Abstract
The combined impact of common and rare exonic variants in COVID-19 host genetics is currently insufficiently understood. Here, common and rare variants from whole-exome sequencing data of about 4000 SARS-CoV-2-positive individuals were used to define an interpretable machine-learning model for predicting COVID-19 severity. First, variants were converted into separate sets of Boolean features, depending on the absence or the presence of variants in each gene. An ensemble of LASSO logistic regression models was used to identify the most informative Boolean features with respect to the genetic bases of severity. The Boolean features selected by these logistic models were combined into an Integrated PolyGenic Score that offers a synthetic and interpretable index for describing the contribution of host genetics in COVID-19 severity, as demonstrated through testing in several independent cohorts. Selected features belong to ultra-rare, rare, low-frequency, and common variants, including those in linkage disequilibrium with known GWAS loci. Noteworthily, around one quarter of the selected genes are sex-specific. Pathway analysis of the selected genes associated with COVID-19 severity reflected the multi-organ nature of the disease. The proposed model might provide useful information for developing diagnostics and therapeutics, while also being able to guide bedside disease management.
Original language | English |
---|---|
Pages (from-to) | 147-173 |
Number of pages | 27 |
Journal | Human Genetics |
Volume | 141 |
Issue number | 1 |
DOIs | |
Publication status | Published - 1 Jan 2022 |
Externally published | Yes |
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}
In: Human Genetics, Vol. 141, No. 1, 01.01.2022, p. 147-173.
Research output: Contribution to journal › Article › Research › peer-review
TY - JOUR
T1 - Common, low-frequency, rare, and ultra-rare coding variants contribute to COVID-19 severity
AU - Fallerini, Chiara
AU - Picchiotti, Nicola
AU - Baldassarri, Margherita
AU - Zguro, Kristina
AU - Daga, Sergio
AU - Fava, Francesca
AU - Benetti, Elisa
AU - Amitrano, Sara
AU - Bruttini, Mirella
AU - Palmieri, Maria
AU - Croci, Susanna
AU - Lista, Mirjam
AU - Beligni, Giada
AU - Valentino, Floriana
AU - Meloni, Ilaria
AU - Tanfoni, Marco
AU - Minnai, Francesca
AU - Colombo, Francesca
AU - Cabri, Enrico
AU - Fratelli, Maddalena
AU - Gabbi, Chiara
AU - Mantovani, Stefania
AU - Frullanti, Elisa
AU - Gori, Marco
AU - Crawley, Francis P.
AU - Butler-Laporte, Guillaume
AU - Richards, Brent
AU - Zeberg, Hugo
AU - Lipcsey, Miklós
AU - Hultström, Michael
AU - Ludwig, Kerstin U.
AU - Schulte, Eva C.
AU - Pairo-Castineira, Erola
AU - Baillie, John Kenneth
AU - Schmidt, Axel
AU - Frithiof, Robert
AU - Mari, Francesca
AU - Renieri, Alessandra
AU - Furini, Simone
AU - Montagnani, Francesca
AU - Tumbarello, Mario
AU - Rancan, Ilaria
AU - Fabbiani, Massimiliano
AU - Rossetti, Barbara
AU - Bergantini, Laura
AU - D’Alessandro, Miriana
AU - Cameli, Paolo
AU - Bennett, David
AU - Anedda, Federico
AU - Marcantonio, Simona
AU - Scolletta, Sabino
AU - Franchi, Federico
AU - Mazzei, Maria Antonietta
AU - Guerrini, Susanna
AU - Conticini, Edoardo
AU - Cantarini, Luca
AU - Frediani, Bruno
AU - Tacconi, Danilo
AU - Raffaelli, Chiara Spertilli
AU - Feri, Marco
AU - Donati, Alice
AU - Scala, Raffaele
AU - Guidelli, Luca
AU - Spargi, Genni
AU - Corridi, Marta
AU - Nencioni, Cesira
AU - Croci, Leonardo
AU - Caldarelli, Gian Piero
AU - Spagnesi, Maurizio
AU - Romani, Davide
AU - Piacentini, Paolo
AU - Bandini, Maria
AU - Desanctis, Elena
AU - Cappelli, Silvia
AU - Canaccini, Anna
AU - Verzuri, Agnese
AU - Anemoli, Valentina
AU - Pisani, Manola
AU - Ognibene, Agostino
AU - Pancrazzi, Alessandro
AU - Lorubbio, Maria
AU - Vaghi, Massimo
AU - Monforte, Antonella D’Arminio
AU - Miraglia, Federica Gaia
AU - Mondelli, Mario U.
AU - Girardis, Massimo
AU - Venturelli, Sophie
AU - Busani, Stefano
AU - Cossarizza, Andrea
AU - Antinori, Andrea
AU - Vergori, Alessandra
AU - Emiliozzi, Arianna
AU - Rusconi, Stefano
AU - Siano, Matteo
AU - Gabrieli, Arianna
AU - Riva, Agostino
AU - Francisci, Daniela
AU - Schiaroli, Elisabetta
AU - Paciosi, Francesco
AU - Tommasi, Andrea
AU - Scotton, Pier Giorgio
AU - Andretta, Francesca
AU - Panese, Sandro
AU - Baratti, Stefano
AU - Scaggiante, Renzo
AU - Gatti, Francesca
AU - Parisi, Saverio Giuseppe
AU - Castelli, Francesco
AU - Quiros-Roldan, Eugenia
AU - Antoni, Melania Degli
AU - Zanella, Isabella
AU - Monica, Matteo Della
AU - Piscopo, Carmelo
AU - Capasso, Mario
AU - Russo, Roberta
AU - Andolfo, Immacolata
AU - Iolascon, Achille
AU - Fiorentino, Giuseppe
AU - Carella, Massimo
AU - Castori, Marco
AU - Aucella, Filippo
AU - Raggi, Pamela
AU - Perna, Rita
AU - Bassetti, Matteo
AU - Biagio, Antonio Di
AU - Sanguinetti, Maurizio
AU - Masucci, Luca
AU - Guarnaccia, Alessandra
AU - Valente, Serafina
AU - Vivo, Oreste De
AU - Doddato, Gabriella
AU - Tita, Rossella
AU - Giliberti, Annarita
AU - Mencarelli, Maria Antonietta
AU - Rizzo, Caterina Lo
AU - Pinto, Anna Maria
AU - Perticaroli, Valentina
AU - Ariani, Francesca
AU - Carriero, Miriam Lucia
AU - Sarno, Laura Di
AU - Alaverdian, Diana
AU - Bargagli, Elena
AU - Mandalà, Marco
AU - Giorli, Alessia
AU - Salerni, Lorenzo
AU - Zucchi, Patrizia
AU - Parravicini, Pierpaolo
AU - Menatti, Elisabetta
AU - Trotta, Tullio
AU - Giannattasio, Ferdinando
AU - Coiro, Gabriella
AU - Lena, Fabio
AU - Lacerenza, Leonardo Gianluca
AU - Coviello, Domenico A.
AU - Mussini, Cristina
AU - Martinelli, Enrico
AU - Mancarella, Sandro
AU - Tavecchia, Luisa
AU - Belli, Mary Ann
AU - Crotti, Lia
AU - Parati, Gianfranco
AU - Sanarico, Maurizio
AU - Raimondi, Francesco
AU - Biscarini, Filippo
AU - Stella, Alessandra
AU - Rizzi, Marco
AU - Maggiolo, Franco
AU - Ripamonti, Diego
AU - Suardi, Claudia
AU - Bachetti, Tiziana
AU - Rovere, Maria Teresa La
AU - Sarzi-Braga, Simona
AU - Bussotti, Maurizio
AU - Capitani, Katia
AU - Dei, Simona
AU - Ravaglia, Sabrina
AU - Artuso, Rosangela
AU - Andreucci, Elena
AU - Gori, Giulia
AU - Pagliazzi, Angelica
AU - Fiorentini, Erika
AU - Perrella, Antonio
AU - Bianchi, Francesco
AU - Bergomi, Paola
AU - Catena, Emanuele
AU - Colombo, Riccardo
AU - Luchi, Sauro
AU - Morelli, Giovanna
AU - Petrocelli, Paola
AU - Iacopini, Sarah
AU - Modica, Sara
AU - Baroni, Silvia
AU - Segala, Francesco Vladimiro
AU - Menichetti, Francesco
AU - Falcone, Marco
AU - Tiseo, Giusy
AU - Barbieri, Chiara
AU - Matucci, Tommaso
AU - Grassi, Davide
AU - Ferri, Claudio
AU - Marinangeli, Franco
AU - Brancati, Francesco
AU - Vincenti, Antonella
AU - Borgo, Valentina
AU - Stefania, Lombardi
AU - Lenzi, Mirco
AU - Pietro, Massimo Antonio Di
AU - Vichi, Francesca
AU - Romanin, Benedetta
AU - Attala, Letizia
AU - Costa, Cecilia
AU - Gabbuti, Andrea
AU - Roberto, Menè
AU - Zuccon, Umberto
AU - Vietri, Lucia
AU - Ceri, Stefano
AU - Pinoli, Pietro
AU - Casprini, Patrizia
AU - Merla, Giuseppe
AU - Squeo, Gabriella Maria
AU - Maffezzoni, Marcello
AU - Bruno, Raffaele
AU - Vecchia, Marco
AU - Colaneri, Marta
AU - Ludovisi, Serena
AU - Marincevic-Zuniga, Yanara
AU - Nordlund, Jessica
AU - Luther, Tomas
AU - Larsson, Anders
AU - Hanslin, Katja
AU - Gradin, Anna
AU - Galien, Sarah
AU - Anderberg, Sara Bulow
AU - Rosén, Jacob
AU - Rubertsson, Sten
AU - Clohisey, Sara
AU - Horby, Peter
AU - Millar, Johnny
AU - Knight, Julian
AU - Montgomery, Hugh
AU - Maslove, David
AU - Ling, Lowell
AU - Nichol, Alistair
AU - Summers, Charlotte
AU - Walsh, Tim
AU - Hinds, Charles
AU - Semple, Malcolm G.
AU - Openshaw, Peter J.M.
AU - Shankar-Hari, Manu
AU - Ho, Antonia
AU - WES/WGS Working Group Within the HGI GenOMICC Consortium GEN-COVID Multicenter Study
N1 - Funding Information: This study is part of the GEN-COVID Multicenter Study, https://sites.google.com/dbm.unisi.it/gen-covid , the Italian multicenter study aimed at identifying the COVID-19 host genetic bases. Specimens were provided by the COVID-19 Biobank of Siena, which is part of the Genetic Biobank of Siena, member of BBMRI-IT, of Telethon Network of Genetic Biobanks (project no. GTB18001), of EuroBioBank and of D-Connect. We thank the CINECA consortium for providing computational resources and the Network for Italian Genomes (NIG) http://www.nig.cineca.it for its support. We thank private donors for the support provided to A.R. (Department of Medical Biotechnologies, University of Siena) for the COVID-19 host genetics research project (D.L n.18 of March 17, 2020). We also thank the COVID-19 Host Genetics Initiative ( https://www.covid19hg.org/ ). We thank Uppsala Intensive Care COVID-19 research group; Tomas Luther, Anders Larsson, Katja Hanslin, Anna Gradin, Sarah Galien, Sara Bulow Anderberg, Jacob Rosén and Sten Rubertsson. We thank the patients and their loved ones who volunteered to contribute to this study at one of the most difficult times in their lives, and the research staff in every intensive care unit who recruited patients at personal risk during the most extreme conditions we have ever witnessed in UK hospitals. Whole-genome sequencing was done by Illumina in partnership with the University of Edinburgh and Genomics England and was funded by UK Department of Health and Social Care, UKRI and LifeArc. The views expressed are those of the authors and not necessarily those of the DHSC, DID, NIHR, MRC, Wellcome Trust or PHE. The Health Research Board of Ireland (Clinical Trial Network Award 2014-12) funds collection of samples in Ireland. This study owes a great deal to the National Institute of Healthcare Research Clinical Research Network (NIHR CRN) and the Chief Scientist Office (Scotland), who facilitate recruitment into research studies in NHS hospitals, and to the global ISARIC and InFACT consortia. We also acknowledge funding provided by the German Research Foundation (DFG) through the NGS competence centres (INST 37/1049-1, INST 216/981-1, INST 257/605-1, INST 269/768-1 and INST 217/988-1) and scientific support through the German COVID multiomics initiative (DeCOI). Recruitment of the COMRI Study/of part of the DeCOI samples was funded by the Klinikum rechts der Isar, Technical University Munich, Munich, Germany. We received additional support by the DFG (LU 1944/3-1, to K.U.L. and SCHU 2419/2-1, to E.C.S.), the BONFOR program of the Medical Faculty of the University of Bonn (2020-1A-15, to A.S.) and the Munich Clinician Scientist Program (MCSP, to E.C.S.). Funding Information: MIUR project “Dipartimenti di Eccellenza 2018-2020” to Department of Medical Biotechnologies University of Siena, Italy (Italian D.L. n.18 March 17, 2020). Private donors for COVID-19 research. “Bando Ricerca COVID-19 Toscana” project to Azienda Ospedaliero-Universitaria Senese. Charity fund 2020 from Intesa San Paolo dedicated to the project/ N. B/2020/0119 “Identificazione delle basi genetiche determinanti la variabilità clinica della risposta a COVID-19 nella popolazione italiana”. The Italian Ministry of University and Research for funding within the “Bando FISR 2020” in COVID-19 and the Istituto Buddista Italiano Soka Gakkai with the 8x1000 funds for funding the project “PAT-COVID: Host genetics and pathogenetic mechanisms of COVID-19” (ID n. 2020-2016_RIC_3). GenOMICC was funded by Sepsis Research (the Fiona Elizabeth Agnew Trust), the Intensive Care Society, a Wellcome-Beit Prize award to J. K. Baillie (Wellcome Trust 103258/Z/13/A) and a BBSRC Institute Program Support Grant to the Roslin Institute (BBS/E/D/20002172, BBS/E/D/10002070 and BBS/E/D/30002275). The Richards research group is supported by the Canadian Institutes of Health Research (CIHR: 365825; 409511, 100558), the McGill Interdisciplinary Initiative in Infection and Immunity (MI4), the Lady Davis Institute of the Jewish General Hospital, the Jewish General Hospital Foundation, the Canadian Foundation for Innovation, the NIH Foundation, Cancer Research UK, Genome Québec, the Public Health Agency of Canada, McGill University, Cancer Research UK [Grant number C18281/A29019] and the Fonds de Recherche Québec Santé (FRQS). JBR is supported by a FRQS Mérite Clinical Research Scholarship. Support from Calcul Québec and Compute Canada is acknowledged. TwinsUK is funded by the Welcome Trust, Medical Research Council, European Union, the National Institute for Health Research (NIHR)-funded BioResource, Clinical Research Facility and Biomedical Research Centre based at Guy’s and St Thomas’ NHS Foundation Trust in partnership with King’s College London. These funding agencies had no role in the design, implementation or interpretation of this study. JBR has served as an advisor to GlaxoSmithKline and Deerfield Capital. His institution has received investigator-initiated grant funding from Eli Lilly, GlaxoSmithKline and Biogen for projects unrelated to this research. He is the founder of 5 Prime Sciences. SweCovid received funding from the European Union’s Horizon 2020 research and innovation program under Grant agreement No 824110, the SciLifeLab/KAW national Covid-19 research program project grants to MH (KAW 2020.0182 and KAW 2020.0241) and the Swedish Research Council Grants to RF (2014-02569 and 2014-07606). Sequencing was performed by the SNP&SEQ Technology Platform in Uppsala. The facility is part of the National Genomics Infrastructure (NGI) Sweden and Science for Life Laboratory. The SNP&SEQ Platform is supported by the Swedish Research Council and the Knut and Alice Wallenberg Foundation. Publisher Copyright: © 2021, The Author(s).
PY - 2022/1/1
Y1 - 2022/1/1
N2 - The combined impact of common and rare exonic variants in COVID-19 host genetics is currently insufficiently understood. Here, common and rare variants from whole-exome sequencing data of about 4000 SARS-CoV-2-positive individuals were used to define an interpretable machine-learning model for predicting COVID-19 severity. First, variants were converted into separate sets of Boolean features, depending on the absence or the presence of variants in each gene. An ensemble of LASSO logistic regression models was used to identify the most informative Boolean features with respect to the genetic bases of severity. The Boolean features selected by these logistic models were combined into an Integrated PolyGenic Score that offers a synthetic and interpretable index for describing the contribution of host genetics in COVID-19 severity, as demonstrated through testing in several independent cohorts. Selected features belong to ultra-rare, rare, low-frequency, and common variants, including those in linkage disequilibrium with known GWAS loci. Noteworthily, around one quarter of the selected genes are sex-specific. Pathway analysis of the selected genes associated with COVID-19 severity reflected the multi-organ nature of the disease. The proposed model might provide useful information for developing diagnostics and therapeutics, while also being able to guide bedside disease management.
AB - The combined impact of common and rare exonic variants in COVID-19 host genetics is currently insufficiently understood. Here, common and rare variants from whole-exome sequencing data of about 4000 SARS-CoV-2-positive individuals were used to define an interpretable machine-learning model for predicting COVID-19 severity. First, variants were converted into separate sets of Boolean features, depending on the absence or the presence of variants in each gene. An ensemble of LASSO logistic regression models was used to identify the most informative Boolean features with respect to the genetic bases of severity. The Boolean features selected by these logistic models were combined into an Integrated PolyGenic Score that offers a synthetic and interpretable index for describing the contribution of host genetics in COVID-19 severity, as demonstrated through testing in several independent cohorts. Selected features belong to ultra-rare, rare, low-frequency, and common variants, including those in linkage disequilibrium with known GWAS loci. Noteworthily, around one quarter of the selected genes are sex-specific. Pathway analysis of the selected genes associated with COVID-19 severity reflected the multi-organ nature of the disease. The proposed model might provide useful information for developing diagnostics and therapeutics, while also being able to guide bedside disease management.
UR - http://www.scopus.com/inward/record.url?scp=85123651761&partnerID=8YFLogxK
U2 - 10.1007/s00439-021-02397-7
DO - 10.1007/s00439-021-02397-7
M3 - Article
C2 - 34889978
AN - SCOPUS:85123651761
SN - 0340-6717
VL - 141
SP - 147
EP - 173
JO - Human Genetics
JF - Human Genetics
IS - 1
ER -