Desmosomal cadherins

Current Opinion in Cell Biology

Volumn 14, Issue 5, 2002, Pages 537-545

  Garrod, David R ^a   Merritt, Anita J ^a   Nie, Zhuxiang ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN;

ANIMAL CELL; CELL ADHESION; CELL DIFFERENTIATION; CELL INTERACTION; DESMOSOME; HUMAN; HUMAN CELL; MORPHOGENESIS; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; CADHERINS; CELL ADHESION; DESMOSOMES; EPIDERMIS; GENOTYPE; HUMANS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PHENOTYPE; PROTEIN BINDING;

ANIMALIA;

EID: 0036774453     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(02)00366-6     Document Type: Review

References (95)

1. North A.J., Bardsley W.G., Hyam J., Bornslaeger E.A., Cordingley H.C., Trinnaman B., Hatzfeld M., Green K.J., Magee A.I., Garrod D.R. Molecular map of the desmosomal plaque. J Cell Sci. 112:1999;4325-4336.
2. Kowalczyk A.P., Bornslaeger E.A., Norvell S.M., Palka H., Green K.J. Desmosomes: intercellular adhesive junctions specialised for attachment of intermediate filaments. Int Rev Cytol. 185:1999;237-302.
3. Hatzfeld M. The armadillo family of structural proteins. Int Rev Cytol. 186:1999;179-224.
4. Garrod D.R., Tselepis C., Runswick S.K., North A.J., Wallis S.R., Chidgey M.A.J. Desmosome adhesion. Adv Mol Cell Biol. 28:2000;165-202.
5. Green K.J., Gaudry C.A. Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol. 1:2000;208-216.
6. Angst B.D., Marcozzi C., Magee A.I. The cadherin superfamily: diversity in form and function. J Cell Sci. 114:2001;629-641.
7. Garrod D.R., Chidgey M.A.J., North A.J., Runswick S.K., Tselepis C. Desmosomes. Barker J., McGrath J., Cell Adhesion and Migration in Skin Disease. 2001;57-85 Harwood Academic Publishers, London.
8. McMillan J.R., Shimizu H. Desmosomes: structure and function in normal and diseased epidermis. J Dermatol. 28:2001;291-298.
9. Garrod D.R., Merritt A.J., Nie Z. Desmosomal adhesion: its structural basis, molecular mechanism and regulation. Mol Membr Biol. 19:2002;81-94.
10. 2+ dependent heterophilic interaction between desmosomal cadherins, desmoglein and desmocollins, contributes to cell-cell adhesion. J Cell Biol. 138:1997;193-201.
11. Marcozzi C., Burdet I.D., Buxton R.S., Magee A.I. Co-expression of both types of desmosomal cadherins and plakoglobin confers strong intercellular adhesion. J Cell Sci. 111:1998;495-509.
12. Tselepis C., Chidgey M., North A., Garrod D.R. Desmosomal adhesion inhibits invasive behaviour. Proc Natl Acad Sci USA. 95:1998;8064-8069.
13. Runswick S.K., O'Hare M.J., Jones J.L., Streuli C.H., Garrod D.R. Desmosomal adhesion regulates epithelial morphogenesis and cell positioning. Nat Cell Biol. 3:2001;823-830. Antiadhesion peptides corresponding to the cell adhesion recognition sites of desmosomal cadherins completely but reversibly blocked the morphogenesis of mouse mammary cells and disrupted cell positioning in aggregates of human lumenal and myoepithelial cells. Desmosomal adhesion appeared to be as important as E-cadherin adhesion for morphogenesis.
14. Overduin M., Harvey T.S., Bagby S., Tong K.I., Yau P., Takeichi M., Ikura M. Solution structure of the epithelial cadherin domain responsible for selective cell adhesion. Science. 267:1995;386-389.
15. Shapiro L., Fannon A.M., Kwong P.D., Thompson A., Lehmann M.S., Grubel G., Legrand J.F., Nielsen J., Colman D.R., Henrickson W.A. Structural basis of cell-cell adhesion by cadherins. Nature. 374:1995;327-374.
16. 2+ dependence and mutational analysis reveal molecular details of E-cadherin homo-association. EMBO J. 18:1999;1738-1747.
17. Sivisankar S., Gumbiner B., Leckband D. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys J. 80:2001;1758-1768.
18. 2+ dependent.
19. Keiffer-Combeau S., Meyer J.-M., Lesot H. Cell-matrix interactions and cell-cell junctions during epithelial histo-morphogenesis in the developing mouse incisor. Int J Dev Biol. 45:2001;733-742.
20. Vasioukhin V., Bauer C., Yin M., Fuchs E. Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell. 100:2000;209-219. During the early stage of calcium induced cell adhesion in keratinocytes, filopodia of adjacent cells interdigitate, driven by actin polymerisation, and form a double-row of adherens junctions, the adhesion zipper. Adhesion is then stabilised by formation of desmosomes between the lateral surfaces of the filopodia.
21. Vasioukhin V., Bowers E., Bauer C., Degenstein L., Fuchs E. Desmoplakin is essential in epidermal sheet formation. Nat Cell Biol. 3:2001;1076-1084. In desmoplakin (DP) mice with conditional knockout of DP in the epidermis, epidermal-cell sheet formation is compromised. The desmosomes are non-adhesive because they lack a fully formed plaque and attachment to the keratin cytoskeleton. Other desmosomal components including plakoglobin, plakophilin 1, Dsc1, Dsg1 and Dsg3 still localise to cell-cell borders. Adherens junctions are also absent indicating a mutual dependence of these junctions.
22. Hatsell M., Cowin P. Deconstructing desmoplakin. Nat Cell Biol. 3:2001;E270-E272.
23. Lenox J.M., Koch P.J., Mahoney M.G., Leiberman M., Stanley J.R., Radice G.L. Postnatal lethality of P-cadherin/desmoglein 3 double knockout mice: demonstration of a cooperative effect of these cell adhesion molecules in tissue homeostasis of stratified squamous epithelia. J Invest Dermatol. 114:2000;948-949.
24. Sato M., Aoyama Y., Kitajima Y. Assembly pathway of desmoglein 3 to desmosomes and its perturbation by pemphigus vulgaris-IgG in cultured keratinocytes, as revealed by time-lapsed labeling immunoelectron microscopy. Lab Invest. 80:2000;1583-1592. During desmosome assembly Dsg3 was first distributed on the cell surface in two small cluster types, simple clusters without keratin intermediate filament (KIF) attachment and half-desmosome-like clusters with KIF attachment on the intracellular surface of the plasma membrane. This suggests that Dsg3 first forms simple clusters at the cell surface, followed by keratin filament attachment and integration of the clusters into desmosomes.
25. Ishii K., Norvell S.M., Bannon L.J., Amargo E.V., Pascoe L.T., Green K.J. Assembly of desmosomal cadherins into desmosomes is isoform dependent. J Invest Dermatol. 117:2001;26-35.
26. Henkler F., Strom M., Mathers K., Cordingley H., Sullivan K., King I. Transgenic misexpression of the differentiation-specific desmocollin isoform 1 in basal keratinocytes. J Invest Dermatol. 116:2001;144-149.
27. Windoffer R, Borchert-Stulträger A, Leuber RE: Desmosomes: interconnected calcium-dependent structures of remarkable stability with significant integral membrane protein turnover. J Cell Sci 2002, in press. Expression of GFP-Dsc2a in cultured cells was used to image desmosomes. Although desmosomes are stable, FRAP reveals that desmocollin within them turns over rapidly. Desmosomes also persist during cell division, and internalised desmosomal halves following low calcium treatment are not re-utilised for desmosome assembly.
28. Chen X., Bonné S., Hatzfeld M., van Roy F., Green K.J. Protein binding and functional characterization of plakophilin 2: evidence for its diverse roles in desmosomes and β-catenin signalling. J Biol Chem. 277:2002;10512-10522. This paper identified the binding partners of the most widely expressed plakophilin, PP2. It has more binding partners than PP1, including desmoplakin, plakoglobin, Dsg1 and 2, and Dsc1a and 2a. Evidence is also provided that PP2 may regulate β-catenin signalling.
29. Troyanovsky S., Troyanovsky R., Eshkind L., Krutovskikh V., Leube R., Franke W. Identification of the plakoglobin-binding domain in desmoglein and its role in plaque assembly and intermediate filament anchorage. J Cell Biol. 127:1994;151-160.
30. Bornslaeger EA, Godsel LM, Corcoran CM, Park JK, Hatzfeld M, Kowalczyk, Green KJ: Plakophilin 1 interferes with plakoglobin binding to desmoplakin, yet together with plakoglobin promotes clustering of desmosomal plaque complexes at cell-cell borders. J Cell Sci 2001, 114:727-738. Both plakophilin 1 (PP1) and plakoglobin bind to desmoplakin, but PP1 binds preferentially and excludes plakoglobin binding. DP and plakoglobin form a complex with the cytoplasmic domain of Dsg1, but full-length desmoplakin also binds to Dsg1 in the absence of plakoglobin. Both plakoglobin and PP1 are required in association with desmoplakin and Dsg1 for formation of structures resembling desmosomal plaques.
31. Bannon L.J., Cabrera B.L., Stack M.S., Green K.J. Isoform-specific differences in the size of desmosomal cadherin/catenin complexes. J Invest Dermatol. 117:2001;1302-1306.
32. Serpente N., Marcozzi C., Roberts G.A., Bao Q., Angst B.D., Hirst E.M.A., Burbett I.D.J., Buxton R.S., Magee A.I. Extracellularly truncated desmoglein 1 compromises desmosomes in MDCK cells. Mol Membr Biol. 17:2000;175-183.
33. Sakuntabhai A., Burge S., Monk S., Hovnanian A. Spectrum of novel ATP2A2 mutations in patients with Darier's disease. Hum Mol Genet. 8:1999;1611-1619.
34. 2+ pump, cause Darier's disease. Nat Genet. 21:1999;271-277.
35. Hu Z., Bonifas J.M., Beech J., Bench G., Shigihara T., Ogawa H., Ikeda S., Mauro T., Epstein E.H. Mutations in ATP2C1, encoding a calcium pump, cause Hailey-Hailey disease. Nat Genet. 24:2000;61-65.
36. Rajasekaran S.A., Palmer L.G., Moon S.Y., Soler A.P., Apodaca G.L., Harper J.F., Zheng Y., Rajaselkaran A.K. Na, K-ATPase activity is required for formation of tight junctions, desmosomes, and induction of polarity in epithelial cells. Mol Biol Cell. 12:2001;3717-3732.
37. Wallis S., Lloyd S., Wise I., Ireland G., Fleming T.P., Garrod D.R. The α-isoform of protein kinase α-C is involved in signalling the response of desmosomes to wounding in cultured epithelial cells. Mol Biol Cell. 11:2000;1077-1092. This is a demonstration that desmosomal adhesion develops from a calcium-dependent state to calcium independence in confluent epithelial cell sheets and that reversion to calcium dependence occurs on wounding. The change from calcium independence to calcium dependence is accompanied by activation of protein kinase C and localisation of PKCα to the cell periphery. Antisense depletion of PKCα promotes calcium independence of desmosomes.
38. Amar L.S., Shabana A.H., Oboeuf M., Martin N., Forest N. Involvement of desmoplakin phosphorylation in the regulation of desmosomes by protein kinase C, in HeLa cells. Cell Adhes Commun. 7:1999;125-138.
39. Aoyama Y., Owada M.K., Kitajima Y. A pathogenic autoantibody, pemphigus vulgaris-IgG, induces phosphorylation of desmoglein 3, and its dissociation from plakoglobin in cultured keratinocytes. Eur J Immunol. 29:1999;2233-2240.
40. Gaudry C.A., Palka H.L., Dusek R.L., Huen A.C., Khandekar M.J., Hudson L.G., Green K.J. Tyrosine-phosphorylated plakoglobin is associated with desmogleins but not desmoplakin after epidermal growth factor receptor activation. J Biol Chem. 276:2001;24871-24880. Epidermal growth receptor tyrosine-phosphorylates plakoglobin. The tyrosine-phosphorylated plakoglobin associates with Dsg2, but not with desmoplakin and is predominantly situated in a membrane-associated Trition-X-100 soluble pool, disassociated from desmoplakin and intermediate filaments. Thus tyrosine phosphorylation of plakoglobin may regulate desmosomal adhesion.
41. Weiske J., Schoneberg T., Schoder W., Hatzfeld M., Taubert R., Huber O. The fate of desmosomal proteins in apoptotic cells. J Biol Chem. 276:2001;41174-41181.
42. Trautmann A., Altznauer F., Akdis M., Simon H.U., Disch R., Brocker E.B., Blaser K., Akdis C.A. The differential fate of cadherins during T-cell-induced keratinocyte apoptosis leads to spongiosis in eczematous dermatitis. J Invest Dermatol. 117:2001;927-934.
43. Garrod D.R., Chidgey M.A.J., North A.J. Desmosomes: differentiation, development, dynamics and disease. Curr Opin Cell Biol. 8:1996;670-678.
44. Messent A.J., Blissett M.J., Smith G.L., North A.J., Magee A., Foreman D., Garrod D.R., Boulton M. Expression of a single pair of desmosomal glycoproteins renders the corneal epithelium unique amongst stratified epithelia. Invest Ophthalmol Vis Sci. 41:2000;8-15.
45. North A.J., Chidgey M.A.J., Clarke J.P., Bardesly W.G., Garrod D.R. Distinct desmocollin isoforms occur in the same desmosomes and show reciprocally graded distributions in bovine nasal epidermis. Proc Natl Acad Sci USA. 93:1996;7701-7705.
46. -/- mice show epidermal hyperproliferation, abnormal expression of keratins 6 and 16, and hair follicle degeneration, suggesting that Dsc1 may play some role in regulating epidermal differentiation.
47. Merritt AJ, Berika M, Zhai W, Kirk SE, Ji B, Hardman MJ, Garrod D: Suprabasal desmoglein 3 expression in the epidermis of transgenic mice results in hyperproliferation and abnormal differentiation. Mol Cell Biol 2002, in press.Misexpression of Dsg3 in the upper epidermis by the keratin 1 promoter causes abnormal epidermal differentiation and hyperproliferation.
48. Elias P.M., Matsuyoshi N., Wu H., Lin C., Wang Z.H., Brown B.E., Stanley J.R. Desmoglein isoform distribution affects stratum corneum structure and function. J Cell Biol. 153:2001;243-249. Ectopic expression of Dsg3 in the upper epidermis was driven by the involucrin promoter. This induced an abnormal stratum corneum with gross scaling and a lamellar histology resembling that of the oral mucosa, causing excessive, lethal transepidermal water loss.
49. Ishii K., Green K.J. Cadherin function: breaking the barrier. Curr Biol. 11:2001;R569-R572.
50. Glaser V. Desmosomes sort it out. J Cell Biol. 154:2002;1101.
51. Gallicano G.I., Bauer C., Fuchs E. Rescuing desmoplakin function in extra-embryonic ectoderm reveals the importance of this protein in embryonic heart, neuroepithelium, skin and vasculature. Development. 128:2001;929-941. Because homozygous desmoplakin mutant embryos did not survive beyond E6.5, the authors rescued the extra-embryonic tissues until mid gestation by aggregation of knockout embryos with tetraploid (WT) morulae. Investigation of the fused embryos demonstrated the importance of desmosomal adhesion in the heart muscle, neuroepithelium and skin (which contain desmosomes) and the microvasculature (which does not contain desmosomes, but possess unusual intercellular junctions composed of desmoplakin, plakoglobin and VE-cadherin).
52. Gallicano G.I., Kouklis P., Bauer C., Yin M., Vasioukhin V., Degenstein L., Fuchs E. Desmoplakin is required early in development for assembly of desmosomes and cytoskeletal linkage. J Cell Biol. 143:1998;2009-2022.
53. Anhalt G.J. Diaz LA: Research advances in pemphigus. J Am Med Assoc. 285:2001;652-654.
54. -/- mice. These recipient mice produced antibody against Dsg3 and developed skin lesions resembling pemphigus vulgaris.
55. Futei Y., Amagai M., Sekiguchi M., Nishifuji K., Fujii Y., Nishikawa T. Use of domain-swapped molecules for conformational epitope mapping of desmoglein 3 in pemphigus vulgaris. J Invest Dermatol. 115:2000;829-834.
56. Sekiguchi M., Futei Y., Fujii Y., Iwasaki T., Nishikawa T., Amagai M. Dominant epitopes recognized by pemphigus antibodies map to the N-terminal adhesive region of desmogleins. J Immunol. 167:2001;5439-5448.
57. Nguyen V.T., Ndove A., Shultz L.D., Pittelkow M.R., Grando S.A. Antibodies against keratinocyte antigens other than desmogleins 1 and 3 can induce pemphigus vulgaris-like lesions. J Clin Invest. 106:2000;1467-1479.
58. Stanley J.R., Nishkawa T., Diaz L.A., Amagai M. Pemphigus: is there another half of the story? J Invest Dermatol. 116:2001;489-490.
59. Stanley J.R., Nishkawa T., Diaz L.A., Amagai M. Reply to editor. J Invest Dermatol. 117:2001;994-995.
60. Grando S.A., Pittelkow M.R., Shultz L.D., Dmochowski M., Nguyen Vu T. Pemphigus: an unfolding story. J Invest Dermatol. 117:2001;990-994.
61. -/- cells restores the response. This is the first evidence that PG plays a central role in pemphigus vularis.
62. Andl C.D., Stanley J.R. Central role of the plakoglobin-binding domain for desmoglein 3 incorporation into desmosomes. J Invest Dermatol. 117:2001;1068-1074. Demonstration that the 87 amino acids long plakoglobin-binding domain in the cytoplasmic tail of Dsg3 is necessary to target this desmosomal cadherin to desmosomes.
63. Muzio L.L., Pannone G., Staibano S., Mignogna M.D., Rubini C., Ruocco E., Rosa G.D., Sciubba J.J. A possible role of catenin dyslocalisation in pemphigus vulgaris pathogenesis. J Cut Pathol. 28:2001;460-469.
64. Amagai M., Matsuyoshi N., Wang Z.H., Andl C., Stanley J.R. Toxin in bullous impetigo and staphylococcal scalded-skin syndrome targets desmoglein 1. Nat Med. 6:2000;1275-1277. This paper demonstrates that proteolytic activity of staphylococcal exfoliative toxin A specifically degrades desmoglein 1.
65. Amagai M, Yamaguchi T, Hanakawa Y, Nishifuji K, Motoyuki S, Stanley JR: Staphylococcal exfoliative toxin B specifically cleaves desmoglein 1. J Invest Dermatol 2002, in press.
66. Scheffers M.S., Bent P.V.D., Prins F., Spruit L., Breuning M.H., Litvinov S.V., Heer E.D., Peters D.J.M. Polycystin-1, the product of the Polycystic kidney disease 1 gene, co-localizes with desmosomes in MDCK cells. Human Mol Genet. 9:2000;2743-2750.
67. Xu G.M., Sikaneta T., Sullivan B.M., Zhang Q., Andreucci M., Stehle T., Drummond I., Arnaout M.A. Polycystin-1 interacts with intermediate filaments. J Biol Chem. 276:2001;46554-46562. This study showed the co-localisation of polycystin-1 with desmoplakin. Even after extraction with a Triton-X-100 containing buffer, a fraction of polycystin-1 remains anchored to the keratin cytoskeleton together with desmoplakin. Thus, this study raises the possibility of desmosomal defects in Polycystic kidney disease.
68. Arnemann J., Sullivan K.H., Magee A.I., King I.A., Buxton R.S. Stratification-related expression of isoforms of the desmosomal cadherins in human epidermis. J Cell Sci. 104:1993;741-750.
69. Schafer S., Koch P.J., Franke W.W. Identification of the ubiquitous human desmoglein, dsg2, and the expression catalogue of the desmoglein subfamily of desmosomal cadherins. Exp Cell Res. 211:1994;391-399.
70. Amagai M., Koch P.J., Nishikawa T., Stanley J.R. Pemphigus vulgaris antigen (desmoglein 3) is localized in the lower epidermis, the site of blister formation in patients. J Invest Dermatol. 106:1996;351-355.
71. Legan P.K., Yue K.K.M., Chidgey M.A.J., Holton J.L., Wilkinson R.W., Garrod D.R. The bovine desmocollin family: a new gene and expression patterns reflecting epithelial cell proliferation and differentiation. J Cell Biol. 126:1994;507-518.
72. King I.A., O'Brien T.J., Buxton R.S. Expression of the 'skin-type' desmosomal cadherin Dsc1 is closely linked to the keratinisation of epithelial tissues during mouse development. J Invest Dermatol. 107:1996;531-538.
73. Nuber U.A., Schafer S., Schmidt A., Koch P.J., Franke W.W. The widespread human desmocollin Dsc2 and tissue-specific patterns of synthesis of various desmocollin subtypes. Eur J Cell Biol. 66:1995;69-74.
74. King I.A., Sullivan K.H., Bennett R., Buxton R.S. The desmocollins of human foreskin epidermis: identification and chromosomal assignment of a third gene and expression patterns of the three isoforms. J Invest Dermatol. 105:1995;314-321.
75. Chitaev N.A., Leube R.E., Troyanovsky R.B., Eshkind L.G., Franke W.W., Troyanovsky S.M. The binding of plakoglobin to desmosomal cadherins: patterns of binding sites and topogenic potential. J Cell Biol. 133:1996;359-369.
76. Chitaev N.A., Averbakh A.Z., Troyanovsky R.B., Troyanovsky S.M. Molecular organization of the desmoglein-plakoglobin complex. J Cell Sci. 111:1998;1941-1949.
77. Troyanovsky S.M., Troyanovsky R.B., Eshkind L.G., Leube R.E., Franke W.W. Identification of amino acid sequence motifs in desmocollin, a desmosomal glycoprotein, that are required for plakoglobin binding and plaque formation. Proc Natl Acad Sci USA. 91:1994;10790-10794.
78. Troyanovsky R.B., Chitaev N.A., Troyanovsky S.M. Cadherin binding sites of plakoglobin: localization, specificity and role in targeting to adhering junctions. J Cell Sci. 109:1996;3069-3078.
79. Hazfeld M., Haffner C., Schulze K., Vinzens U. The function of plakophilin 1 in desmosome assembly and actin filament organization. J Cell Biol. 149:2000;209-222.
80. Wal J.K. III, Nieset J.E., Bubulya P.A.S., Sadler T.M., Johnson K.R., Wheelock M.J. The amino- and carboxyl-terminal tails of β-catenin reduces its affinity for desmoglein 2. J Cell Sci. 113:2000;1737-1745.
81. Smith E.A., Fuchs E. Defining the interaction between intermediate filaments and desmosomes. J Cell Biol. 141:1998;1229-1241.
82. Koch P.J., Mahoney M.G., Ishikawa H., Pulkkinen L., Uitto J., Shultz L., Murphy G.F., Whitaker M.D., Stanley J.R. 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. 137:1997;1091-1102.
83. Allen E., Yu Q.-C., Fuchs E. Mice expressing a mutant desmosomal cadherin exhibit abnormalities in desmosomes, proliferation and epidermal differentiation. J Cell Biol. 133:1996;1367-1382.
84. Ruiz P., Brinkmann V., Ledermann B., Behrend M., Grund C., Thalhammer C., Vogel F., Birchmeier C., Gunthert U., Franke W.W., Birchmeier W. Targeted mutation of plakoglobin in mice reveals essential functions of desmosomes in the embryonic heart. J Cell Biol. 135:1996;215-225.
85. Bierkamp C., Mclaughlin K.J., Schwarz H., Huber O., Kemler R. Embryonic heart and skin defects in mice lacking plakoglobin. Dev Biol. 180:1996;780-785.
86. Charpentier E., Lavker R.M., Acquista E., Cowin P. Plakoglobin suppresses epithelial proliferation and hair growth in vivo. J Cell Biol. 149:2000;503-519.
87. 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. N-terminal deletion in a desmosomal cadherin causes the autosomal dominant skin disease striate palmoplantar keratoderma. Hum Mol Genet. 8:1999;971-976.
88. Hunt D.M., Rickman L., Whittock N.V., Eady R.A., Simrak D., Dopping Hepenstal P.J., Stevens H.P., Armstong D.K., Hennies H.C., Kuster W., et al. Spectrum of dominant mutations in the desmosomal cadherin desmoglein 1, causing the skin disease striate palmoplantar keratoderma. Eur J Hum Genet. 9:2001;197-203.
89. Armstrong D.K., McKenna K.E., Purkis P.E., Green K.J., Eady R.A., Leigh I.M., Hughes A.E. Haploinsufficiency of desmoplakin causes a striate subtype of palmoplantar keratoderma. Hum Mol Genet. 8:1999;143-148.
90. Whittock N.V., Ashton G.H., Dopping Hepenstal P.J., Gratian M.J., Keane F.M., Eady R.A., McGrath J.A. Striate palmoplantar keratoderma resulting from desmoplakin haploinsufficiency. J Invest Dermatol. 113:1999;940-946.
91. Norgett E.E., Hatsell S., Carvajal H.L., Cabeza J.C., Purkis P.E., Whittock N., Leigh I.M., Stevens H.P., Kelsell D.P. Recessive mutation in desmoplakin disrupts desmoplakin-intermediate filament interactions and causes dilated cardiomyopathy, woolly hair and keratoderma. Hum Mol Genet. 9:2000;2761-2766.
92. Whittock N.V., Wan H., Morely S., Garzon M.C., Kristal L., Hyde P., McLean W.H.I., Pulkkinen L., Uitto J., Christiano A.M., Eady R.A.J., McGrath J.A. Compound heterozygosity for non-sense and mis-sense mutations in desmoplakin underlies skin fragility/woolly hair syndrome. J Invest Dermatol. 118:2002;232-238.
93. McKoy G., Protonotarios N., Crosby A., Tsatsopoulou A., Anastasakis A., Coonar A., Norman M., Baboonian C., Jeffery S., McKenna W.J. Identification of a deletion in plakoglobin in arrhythmogenic right ventricular cardiomyopathy with palmoplantar keratoderma and woolly hair (Naxos disease). Lancet. 355:2000;2119-2124.
94. McGrath J.A., McMillan J.R., Shemanko C.S., Runswick S.K., Leigh I.M., Lane E.B., Garrod D.R., Eady R.A. Mutations in the plakophilin 1 gene result in ectodermal dysplasia/skin fragility syndrome. Nat Genet. 2:1997;240-244.
95. McGrath J.A., Hoeger P.H., Christiano A.M., McMillan J.R., Mellerio J.E., Ashton G.H., Dopping Hepenstal P.J., Lake B.D., Leigh I.M., Harper J.I., Eady R.A. Skin fragility and hypohidrotic ectodermal dysplasia resulting from ablation of plakophilin 1. Br J Dermatol. 140:1999;297-307.