ArticleAmerican journal of human genetics2026
Clinical, in vitro, and in vivo evidence of WAPL as a cohesinopathy-associated gene and phenotypic driver of 10q22.3q23.2 genomic disorder.
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151 authors.
Philip M BooneDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA; Cornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA; Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA. Electronic address: philip.boone@childrens.harvard.edu.
Serkan ErdinCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Abucar MohamedSection on Epigenetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD, USA.
Sadegheh HaghshenasVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Kamli N W FaourDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA.
Emeline KaoInstitutional Centers for Clinical and Translational Research, Boston Children's Hospital, Boston, MA, USA.
Jack FuCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Chiara AuwerxCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USA.
Ricardo HarripaulCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Bimal JanaCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Danielle SpringerMurine Phenotyping Core Facility, National Heart Lung and Blood Institute, Bethesda, MD, USA.
Grey HallstromEpigenetics Institute, University of Pennsylvania School of Medicine, Philadelphia, PA, USA.
Celine E F de EschCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Erica DenhoffInstitutional Centers for Clinical and Translational Research, Boston Children's Hospital, Boston, MA, USA.
Lauren HolmesInstitutional Centers for Clinical and Translational Research, Boston Children's Hospital, Boston, MA, USA.
Kiana MohajeriCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
John LemanskiCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Jennifer KerkhofVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Haley McConkeyVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Jessica RzasaVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Madison J McCuneCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Michael A LevyVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Julia GrafsteinSection on Epigenetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD, USA.
Matthew LarsonCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Zsabre WrightCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Roberta L BeauchampCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Diane LucenteCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Rami Abou JamraUniversity of Leipzig Medical Center, Leipzig, Germany.
Neena AgrawalPediatric Genetics and Genomic Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
Pankaj B AgrawalThe Manton Center for Orphan Disease Research, Boston Children's Hospital, Boston, MA, USA.
Erica F AndersenARUP Laboratories, Salt Lake City, UT, USA.
Emanuela ArgilliUniversity of California, San Francisco, San Francisco, CA, USA.
Renee AraizaMutant Mouse Resource and Research Center, University of California, Davis, Davis, CA, USA.
Sonia BallalCornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA; Division of Gastroenterology, Boston Children's Hospital, Boston, MA, USA.
Megan F BaxterCentre for Human Genetics and Oxford NIHR Biomedical Research Centre, University of Oxford, Oxford, UK; Guy's and St Thomas' Hospital, London, UK.
Gaber BergantClinical Institute for Genomic Medicine, UMC Ljubljana, Ljubljana, Slovenia.
Astrid BertscheDepartment of Pediatric Neurology and Inherited Metabolic Diseases, University Medicine Greifswald, Greifswald, Germany.
Riya BhavsarCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Debora R BortolaHuman Genome and Stem Cell Research Center, Department of Genetics and Evolutionary Biology of the Institute of Biosciences, Universidade de São Paulo, Sao Paulo, Brazil; Unidade de Genética, Instituto da Criança, Hospital das Clínicas da Faculdade de Medicina, Universidade de São Paulo, Sao Paulo, Brazil.
Viktoria BotheUniversity of Leipzig Medical Center, Leipzig, Germany.
Charlotte Brasch-AndersenDepartment of Clinical Genetics, Odense University Hospital, Odense, Denmark.
Dominique BraunDepartment of Human Genetics, Inselspital Bern, University of Bern, Bern, Switzerland.
Ange-Line BruelUniversité Bourgogne Europe, CHU Dijon Bourgogne, Laboratoire de Génomique Médicale, Centre Neomics, FHU-TRANSLAD, Centre de recherche Translationnelle en Médecine moléculaire - Inserm UMR1231, equipe GAD, Dijon, France.
Catherine BuchananDell Children's Medical Group, Austin, TX, USA.
Nicholas D BurtCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Laura M L CarvalhoHuman Genome and Stem Cell Research Center, Department of Genetics and Evolutionary Biology of the Institute of Biosciences, Universidade de São Paulo, Sao Paulo, Brazil.
Luigi ChiriattiMolecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
Benjamin CogneService de Génétique Médicale, CHU Nantes, Nantes Université, CNRS, INSERM, l'institut du thorax, Nantes, France.
Ryan CollinsCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Amy CrunkGeneDx, LLC, Gaithersburg, MD, USA.
Benjamin CurrallCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Andree Delahaye-DuriezUnité Fonctionnelle de Médecine Génomique et Génétique Clinique, Hôpital Jean Verdier, Assistance Publique - Hôpitaux de Paris, Université Sorbonne Paris Nord, Bondy, France.
Julian DelanneInserm, CTM UMR1231, equipe GAD, FHU TRANSLAD, Centre de génétique, Centre de référence Anomalies du Développement et Syndromes Malformatifs, Centre de référence Déficiences Intellectuelles de Causes Rares, et Centre de référence GénoPsy, FHU TRANSLAD, Equipe GAD INSERM UMR1231, Université Bourgogne Europe, CHU Dijon Bourgogne, Inserm, Dijon, France.
Anne-Sophie Denommé-PichonUniversité Bourgogne Europe, CHU Dijon Bourgogne, Laboratoire de Génomique Médicale, Centre Neomics, FHU-TRANSLAD, Centre de recherche Translationnelle en Médecine moléculaire - Inserm UMR1231, equipe GAD, Dijon, France.
Koenraad DevriendtUZ Leuven, Leuven, Belgium.
Aloysius DomingoCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Laura DuncanMedical Genetics and Genomic Medicine, Vanderbilt University Medical Center, Nashville, TN, USA.
Laurence FaivreInserm, CTM UMR1231, equipe GAD, FHU TRANSLAD, Centre de génétique, Centre de référence Anomalies du Développement et Syndromes Malformatifs, Centre de référence Déficiences Intellectuelles de Causes Rares, et Centre de référence GénoPsy, FHU TRANSLAD, Equipe GAD INSERM UMR1231, Université Bourgogne Europe, CHU Dijon Bourgogne, Inserm, Dijon, France.
Laura FamularoPediatric Genetics, University of Virginia School of Medicine, Charlottesville, VA, USA.
Anne FultonCornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA.
Casie A GenettiDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA; The Manton Center for Orphan Disease Research, Boston Children's Hospital, Boston, MA, USA.
Tamar HarelDepartment of Genetics, Hadassah Medical Center, Jerusalem, Israel; Faculty of Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
Marketa HavlovicovaDepartment of Biology and Medical Genetics, Second Faculty of Medicine, Charles University and Motol and Homolka University Hospital, Prague, Czechia.
Jenny HiggsLiverpool Centre for Genomic Medicine, Liverpool Women's NHS Foundation Trust, Liverpool, UK.
Marine HoulierAssistance Publique, Hôpitaux de Paris, Paris, France.
Maria IasconeMedical Genetics Lab, ASST Papa Giovanni XXIII, Bergamo, Italy.
LaDonna ImmkenDell Children's Medical Group, Austin, TX, USA.
Bertrand IsidorCHU Nantes, Nantes Université, CNRS, INSERM, l'institut du thorax, Nantes, France.
Frank J KaiserInstitute of Human Genetics, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.
Kaycee KarboneDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA.
Margaret KennaCornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA.
Amjad KhanFaculty of Biological Sciences, Department of Zoology, University of Lakki Marwat, Khyber Pakhtunkhwa, Pakistan.
Lara Kristina KimmigInstitute of Human Genetics, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.
Tjitske KleefstraRadboud University Medical Center, Nijmegen, the Netherlands.
Eva-Maria KrausInstitute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.
Ana C V KrepischiHuman Genome and Stem Cell Research Center, Department of Genetics and Evolutionary Biology of the Institute of Biosciences, Universidade de São Paulo, Sao Paulo, Brazil.
Ilona KreyInstitute of Human Genetics, Hebrew University of Jerusalem, Jerusalem, Israel.
Roger L LaddaDepartment of Pediatrics, Penn State Health Children's Hospital, Hershey, PA, USA.
Louise LanoueMouse Biology Program, University of California, Davis, Davis, CA, USA.
Cedric Le CaignecNantes University Hospital Center, Nantes, France.
Zoe K LewisARUP Laboratories, Salt Lake City, UT, USA.
Gloria LimaTCR2 Therapeutics, Cambridge, MA, USA.
Sally Ann LynchChildren's Health Ireland at Crumlin, Dublin, Ireland.
Milan MacekDepartment of Biology and Medical Genetics, Second Faculty of Medicine, Charles University and Motol and Homolka University Hospital, Prague, Czechia.
Olivier MaierStiftung Ostschweizer Kinderspital, KER-Zentrum, St. Gallen, Switzerland.
Silvia MaitzService of Medical Genetics, Oncologic Institute of Southern Switzerland, EOC, Lugano, Switzerland.
Alison MaleGreat Ormond Street Hospital for Children, London, UK.
Marcela MalikovaDepartment of Biology and Medical Genetics, Second Faculty of Medicine, Charles University and Motol and Homolka University Hospital, Prague, Czechia.
Victoria McKayLiverpool Women's NHS Foundation Trust, Liverpool, UK.
Oana MoldovanHospital de Santa Maria, CHULN, Lisbon, Portugal.
Danielle MonteilNaval Medical Center, Portsmouth, VA, USA.
Mariana Moysés OliveiraCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Jeeva MunasingheMouse Imaging Facility, National Institute of Neurological Disorders and Stroke, Bethesda, MD, USA.
Sachiko NakamoriMurine Phenotyping Core Facility, National Heart Lung and Blood Institute, Bethesda, MD, USA.
Sonja NeuserInstitute of Human Genetics, University of Leipzig Medical Center, Leipzig, Germany.
Mathilde NizonService de Génétique Médicale, CHU Nantes, Nantes Université, CNRS, INSERM, l'institut du thorax, Nantes, France.
Xander NuttleCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Kathryn O'KeefeCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Laura OrecHeidelberg University, Medical Faculty of Heidelberg, Department of Pediatrics I, Division of Pediatric Neurology and Metabolic Medicine, Heidelberg, Germany.
Ilaria ParentiInstitute of Human Genetics, University Hospital Essen, University of Duisburg-Essen, Essen, Germany.
Borut PeterlinClinical Institute for Genomic Medicine, UMC Ljubljana, Ljubljana, Slovenia.
Rolph PfundtRadboud University Medical Center, Nijmegen, the Netherlands.
Jill PounceyChildren's Hospital at Erlanger, Chattanooga, TN, USA.
Francesca Clementina RadioMolecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
Leema RobertGuy's and St Thomas' Hospital, London, UK.
Lance RodanDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA.
Hallel Rosenberg-FoglerDepartment of Genetics, Hadassah Medical Center, Jerusalem, Israel.
Jill A RosenfeldBaylor College of Medicine, Houston, TX, USA; Baylor Genetics Laboratories, Houston, TX, USA.
Hana SafraouUniversité Bourgogne Europe, CHU Dijon Bourgogne, Laboratoire de Génomique Médicale, Centre Neomics, FHU-TRANSLAD, Centre de recherche Translationnelle en Médecine moléculaire - Inserm UMR1231, equipe GAD, Dijon, France.
Monica SalaniCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Sophia SchliesskeUniversity of Leipzig Medical Center, Leipzig, Germany.
Eleanor G SeabyTranslational Genomics Group, Broad Institute of Harvard and MIT, Boston, MA, USA; Department of Paediatrics, Imperial College London, London, UK; Human Developmental and Health, University of Southampton, Southampton, UK.
Susan L SellDepartment of Pediatrics, Penn State Health Children's Hospital, Hershey, PA, USA.
A Eliot ShearerCornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA.
Elliott SherrUniversity of California, San Francisco, San Francisco, CA, USA.
Amelle ShillingtonCincinnati Children's Hospital Medical Center, Cincinnati, OH, USA.
Dorothea SieboldVanderbilt University Medical Center, Nashville, TN, USA.
Margje SinnemaMaastricht University Medical Center+, Maastricht, the Netherlands.
Laura SmithCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA.
Alexander P A StegmannMaastricht University Medical Center+, Maastricht, the Netherlands.
Cathy A StevensUniversity of Tennessee College of Medicine, Chattanooga, TN, USA.
Servi J C StevensMaastricht University Medical Center+, Maastricht, the Netherlands.
Eric SuretteBoston College, Newton, MA, USA.
Marco TartagliaMolecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, Rome, Italy.
Jenny C TaylorCentre for Human Genetics and Oxford NIHR Biomedical Research Centre, University of Oxford, Oxford, UK.
Michelle L ThompsonHudsonAlpha Institute for Biotechnology, Huntsville, AL, USA.
Pernille M TørringOdense University Hospital, Odense, Denmark.
Frederic Tran Mau ThemUniversité Bourgogne Europe, CHU Dijon Bourgogne, Laboratoire de Génomique Médicale, Centre Neomics, FHU-TRANSLAD, Centre de recherche Translationnelle en Médecine moléculaire - Inserm UMR1231, equipe GAD, Dijon, France.
Olga TsoulakiManchester University Hospitals Foundation Trust, Manchester, UK.
Muhammad UmairDepartment of Life Sciences, School of Science, University of Management and Technology, Lahore, Pakistan; Medical Genomics Research Department, King Abdullah International Medical Research Center, King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Els VanhoutteMaastricht University Medical Center+, Maastricht, the Netherlands.
Marie VincentService de Génétique Médicale, CHU Nantes, Nantes Université, CNRS, INSERM, l'institut du thorax, Nantes, France.
Antonio VitobelloUniversité Bourgogne Europe, CHU Dijon Bourgogne, Laboratoire de Génomique Médicale, Centre Neomics, FHU-TRANSLAD, Centre de recherche Translationnelle en Médecine moléculaire - Inserm UMR1231, equipe GAD, Dijon, France.
Lydia von WintzingerodeUniversity of Leipzig Medical Center, Leipzig, Germany.
Amy WattTCR2 Therapeutics, Cambridge, MA, USA.
Marketa WayhelovaDepartment of Biology and Medical Genetics, Second Faculty of Medicine, Charles University and Motol and Homolka University Hospital, Prague, Czechia.
Ingrid M WentzensenGeneDx, LLC, Gaithersburg, MD, USA.
William WilsonPediatric Genetics, University of Virginia School of Medicine, Charlottesville, VA, USA.
Monica H WojcikDivision of Genetics and Genomics, Boston Children's Hospital, Boston, MA, USA; Division of Newborn Medicine, Boston Children's Hospital, Boston, MA, USA.
Bo YuanBaylor College of Medicine, Houston, TX, USA.
Giuseppe ZampinoCenter for Rare Diseases, Department of Human and Child Health and Public Health, Fondazione Policlinico Universitario A. Gemelli, Rome, Italy.
Siddharth SrivastavaCornelia de Lange Syndrome and Related Disorders Clinic, Boston Children's Hospital, Boston, MA, USA; Division of Neurogenetics and Neurodevelopment, Department of Neurology, Boston Children's Hospital, Boston, MA, USA.
Dominik S WestphalInstitute of Human Genetics, Landeskrankenhaus University Hospital, Paracelsus Medical Private University, Salzburg, Austria.
Korbinian M RiedhammerInstitute of Human Genetics, Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich, Munich, Germany; Department of Nephrology, Klinikum rechts der Isar, School of Medicine and Health, Technical University of Munich, Munich, Germany; Department of Pediatrics, Division of Nephrology, Boston Children's Hospital, Harvard Medical School, Boston, MA, USA; Institute of Anatomy, Medical Faculty, University of Bonn, Bonn, Germany.
Eric JoyceEpigenetics Institute, University of Pennsylvania School of Medicine, Philadelphia, PA, USA.
Rachita YadavCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
James F GusellaCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA; Molecular Neurogenetics Unit, Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Department of Genetics, Blavatnik Institute, Harvard Medical School, Boston, MA, USA.
Derek J C TaiCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA.
Bekim SadikovicVerspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON, Canada.
Karl E PfeiferSection on Epigenetics, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD, USA.
Michael E TalkowskiCenter for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA; Program in Medical and Population Genetics, Broad Institute of MIT and Harvard, Cambridge, MA, USA; Department of Neurology, Harvard Medical School, Boston, MA, USA. Electronic address: mtalkowski@mgh.harvard.edu.
Funding
No grant is acknowledged in the PubMed record.
Abstract
Cohesin orchestrates gene expression via three-dimensional chromosome folding. Genes encoding cohesin and cohesin loaders have been associated with Mendelian disorders, whereas genes encoding cohesin release factors, including WAPL and its binding partners PDS5A and PDS5B, have not. We explored the relevance of cohesin release factors in Mendelian disease by phenotyping individuals with heterozygous predicted damaging variants in WAPL (n = 27), PDS5A (n = 8), and PDS5B (n = 8), by modeling WAPL deficiency in human cells and mice, and by aggregating disease association statistics from consortia studies. We identified a WAPL-related disorder featuring developmental delay, intellectual disability, and risk of other developmental anomalies. Similarities between individuals with damaging WAPL variants and those with large, recurrent 10q22.3q23.2 (10q) deletions encompassing WAPL nominate WAPL as a driver gene within this genomic disorder region. While individuals with PDS5A or PDS5B variants exhibited features of developmental disorders, neither cohort-based statistics nor subject phenotyping associated these genes with specific phenotypes. We used CRISPR to generate truncating variants in WAPL and 10q deletion or duplication in human induced pluripotent stem cells (iPSCs) and induced neurons. Transcriptomics identified significant overlap between WAPL haploinsufficiency and 10q deletion differentially expressed genes. Mice with 50% Wapl expression exhibited mild deficits of growth and learning/memory, whereas those with 25% residual Wapl displayed birth defects and postnatal lethality, revealing a dosage liability threshold below the level of heterozygosity. In summary, we delineated a genetic condition caused by cohesin release factor deficiency, nominated WAPL as a driver gene within a genomic disorder region, and further illuminated dosage sensitivity of human cohesin.
Indexed as
Cell Cycle ProteinsChromosomal Proteins, Non-HistoneChromosomes, Human, Pair 10Intellectual DisabilityNuclear ProteinsAnimalsCarrier ProteinsCohesinsDevelopmental DisabilitiesDNA-Binding ProteinsFemaleHumansMaleMicePhenotypeProto-Oncogene ProteinsCarrier ProteinsCell Cycle ProteinsChromosomal Proteins, Non-HistoneCohesinsDNA-Binding ProteinsNuclear ProteinsPDS5A protein, humanPDS5B protein, humanProto-Oncogene ProteinsTranscription FactorsWAPL protein, humancohesin release factorPDS5APDS5BtranscriptionWAPL
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