Rapid Decay of α6 Integrin Caused by a Mis-Sense Mutation in the Propeller Domain Results in Severe Junctional Epidermolysis Bullosa with Pyloric Atresia

Journal of Investigative Dermatology

Volumn 121, Issue 6, 2003, Pages 1336-1343

  Allegra, Maryline ^a   Gagnoux Palacios, Laurent ^a   Gache, Yannick ^a   Roques, Stéphanie ^a   Lestringant, Gilles ^b,c   Ortonne, Jean Paul ^a   Meneguzzi, Guerrino ^a  

^a INSERM   (France)

^b TAWAM HOSPITAL   (United Arab Emirates)

^c Brit Forces in Germany Hlth Serv   (Germany)

Author keywords

Integrin 6 4; Lysosome; Proteasome; Skin blistering disease; propeller

Indexed keywords

ALPHA6 INTEGRIN; ALPHA6BETA4 INTEGRIN; BETA4 INTEGRIN; CYTOSINE; INTEGRIN RECEPTOR; LEUCINE; MESSENGER RNA; POLYPEPTIDE; SERINE; THYMINE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; BULLOUS SKIN DISEASE; CASE REPORT; CONTROLLED STUDY; EPIDERMOLYSIS BULLOSA; GENE EXPRESSION; HOMOZYGOSITY; HUMAN; HUMAN CELL; HUMAN TISSUE; LETHALITY; LYSOSOME; MALE; MISSENSE MUTATION; NEWBORN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; PYLORUS ATRESIA; STOMACH DISEASE; STOP CODON;

EID: 0346363881     PISSN: 0022202X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1523-1747.2003.12625.x     Document Type: Article

References (51)

1. Borradori L, Sonnenberg A: Structure and function of hemidesmosomes: More than simple adhesion complexes. J Invest Dermatol 112:411-418, 1999
2. Bross P, Corydon TJ, Andresen BS, Jorgensen MM, Bolund L, Gregersen N: Protein misfolding and degradation in genetic diseases. Hum Mutat 14:186-198, 1999
3. Chapman RE, Munro S: Retrieval of TGN proteins from the cell surface requires endosomal acidification. EMBO J 13:2305-2312, 1994
4. Chavanas S, Pulkkinen L, Gache Y, et al: A homozygous nonsense mutation in the PLEC1 gene in patients with epidermolysis bullosa simplex with muscular dystrophy. J Clin Invest 98:2196-2200, 1996
5. Chen C, Okayama H: High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol 7:2745-2752, 1987
6. Dowling J, Yu QC, Fuchs E: Beta4 integrin is required for hemidesmosome formation, cell adhesion and cell survival. J Cell Biol 134:559-572, 1996
7. Ellgaard L, Molinari M, Helenius A: Setting the standards: Quality control in the secretory pathway. Science 286:1882-1888, 1999
8. Fine JD: Inherited epidermolysis bullosa. Selected outcomes and a revised classification system. Pediatr Dermatol 17:75-83, 2000
9. 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 97:2289-2298, 1996
10. Gagnoux-Palacios L, Vailly J, Durand-Clement M, Wagner E, Ortonne JP, Meneguzzi G: Functional re-expression of laminin-5 in laminin-gamma2-deficient human keratinocytes modifies cell morphology, motility, and adhesion. J Biol Chem 271:18437-18444, 1996
11. Gagnoux-Palacios L, Gache Y, Ortonne JP, Meneguzzi G: Hemidesmosome assembly assessed by expression of a wild-type integrin beta 4 cDNA in junctional epidermolysis bullosa keratinocytes. Lab Invest 77:459-468, 1997
12. Gagnoux-Palacios L, Allegra M, Spirito F, Pommeret O, Romero C, Ortonne JP, Meneguzzi G: The short arm of ehe laminin gamma2 chain plays a pivotal role in the incorporation of laminin 5 into the extracellular matrix and in cell adhesion. J Cell Biol 153:835-850, 2001
13. Georges-Labouesse E, Messaddeq N, Yehia G, Cadalbert L, Dierich A, Le Meur M: Absence of integrin alpha 6 leads to epidermolysis bullosa and neonatal death in mice. Nat Genet 13:370-373, 1996
14. Guerrero-Estco M, Ruiz-Velasco N, Munoz M, Teixido J: Role of two conserved glycine residues in the beta-propeller domain of the integrin alpha4 subunit in VLA-4 conformation and function. FEBS Lett 429:123-128, 1998
15. Hemler ME, Crouse C, Sonnenberg A: Association of the VLA alpha 6 subunit with a novel protein. A possible alternative to the common VLA beta 1 subunit on certain cell lines. J Biol Chem 264:6529-6535, 1989
16. 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 116:1497-1506, 1992
17. Hogervorst F, von Kuikman I, dem Borne AE, Sonnenberg A: Cloning and sequence analysis of beta-4 cDNA. An integrin subunit that contains a unique 118 kd cytoplasmic domain. EMBO J 9:765-770, 1990
18. Hogervorst F, Kuikman I, van Kessel AG, Sonnenberg A: Molecular cloning of the human alpha 6 integrin subunit. Alternative splicing of alpha 6 mRNA and chromosomal localization of the alpha 6 and beta 4 genes. Eur J Biochem 199:425-433, 1991
19. Hogervorst F, Admiraal LG, Niessen C, Kuikman I, Janssen H, Daams H, Sonnenberg A: Biochemical characterization and tissue distribution of the A and B variants of the integrin alpha 6 subunit. J Cell Biol 121:179-191, 1993a
20. Hogervorst F, Kuikman I, Noteboom E, Sonnenberg A: The role of phosphorylation in activation of the alpha 6A beta 1 laininin receptor. J Biol Chem 268:18427-18430, 1993b
21. Huang C, Springer TA: Folding of the beta-propeller domain of the integrin alphaL subunit is independent of the I domain and dependent on the beta2 subunit. Proc Natl Acad Sci USA 94:3162-3167, 1997
22. Hynes RO: Integrins. Versatility, modulation, and signaling in cell adhesion. Cell 69:11-25, 1992
23. Kamata T, Tieu KK, Irie A, Springer TA, Takada Y: Amino acid residues in the alpha IIb subunit that are critical for ligand binding to integrin alpha IIbbeta 3 are clustered in the beta-propeller model. J Biol Chem 276:44275-44283, 2001
24. Kennel SJ, Epler RG, Lankford TK, et al: Second generation monoclonal antibodies to the human integrin alpha 6 beta 4. Hybridoma 9:243-255, 1990
25. Koster J, Kuikman I, Kreft M, Sonnenberg A: Two different mutations in the cytoplasmic domain of the integrin beta 4 subunit in nonlethal forms of epidermolysis bullosa prevent interaction of beta 4 with plectin. J Invest Dermatol 117:1405-1411, 2001
26. Lee EC, Lotz MM, Steele GD Jr, Mercurio AM: The integrin alpha 6 beta 4 is a laminin receptor. J Cell Biol 117:671-678, 1992
27. Lehmann M, Rigot V, Seidah NG, Marvaldi J, Lissitzky JC: Lack of integrin alpha-chain endoproteolytic cleavage in furin-deficient human colon adenocarcinoma cells LoVo. Biochem J 317:803-809, 1996
28. Lenter M, Vestweber D: The integrin chains beta 1 and alpha 6 associate with the chaperone calnexin prior to integrin assembly. J Biol Chem 269:12263-12268, 1994
29. Lestringant GG, Akel SR, Qayed KI: The pyloric atresia-junctional epidermolysis bullosa syndrome. Report of a case and review of the literature. Arch Dermatol 128:1083-1086, 1992
30. Liu Y, Choudhury P, Cabral CM, Sifers RN: Intracellular disposal of incompletely folded human alpha1-antitrypsin involves release from calnexin and post-translational trimming of asparagine-linked oligosaccharides. J Biol Chem 272:7946-7951, 1997
31. Lu C, Oxvig C, Springer TA: The structure of the beta-propeller domain and C-terminal region of the integrin alphaM subunit. Dependence on beta subunit association and prediction of domains. J Biol Chem 273:15138-15147, 1998
32. McIntosh I, Hamosh A, Dietz HC: Nonsense mutations and diminished mRNA levels. Nat Genet 4:219, 1993
33. Nakano A, Pulkkinen L, Murrell D, et al: Epidermolysis bullosa with congenital pyloric atresia. Novel mutations in the beta 4 integrin gene (ITGB4) and genotype/phenotype correlations. Pediatr Res 49:618-626, 2001
34. van der Neut R, Krimpenfort P, Calafat J, Niessen CM, Sonnenberg A: Epithelial detachment due to absence of hemidesmosomes in integrin beta 4 null mice. Nat Genet 13:366-369, 1996
35. Niessen CM, Hogervorst F, Jaspars LH, et. al: The alpha 6 beta 4 integrin is a receptor for both laminin and kalinin. Exp Cell Res 211:360-367, 1994
36. Niessen CM, van der Raaij-Helmer MH, Hulsman EH, van der Neut R, Jonkman MF, Sonnenberg A: Deficiency of the integrin beta 4 subunit in junctional epidermolysis bullosa with pyloric atresia: Consequences for hemidesmosome formation and adhesion properties. J Cell Sci 109:1695-1706, 1996
37. Okazaki Y, Ohno H, Takase K, Ochiai T, Saito T: Cell surface expression of calnexin, a molecular chaperone in the endoplasmic reticulum. J Biol Chem 275:35751-35758, 2000
38. Pulkkinen L, Kim DU, Uitto J: Epidermolysis bullosa with pyloric atresia: Novel mutations in the beta4 integrin gene (ITGB4). Am J Pathol 152:157-166, 1998
39. Qu D, Teckman JH, Omura S, Perlmutter DH: Degradation of a mutant secretory protein, alpha1-antitrypsin Z, in the endoplasmic reticulum requires proteasome activity. J Biol Chem 271:22791-22795, 1996
40. Rheinwald JG, Green H: Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 6:331-343, 1975
41. Rigot V, Andre F, Lehmann M, Lissitzky JC, Marvaldi J, Luis J: Biogenesis of alpha6beta4 integrin in a human colonic adenocarcinoma cell line involvement of calnexin. Eur J Biochem 261:659-666, 1999
42. Ruzzi L, Gagnoux-Palacios L, Pinola M, Belli S, Meneguzzi G, D'Alessio M, Zambruno G: A homozygous mutation in the integrin alpha6 gene in junctional epidermolysis bullosa with pyloric atresia. J Clin Invest 99:2826-2831, 1997
43. Schaapveld RQ, Borradori L, Geerts D, et al: Hemidesmosome formation is initiated by the beta4 integrin subunit, requires complex formation of beta4 and HD1/ plectin, and involves a direct interaction between beta4 and the bullous pemphigoid antigen 180. J Cell Biol 142:271-284, 1998
44. Sondek J, Bohm A, Lambright DG, Hamin HE, Sigler PB: Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379:369-374, 1996
45. Sonnenberg A, Janssen H, Hogervorst F, Calafat J, Hilgers J: A complex of platelet glycoproteins Ic and IIa identified by a rat monoclonal antibody. J Biol Chem 262:10376-10383, 1987
46. Soto C: Protein misfolding and disease; protein refolding and therapy. FEBS Lett 498:204-207, 2001
47. Springer TA: Folding of the N-terminal, ligand-binding region of integrin alpha-subunits into a beta-propeller domain. Proc Natl Acad Sci USA 94:65-72, 1997
48. Thompson JD, Higgins DG, Gibson TJ: Cluscal W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680, 1994
49. Verrando P, Blanchet-Bardon C, Pisani A, et al: Monoclonal antibody GB3 defines a widespread defect of several basement membranes and a keratinocyte dysfunction in patients with lethal junctional epidermolysis bullosa. Lab Invest 64:85-92, 1991
50. Vidal F, Aberdam D, Miquel C, et al: Integrin beta 4 mutations associated with junctional epidermolysis bullosa with pyloric atresia. Nat Genet 10:229-234, 1995
51. Xiong JP, Stehle T, Diefenbach B, et al: Crystal structure of the extracellular segment of integrin alpha Vbeta3. Science 294:339-345, 2001