Hemidesmosomes: Roles in adhesion, signaling and human diseases

Current Opinion in Cell Biology

Volumn 8, Issue 5, 1996, Pages 647-656

  Borradori, Luca ^a   Sonnenberg, Arnoud ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

INTEGRIN; MEMBRANE PROTEIN;

AMINO ACID SEQUENCE; BINDING AFFINITY; BLISTER; CARBOXY TERMINAL SEQUENCE; CELL ADHESION; CELL FUNCTION; EPIDERMOLYSIS BULLOSA; EXTRACELLULAR MATRIX; GENE MUTATION; GENE TARGETING; GENETIC TRANSFECTION; HEMIDESMOSOME; HUMAN; KERATINOCYTE; MUTAGENESIS; PEMPHIGOID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION;

EID: 0030272476     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0955-0674(96)80106-2     Document Type: Article

References (74)

1. Schwarz MA, Owaribe K, Kartenbeck J, Franke WW: Desmosomes and hemidesmosomes: constitutive molecular components. Annu Rev Cell Biol 1990, 6:461-491.
2. Stanley JR: Autoantibodies against adhesion molecules and structures in blistering skin diseases. J Exp Med 1995, 181:1-4.
3. Christiane AM, Ditto J: Molecular complexity of the cutaneous basement membrane zone. Revelations from the paradigms of epidermolysis bullosa. Exp Dermatol 1996, 5:1-11.
4. Jones JCR, Asmuth J, Baker SE, Langhofer M, Roth SI, Hopkinson SB: Hemidesmosomes: extracellular matrix/intermediate filament connectors. Exp Cell Res 1994, 213:1-11.
5. Stanley JR, Tanaka T, Mueller S, Klaus-Kovtun V, Roop D: Isolation of cDNA for bullous pemphigoid antigen by use of patients' autoantibodies. J Clin Invest 1988, 82:1864-1870.
6. Skalli O, Jones JCR, Gagescu R, Goldman RD: IFAP 300 is common to desmosomes and hemidesmosomes and is a possible linker of intermediate filaments to these junctions. J Cell Biol 1994, 125:159-170.
7. Foisner R, Wiche G: Intermediate filament-associated proteins. Curr Opin Cell Biol 1991, 3:75-81.
8. 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.
9. Kurpakus MA, Jones JCR: A novel hemidesmosomal plaque component: tissue distribution and incorporation into assembling hemidesmosomes in an in vitro model. Exp Cell Res 1991, 194:139-146.
10. Foisner R, Leichtfried FE, Herrmann H, Small JV, Lawson D, Wiche G: Cytoskeleton-associated plectin: in situ localization, in vitro reconstitution, and binding to immobilized intermediate filament proteins. J Cell Biol 1988, 106:723-733.
11. Wiche G, Gromov D, Donovan A, Castanon MJ, Fuchs E: Expression of plectin mutant cDNA in cultured cells indicates a role of COOH-terminal domain in intermediate filament association. J Cell Biol 1993, 121:607-619.
12. Tanaka T, Parry DAD, Klaus-Kovtun V, Steinert PM, Stanley JR: Comparison of molecularly cloned bullous pemphigoid antigen to desmoplakin I confirms that they define a new family of cell adhesion junction plaque proteins. J Biol Chem 1991, 266:12555-12559.
13. Green KJ, Virata MLA, Elgart GW, Stanley JR, Parry DAD: Comparative structural analysis of desmoplakin, bullous pemphigoid antigen and plectin: members of a new gene family involved in organization of intermediate filaments. Int J Biol Macromol 1992, 14:145-153.
14. Stappenbeck TS, Bornslaeger EA, Corcoran CM, Luu HH, Virata MLA, Green KJ: Functional analysis of desmoplakin domains: specification of the interaction with keratin versus vimentin intermediate filament networks. J Cell Biol 1993, 123:691-705.
15. Turner CE, Burridge K: Transmolecular assemblies in cell-extracellular matrix interactions. Curr Opin Cell Biol 1991, 3:849-853.
16. Yang H-Y, Lieska NE, Goldman AE, Goldman RD: A 300,000-molwt intermediate filament-associated protein in baby hamster kidney (BHK-21) cells. J Cell Biol 1985, 100:620-631.
17. Smith RID, Eady RAJ, Leigh IM, McMillan JR, Rugg EL, Kelsell DP, Bryant SP, Spurr NK, Geddes JF, Kirtschig G et al.: Plectin deficiency: hereditary basis for muscular dystrophy with epidermolysis bullosa simplex. Nat Genet 1996, in press. See annotation [18].
18. McLean WHI, Pulkkinen L, Smith FJD, Rugg EL, Lane EB, Bullrich F, Burgeson RE, Amano S, Hudson DL, Owaribe K et al.: Loss of plectin causes epidermolysis bullosa with muscular dystrophy: cDNA cloning and genomic organisation. Genes Dev 1996, in press. This report and [17,64] demonstrate that, in a distinct form of epidermolysis bullosa associated with muscular dystrophy, loss of immunoreactivity for plectin and the hemidesmosomal component HD1 is found. Furthermore, this study and [17] also provide evidence that mutations in the gene encoding plectin underlie this disorder.
19. Wiche G, Becker B, Luber K, Weiter G, Castanon MJ, Hauptmann R, Stratowa C, Stewart M: Cloning and sequencing 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.
20. cdc2 kinase and mapping of a single phosphorylation site. J Biol Chem 1996, 271:8203-8208.
21. Giudice GJ, Emery DJ, Diaz LA: Cloning and primary structural analysis of the bullous pemphigoid autoantigen BP180. J Invest Dermatol 1992, 99:243-250.
22. Stepp MA, Spurr-Michaud S, Tisdale A, Elwell J, Gipson IK: α6β4 integrin heterodimer is a component of hemidesmosomes. Proc NatlAcad Sci USA 1990, 87:8970-8974.
23. Jones JCR, Kurpakus MA, Cooper HM, Quaranta V: A function for the integrin α6β4 in the hemidesmosome. Cell Regul 1991, 2:427-438.
24. Sonnenberg A, Calafat J, Janssen H, Daams H, Van der Raaij-Helmer LMH, Falcioni R, Kennel SJ, Aplin JD, Baker J, Loizidou M, Garrod D: Integrin α6/β4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 1991, 113:907-917.
25. Carter WG, Ryan MC, Gahr PJ: Epiligrin, a new cell adhesion ligand for integrin α3β1 in epithelial basement membranes. Cell 1991, 65:599-610.
26. Sonnenberg A, De Melker AA, Martinez de Velasco AM, Janssen H, Calafat J, Niessen CM: Formation of hemidesmosomes in cells of a transformed murine mammary tumor cell line and mechanisms involved in adherence of these cells to laminin and kalinin. J Cell Sci 1993, 106:1083-1102.
27. Rousselle P, Aumailley M: Kalinin is more efficient than laminin in promoting adhesion of primary keratinocytes and some other epithelial cells and has a different requirement for integrin receptors. J Cell Biol 1994, 125:205-214.
28. Yurchenco PD, O'Rear JJ: Basal lamina assembly. Curr Opin Cell Biol 1994, 6:674-681.
29. 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.
30. Verrando P, Blanchet-Bardon C, Pisani A, Thomas L, Cambazard F, Eady RAJ, Schofield O, Ortonne JP : Monoclonal antibody GB3 defines a widespread defect of several basement membranes and a keratinocyte dysfunction in patients with lethal functional epidermolysis bullosa. Lab Invest 1991, 64:85-92.
31. Marinkovich MP, Lunstrum GP, Burgeson RE: The anchoring filament proten kalinin is synthesized and secreted as a high molecular weight protein precursor. J Biol Chem 1992, 267:17900-17906.
32. Rousselle P, Golbik R, Van der Rest M, Aumailley M: Structural requirement for cell adhesion to kalinin (laminin-5). J Biol Chem 1995, 270:13766-13770.
33. 4 integrin is a receptor for both laminin and kalinin. Exp Cell Res 1994, 211:360-367.
34. Champliaud M-F, Lunstrum GP, Rousselle P, Nishiyama T, Keene DR, Burgeson RE: Human amnion contains a novel laminin variant, laminin 7, which like laminin 6, covalently associates with laminin 5 to promote stable epthelial-stromal adhesion. J Cell Biol 1996, 132:1189-1198. In this study, the covalent association of laminin 5 with laminin 6 (which consists of chains α3β1γ1) and/ or laminin 7 (α3β2γ1) is proposed to be a mechanism for the stable association of laminin 5 with the basement membrane.
35. Mayer U, Pöschl E, Gerecke DR, Wagman DW, Burgeson RE, Timpl R: Low nidogen affinity of laminin-5 can be attributed to two serine residues in EGF-like motif γ2III4. FEBS Lett 1995, 365:129-132. This paper shows that the low nidogen-binding affinity of laminin 5 results from the replacement of two amino acids in one of the two regions identified in the fourth EGF repeat of the γ1 laminin chain that contributes to high-affinity binding.
36. Mercurio AM: Laminin receptors: achieving specificity through cooperation. Trends Cell Biol 1995, 5:419-423. See annotation [37].
37. Delwel GO, Sonnenberg A: Laminin isoforms and their integrin receptors. In Adhesion Receptors as Therapeutic Targets. Edited by Norton MA. Boca Raton: CRC Press; 1996:9-36. This chapter, together with [36], provides a review of the various laminin isoforms and their functions in cell adhesion, development and differentiation, and discusses their integrin receptors which link laminin matrices to intracellular signalling pathways.
38. Jaspars LH, De Melker AA, Bonnet P, Sonnenberg A, Meijer CJLM: Distribution of several variant laminin chains and their integrin receptors in human secondary lymphoid tissue. Colocalization suggests that α6β4 integrin is a receptor for laminin 5 in human secondary lymphoid follicles. Cell Adhesion Commun 1996, in press.
39. Niessen CM, Cremona O, Daams H, Ferraresi S, Sonnenberg A, Marchisio PC: Expression of the integrin α6β4 in peripheral nerves: localization in Schwann and perineural cells and different variants of the β subunit J Cell Sci 1994, 107:543-552.
40. Spinardi L, Ren YL, Sanders R, Giancotti FG: The β4 subunit cytoplasmic domain mediates the interaction of α6β4 integrin with the cytoskeleton of hemidesmosomes. Mol Biol Cell 1993, 4:871-884.
41. Spinardi L, Einheber S, Cullen T, Milner TA, Giancotti FG: A recombinant tail-less integrin β4 subunit disrupts hemidesmosomes, but does not suppress α6β4-mediated cell adhesion to laminins. J Cell Biol 1995, 129:473-487. This work and that detailed in [40] have provided important data on the function of the cytoplasmic domain of the integrin β4 subunit in the localization of the α6β4 integrin in hemidesmosomes. Overexpression of a β4 subunit lacking the cytoplasmic domain has a dominant-negative effect on hemidesmosome assembly.
42. Mainiero 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. An excellent paper which reports that signal transduction by the α6β4 integrin is mediated by an associated tyrosine kinase and that phosphorylation at a TAM in the β4 cytoplasmic domain regulates the incorporation of the α6β4 integrin into hemidesmosomes. Phosphorylation of a distinct site(s) in the β4 cytoplasmic domain is (are) involved in the binding of Shc/Grb2 and possibly in the activation of the Ras/mitogen-activated protein kinase (MARK) kinase pathway.
43. Mainiero F, Pepe A, Yeon M, Ren Y, Giancotti FG: The intracellular functions of α6β4 integrin are regulated by EGF. J Cell Biol 1996, 134:241-253. This paper shows that EGF-dependent signals interfere with the ability of activated α6β4 integrin to associate with both signaling and cytoskeletal molecules.
44. Uematsu J, Nishizawa Y, Sonnenberg A, Owaribe K: Demonstration of type II hemidesmosomes in a mammary gland epithelial cell line, BMGE-H. J Biochem 1994, 115:469-476.
45. Hopkinson SB, Baker SE, Jones JCR: Molecular genetic studies of a human epidermal autoantigen (the 180-kD bullous pemphigoid antigen/BP180): identification of functionally important sequences within the BP180 molecule and evidence for an interaction between BP180 and α6 integrin. J Cell Biol 1995, 130:117-125. The authors have expressed mutant forms of BP180 in the epithelial 804G cell line and identified functionally important domains within BP180 that are required for its targeting into hemidesmosomes. A BP180 molecule lacking the collagenous extracellular domain is colocalized with the integrins α6β4 or α6β1 in cell lines that lack endogenous BP180 and is further coprecipitated with the integrin α6 subunit from extracts of cells transfected with this mutant form of BP180.
46. Niessen CM, Van der Raaij-Helmer LMH, Hulsman EHM, Van der Neut R, Jonkman MF, Sonnenberg A: Deficiency of the integrin β4 subunit in junctional epidermolysis bullosa with pyloric atresia: consequences for hemidesmosome formation and adhesion properties. J Cell Sei 1996, 109:1695-1706.
47. Langhofer M, Hopkinson SB, Jones JC: The matrix secreted by 804G cells contains laminin-related components that participate in hemidesmosome assembly in vitro. J Cell Sei 1993, 105:753-764.
48. Hormia M, Falk-Marzillier J, Plopper G, Jones JCR, Quaranta V: Rapid spreading and mature hemidesmosomes formation in HaCaT keratinocytes induced by incubation with soluble laminin-5r. J Invest Dermatol 1995, 105:557-561.
49. Tamura R, Rozzo C, Starr L, Chambers J, Reichardt LF, Cooper HM, Quaranta V: Epithelial integrin α6β4: complete primary structure of α6 and variant forms of β4. J Cell Biol 1990, 111:1593-1604.
50. Giancotti FG, Stepp MA, Suzuki S, Engvall E, Ruoslahti E: Proteolytic processing of endogenous and recombinant β4 integrin subunit J Cell Biol 1992, 118:951-959.
51. Clarke AS, Lotz MM, Chao C, Mercurio AM: Activation of the p21 pathway of growth arrest and apoptosis by the β4 integrin cytoplasmic domain. J Biol Chem 1995, 270:22673-22676.
52. Xia Y, Gil SG, Carter WG: Anchorage mediated by integrin α6β4 to laminin 5 (epiligrin) regulates tyrosine phosphorylation of a membrane-associated 80-kD protein. J Cell Biol 1995, 132:727-740.
53. Quo L, Degenstein L, Dowling J, Yu QC, Wollmann R, Perman 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. Describes the first gene-targeting experiment to study a hemidesmosomal component. Null-mutant mice for BPAG1/BP230 have discrete signs of skin fragility that predominantly involve hairless body regions in response to mechanical trauma A moderate retardation of the wound-healing process was also observed, suggesting that detachment of the cytoskeleton from hemidesmosomes affects the migration capacity of epidermal cells. Unexpectedly, the mice also showed neurological degeneration similar to that observed in dt/dt mice. See also [54].
54. Brown A, Bernier G, Mathieu M, Rossant J, Kothary R: The mouse dystonia musculorum gene is a neural isoform of bullous pemphigoid antigen 1. Nat Genet 1995, 10:301-306. An excellent study which identified the candidate dystonia musculorum gene, which encodes dystonin, and showed that the products of this gene are neural isoforms of BP230. These findings provide an explanation for the neurological phenotype observed in BP230-null mutant mice [53].
55. Van der Neut R, Krimpenfort P, Calafat J, Niessen CM, Sonnenberg A: Epithelial detachment due to absence of hemidesmosomes in integrin β4 null mice. Nat Genet 1996, 13:366-369. This report and [57] indicate that the integrin β4 and α6 subunits are critical in the assembly of hemidesmosomes and in their linkage to the keratin filament system and extracellular matrix in mice. Interestingly, in a β4-deficient patient [46] hemidesomomes are still observed, although their number is reduced and most of them appeared to be rudimentary. This suggests that in the absence of integrin α6β4, hemidesmosome formation can be initiated in humans, but not in mice.
56. Lloyd C, Yu Q-C, Cheng J, Turksen K, Degenstein L, Hutton E, Fuchs E: The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J Cell Biol 1995, 129:1329-1344.
57. Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M: Absence of the alpha-6 integrin leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 1996, 13:370-373. See annotation [55].
58. Vidai F, Aberdam D, Miquel C, Christiane AM, Pulkkinen L, Ditto J, Ortonne JP, Meneguzzi G: Integrin β4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat Genet 1995, 10:229-234. The first report of mutations in the β4 gene in a distinct subgroup of patients with junctional epidermolysis bullosa.
59. Shimizu H, Suzumori K, Hatta N, Nishikawa T: Absence of detectable 016 Integrin in pyloric atresia-junctional epidermolysis bullosa syndrome and its application for prenatal diagnosis in a family at risk for recurrence. Arch Dermatol 1996, in press.
60. Jonkman MF, De Jong MCJM, Heeres K, Pas HH, Van der Meer JB, Owaribe K, Martinez de Velasco AM, Niessen CM, Sonnenberg A: 180-kD bullous pemphigoid antigen (BP180) is deficient in generalized atrophic benign epidermolysis bullosa. J Clin Invest 1995, 95:1345-1352.
61. McGrath JA, Gatalica B, Christiane AM, Li K, Owaribe K, McMillan JR, Eady RAJ, Ditto J: Mutations in the 180-kD bullous pemphigoid antigen (BPAG2), a hemidesmosomal transmembrane collagen (COL17A1), in generalized atrophic benign epidermolysis bullosa. War Genet 1995, 11:83-86.
62. McGrath JA, Pulkkinen L, Christiane AM, Leigh IM, Eady RAJ, Ditto J: Altered taminin 5 expression due to mutations in the gene encoding the β3 chain (LAMB3) in generalized atrophie benign epidermolysis bullosa. J Invest Dermatol 1995, 104:467-474.
63. Marinkovich MP, Taylor TB, Keen DR, Burgeson RE, Zone JJ: LAD-1, the linear IgA bullous dermatosis autoantigen, is a novel 120-kD anchoring filament protein synthesized by epidermal cells. J Invest Dermatol 1996, 106:734-738.
64. Gache Y, Chavanas S, Lacour JP, Wiche G, Owaribe K, Meneguzzi G, Ortonne JP: Defective expression of plectin/HD1 in epidermolysis bullosa simplex with muscular dystrophy. J Clin Invest 1996, 97:2289-2298. See annotation [18].
65. Aberdam D, Galliano M-F, Vailry J, Pulkkinen L, Bonifas J, Christiane AM, Tryggvason K, Ditto J, Epstein EH Jr, Ortonne JP, Meneguzzi G: Herlitz's junctional epidermolysis bullosa is linked to mutations in the gene (LAMC2) for the gamma 2 subunit of nicein/kalinin (laminin-5). Waf Genet 1994, 6:299-304.
66. Pulkkinen L, Christiane AM, Airenne T, Haakana H, Tryggvason K, Ditto J: Mutations in the γ2 chain gene (LAMC2) of kalinin/laminin S in the junctional forms of epidermolysis bullosa. Nat Genet 1994, 6:293-298.
67. Pulkkinen L, Christiano AM, Gerecke D, Wagman DW, Burgeson RE, Pittelkow MR, Ditto J: A homozygous nonsense mutation in the β3 chain gene of laminin 5 (LAMB3) in Herlitz junctional epidermolysis bullosa. Genomics 1994, 24:357-360.
68. Kivirikko S, McGrath JA, Baudoin C, Aberdam D, Ciatti S, Dunnill MG, McMillan JR, Eady RA, Ortonne J-P, Meneguzzi G et al.: A homozygous nonsense mutation in the α3 chain gene of laminin 5 (LAMA3) in lethal (Herlitz) junctional epidermolysis bullosa. Hum Mol Genet 1995, 4:959-962. This study and [65-67] have identified the first mutations in the three laminin 5 genes. A monoclonal antibody directed against laminin 5, namely GB3, has previously been found to be nonreactive with the cutaneous basement membrane of several patients with lethal junctional epidermolysis bullosa [30].
69. Christiano A, Ryyänen M, Ditto J: Dominant dystrophic epidermolysis bullosa: identification of a Gly→Ser substitution in the triple helical domain of type VII collagen. Proc Natl Acad Sci USA 1994, 91:3549-3553.
70. 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.
71. Giudice GJ, Emery DJ, Zelickson BD, Anhalt 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.
72. Liu Z, Diaz LA, Troy JL, Taylor AF, Emery DJ, Fairley JA, Giudice GJ: A passive transfer model of the organ-specific autoimmune disease, bullous pemphigoid, using antibodies generated against the hemidesmosomal antigen, BP180. J Clin Invest 1993, 92:2480-2488.
73. Liu Z, Giudice GJ, Swartz Si, Fairley JA, Till GO, Troy JL, Diaz LA: The role of complement in experimental bullous pemphigoid. J Clin Invest 1995, 95:1539-1544. Bullous pemphigoid is one of the best defined autoimmune blistering disorders of the skin associated with circulating autoantibodies directed against BP230 and BP180. However, no good animal model to assess the pathogenicity of these autoantibodies existed until now. In this study and [72], rabbit antibodies raised against one immunodominant region of BP180 were shown, when injected into neonatal mice, to induce, via complement activation, & blistering disorder mimicking bullous pemphigoid.
74. Kirtschig G, Marinkovich MR Burgeson RE, Yancey KB: Antibasement membrane autoantibodies in patients with antiepiligrin cicatricial pemphigoid bind the α subunit of laminin 5. J Invest Dermatol 1995, 105:543-548.