Identification of a robust DNA methylation signature for Fanconi anemia.

DNA methylation profiling Fanconi anemia classifier diagnostic tool episignature gene conversion hematological disorders machine learning mosaicism variant classification

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:
02 11 2023
Historique:
received: 29 06 2023
revised: 26 09 2023
accepted: 27 09 2023
pmc-release: 02 05 2024
medline: 6 11 2023
pubmed: 22 10 2023
entrez: 21 10 2023
Statut: ppublish

Résumé

Fanconi anemia (FA) is a clinically variable and genetically heterogeneous cancer-predisposing disorder representing the most common bone marrow failure syndrome. It is caused by inactivating predominantly biallelic mutations involving >20 genes encoding proteins with roles in the FA/BRCA DNA repair pathway. Molecular diagnosis of FA is challenging due to the wide spectrum of the contributing gene mutations and structural rearrangements. The assessment of chromosomal fragility after exposure to DNA cross-linking agents is generally required to definitively confirm diagnosis. We assessed peripheral blood genome-wide DNA methylation (DNAm) profiles in 25 subjects with molecularly confirmed clinical diagnosis of FA (FANCA complementation group) using Illumina's Infinium EPIC array. We identified 82 differentially methylated CpG sites that allow to distinguish subjects with FA from healthy individuals and subjects with other genetic disorders, defining an FA-specific DNAm signature. The episignature was validated using a second cohort of subjects with FA involving different complementation groups, documenting broader genetic sensitivity and demonstrating its specificity using the EpiSign Knowledge Database. The episignature properly classified DNA samples obtained from bone marrow aspirates, demonstrating robustness. Using the selected probes, we trained a machine-learning model able to classify EPIC DNAm profiles in molecularly unsolved cases. Finally, we show that the generated episignature includes CpG sites that do not undergo functional selective pressure, allowing diagnosis of FA in individuals with reverted phenotype due to gene conversion. These findings provide a tool to accelerate diagnostic testing in FA and broaden the clinical utility of DNAm profiling in the diagnostic setting.

Identifiants

pubmed: 37865086
pii: S0002-9297(23)00352-X
doi: 10.1016/j.ajhg.2023.09.014
pmc: PMC10645556
pii:
doi:

Substances chimiques

Fanconi Anemia Complementation Group Proteins 0
Proteins 0
DNA 9007-49-2

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Pagination

1938-1949

Informations de copyright

Copyright © 2023 American Society of Human Genetics. Published by Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests Dr. Sadikovic is a shareholder in EpiSign Inc, a software company involved in commercialization of EpiSign Technology.

Références

Genes (Basel). 2022 Nov 19;13(11):
pubmed: 36421837
Nat Rev Cancer. 2003 Jan;3(1):23-34
pubmed: 12509764
Am J Med Genet. 1998 Oct 12;79(5):403-5
pubmed: 9779812
Genet Med. 2021 Jan;23(1):34-46
pubmed: 32973355
Oncogene. 2002 May 13;21(21):3368-76
pubmed: 12032775
Oncotarget. 2017 Jun 20;8(25):40359-40372
pubmed: 28423717
Blood. 2003 Feb 15;101(4):1249-56
pubmed: 12393516
Cytogenet Genome Res. 2002;98(2-3):126-35
pubmed: 12697994
HGG Adv. 2021 Dec 03;3(1):100075
pubmed: 35047860
Mutat Res. 2009 Jul 31;668(1-2):4-10
pubmed: 19622403
Clin Genet. 2015 Jul;88(1):13-24
pubmed: 25307146
Science. 2021 Sep 24;373(6562):1464-1468
pubmed: 34554789
Genes Dev. 2010 Aug 15;24(16):1680-94
pubmed: 20713514
Nat Rev Mol Cell Biol. 2016 Jun;17(6):337-49
pubmed: 27145721
Cytogenet Genome Res. 2014;144(1):15-27
pubmed: 25227706
Front Mol Biosci. 2021 Jul 07;8:685440
pubmed: 34307454
Genome Biol. 2021 Jun 8;22(1):173
pubmed: 34103055
Curr Protoc Hum Genet. 2015 Apr 01;85:8.7.1-8.7.17
pubmed: 25827349
Am J Hum Genet. 2020 Mar 5;106(3):356-370
pubmed: 32109418
Epigenetics Chromatin. 2015 Jan 27;8:6
pubmed: 25972926
Nat Rev Mol Cell Biol. 2019 Oct;20(10):590-607
pubmed: 31399642
Hematology Am Soc Hematol Educ Program. 2022 Dec 9;2022(1):649-657
pubmed: 36485157
Nucleic Acids Res. 2015 Apr 20;43(7):e47
pubmed: 25605792
Clin Epigenetics. 2020 Jan 7;12(1):7
pubmed: 31910894
Nature. 2015 Feb 19;518(7539):317-30
pubmed: 25693563
Genet Med. 2015 May;17(5):405-24
pubmed: 25741868
Clin Epigenetics. 2021 Aug 11;13(1):157
pubmed: 34380541
Mutat Res Rev Mutat Res. 2019 Apr - Jun;780:37-47
pubmed: 31395347
PLoS Genet. 2007 Jul;3(7):e110
pubmed: 17616978
PLoS Genet. 2008 Aug 15;4(8):e1000155
pubmed: 18704159
Trends Cancer. 2022 Jun;8(6):467-481
pubmed: 35232683
Genet Med. 2018 Mar;20(3):291-293
pubmed: 29388946
Genome Biol. 2018 May 29;19(1):64
pubmed: 29843789
Genet Med. 2021 Jun;23(6):1065-1074
pubmed: 33547396
Nat Rev Genet. 2013 Mar;14(3):204-20
pubmed: 23400093
Genome Res. 2012 Feb;22(2):407-19
pubmed: 21613409
Am J Hum Genet. 2019 Apr 4;104(4):685-700
pubmed: 30929737
Bioinformatics. 2017 Feb 15;33(4):558-560
pubmed: 28035024
Nat Rev Genet. 2012 May 29;13(7):484-92
pubmed: 22641018
Nat Rev Genet. 2021 Dec;22(12):774-790
pubmed: 34341555
EMBO J. 2012 Jan 18;31(2):351-65
pubmed: 22068055
Nat Methods. 2018 Feb;15(2):123-126
pubmed: 29309061
Bioinformatics. 2017 Dec 15;33(24):3982-3984
pubmed: 28961746
Genes (Basel). 2020 Dec 21;11(12):
pubmed: 33371494

Auteurs

Daria Pagliara (D)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Andrea Ciolfi (A)

Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Lucia Pedace (L)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Sadegheh Haghshenas (S)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada.

Marco Ferilli (M)

Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Michael A Levy (MA)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada.

Evelina Miele (E)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Claudia Nardini (C)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Camilla Cappelletti (C)

Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Raissa Relator (R)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada.

Angela Pitisci (A)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Rita De Vito (R)

Department of Laboratories, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Simone Pizzi (S)

Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Jennifer Kerkhof (J)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada.

Haley McConkey (H)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada; Department of Pathology and Laboratory Medicine, Western University, London, ON N6A 3K7, Canada.

Francesca Nazio (F)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy.

Sarina G Kant (SG)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 Rotterdam, the Netherlands.

Maddalena Di Donato (M)

Laboratory of Medical Genetics, Translational Cytogenomics Research Unit, Bambino Gesù Children Hospital, IRCCS, 00146 Rome, Italy.

Emanuele Agolini (E)

Laboratory of Medical Genetics, Translational Cytogenomics Research Unit, Bambino Gesù Children Hospital, IRCCS, 00146 Rome, Italy.

Marta Matraxia (M)

Laboratory of Medical Genetics, Translational Cytogenomics Research Unit, Bambino Gesù Children Hospital, IRCCS, 00146 Rome, Italy.

Barbara Pasini (B)

AOU Città della salute e della scienza di Torino, Molinette's Hospital, 10126 Torino, Italy.

Alessandra Pelle (A)

AOU Città della salute e della scienza di Torino, Molinette's Hospital, 10126 Torino, Italy.

Tiziana Galluccio (T)

Laboratory of Transplant Immunogenetics, Department of Hematology/Oncology, Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, 00146 Rome, Italy.

Antonio Novelli (A)

Laboratory of Medical Genetics, Translational Cytogenomics Research Unit, Bambino Gesù Children Hospital, IRCCS, 00146 Rome, Italy.

Tahsin Stefan Barakat (TS)

Department of Clinical Genetics, Erasmus MC University Medical Center, 3015 Rotterdam, the Netherlands; ENCORE Expertise Center for Neurodevelopmental Disorders, Erasmus MC University Medical Center, 3015 Rotterdam, the Netherlands.

Marco Andreani (M)

Laboratory of Transplant Immunogenetics, Department of Hematology/Oncology, Cell and Gene Therapy, IRCCS Bambino Gesù Children's Hospital, 00146 Rome, Italy.

Francesca Rossi (F)

Department of Woman, Child and of General and Specialist Surgery, University of Campania "Luigi Vanvitelli," 80138 Naples, Italy.

Cristina Mecucci (C)

Institute of Hematology and Center for Hemato-Oncology Research, University and Hospital of Perugia, 06123 Perugia, Italy.

Anna Savoia (A)

Department of Neurosciences, Biomedicine and Movement Sciences, University of Verona, 37134 Verona, Italy.

Bekim Sadikovic (B)

Verspeeten Clinical Genome Centre, London Health Sciences Centre, London, ON N6A 5W9, Canada; Department of Pathology and Laboratory Medicine, Western University, London, ON N6A 3K7, Canada.

Franco Locatelli (F)

Department of Hematology/Oncology and Cell and Gene Therapy, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy; Department of Pediatrics, Catholic University of the Sacred Hearth, 00168 Rome, Italy. Electronic address: franco.locatelli@opbg.net.

Marco Tartaglia (M)

Molecular Genetics and Functional Genomics, Bambino Gesù Children's Hospital, IRCCS, 00146 Rome, Italy. Electronic address: marco.tartaglia@opbg.net.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH