Dystrophic epidermolysis bullosa

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1 Dystrophic epidermolysis bullosa Novel insights into the genotype-phenotype correlation and somatic mosaicism Peter C. van den Akker

2 Publication of this thesis was financially supported by: Graduate School of Medical Sciences of the UMCG University of Groningen Shire Mölnlycke Healthcare MediZorg BV Rochester Medical BV Greiner Bio-One BV Urgo Medical Netherlands BV DEBRA Nederland Stichting Vlinderkind Their support is gratefully acknowledged. Cover image: Butterfly, Greetje van den Akker, 2013 (www.greetjevdakker.exto.nl) Cover design: Peter van den Akker, Optima Grafische Communicatie Layout and printing: Optima Grafische Communicatie, Rotterdam, the Netherlands (www.ogc. nl) Copyright: Peter van den Akker, 2013 All rights reserved. No part of this thesis may be reproduced in any form or by any means, electronic, mechanical, by photocopying, or otherwise, without prior written permission of the author. The copyrights of the publications remain with the publisher, unless stated otherwise. The research described in this thesis was supported by a grant from the Netherlands Organization for Health Research and Development (ZonMw AGIKO stipendium, grant ). Financial support from the J.P. Nater Foundation, the Simons-foundation, the J.C. de Cock foundation, and Stichting Vlinderkind (Dutch Butterfly Child foundation) for parts of the studies described in this thesis is gratefully acknowledged. ISBN: (E-book)

3 Dystrophic epidermolysis bullosa Novel insights into the genotype-phenotype correlation and somatic mosaicism Proefschrift ter verkrijging van het doctoraat in de Medische Wetenschappen aan de Rijksuniversiteit Groningen op gezag van de Rector Magnificus, dr. E. Sterken, in het openbaar te verdedigen op woensdag 6 november 2013 om uur door Peter Christiaan van den Akker geboren op 6 juli 1979 te Rotterdam

4 Promotores: Beoordelingscommissie: Prof. dr. M.F. Jonkman Prof. dr. R.M.W. Hofstra Prof. J.A. McGrath Prof. dr. M.A.M. van Steensel Prof. dr. R.H. Sijmons

5 Paranimfen: Marieke Bolling Marjon Pasmooij To all butterfly children

6 Stellingen behorend bij het proefschrift Dystrophic epidermolysis bullosa Novel insights into the genotype-phenotype correlation and somatic mosaicism 1. In de 2007 consensus classificatie mist een late-onset severe generalized fenotype van recessieve dystrofische epidermolysis bullosa (dit proefschrift). 2. Het inversa subtype van recessieve dystrofische epidermolysis bullosa wordt veroorzaakt door een specifieke set van recessieve arginine en glycine substituties in het triple-helix domein van type VII collageen (dit proefschrift). 3. Behoudens dat dominante glycine substituties in COL7A1 dominante dystrofische epidermolysis bullosa veroorzaken, bestaat er geen duidelijke genotype-fenotype correlatie voor dit ziektebeeld (dit proefschrift). 4. Een vrij toegankelijke online database waarin de genotypische en fenotypische kenmerken van alle patiënten met dystrofische epidermolysis bullosa zijn opgenomen is essentieel voor genetische counseling (dit proefschrift). 5. Alle patiënten met een recessieve vorm van epidermolysis bullosa hebben revertante cellen; de kunst is alleen om die cellen te vinden (dit proefschrift). 6. Revertante keratinocyten hebben binnen een tijdsvenster tijdens de ontwikkeling van het individu een enorm groeivoordeel ten opzichte van hun mutante buren (dit proefschrift). 7. In families met dystrofische epidermolysis bullosa waarin geen COL7A1 mutaties gevonden worden heeft het geen zin om met next generation sequencing technieken op zoek te gaan naar nieuwe genen (dit proefschrift). 8. Door het bestuderen van families met mendeliaans overervende aandoeningen kunnen genen geïdentificeerd worden die een belangrijke rol spelen in de pathogenese van hun complexe evenknie (Jordan et al., AJHG 2012;90:784). 9. Er moet meer aandacht uitgaan naar het verbeteren van in silico predictie, aangezien het verrichten van een functionele test voor elke potentieel pathogene variant die met whole exome en genome sequencing gedetecteerd wordt niet doenlijk is.

7 10. De introductie van targeted next generation sequencing huidpanels in de diagnostiek zal bij een substantieel groter deel van de patiënten met heterogene genodermatosen tot een diagnose leiden. 11. De klinisch geneticus van de toekomst is een superspecialist die werkzaam is op het grensvlak met een ander specialisme en betrokken zal zijn bij de behandeling van erfelijke aandoeningen. 12. The beginning of knowledge is the discovery of something we don t understand (Frank Herbert). 13. Elke formule in een boek halveert het aantal lezers (Stephen Hawking). 14. Geen tijd hebben bestaat niet; als je geen tijd hebt, moet je beter plannen (Roel Hordijk). 15. De helft van de bakerpraatjes voorspelt het geslacht van een ongeboren kind juist (ongepubliceerd proefondervindelijk onderzoek). Peter van den Akker Groningen, 6 november 2013

8 Table of contents Stellingen 6 List of abbreviations 10 Chapter 1 Introduction 13 General Introduction 15 Dystrophic epidermolysis bullosa 26 Part One: the genotype-phenotype correlation for dystrophic 30 epidermolysis bullosa Part Two: somatic mosaicism in dystrophic epidermolysis bullosa 37 Aims and outline of the thesis 44 Chapter 2 Historical perspective on dystrophic epidermolysis bullosa 61 Chapter 3 Design and validation of a Conformation-Sensitive Capillary Electrophoresis system for mutation identification of the COL7A1 gene with automated peak comparison Genet Test Mol Biomarkers. 2009;13(5): Part One The genotype-phenotype correlation for dystrophic epidermolysis bullosa 99 Chapter 4 Long-term follow-up of patients with recessive dystrophic epidermolysis bullosa in the Netherlands: expansion of the mutation database and unusual phenotype-genotype correlations. J Dermatol Sci. 2009;56(1): Chapter 5 The inversa type of recessive dystrophic epidermolysis bullosa is caused by specific arginine and glycine substitutions in type VII collagen. J Med Genet. 2011;48(3): Chapter 6 The genotype-phenotype correlation in dominant dystrophic epidermolysis bullosa. 161

9 Chapter 7 The International Dystrophic Epidermolysis Bullosa Patient Registry: an online database of dystrophic epidermolysis bullosa patients and their COL7A1 mutations. Hum Mutat. 2011;32(10): Part Two Somatic mosaicism in dystrophic epidermolysis bullosa 211 Chapter 8 Somatic mosaicism for the COL7A1 mutation p.gly2034arg in the unaffected mother of a patient with dystrophic epidermolysis bullosa pruriginosa. 213 Chapter 9 Natural gene therapy in dystrophic epidermolysis bullosa. Arch Dermatol. 2012;148(2): Chapter 10 A late-but-fitter revertant cell explains the high frequency of revertant mosaicism in epidermolysis bullosa. 235 Chapter 11 Discussion and future perspectives 249 Summary 281 Nederlandse samenvatting 291 Dankwoord/Acknowledgements 303 List of author affiliations 314 List of publications 317 Curriculum vitae 321

10 List of abbreviations AD autosomal dominant AFs anchoring fibrils AON antisense oligonucleotide APSS acral peeling skin syndrome AR autosomal recessive AR-EBS autosomal recessive EBS AS arginine substitution BDN bullous dermolysis of the newborn BK basal keratinocyte BMP bone morphogenetic protein BMP-1 bone morphogenetic protein-1 (also type 1 procollagen C-proteinase) BMZ basement membrane zone bp base pair BP180 bullous pemphigoid 180, also type XVII collagen BP230 bullous pemphigoid 230 BPAG1-e epidermal isoform of bullous pemphigoid antigen-1 cdna complementary DNA CLAS congenital localized absence of skin COL collagenous subdomain in triple-helix domain COLVII type VII collagen CSCE conformation-sensitive capillary electrophoresis DDEB dominant dystrophic epidermolysis bullosa DDEB-ac DDEB, acral type DDEB-gen DDEB, generalized type DDEB-na DDEB, nails only type DDEB-Pr DDEB, pruriginosa type DDEB-Pt DDEB, pretibial type DEB dystrophic epidermolysis bullosa DEB-Pr DEB, pruriginosa type DEB-u DEB, unknown subtype DEJ dermo-epidermal junction DGGE denaturing gradient gel electrophoresis EB epidermolysis bullosa EBS epidermolysis bullosa simplex EM electron microscopy ESE exonic-splicing enhancer FFH-1 fermitin family homologue-1 (also kindlin-1) Gly-Xaa-Yaa / Gly-X-Y amino acid triplet repeat starting with glycine GS glycine substitution

11 HGMD IF IM ipsc IVS JEB JEB-H JEB-lo JEB-nH JEB-nH-gen KS LOVD moab MMP-1 NC1 NC2 NMD OMIM / MIM PCR PGD pro-α1(vii) peptide PTC RDEB RDEB-HS RDEB-I RDEB-nHS RDEB-O RDEB-O+Ps RDEB-sev gen RDEB-u REB RM SCC SNP THD UMCG Human Gene Mutation Database immunofluorescence imperfection in triple-helix domain induced pluripotent stem cell intervening sequence (i.e. intron) junctional epidermolysis bullosa JEB, Herlitz type JEB, late-onset type JEB, non-herlitz type generalized JEB, non-herlitz type Kindler syndrome Leiden Open Variation Database (www.lovd.nl) monoclonal antibody matrix metalloproteinase-1 amino-terminal non-collagenous 1 domain of type VII collagen carboxyl-terminal non-collagenous 2 domain of type VII collagen nonsense-mediated mrna decay (Online) Mendelian Inheritance of Man catalog (www.omim.org) polymerase chain reaction pre-implantation genetic diagnosis type VII collagen α1 precursor chain premature termination codon recessive dystrophic epidermolysis bullosa RDEB, Hallopeau-Siemens RDEB, inversa RDEB, non-hallopeau-siemens RDEB, generalized other RDEB, generalized other with pseudosyndactyly RDEB, severe generalized RDEB, unknown subtype recessive EB revertant mosaicism squamous cell carcinoma single nucleotide polymorphism triple-helix domain University Medical Center Groningen

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