The dermal-epidermal junction

Current Opinion in Cell Biology

Volumn 9, Issue 5, 1997, Pages 651-658

  Burgeson, Robert E ^a   Christiano, Angela M ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION MOLECULE; COLLAGEN TYPE 7; CYTOSKELETON PROTEIN; INTEGRIN; MEMBRANE PROTEIN; PEMPHIGUS ANTIBODY; STRUCTURAL PROTEIN;

BULLOUS SKIN DISEASE; CELL ADHESION; CELL MIGRATION; CELL SPECIFICITY; CELL TYPE; DERMOEPIDERMAL JUNCTION; EPIDERMOLYSIS BULLOSA; EXTRACELLULAR MATRIX; GENE DISRUPTION; GENE MUTATION; HEMIDESMOSOME; HUMAN; KERATINOCYTE; PEMPHIGOID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

MUS MUSCULUS; PEMPHIGUS;

EID: 0030752760     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(97)80118-4     Document Type: Article

References (49)

1. Timpl R: Macromolecular organization of basement membranes. Curr Opin Cell Biol 1996, 8:618-624.
2. Borradori L, Sonnenberg A: Hemidesmosomes: roles in adhesion, signalling and human diseases. Curr Opin Cell Biol 1996, 8:647-656.
3. McKee PH: Normal histology of the skin. In Pathology of the Skin. Barcelona: Mosby-Wolfe; 1996:1.3-1.29.
4. Holbrook KA, Smith LT: Morphology of connective tissue: structure of the skin and tendon. In Connective Tissue and Its Heritable Disorders. Edited by Royce PM, Steinman B. New York: Wiley-Liss; 1993:51-71.
5. Christiano AM, Uitto J: Molecular complexity of the cutaneous basement membrane zone. Revelations from the paradigms of epidermolysis bullosa. Exp Dermatol 1996, 5:1-11.
6. Fuchs E: Of mice and men: genetic disorders of the cytoskeleton. Mol Biol Cell 1997, 8:189-203.
7. Corden LD, McLean WHI: Human keratin diseases: hereditary fragility of specific epithelial tissues. Exp Dermatol 1996, 5:297-307.
8. Christiano AM, Uitto J: functional forms of epidermolysis bullosa. In Textbook of Molecular Medicine. Edited by Jameson JL Cambridge, MA: Blackwell Science Inc; 1997:in press.
9. Uitto J, Christiano AM: Dystrophic forms of epidermolysis bullosa. In Textbook of Molecular Medicine. Edited by Jameson JL. Cambridge, MA: Blackwell Science Inc; 1997:in press.
10. Hieda Y, Nishizawa Y, Uematsu J, Owaribe K: Identification of a new hemidesmosomal protein, HD1: a major, high molecular mass component of isolated hemidesmosomes. J Cell Biol 1992, 116:1497-1506.
11. Wiche G, Becker B, Luber K, Weitzer G, Castanon MJ, Hauptmann R, Stratowa C, Stewart M: Cloning and sequence of rat plectin indicates a 466-kD polypeptide chain with a three-domain structure based on a central alpha-helical coiled coil. J Cell Biol 1991, 114:83-99.
12. McLean WHI, Pulkkinen L, Smith FJD, Rugg EL, Lane EB, Bullrich F, Burgeson RE, Amano S, Hudson DL, Owanibe K et al.: Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organization. Genes Dev 1996, 10:1724-1735. This paper documents the characterization of the human plectin gene, and demonstrates the first known mutations underlying epidermolysis bullosa with muscular dystrophy (EB-MD). Identification of mutations in a single gene in EB-MD unequivocally proved that both EB and MD were the result of a defect in the same gene.
13. Fujiwara S, Kohno K, Iwamatsu A, Naito I, Shinkai H: Identification of a 450-kDa human epidermal autoantigen as a new member of the plectin family. J Invest Dermatol 1996, 106:1125-1130.
14. Uitto J, Pulkkinen L, Smith, FJD, McLean WHI: Plectin and human genetic disorders of the skin and muscle. Exp Dermatol 1996, 5:237-246.
15. Sawamura D, Li K, Chu M-L, Uitto J: Human bullous pemphigoid antigen (BPAG1): amino acid sequences deduced from cloned cDNAs predict biologically important peptide segments and protein domains. J Biol Chem 1991, 266:17784-17790.
16. Stanley JR, Tanaka T, Mueller S, Klaus-Kovtun V, Roop D: Isolation of cDNAs for bullous pemphigoid antigen by use of patients' autoantibodies. J Clin Invest 1988, 82:1864-1870.
17. Guo L, Degenstein L, Dowling J, Yu QC, Wollmann R, Periman B, Fuchs E: Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell 1995, 81:233-243.
18. Yang Y, Dowling J, Yu Q-C, Kouklis P, Cleveland DW, Fuchs E: An essential cytoskeletal linker protein connecting actin microfilaments to intermediate filaments. Cell 1996, 86:655-665. This work extends the observations by the same group [17] of a skin and neuromuscular phenotype resulting from ablation of the bullous pemphigoid antigen 1 (BPAG1) gene. In this study, the authors demonstrate the existence of two differentially expressed isoforms of BPAG1; one is expressed in the epidermis and the second in the neural network. The authors go on to show that BPAG1 serves as a tethering protein between the actin filament and intermediate filament networks. These results explain the development of the two seemingly disparate phenotypes in the BPAG1 knockout mouse [17].
19. Brown A, Copeland NG, Gilbert DJ, Jenkins NA, Rossant J, Kothary R: The genomic structure of an insertional mutation in the dystonia musculorum locus. Genomics 1994, 20:371-376.
20. Giudice GJ, Emery DJ, Diaz LA: Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 1992, 99:243-250.
21. Giudice GJ, Emery DJ, Zelickson BD, Ahnalt GJ, Liu Z, Diaz LA: Bullous pemphigoid and herpes gestationis autoantibodies recognize a common non-collagenous site on the BP180 ectodomain. J Immunol 1993, 151:5742-5750.
22. McGrath JA, Gatalica B, Christiano AM, Li K, Owaribe K, McMillan JR, Eddy RAJ, Uitto J: Mutations in the 180-kD bullous pemphigoid antigen, a hemidesmosomal transmembrane collagen, in generalized atrophic benign epidermolysis bullosa. Nat Genet 1995, 11:83-86.
23. McGrath JA, Gatalica B, Li, Dunnill MGS, McMillan JR, Christiano AM, Eady RAJ, Uitto J: Compound heterozygosity for a dominant glycine substitution and a recessive internal duplication mutation in the type XVII collagen gene results in junctional epidermolysis bullosa and abnormal dentition. Am J Path 1996, 148:1787-1796. This paper, together with [22], is among the large emerging body of literature that implicates the importance of mutations in the bullous pemphigoid antigen 2 gene in generalized atrophic benign epidermolysis bullosa (GABEB). A more detailed summary of GABEB-associated mutations may be found in [8].
24. Hynes RO: Integrins: versatility, modulation, and signaling in cell adhesion. Cell 1992, 69:11-25.
25. Roberts GP: Characterization of the antigens recognized by two monoclonal antibodies reactive with basal-layer keratinocytes of human epidermis. Biochem J 1994, 299:659-664.
26. Carter WG, Kaur P, Gil SG, Gahr PJ, Wayner EA: Distinct functions for integrins α3β1 in focal adhesions and α6β4/bullous pemphigoid antigen in a new stable anchoring contact (SAC) of keratinocytes: relation to hemidesmosomes. J Cell Biol 1990, 111:3141-3154.
27. Stepp MA, Spurr-Michaud S, Tisdale A, Elwell J, Gipson IK: α6β4 integrin heterodimer is a component of hemidesmosomes. Proc Natl Acad Sci USA 1990, 87:8970-8974.
28. Vidal F, Aberdam D, Miquel C, Christiano AM: Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat Genet 1995, 10:229-234.
29. •].
30. •] are the first among an emerging body of evidence that implicates the involvement of the integrin α6 and β4 genes in junctional epidermolysis bullosa with pyloric atresia (JEB-PA). A more detailed summary of JEB-PA mutations may be found in [8].
31. ••].
32. •] in that it is lethal in the neonatal period.
33. DiPersio CM, Hodivala-Dilke KM, Jaenisch R, Kreidberg JA, Hynes RO: α3β1 integrin is required for normal development of the epidermal basement membrane. J Cell Biol 1997, 137:729-742. In this study, the role of α3β1 integrin was investigated by studying the skin of α3-deficient mice. The extracellular matrix was disorganized in these mice, and this was accompanied by blistering at the dermal-epidermal junction (DEJ). Interestingly, laminin 5 remained associated with both the roof and the base of intra-DEJ blisters, suggesting that rupture of the basement membrane itself occurred, as oppposed to detachment from the basement membrane which occurs in junctional epidermolysis bullosa. No human phenotype has yet been associated with mutations in α3 integrin; however, a role for this integrin in establishment and/or maintenance of DEJ integrity is clearly implied.
34. Champliaud M-F, Lunstrum GP, Rousselle P, Nishiyama T, Keene D, Burgeson RE: Human amnion contains a novel laminin variant, laminin 7, which like laminin 6, covalently associates with laminin 5 to promote epithelial-stromal attachment J Cell Biol 1996, 132:1189-1198. In this study, the association of laminin 5 with laminin 6 and possibly laminin 7 is put forth as a mechanistic model for the stable association of laminin 5 with the basement membrane.
35. Rousselle P, Lunstrum GP, Keene DR, Burgeson RE: Kalinin: an epithelium-specific basement membrane adhesion molecule that is a component of anchoring filaments. J Cell Biol 1991, 114:567-576.
36. •,37]. It is now understood that different types and combinations of mutations in the laminin 5 genes dictate the severity of the clinical phenotype. For an extended listing of laminin 5 gene mutations in the different forms of JEB, please refer to [5,8].
37. McGrath JA, Pulkkinen L, Christiano AM, Leigh IM, Eady RAJ, Uitto J: Altered laminin 5 expression due to mutations in the gene encoding the β3 chain (LAMB3) in generalized atrophic benign epidermolysis bullosa. J Invest Dermatol 1995, 104:467-474.
38. Kirtschig G, Marinkovich MP, Burgeson RE, Yancey KB: Anti-basement membrane antibodies in patients with anti-epiligrin cicatricial pemphigoid bind the a subunit of laminin 5. J Invest Dermatol 1995, 105:543-548.
39. Rousselle P, Keene DR, Ruggiero F, Champliaud M-F, van der Rest M, Burgeson RE: Laminin 5 binds the NC-1 domain of type VII collagen. J Cell Biol 1997, in press. This study unequivocally demonstrates, for the first time, a critical association within the anchoring complex that consists of a direct connection between laminin 5 and the amino-terminal domain of type VII collagen.
40. Suzuki N, Labosky PA, Furuta Y, Hargett L, Dunn R, Fogo AB, Takahara K, Peters DM, Greenspan DS, Hogan BL: Failure of ventral body wall closure in mouse embryos lacking a procollagen C-proteinase encoded by Bmp1, a mammalian gene related to Drosophila tolloid. Development 1996, 122:3587-3595. This study describes the phenotype of a mouse in which the bone morphogenetic protein 1 (Bmp1) gene was disrupted by targeted ablation. Homozygous mutant mice displayed normal skeletal development, with the exception of reduced ossification of some bones of the skull. They showed a persistent herniation of the gut in the untilical region as a result of absence of a critical amniotic fold, and died in the neonatal period. The extracellular matrix of the amnion contained collagen fibrils with abnormal morphology, consistent with the abnormal processing of procollagen molecules that occurs in the absence of Bmp-1, the metalloprotease that cleaves the carboxy-terminal propeptide of collagens I, II and III.
41. Miner JH, Patton BL, Lentz SI, Gilbert DJ, Snider WD, Jenkins NA, Copeland NG, Sanes JR: The laminin a chains: expression, developmental transitions, and chromosomal locations of α1-5, identification of heterotrimeric laminins 8-11, and cloning of a novel α3 isoform. J Cell Biol 1997, 137:685-701. This paper conclusively demonstrates the existence of mouse α4 and α5 laminin chains, and details the tissue and cell type specific expression of the laminin α1-α5 chains during development. In particular, biochemical data support the existence of four novel laminin heterotrimers, laminins 8-11.
42. Burgeson RE: Type VII collagen, anchoring fibrils and epidermolysis bullosa. J Invest Dermatol 1993, 101:252-255.
43. McGrath JA, Ishida-Yamamoto A, O'Grady A, Leigh IM, Eady RAJ: Structural variations in anchoring fibrils in dystrophic epidermolysis bullosa: correlation with type VII collagen expression. J Invest Dermatol 1993, 100:366-372.
44. Gammon WR: Epidermolysis bullosa acquisita: a disease of autoimmunity to type VII collagen. J Autoimmun 1991, 4:59-71.
45. Gammon WR, Woodley DT, Dole KC, Briggaman RA: Evidence that anti-basement membrane zone antibodies in bullous eruption of systemic lupus erythematosus recognize epidermolysis bullosa acquisita antigen. J Invest Dermatol 1985, 84:472-476.
46. •] for interesting genetic evidence in support of a role for type VII collagen in the pathogenesis of inflammatory bowel disease.
47. Leivo I, Tani T, Laitinen L, Bruns R, Kivilaasko E, Lehto VP, Burgeson RE, Virtanen I: Anchoring complex components laminin 5 and type VII collagen in intestine: association with migrating and differentiating enterocytes. J Histochem Cytochem 1996, 44:1267-1277. This is a detailed histochemical analysis of the expression patterns of laminin 5, type VII collagen and α3, α6 and β4 integrins in the developing and adult human intestine. Electron microscopy revealed the presence of both anchoring filaments and anchoring fibrils in the intestine, but no evidence of hemidesmosomal plaques. Absence of hemidesmosomes in the presence of the other anchoring complex components suggests unique mechanisms for epithelial cell attachment in the intestine.
48. •] would suggest a significant connection.
49. Maniero F, Pepe A, Wary KK, Spinardi L, Mohammadi M, Schlessinger J, Giancotti FG: Signal transduction by the α6β4 integrin: distinct β4 subunit sites mediate recruitment of Shc/Grb2 and association with the cytoskeleton of hemidesmosomes. EMBO J 1995, 14:4470-4481.