An HNRNPK-specific DNA methylation signature makes sense of missense variants and expands the phenotypic spectrum of Au-Kline syndrome.


Journal

American journal of human genetics
ISSN: 1537-6605
Titre abrégé: Am J Hum Genet
Pays: United States
ID NLM: 0370475

Informations de publication

Date de publication:
06 10 2022
Historique:
received: 27 05 2022
accepted: 29 08 2022
pubmed: 22 9 2022
medline: 12 10 2022
entrez: 21 9 2022
Statut: ppublish

Résumé

Au-Kline syndrome (AKS) is a neurodevelopmental disorder associated with multiple malformations and a characteristic facial gestalt. The first individuals ascertained carried de novo loss-of-function (LoF) variants in HNRNPK. Here, we report 32 individuals with AKS (26 previously unpublished), including 13 with de novo missense variants. We propose new clinical diagnostic criteria for AKS that differentiate it from the clinically overlapping Kabuki syndrome and describe a significant phenotypic expansion to include individuals with missense variants who present with subtle facial features and few or no malformations. Many gene-specific DNA methylation (DNAm) signatures have been identified for neurodevelopmental syndromes. Because HNRNPK has roles in chromatin and epigenetic regulation, we hypothesized that pathogenic variants in HNRNPK may be associated with a specific DNAm signature. Here, we report a unique DNAm signature for AKS due to LoF HNRNPK variants, distinct from controls and Kabuki syndrome. This DNAm signature is also identified in some individuals with de novo HNRNPK missense variants, confirming their pathogenicity and the phenotypic expansion of AKS to include more subtle phenotypes. Furthermore, we report that some individuals with missense variants have an "intermediate" DNAm signature that parallels their milder clinical presentation, suggesting the presence of an epi-genotype phenotype correlation. In summary, the AKS DNAm signature may help elucidate the underlying pathophysiology of AKS. This DNAm signature also effectively supported clinical syndrome delineation and is a valuable aid for variant interpretation in individuals where a clinical diagnosis of AKS is unclear, particularly for mild presentations.

Identifiants

pubmed: 36130591
pii: S0002-9297(22)00403-7
doi: 10.1016/j.ajhg.2022.08.014
pmc: PMC9606382
pii:
doi:

Substances chimiques

Chromatin 0
Heterogeneous-Nuclear Ribonucleoprotein K 0
HNRNPK protein, human 146410-60-8

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1867-1884

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests H.T.B. is a consultant for Mahzi therapeutics.

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Auteurs

Sanaa Choufani (S)

Genetics and Genome Biology Program, Research Institute, the Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.

Vanda McNiven (V)

Division of Clinical and Metabolic Genetics, Department of Pediatrics, the Hospital for Sick Children, University of Toronto, Toronto, ON M5G 1X8, Canada; Fred A. Litwin Family Centre in Genetic Medicine, University Health Network and Mount Sinai Hospital, Toronto, ON M5T 3L9, Canada.

Cheryl Cytrynbaum (C)

Genetics and Genome Biology Program, Research Institute, the Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Division of Clinical and Metabolic Genetics, Department of Pediatrics, the Hospital for Sick Children, University of Toronto, Toronto, ON M5G 1X8, Canada.

Maryam Jangjoo (M)

Genetics and Genome Biology Program, Research Institute, the Hospital for Sick Children, Toronto, ON M5G 1X8, Canada.

Margaret P Adam (MP)

Division of Genetic Medicine, Department of Pediatrics, University of Washington, Seattle, WA 98105, USA.

Hans T Bjornsson (HT)

McKusick-Nathans Institute of Genetic Medicine, Department of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Faculty of Medicine, University of Iceland, Reykjavik 101, Iceland.

Jacqueline Harris (J)

Kennedy Krieger Institute, Baltimore, MD 21205, USA.

David A Dyment (DA)

Children's Hospital of Eastern Ontario Research Institute, University of Ottawa, Ottawa, ON K1H 5B2, Canada.

Gail E Graham (GE)

Division of Genetics, Children's Hospital of Eastern Ontario, University of Ottawa, Ottawa, ON K1H 8L1, Canada.

Marjan M Nezarati (MM)

Genetics Program, North York General Hospital, Toronto, ON M2K 1E1, Canada.

Ritu B Aul (RB)

Mackenzie Health, Richmond Hill, ON L4C 4Z3, Canada.

Claudia Castiglioni (C)

Departmento de Neurologica Pediatrica, Clinica Las Condes, Santiago 7591046, Chile.

Jeroen Breckpot (J)

Center for Human Genetics, University Hospitals Leuven, Leuven 3000, Belgium.

Koen Devriendt (K)

Center for Human Genetics, University Hospitals Leuven, Leuven 3000, Belgium.

Helen Stewart (H)

Oxford Centre for Genomic Medicine, Nuffield Orthopaedic Centre, Oxford University Hospitals, NHS Foundation Trust, Headington, Oxford OX3 7HE, UK.

Benito Banos-Pinero (B)

Oxford Regional Genetics Laboratories, Oxford University Hospitals NHS Foundation Trust, Oxford OX3 7LE, UK.

Sarju Mehta (S)

Department of Clinical Genetics, Addenbrookes Hospital, Cambridge CB2 0QQ, UK.

Richard Sandford (R)

Department of Clinical Genetics, Addenbrookes Hospital, Cambridge CB2 0QQ, UK.

Carolyn Dunn (C)

Department of Clinical Genetics, Addenbrookes Hospital, Cambridge CB2 0QQ, UK.

Remi Mathevet (R)

Centre de génétique humaine, CHU Besançon, Université de Bourgogne Franche-Comté, Besançon 25000, France.

Lionel van Maldergem (L)

Centre de génétique humaine, CHU Besançon, Université de Bourgogne Franche-Comté, Besançon 25000, France.

Juliette Piard (J)

Centre de génétique humaine, CHU Besançon, Université de Bourgogne Franche-Comté, Besançon 25000, France.

Elise Brischoux-Boucher (E)

Centre de génétique humaine, CHU Besançon, Université de Bourgogne Franche-Comté, Besançon 25000, France.

Antonio Vitobello (A)

Inserm UMR1231 GAD, Génétique des Anomalies du Développement, Fédération Hospitalo-Universitaire Médecine Translationnelle et Anomalies du Développement, CHU Dijon Bourgogne - Université de Bourgogne, Dijon 21079, France; UF diagnostic génomiques et maladies rares et FHU TRANSLAD, Centre Hospitalier Universitaire de Dijon-Bourgogne, Dijon 21079, France.

Laurence Faivre (L)

Inserm UMR1231 GAD, Génétique des Anomalies du Développement, Fédération Hospitalo-Universitaire Médecine Translationnelle et Anomalies du Développement, CHU Dijon Bourgogne - Université de Bourgogne, Dijon 21079, France; Centre de référence Anomalies du Développement et syndromes malformatifs et FHU TRANSLAD, Centre Hospitalier Universitaire de Dijon-Bourgogne, Dijon 21079, France.

Marie Bournez (M)

Inserm UMR1231 GAD, Génétique des Anomalies du Développement, Fédération Hospitalo-Universitaire Médecine Translationnelle et Anomalies du Développement, CHU Dijon Bourgogne - Université de Bourgogne, Dijon 21079, France; Centre de référence Anomalies du Développement et syndromes malformatifs et FHU TRANSLAD, Centre Hospitalier Universitaire de Dijon-Bourgogne, Dijon 21079, France.

Frederic Tran-Mau (F)

Inserm UMR1231 GAD, Génétique des Anomalies du Développement, Fédération Hospitalo-Universitaire Médecine Translationnelle et Anomalies du Développement, CHU Dijon Bourgogne - Université de Bourgogne, Dijon 21079, France; UF diagnostic génomiques et maladies rares et FHU TRANSLAD, Centre Hospitalier Universitaire de Dijon-Bourgogne, Dijon 21079, France.

Isabelle Maystadt (I)

Département de Génétique Clinique, Institut de Pathologie et de Génétique, Gosselies 6041, Belgium.

Alberto Fernández-Jaén (A)

Department of. Pediatrics and Neurology, Hospital Universitario Quirónsalud, School of Medicine, Universidad Europea de Madrid, Madrid 28224, Spain.

Sara Alvarez (S)

Genonics and Medicine, NIMGenetics, Madrid 28108, Spain.

Irene Díez García-Prieto (ID)

Genonics and Medicine, NIMGenetics, Madrid 28108, Spain.

Fowzan S Alkuraya (FS)

Department of Translational Genomics, Center for Genomic Medicine, King Faisal Specialist Hospital and Research Center, Riyadh 11211, Saudi Arabia.

Hessa S Alsaif (HS)

Department of Translational Genomics, Center for Genomic Medicine, King Faisal Specialist Hospital and Research Center, Riyadh 11211, Saudi Arabia; Center of Excellence for Biomedicine, King Abdulaziz City for Science and Technology, Riyadh 12354, Saudi Arabia.

Zuhair Rahbeeni (Z)

Department of Translational Genomics, Center for Genomic Medicine, King Faisal Specialist Hospital and Research Center, Riyadh 11211, Saudi Arabia.

Karen El-Akouri (K)

Department of Adult and Pediatric Medical Genetics, Hamad Medical Corporation, Doha 3050, Qatar; Division of Genetic and Genomic Medicine, Sidra Medicine, Doha 26999, Qatar.

Mariam Al-Mureikhi (M)

Department of Adult and Pediatric Medical Genetics, Hamad Medical Corporation, Doha 3050, Qatar; Division of Genetic and Genomic Medicine, Sidra Medicine, Doha 26999, Qatar.

Rebecca C Spillmann (RC)

Department of Pediatrics-Medical Genetics, Duke University, Durham, NC 27710, USA.

Vandana Shashi (V)

Department of Pediatrics-Medical Genetics, Duke University, Durham, NC 27710, USA.

Pedro A Sanchez-Lara (PA)

Department of Pediatrics, Medical Genetics, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.

John M Graham (JM)

Department of Pediatrics, Medical Genetics, Cedars-Sinai Medical Center, Los Angeles, CA 90048, USA.

Amy Roberts (A)

Department of Cardiology, Boston Children's Hospital, Harvard Medical School, Boston, MA 02115, USA.

Odelia Chorin (O)

Center for Human Genetics & Genomics and, Department of Pediatrics, NYU Grossman School of Medicine, New York City, NY 10016, USA.

Gilad D Evrony (GD)

Center for Human Genetics & Genomics and, Department of Pediatrics, NYU Grossman School of Medicine, New York City, NY 10016, USA.

Minna Kraatari-Tiri (M)

PEDEGO Research Unit, Medical Research Centre and Department of Clinical Genetics, University of Oulu and Oulu University Hospital, Oulu 90220, Finland.

Tracy Dudding-Byth (T)

The University of Newcastle, Newcastle 2308, Australia.

Anamaria Richardson (A)

Faculty of Medicine, Department of Pediatrics, BC Children's Hospital and the University of British Columbia, Vancouver, BC V6H 3N1, Canada.

David Hunt (D)

Wessex Clinical Genetics Service, University Hospital Southampton NHS Foundation Trust, Southampton, UK; Human Development and Health, Faculty of Medicine, University of Southampton, Southampton, UK.

Laura Hamilton (L)

Wessex Clinical Genetics Service, University Hospital Southampton NHS Foundation Trust, Southampton, UK.

Sarah Dyack (S)

Division of Medical Genetics, Department of Pediatrics, Dalhousie University, Halifax, NS B3K 6R8, Canada.

Bryce A Mendelsohn (BA)

Department of Medical Genetics, Kaiser Permanente Oakland, 3505 Broadway, Oakland, CA 94611, USA.

Nicolás Rodríguez (N)

Pediatrician Department, Hospital General Universitario de Alicante Dr. Balmis, Pintor Baeza, 11, 03010 Alicante, Spain.

Rosario Sánchez-Martínez (R)

Internal Medicine Department, Hospital General Universitario de Alicante Dr. Balmis, Institute for Health and Biomedical Research of Alicante, Pintor Baeza, 11, 03010 Alicante, Spain.

Jair Tenorio-Castaño (J)

CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, Madrid 28042, Spain; INGEMM-Idipaz, Institute of Medical and Molecular Genetics, University Hospital La Paz, Madrid 28046 Spain; ITHACA, European Reference Network, Brussels 1000, Belgium.

Julián Nevado (J)

CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, Madrid 28042, Spain; INGEMM-Idipaz, Institute of Medical and Molecular Genetics, University Hospital La Paz, Madrid 28046 Spain; ITHACA, European Reference Network, Brussels 1000, Belgium.

Pablo Lapunzina (P)

CIBERER, Centro de Investigación Biomédica en Red de Enfermedades Raras, Madrid 28042, Spain; INGEMM-Idipaz, Institute of Medical and Molecular Genetics, University Hospital La Paz, Madrid 28046 Spain; ITHACA, European Reference Network, Brussels 1000, Belgium.

Pilar Tirado (P)

Neuropediatrics Service, La Paz University Hospital, Madrid 28046, Spain.

Maria-Teresa Carminho Amaro Rodrigues (MT)

Department of Genetic Medicine, University Hospitals of Geneva, 1205 Geneva, Switzerland.

Lina Quteineh (L)

Department of Genetic Medicine, University Hospitals of Geneva, 1205 Geneva, Switzerland.

A Micheil Innes (AM)

Alberta Children's Hospital Research Institute for Child and Maternal Health, Department of Medical Genetics, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada.

Antonie D Kline (AD)

Harvey Institute for Human Genetics, Greater Baltimore Medical Center, Baltimore, MD 21204, USA.

P Y Billie Au (PYB)

Alberta Children's Hospital Research Institute for Child and Maternal Health, Department of Medical Genetics, Cumming School of Medicine, University of Calgary, Calgary, AB T2N 4N1, Canada. Electronic address: billie.au@albertahealthservices.ca.

Rosanna Weksberg (R)

Genetics and Genome Biology Program, Research Institute, the Hospital for Sick Children, Toronto, ON M5G 1X8, Canada; Division of Clinical and Metabolic Genetics, Department of Pediatrics, the Hospital for Sick Children, University of Toronto, Toronto, ON M5G 1X8, Canada. Electronic address: rweksb@sickkids.ca.

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