Epigenome-wide association study of COVID-19 severity with respiratory failure
Manuel Castro de Moura,
Veronica Davalos,
Laura Planas-Serra,
Damiana Alvarez-Errico,
Carles Arribas,
Montserrat Ruiz,
Sergio Aguilera-Albesa,
Jesús Troya,
Juan Valencia-Ramos,
Valentina Vélez-Santamaria,
Agustí Rodríguez-Palmero,
Judit Villar-Garcia,
Juan P. Horcajada,
Sergiu Albu,
Carlos Casasnovas,
Anna Rull,
Laia Reverte,
Beatriz Dietl,
David Dalmau,
Maria J. Arranz,
Laia Llucià-Carol,
Anna M. Planas,
Jordi Pérez-Tur,
Israel Fernandez-Cadenas,
Paula Villares,
Jair Tenorio,
Roger Colobran,
Andrea Martin-Nalda,
Pere Soler-Palacin,
Francesc Vidal,
Aurora Pujol,
Manel Esteller
Affiliations
Manuel Castro de Moura
Josep Carreras Leukaemia Research Institute (IJC), 08916 Badalona, Barcelona, Catalonia, Spain
Veronica Davalos
Josep Carreras Leukaemia Research Institute (IJC), 08916 Badalona, Barcelona, Catalonia, Spain
Laura Planas-Serra
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain
Damiana Alvarez-Errico
Josep Carreras Leukaemia Research Institute (IJC), 08916 Badalona, Barcelona, Catalonia, Spain
Carles Arribas
Josep Carreras Leukaemia Research Institute (IJC), 08916 Badalona, Barcelona, Catalonia, Spain
Montserrat Ruiz
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain
Sergio Aguilera-Albesa
Navarra Health Service Hospital, Pamplona, Spain
Jesús Troya
Infanta Leonor University Hospital, Madrid, Spain
Juan Valencia-Ramos
University Hospital of Burgos, Burgos, Spain
Valentina Vélez-Santamaria
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain; Bellvitge University Hospital, L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain
Agustí Rodríguez-Palmero
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain; University Hospital Germans Trias i Pujol, Badalona, Barcelona, Catalonia, Spain
Judit Villar-Garcia
Hospital del Mar - IMIM Biomedical Research Institute, Barcelona, Catalonia, Spain
Juan P. Horcajada
Hospital del Mar - IMIM Biomedical Research Institute, Barcelona, Catalonia, Spain
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain; Bellvitge University Hospital, L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain
Anna Rull
Hospital Universitari de Tarragona Joan XXIII, IISPV, Universitat Rovira i Virgili, Tarragona, Catalonia, Spain
Laia Reverte
Hospital Universitari de Tarragona Joan XXIII, IISPV, Universitat Rovira i Virgili, Tarragona, Catalonia, Spain
Beatriz Dietl
Servei de malalties infeccioses Hospital Universitari MutuaTerrassa, Universitat de Barcelona, Barcelona, Catalonia, Spain
David Dalmau
MutuaTerrassa Research and Innovation Foundation, HIV/AIDS Unit Hospital Universitari MutuaTerrassa, University of Barcelona, Barcelona, Catalonia, Spain
Maria J. Arranz
Fundaciò Docència i Recerca Mutua Terrassa i Hospital Universitari Mutua Terrassa, Barcelona, Catalonia, Spain
Laia Llucià-Carol
Stroke Pharmacogenomics and Genetics Group, Sant Pau Institute of Research, Sant Pau Hospital, Barcelona, Catalonia, Spain
Anna M. Planas
Department of Brain Ischemia and Neurodegeneration, Institut d'Investigacions Biomèdiques de Barcelona (IIBB), Consejo Superior de Investigaciones Científicas (CSIC), Area of Neurosciences, Institut d'Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), Barcelona, Catalonia, Spain
Jordi Pérez-Tur
Institut de Biomedicina de València-CSIC, CIBERNED, Unitat Mixta de Neurologia i Genètica, IIS La Fe, Vallencia, Spain
Israel Fernandez-Cadenas
Stroke Pharmacogenomics and Genetics Group, Sant Pau Institute of Research, Sant Pau Hospital, Barcelona, Catalonia, Spain
Paula Villares
Internal Medicine Department, Hospital HM Sanchinarro, HM Hospitales, Madrid, Spain
Jair Tenorio
INGEMM-Instituto de Genética Médica y Molecular, Hospital Universitario La Paz, Madrid, Spain; Center for Biomedical Research on Rare Diseases (CIBERER), ISCIII, Madrid, Spain
Roger Colobran
Immunology Division, Genetics Department, Hospital Universitari Vall d'Hebron, Vall d'Hebron Research Institute, Vall d'Hebron Barcelona Hospital Campus, UAB, Barcelona, Catalonia, Spain
Andrea Martin-Nalda
Pediatric Infectious Diseases and Immunodeficiencies Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Catalonia, Spain
Pere Soler-Palacin
Pediatric Infectious Diseases and Immunodeficiencies Unit, Hospital Universitari Vall d'Hebron, Vall d'Hebron Barcelona Hospital Campus, Barcelona, Catalonia, Spain
Francesc Vidal
Hospital Universitari de Tarragona Joan XXIII, IISPV, Universitat Rovira i Virgili, Tarragona, Catalonia, Spain
Aurora Pujol
Neurometabolic Diseases Laboratory, Bellvitge Biomedical Research Institute (IDIBELL), 08908 L'Hospitalet de Llobregat, Barcelona, Catalonia, Spain; Center for Biomedical Research on Rare Diseases (CIBERER), ISCIII, Madrid, Spain; Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Catalonia, Spain; Corresponding authors.
Manel Esteller
Josep Carreras Leukaemia Research Institute (IJC), 08916 Badalona, Barcelona, Catalonia, Spain; Centro de Investigación Biomédica en Red de Cancer (CIBERONC), Spain; Institucio Catalana de Recerca i Estudis Avançats (ICREA), Barcelona, Catalonia, Spain; Physiological Sciences Department, School of Medicine and Health Sciences, University of Barcelona (UB), Catalonia, Spain; Corresponding authors.
Background: Patients infected with the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), responsible for the coronavirus disease 2019 (COVID-19), exhibit a wide spectrum of disease behaviour. Since DNA methylation has been implicated in the regulation of viral infections and the immune system, we performed an epigenome-wide association study (EWAS) to identify candidate loci regulated by this epigenetic mark that could be involved in the onset of COVID-19 in patients without comorbidities. Methods: Peripheral blood samples were obtained from 407 confirmed COVID-19 patients ≤ 61 years of age and without comorbidities, 194 (47.7%) of whom had mild symptomatology that did not involve hospitalization and 213 (52.3%) had a severe clinical course that required respiratory support. The set of cases was divided into discovery (n = 207) and validation (n = 200) cohorts, balanced for age and sex of individuals. We analysed the DNA methylation status of 850,000 CpG sites in these patients. Findings: The DNA methylation status of 44 CpG sites was associated with the clinical severity of COVID-19. Of these loci, 23 (52.3%) were located in 20 annotated coding genes. These genes, such as the inflammasome component Absent in Melanoma 2 (AIM2) and the Major Histocompatibility Complex, class I C (HLA-C) candidates, were mainly involved in the response of interferon to viral infection. We used the EWAS-identified sites to establish a DNA methylation signature (EPICOVID) that is associated with the severity of the disease. Interpretation: We identified DNA methylation sites as epigenetic susceptibility loci for respiratory failure in COVID-19 patients. These candidate biomarkers, combined with other clinical, cellular and genetic factors, could be useful in the clinical stratification and management of patients infected with the SARS-CoV-2. Funding: The Unstoppable campaign of the Josep Carreras Leukaemia Foundation, the Cellex Foundation and the CERCA Programme/Generalitat de Catalunya.