TY - JOUR
T1 - Whole-genome sequencing of a sporadic primary immunodeficiency cohort
AU - Primary Immunodeficiency Consortium for the NIHR Bioresource
AU - Thaventhiran, James E D
AU - Lango Allen, Hana
AU - Burren, Oliver S
AU - Rae, William
AU - Greene, Daniel
AU - Staples, Emily
AU - Zhang, Zinan
AU - Farmery, James H R
AU - Simeoni, Ilenia
AU - Rivers, Elizabeth
AU - Maimaris, Jesmeen
AU - Penkett, Christopher J
AU - Stephens, Jonathan
AU - Deevi, Sri V V
AU - Sanchis-Juan, Alba
AU - Gleadall, Nicholas S
AU - Thomas, Moira J
AU - Sargur, Ravishankar B
AU - Gordins, Pavels
AU - Baxendale, Helen E
AU - Brown, Matthew
AU - Tuijnenburg, Paul
AU - Worth, Austen
AU - Hanson, Steven
AU - Linger, Rachel J
AU - Buckland, Matthew S
AU - Rayner-Matthews, Paula J
AU - Gilmour, Kimberly C
AU - Samarghitean, Crina
AU - Seneviratne, Suranjith L
AU - Sansom, David M
AU - Lynch, Andy G
AU - Megy, Karyn
AU - Ellinghaus, Eva
AU - Ellinghaus, David
AU - Jorgensen, Silje F
AU - Karlsen, Tom H
AU - Stirrups, Kathleen E
AU - Cutler, Antony J
AU - Kumararatne, Dinakantha S
AU - Chandra, Anita
AU - Edgar, J David M
AU - Herwadkar, Archana
AU - Cooper, Nichola
AU - Grigoriadou, Sofia
AU - Huissoon, Aarnoud P
AU - Goddard, Sarah
AU - Jolles, Stephen
AU - Lyons, Paul A
AU - Smith, Kenneth G C
AU - Evans, D Gareth
AU - Daniels, M J
N1 - Funding Information:
Acknowledgements The NBR-RD PID Consortium is part of the NIHR BioResource, for which funding was provided by the NIHR (NIHR, grant number RG65966). We acknowledge the participation of all NIHR BioResource volunteers, and thank the NIHR BioResource centre and staff for their contribution. J.E.D.T. is supported by the Medical Research Council (MRC) (RG95376 and MR/L006197/1); A.J.T. is supported by the Wellcome Trust (104807/Z/14/Z) and the NIHR Biomedical Research Centre at Great Ormond Street Hospital for Children NHS Foundation Trust and University College London; K.G.C.S. is supported by the MRC (programme grant MR/L019027) and is a Wellcome Investigator; A.J.C. was supported by the Wellcome Trust (091157/Z/10/Z, 107212/Z/15/Z, 100140/Z/12/Z, 203141/Z/16/Z), JDRF (9-2011-253, 5-SRA-2015-130-A-N), NIHR Oxford Biomedical Research Centre and NIHR Cambridge Biomedical Research Centre; E.E. has received funding from the European Union Seventh Framework Programme (FP7-PEOPLE-2013-COFUND) under grant agreement number 609020-Scientia Fellows; E.R. is supported by the Wellcome Trust (201250/Z/16/Z); D.E. is supported by the German Federal Ministry of Education and Research (BMBF) within the framework of the e:Med research and funding concept (SysInflame grant 01ZX1306A; GB-XMAP grant 01ZX1709) and funded by the Deutsche Forschungsgemeinschaft (DFG; German Research Foundation) under Germany’s Excellence Strategy (EXC 2167-390884018). The NIHR Cambridge Biomedical Research Centre (BRC) is a partnership between Cambridge University Hospitals NHS Foundation Trust and the University of Cambridge, funded by the NIHR. This research was co-funded by the support listed above and the NIHR Cambridge BRC.
Publisher Copyright:
© 2020, The Author(s), under exclusive licence to Springer Nature Limited.
Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.
PY - 2020/5/6
Y1 - 2020/5/6
N2 - Primary immunodeficiency (PID) is characterized by recurrent and often life-threatening infections, autoimmunity and cancer, and it poses major diagnostic and therapeutic challenges. Although the most severe forms of PID are identified in early childhood, most patients present in adulthood, typically with no apparent family history and a variable clinical phenotype of widespread immune dysregulation: about 25% of patients have autoimmune disease, allergy is prevalent and up to 10% develop lymphoid malignancies1-3. Consequently, in sporadic (or non-familial) PID genetic diagnosis is difficult and the role of genetics is not well defined. Here we address these challenges by performing whole-genome sequencing in a large PID cohort of 1,318 participants. An analysis of the coding regions of the genome in 886 index cases of PID found that disease-causing mutations in known genes that are implicated in monogenic PID occurred in 10.3% of these patients, and a Bayesian approach (BeviMed4) identified multiple new candidate PID-associated genes, including IVNS1ABP. We also examined the noncoding genome, and found deletions in regulatory regions that contribute to disease causation. In addition, we used a genome-wide association study to identify loci that are associated with PID, and found evidence for the colocalization of-and interplay between-novel high-penetrance monogenic variants and common variants (at the PTPN2 and SOCS1 loci). This begins to explain the contribution of common variants to the variable penetrance and phenotypic complexity that are observed in PID. Thus, using a cohort-based whole-genome-sequencing approach in the diagnosis of PID can increase diagnostic yield and further our understanding of the key pathways that influence immune responsiveness in humans.
AB - Primary immunodeficiency (PID) is characterized by recurrent and often life-threatening infections, autoimmunity and cancer, and it poses major diagnostic and therapeutic challenges. Although the most severe forms of PID are identified in early childhood, most patients present in adulthood, typically with no apparent family history and a variable clinical phenotype of widespread immune dysregulation: about 25% of patients have autoimmune disease, allergy is prevalent and up to 10% develop lymphoid malignancies1-3. Consequently, in sporadic (or non-familial) PID genetic diagnosis is difficult and the role of genetics is not well defined. Here we address these challenges by performing whole-genome sequencing in a large PID cohort of 1,318 participants. An analysis of the coding regions of the genome in 886 index cases of PID found that disease-causing mutations in known genes that are implicated in monogenic PID occurred in 10.3% of these patients, and a Bayesian approach (BeviMed4) identified multiple new candidate PID-associated genes, including IVNS1ABP. We also examined the noncoding genome, and found deletions in regulatory regions that contribute to disease causation. In addition, we used a genome-wide association study to identify loci that are associated with PID, and found evidence for the colocalization of-and interplay between-novel high-penetrance monogenic variants and common variants (at the PTPN2 and SOCS1 loci). This begins to explain the contribution of common variants to the variable penetrance and phenotypic complexity that are observed in PID. Thus, using a cohort-based whole-genome-sequencing approach in the diagnosis of PID can increase diagnostic yield and further our understanding of the key pathways that influence immune responsiveness in humans.
KW - Actin-Related Protein 2-3 Complex/genetics
KW - Bayes Theorem
KW - Cohort Studies
KW - Female
KW - Genome-Wide Association Study
KW - Humans
KW - Male
KW - Primary Immunodeficiency Diseases/diagnosis
KW - Protein Tyrosine Phosphatase, Non-Receptor Type 2/genetics
KW - RNA-Binding Proteins/genetics
KW - Regulatory Sequences, Nucleic Acid/genetics
KW - Suppressor of Cytokine Signaling 1 Protein/genetics
KW - Transcription Factors/genetics
KW - Whole Genome Sequencing
UR - http://dx.doi.org/10.1038/s41586-020-2265-1
U2 - 10.1038/s41586-020-2265-1
DO - 10.1038/s41586-020-2265-1
M3 - Article
C2 - 32499645
SN - 0028-0836
VL - 583
SP - 90
EP - 95
JO - Nature
JF - Nature
IS - 7814
ER -