Disorders of the cutaneous basement membrane zone-The paradigm of epidermolysis bullosa

Matrix Biology

Volumn 33, Issue , 2014, Pages 29-34

  Bruckner Tuderman, Leena ^a,b   Has, Cristina ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Adhesion; Blister; BMZ; BPAG1; Cell matrix adhesion; DEB; Dermal epidermal junction; EB; JEB; Kindler syndrome; KS; Skin fragility

Indexed keywords

ADHESION; BLISTER; CELL-MATRIX ADHESION; DERMAL-EPIDERMAL JUNCTION; KINDLER SYNDROME; SKIN FRAGILITY;

ANIMALS; BASEMENT MEMBRANE; CELL ADHESION; EPIDERMOLYSIS BULLOSA; EXTRACELLULAR MATRIX PROTEINS; GENETIC PREDISPOSITION TO DISEASE; GENETIC THERAPY; HUMANS; MUTATION; PHENOTYPE; SKIN;

EID: 84894254991     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.07.007     Document Type: Review

References (71)

1. Almaani N., Nagy N., Liu L., Dopping-Hepenstal P.J., Lai-Cheong J.E., Clements S.E., Techanukul T., Tanaka A., Mellerio J.E., McGrath J.A. Revertant mosaicism in recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 2010, 130:1937-1940.
2. Aumailley M., Has C., Tunggal L., Bruckner-Tuderman L. Molecular basis of inherited skin-blistering disorders, and therapeutic implications. Expert Rev. Mol. Med. 2006, 8:1-21.
3. Bandyopadhyay A., Rothschild G., Kim S., Calderwood D.A., Raghavan S. Functional differences between kindlin-1 and kindlin-2 in keratinocytes. J. Cell Sci. 2012, 125:2172-2184.
4. Behrens D.T., Villone D., Koch M., Brunner G., Sorokin L., Robenek H., Bruckner-Tuderman L., Bruckner P., Hansen U. The epidermal basement membrane is a composite of separate laminin- or collagen IV-containing networks connected by aggregated perlecan, but not by nidogens. J. Biol. Chem. 2012, 287:18700-18709.
5. Breitkreutz D., Koxholt I., Thiemann K., Nischt R. Skin basement membrane: the foundation of epidermal integrity-BM functions and diverse roles of bridging molecules nidogen and perlecan. Biomed. Res. Int. 2013, 2013:179784.
6. Bruckner-Tuderman L., Has C. Molecular heterogeneity of blistering disorders: the paradigm of epidermolysis bullosa. J. Invest. Dermatol. 2012, 132:E2-E5.
7. Bruckner-Tuderman L., McGrath J.A., Robinson E.C., Uitto J. Progress in epidermolysis bullosa research. Summary of DebRA International Research Conference 2012. J. Invest. Dermatol. 2013, (in press).
8. Burgeson R.E., Christiano A.M. The dermal-epidermal junction. Curr. Opin. Cell Biol. 1997, 9:651-658.
9. Chung H.J., Uitto J. Epidermolysis bullosa with pyloric atresia. Dermatol. Clin. 2010, 28:43-54.
10. Dang N., Klingberg S., Rubin A.I., Edwards M., Borelli S., Relic J., Marr P., Tran K., Turner A., Smith N., Murrell D.F. Differential expression of pyloric atresia in junctional epidermolysis bullosa with ITGB4 mutations suggests that pyloric atresia is due to factors other than the mutations and not predictive of a poor outcome: three novel mutations and a review of the literature. Acta Derm. Venereol. 2008, 88:438-448.
11. De Luca M., Pellegrini G., Mavilio F. Gene therapy of inherited skin adhesion disorders: a critical overview. Br. J. Dermatol. 2009, 161:19-24.
12. de Souza M.P., Rangel Miller V. Significance of patient registries for dermatological disorders. J. Invest. Dermatol. 2012, 132:1749-1752.
13. Di Salvio M., Piccinni E., De Zenzo G., Orecchia A., Gianfarani F., Conti A., Zambruno G., Odorisio T., Castiglia D. Diverse TGF-beta signaling in fibroblasts from phenotypically discordant monozygotic twins with recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 2012, 132:S90. (Abstract).
14. Diociaiuti A., Castiglia D., Morini F., Boldrini R., Fortugno P., Zambruno G., El Hachem M. Long-term follow-up of a spontaneously improving patient with junctional epidermolysis bullosa associated with ITGB4 c.3977-19T>A splicing mutation. Acta Derm. Venereol. 2013, 93:116-118.
15. Domogatskaya A., Rodin S., Tryggvason K. Functional diversity of laminins. Annu. Rev. Cell Dev. Biol. 2012, 28:523-553.
16. Fine J.D., Eady R.A., Bauer E.A., Bauer J.W., Bruckner-Tuderman L., Heagerty A., Hintner H., Hovnanian A., Jonkman M.F., Leigh I., McGrath J.A., Mellerio J.E., Murrell D.F., Shimizu H., Uitto J., Vahlquist A., Woodley D., Zambruno G. The classification of inherited epidermolysis bullosa (EB): Report of the Third International Consensus Meeting on Diagnosis and Classification of EB. J. Am. Acad. Dermatol. 2008, 58:931-950.
17. Franzke C.W., Bruckner P., Bruckner-Tuderman L. Collagenous transmembrane proteins: recent insights into biology and pathology. J. Biol. Chem. 2005, 280:4005-4008.
18. Gache Y., Allegra M., Bodemer C., Pisani-Spadafora A., de Prost Y., Ortonne J.P., Meneguzzi G. Genetic bases of severe junctional epidermolysis bullosa presenting spontaneous amelioration with aging. Hum. Mol. Genet. 2001, 10:2453-2461.
19. Has C., Kern J.S. Collagen XVII. Dermatol. Clin. 2010, 28:61-66.
20. Has C., Castiglia D., del Rio M., Diez M.G., Piccinni E., Kiritsi D., Kohlhase J., Itin P., Martin L., Fischer J., Zambruno G., Bruckner-Tuderman L. Kindler syndrome: extension of FERMT1 mutational spectrum and natural history. Hum. Mutat. 2011, 32:1204-1212.
21. Has C., Sparta G., Kiritsi D., Weibel L., Moeller A., Vega-Warner V., Waters A., He Y., Anikster Y., Esser P., Straub B.K., Hausser I., Bockenhauer D., Dekel B., Hildebrandt F., Bruckner-Tuderman L., Laube G.F. Integrin alpha3 mutations with kidney, lung, and skin disease. N. Engl. J. Med. 2012, 366:1508-1514.
22. He Y., Esser P., Heinemann A., Bruckner-Tuderman L., Has C. Kindlin-1 and -2 have overlapping functions in epithelial cells implications for phenotype modification. Am. J. Pathol. 2011, 178:975-982.
23. Heinemann A., He Y., Zimina E., Boerries M., Busch H., Chmel N., Kurz T., Bruckner-Tuderman L., Has C. Induction of phenotype modifying cytokines by FERMT1 mutations. Hum. Mutat. 2011, 32:397-406.
24. Hohenester E., Yurchenco P.D. Laminins in basement membrane assembly. Cell Adhes. Migr. 2013, 7:56-63.
25. Jobard F., Bouadjar B., Caux F., Hadj-Rabia S., Has C., Matsuda F., Weissenbach J., Lathrop M., Prud'homme J.F., Fischer J. Identification of mutations in a new gene encoding a FERM family protein with a pleckstrin homology domain in Kindler syndrome. Hum. Mol. Genet. 2003, 12:925-935.
26. Keene D.R., Sakai L.Y., Lunstrum G.P., Morris N.P., Burgeson R.E. Type VII collagen forms an extended network of anchoring fibrils. J. Cell Biol. 1987, 104:611-621.
27. Kern J.S., Loeckermann S., Fritsch A., Hausser I., Roth W., Magin T.M., Mack C., Muller M.L., Paul O., Ruther P., Bruckner-Tuderman L. Mechanisms of fibroblast cell therapy for dystrophic epidermolysis bullosa: high stability of collagen VII favors long-term skin integrity. Mol. Ther. 2009, 17:1605-1615.
28. Kiritsi D., Kern J.S., Schumann H., Kohlhase J., Has C., Bruckner-Tuderman L. Molecular mechanisms of phenotypic variability in junctional epidermolysis bullosa. J. Med. Genet. 2011, 48:450-457.
29. Kiritsi D., He Y., Pasmooij A.M., Onder M., Happle R., Jonkman M.F., Bruckner-Tuderman L., Has C. Revertant mosaicism in a human skin fragility disorder results from slipped mispairing and mitotic recombination. J. Clin. Invest. 2012, 122:1742-1746.
30. Kuttner V., Mack C., Rigbolt K.T., Kern J.S., Schilling O., Busch H., Bruckner-Tuderman L., Dengjel J. Global remodelling of cellular microenvironment due to loss of collagen VII. Mol. Syst. Biol. 2013, 9:657.
31. Lai-Cheong J.E., McGrath J.A. Kindler syndrome. Dermatol. Clin. 2010, 28:119-124.
32. Lai-Cheong J.E., Ussar S., Arita K., Hart I.R., McGrath J.A. Colocalization of kindlin-1, kindlin-2, and migfilin at keratinocyte focal adhesion and relevance to the pathophysiology of Kindler syndrome. J. Invest. Dermatol. 2008, 128:2156-2165.
33. Lai-Cheong J.E., Moss C., Parsons M., Almaani N., McGrath J.A. Revertant mosaicism in Kindler syndrome. J. Invest. Dermatol. 2012, 132:730-732.
34. Laimer M., Lanschuetzer C.M., Diem A., Bauer J.W. Herlitz junctional epidermolysis bullosa. Dermatol. Clin. 2010, 28:55-60.
35. Margadant C., Charafeddine R.A., Sonnenberg A. Unique and redundant functions of integrins in the epidermis. FASEB J. 2010, 24:4133-4152.
36. Margadant C., Kreft M., de Groot D.J., Norman J.C., Sonnenberg A. Distinct roles of talin and kindlin in regulating integrin alpha5beta1 function and trafficking. Curr. Biol. 2012, 22:1554-1563.
37. Margadant C., Kreft M., Zambruno G., Sonnenberg A. Kindlin-1 regulates integrin dynamics and adhesion turnover. PLoS One 2013, 8:e65341.
38. Mavilio F., Pellegrini G., Ferrari S., Di Nunzio F., Di Iorio E., Recchia A., Maruggi G., Ferrari G., Provasi E., Bonini C., Capurro S., Conti A., Magnoni C., Giannetti A., De Luca M. Correction of junctional epidermolysis bullosa by transplantation of genetically modified epidermal stem cells. Nat. Med. 2006, 12:1397-1402.
39. McLean W.H., Irvine A.D., Hamill K.J., Whittock N.V., Coleman-Campbell C.M., Mellerio J.E., Ashton G.S., Dopping-Hepenstal P.J., Eady R.A., Jamil T., Phillips R., Shabbir S.G., Haroon T.S., Khurshid K., Moore J.E., Page B., Darling J., Atherton D.J., Van Steensel M.A., Munro C.S., Smith F.J., McGrath J.A. An unusual N-terminal deletion of the laminin alpha3a isoform leads to the chronic granulation tissue disorder laryngo-onycho-cutaneous syndrome. Hum. Mol. Genet. 2003, 12:2395-2409.
40. Mikesh L.M., Aramadhaka L.R., Moskaluk C., Zigrino P., Mauch C., Fox J.W. Proteomic anatomy of human skin. J. Proteome 2013, 84:190-200.
41. Nicolaou N., Margadant C., Kevelam S.H., Lilien M.R., Oosterveld M.J., Kreft M., van Eerde A.M., Pfundt R., Terhal P.A., van der Zwaag B., Nikkels P.G., Sachs N., Goldschmeding R., Knoers N.V., Renkema K.Y., Sonnenberg A. Gain of glycosylation in integrin alpha3 causes lung disease and nephrotic syndrome. J. Clin. Invest. 2012, 122:4375-4387.
42. Nyström A., Velati D., Mittapalli V.R., Kern J.S., Fritsch A., Bruckner-Tuderman L. Collagen VII plays a dual role in wound healing. J. Clin. Invest. 2013, 123:3498-3509.
43. Pacho F., Zambruno G., Calabresi V., Kiritsi D., Schneider H. Efficiency of translation termination in humans is highly dependent upon nucleotides in the neighbourhood of a (premature) termination codon. J. Med. Genet. 2011, 48:640-644.
44. Pasmooij A.M., Garcia M., Escamez M.J., Nijenhuis A.M., Azon A., Cuadrado-Corrales N., Jonkman M.F., Del Rio M. Revertant mosaicism due to a second-site mutation in COL7A1 in a patient with recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 2010, 130:2407-2411.
45. Pasmooij A.M., Jonkman M.F., Uitto J. Revertant mosaicism in heritable skin diseases - mechanisms of natural gene therapy. Discov. Med. 2012, 14:167-179.
46. Pasmooij A.M., Nijenhuis M., Brander R., Jonkman M.F. Natural gene therapy may occur in all patients with generalized non-Herlitz junctional epidermolysis bullosa with COL17A1 mutations. J. Invest. Dermatol. 2012, 132:1374-1383.
47. Poulter J.A., El-Sayed W., Shore R.C., Kirkham J., Inglehearn C.F., Mighell A.J. Whole-exome sequencing, without prior linkage, identifies a mutation in LAMB3 as a cause of dominant hypoplastic amelogenesis imperfecta. Eur. J. Hum. Genet. 2013, (Epub).
48. Pruneddu S., Castiglia D., Floriddia G., Cottoni F., Zambruno G. COL7A1 Recessive mutations in two siblings with distinct subtypes of dystrophic epidermolysis bullosa: pruriginosa versus nails only. Dermatology 2011, 222:10-14.
49. Qu H., Wen T., Pesch M., Aumailley M. Partial loss of epithelial phenotype in kindlin-1-deficient keratinocytes. Am. J. Pathol. 2012, 180:1581-1592.
50. Remington J., Wang X., Hou Y., Zhou H., Burnett J., Muirhead T., Uitto J., Keene D.R., Woodley D.T., Chen M. Injection of recombinant human type VII collagen corrects the disease phenotype in a murine model of dystrophic epidermolysis bullosa. Mol. Ther. 2009, 17:26-33.
51. Schmidt E., Zillikens D. Pemphigoid diseases. Lancet 2013, 381:320-332.
52. Schumann H., Kiritsi D., Pigors M., Hausser I., Kohlhase J., Peters J., Ott H., Hyla-Klekot L., Gacka E., Sieron A.L., Valari M., Bruckner-Tuderman L., Has C. Phenotypic spectrum of epidermolysis bullosa associated with alpha6beta4 integrin mutations. Br. J. Dermatol. 2013, 169:115-124.
53. Siegel D.H., Ashton G.H., Penagos H.G., Lee J.V., Feiler H.S., Wilhelmsen K.C., South A.P., Smith F.J., Prescott A.R., Wessagowit V., Oyama N., Akiyama M., Al Aboud D., Al Aboud K., Al Githami A., Al Hawsawi K., Al Ismaily A., Al-Suwaid R., Atherton D.J., Caputo R., Fine J.D., Frieden I.J., Fuchs E., Haber R.M., Harada T., Kitajima Y., Mallory S.B., Ogawa H., Sahin S., Shimizu H., Suga Y., Tadini G., Tsuchiya K., Wiebe C.B., Wojnarowska F., Zaghloul A.B., Hamada T., Mallipeddi R., Eady R.A., McLean W.H., McGrath J.A., Epstein E.H. Loss of kindlin-1, a human homolog of the Caenorhabditis elegans actin-extracellular-matrix linker protein UNC-112, causes Kindler syndrome. Am. J. Hum. Genet. 2003, 73:174-187.
54. Sterk L.M., Geuijen C.A., Oomen L.C., Calafat J., Janssen H., Sonnenberg A. The tetraspan molecule CD151, a novel constituent of hemidesmosomes, associates with the integrin alpha6beta4 and may regulate the spatial organization of hemidesmosomes. J. Cell Biol. 2000, 149:969-982.
55. Titeux M., Pendaries V., Tonasso L., Decha A., Bodemer C., Hovnanian A. A frequent functional SNP in the MMP1 promoter is associated with higher disease severity in recessive dystrophic epidermolysis bullosa. Hum. Mutat. 2008, 29:267-276.
56. Tolar J., Blazar B.R., Wagner J.E. Concise review: Transplantation of human hematopoietic cells for extracellular matrix protein deficiency in epidermolysis bullosa. Stem Cells 2011, 29:900-906.
57. Uitto J. Milestones in genetics of structural skin disorders. J. Invest. Dermatol. 2012, 132:E1.
58. Uitto J. Molecular therapeutics for heritable skin diseases. J. Invest. Dermatol. 2012, 132:E29-E34.
59. Uitto J. Rare heritable skin diseases: targets for regenerative medicine. J. Invest. Dermatol. 2012, 132:2485-2488.
60. Ussar S., Moser M., Widmaier M., Rognoni E., Harrer C., Genzel-Boroviczeny O., Fassler R. Loss of kindlin-1 causes skin atrophy and lethal neonatal intestinal epithelial dysfunction. PLoS Genet. 2008, 4:e1000289.
61. Van Agtmael T., Bruckner-Tuderman L. Basement membranes and human disease. Cell Tissue Res. 2010, 339:167-188.
62. Van den Bergh F., Eliason S.L., Burmeister B.T., Giudice G.J. Collagen XVII (BP180) modulates keratinocyte expression of the proinflammatory chemokine, IL-8. Exp. Dermatol. 2012, 21:605-611.
63. Vanacore R.M., Shanmugasundararaj S., Friedman D.B., Bondar O., Hudson B.G., Sundaramoorthy M. The alpha1.alpha2 network of collagen IV. Reinforced stabilization of the noncollagenous domain-1 by noncovalent forces and the absence of Met-Lys cross-links. J. Biol. Chem. 2004, 279:44723-44730.
64. Villone D., Fritsch A., Koch M., Bruckner-Tuderman L., Hansen U., Bruckner P. Supramolecular interactions in the dermo-epidermal junction zone: anchoring fibril-collagen VII tightly binds to banded collagen fibrils. J. Biol. Chem. 2008, 283:24506-24513.
65. Wagner J.E., Ishida-Yamamoto A., McGrath J.A., Hordinsky M., Keene D.R., Woodley D.T., Chen M., Riddle M.J., Osborn M.J., Lund T., Dolan M., Blazar B.R., Tolar J. Bone marrow transplantation for recessive dystrophic epidermolysis bullosa. N. Engl. J. Med. 2010, 363:629-639.
66. Wiche G., Winter L. Plectin isoforms as organizers of intermediate filament cytoarchitecture. BioArchitecture 2011, 1:14-20.
67. Wong T., Gammon L., Liu L., Mellerio J.E., Dopping-Hepenstal P.J., Pacy J., Elia G., Jeffery R., Leigh I.M., Navsaria H., McGrath J.A. Potential of fibroblast cell therapy for recessive dystrophic epidermolysis bullosa. J. Invest. Dermatol. 2008, 128:2179-2189.
68. Woodley D.T., Wang X., Amir M., Hwang B., Remington J., Hou Y., Uitto J., Keene D., Chen M. Intravenously injected recombinant human type vii collagen homes to skin wounds and restores skin integrity of dystrophic epidermolysis bullosa. J. Invest. Dermatol. 2013, 133:1910-1913.
69. Yancey K.B., Hintner H. Non-Herlitz junctional epidermolysis bullosa. Dermatol. Clin. 2010, 28:67-77.
70. Yuen W.Y., Duipmans J.C., Molenbuur B., Herpertz I., Mandema J.M., Jonkman M.F. Long-term follow-up of patients with Herlitz-type junctional epidermolysis bullosa. Br. J. Dermatol. 2012, 167:374-382.
71. Yuen W.Y., Sinke R.J., Jonkman M.F. ITGB4-associated non-Herlitz junctional epidermolysis bullosa: report of two new cases carrying two novel ITGB4 mutations. Br. J. Dermatol. 2013, 168:432-434.