type of desmoglein gene. Eur J Cell Biol. 55: 200–208.
   PubMed Web of Science ®Google Scholar
• Koch PJ, Goldschmidt MD, Walsh MJ, Zimbelmann R, Schmelz M, Franke WW (1991b). Amino acid sequence of bovine muzzle epithelial desmocollin derived from cloned cDNA: a novel subtype of desmosomal cadherins. Differentiation. 47: 29–36.
   PubMed Web of Science ®Google Scholar
• Koch PJ, Goldschmidt MD, Zimbelmann R, Troyanovsky R, Franke WW (1992). Complexity and expression patterns of the desmosomal cadherins. Proc Natl Acad Sci U S A. 89: 353–357.
   PubMed Web of Science ®Google Scholar
• Koch PJ, Mahoney MG, Ishikawa H, Pulkkinen L, Uitto J, Shultz L, Murphy GF, Whitaker-Menezes D, Stanley JR (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.
   PubMed Web of Science ®Google Scholar
• Koch PJ, Walsh MJ, Schmelz M, Goldschmidt MD, Zimbelmann R, Franke WW (1990). Identification of desmoglein, a constitutive desmosomal glycoprotein, as a member of the cadherin family of cell adhesion molecules. Eur J Cell Biol. 53: 1–12.
   PubMed Web of Science ®Google Scholar
• Koster MI (2010). p63 in skin development and ectodermal dysplasias. J Invest Dermatol130: 2352–2358.
   PubMed Web of Science ®Google Scholar
• Koster MI, Dai D, Marinari B, Sano Y, Costanzo A, Karin M, Roop DR (2007). p63 induces key target genes required for epidermal morphogenesis. Proc Natl Acad Sci U S A. 104: 3255–3260.
   PubMed Web of Science ®Google Scholar
• Koster MI, Marinari B, Payne AS, Kantaputra PN, Costanzo A, Roop DR (2009). DeltaNp63 knockdown mice: A mouse model for AEC syndrome. Am J Med Genet A. 149A: 1942–1947.
   PubMed Web of Science ®Google Scholar
• Li J, Swope D, Raess N, Cheng L, Muller EJ, Radice GL (2011). Cardiac tissue-restricted deletion of plakoglobin results in progressive cardiomyopathy and activation of {beta}-catenin signaling. Mol Cell Biol. 31: 1134–1144.
   PubMed Web of Science ®Google Scholar
• Li Mura IE, Bauce B, Nava A, Fanciulli M, Vazza G, Mazzotti E, Rigato I, De Bortoli M, Beffagna G, Lorenzon A, Calore M, Dazzo E, Nobile C, Mostacciuolo ML, Corrado D, Basso C, Daliento L, Thiene G, Rampazzo A (2013). Identification of a PKP2 gene deletion in a family with arrhythmogenic right ventricular cardiomyopathy. Eur J Hum Genet. 21: 1226–1231.
   PubMed Web of Science ®Google Scholar
• Lichti U, Anders J, Yuspa SH (2008). Isolation and short-term culture of primary keratinocytes, hair follicle populations and dermal cells from newborn mice and keratinocytes from adult mice for in vitro analysis and for grafting to immunodeficient mice. Nat Protoc. 3: 799–810.
   PubMed Web of Science ®Google Scholar
• Lopardo T, Lo Iacono N, Marinari B, Giustizieri ML, Cyr DG, Merlo G, Crosti F, Costanzo A, Guerrini L (2008). Claudin-1 is a p63 target gene with a crucial role in epithelial development. PLoS.ONE. 3: e2715.
   PubMedGoogle Scholar
• Mahoney MG, Hu Y, Brennan D, Bazzi H, Christiano AM, Wahl JK III (2006). Delineation of diversified desmoglein distribution in stratified squamous epithelia: implications in diseases. Exp Dermatol. 15: 101–109.
   PubMed Web of Science ®Google Scholar
• Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013). RNA-guided human genome engineering via Cas9. Science. 339: 823–826.
   PubMed Web of Science ®Google Scholar
• Marinari B, Ballaro C, Koster MI, Giustizieri ML, Moretti F, Crosti F, Papoutsaki M, Karin M, Alema S, Chimenti S, Roop DR, Costanzo A (2009). IKKalpha is a p63 transcriptional target involved in the pathogenesis of ectodermal dysplasias. J Invest Dermatol. 129: 60–69.
   PubMed Web of Science ®Google Scholar
• McGrath JA, Duijf PH, Doetsch V, Irvine AD, de Waal R, Vanmolkot KR, Wessagowit V, Kelly A, Atherton DJ, Griffiths WA, Orlow SJ, van Haeringen A, Ausems MG, Yang A, McKeon F, Bamshad MA, Brunner HG, Hamel BC, van Bokhoven H (2001). Hay-Wells syndrome is caused by heterozygous missense mutations in the SAM domain of p63. Hum Mol Genet. 10: 221–229.
   PubMed Web of Science ®Google Scholar
• Nie Z, Merritt A, Rouhi-Parkouhi M, Tabernero L, Garrod D (2011). Membrane-impermeable cross-linking provides evidence for homophilic, isoform-specific binding of desmosomal cadherins in epithelial cells. J Biol Chem. 286: 2143–2154.
   PubMed Web of Science ®Google Scholar
• Okita K, Ichisaka T, Yamanaka S (2007). Generation of germline-competent induced pluripotent stem cells. Nature. 448: 313–317.
   PubMed Web of Science ®Google Scholar
• Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, Cowan C, Hochedlinger K, Daley GQ (2008a). Disease-specific induced pluripotent stem cells. Cell. 134: 877–886.
   PubMed Web of Science ®Google Scholar
• Park IH, Lerou PH, Zhao R, Huo H, Daley GQ (2008b). Generation of human-induced pluripotent stem cells. Nat.Protoc. 3: 1180–1186.
   PubMed Web of Science ®Google Scholar
• Parsa R, Yang A, McKeon F, Green H (1999). Association of p63 with proliferative potential in normal and neoplastic human keratinocytes. J. Invest Dermatol. 113: 1099–1105.
   PubMed Web of Science ®Google Scholar
• Payne AS, Yan AC, Ilyas E, Li W, Seykora JT, Young TL, Pawel BR, Honig PJ, Camacho J, Imaizumi S, Heymann WR, Schnur RE (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.
   PubMed Web of Science ®Google Scholar
• Petrof G, Mellerio JE, McGrath JA (2012). Desmosomal genodermatoses. Br J Dermatol. 166: 36–45.
   PubMed Web of Science ®Google Scholar
• Rafei D, Muller R, Ishii N, Llamazares M, Hashimoto T, Hertl M, Eming R (2011). IgG autoantibodies against desmocollin 3 in pemphigus sera induce loss of keratinocyte adhesion. Am J Pathol. 178: 718–723.
   PubMed Web of Science ®Google Scholar
• Rinne T, Brunner HG, H. van Bokhoven H (2007). p63-associated disorders. Cell Cycle. 6: 262–268.
   PubMed Web of Science ®Google Scholar
• Ruiz P, Brinkmann V, Ledermann B, Behrend M, Grund C, Thalhammer C, Vogel F, Birchmeier C, Günthert U, Franke WW, Birchmeier W (1996). Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J Cell Biol. 135: 215–225.
   PubMed Web of Science ®Google Scholar
• Schmidt A, Koch PJ (2007). Desmosomes: just cell adhesion or is there more?Cell Adh Migr. 1: 28–32.
   PubMed Web of Science ®Google Scholar
• Sen GL, Boxer LD, Webster DE, Bussat RT, Qu K, Zarnegar BJ, Johnston D, Siprashvili Z, Khavari PA (2012). ZNF750 is a p63 target gene that induces KLF4 to drive terminal epidermal differentiation. Dev Cell. 22: 669–677.
   PubMed Web of Science ®Google Scholar
• Siegfried E, Bree A, Fete M, Sybert VP (2005). Skin erosions and wound healing in ankyloblepharon-ectodermal defect-cleft lip and/or palate. Arch. Dermatol. 141: 1591–1594.
   PubMed Web of Science ®Google Scholar
• Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007). Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 131: 861–872.
   PubMed Web of Science ®Google Scholar
• Testoni B, Mantovani R (2006). Mechanisms of transcriptional repression of cell-cycle G2/M promoters by p63. Nucleic Acids Res. 34: 928–938.
   PubMed Web of Science ®Google Scholar
• Theis DG, Koch PJ, Franke WW (1993). Differential synthesis of type 1 and type 2 desmocollin mRNAs in human stratified epithelia. Int J Dev Biol. 37: 101–110.
   PubMed Web of Science ®Google Scholar
• Tokonzaba E, Chen J, Cheng X, Den Z, Ganeshan R, Műller EJ, Koch PJ (2013). Plakoglobin as a Regulator of Desmocollin Gene Expression. J Invest Dermatol. 133: 2732–2740.
   PubMed Web of Science ®Google Scholar
• Tolar J, Xia L, Riddle MJ, Lees CJ, Eide CR, McElmurry RT, Titeux M, Osborn MJ, Lund TC, Hovnanian A, Wagner JE, Blazar BR (2011). Induced pluripotent stem cells from individuals with recessive dystrophic epidermolysis bullosa. J Invest Dermatol. 131: 848–856.
   PubMed Web of Science ®Google Scholar
• Truong AB, Kretz M, Ridky TW, Kimmel R, Khavari PA (2006). p63 regulates proliferation and differentiation of developmentally mature keratinocytes. Genes and Development. 20: 3185–3197.
   PubMed Web of Science ®Google Scholar
• Vanderhooft SL, Stephan MJ, Sybert VP (1993). Severe skin erosions and scalp infections in AEC syndrome. Pediatr.Dermatol. 10: 334–340.
   PubMed Web of Science ®Google Scholar
• Vasioukhin V, Bowers E, Bauer C, Degenstein L, Fuchs E (2001). Desmoplakin is essential in epidermal sheet formation. Nat Cell Biol. 3: 1076–1085.
   PubMed Web of Science ®Google Scholar
• Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dötsch V, Andrews NC, Caput D, 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.
   PubMed Web of Science ®Google Scholar
• Zarnegar BJ, Webster DE, Lopez-Pajares V, Vander Stoep Hunt B, Qu K, Yan KJ, Berk DR, Sen GL, Khavari PA (2012). Genomic profiling of a human organotypic model of AEC syndrome reveals ZNF750 as an essential downstream target of mutant TP63. Am J Hum Genet. 91: 435–443.
   PubMed Web of Science ®Google Scholar