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Pervasive Sharing of Genetic Effects in Autoimmune Disease
Open accessAbstract
Genome-wide association (GWA) studies have identified numerous, replicable, genetic associations between common single nucleotide polymorphisms (SNPs) and risk of common autoimmune and inflammatory (immune-mediated) diseases, some of which are shared between two diseases. Along with epidemiological and clinical evidence, this suggests that some genetic risk factors may be shared across diseases-as is the case with alleles in the Major Histocompatibility Locus. In this work we evaluate the extent of this sharing for 107 immune disease-risk SNPs in seven diseases: celiac disease, Crohn's disease, multiple sclerosis, psoriasis, rheumatoid arthritis, systemic lupus erythematosus, and type 1 diabetes. We have developed a novel statistic for Cross Phenotype Meta-Analysis (CPMA) which detects association of a SNP to multiple, but not necessarily all, phenotypes. With it, we find evidence that 47/107 (44%) immune-mediated disease risk SNPs are associated to multiple-but not all-immune-mediated diseases (SNP-wise P(CPMA)<0.01). We also show that distinct groups of interacting proteins are encoded near SNPs which predispose to the same subsets of diseases; we propose these as the mechanistic basis of shared disease risk. We are thus able to leverage genetic data across diseases to construct biological hypotheses about the underlying mechanism of pathogenesis.
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![Figure 1 Patterns of association across diseases correlate with protein-protein interactions. A: 47 SNPs with evidence of association to multiple diseases (Pcpma<0.01) fall into groups clustered by the pattern of association across diseases. Clusters are numbered arbitrarily. B: Clusters show different patterns of association across diseases. We summarize the differential disease effects of each cluster with a cumulative association statistic (Fisher's method for combining p values). These patterns are different for each cluster, suggesting each represents a different co-morbid mechanism. Note that these figures are based on the same underlying association statistics the clustering in the first panel is derived from. C: proteins encoded within the linkage disequilibrium scope around SNPs in the same cluster interact either directly or via common intermediates. Three of our four clusters have significant protein inter-connectivity (permuted P<0.05; see Materials and Methods and [19] for details).](/paper-figures/38746ea8fd7b4dd18eb89497c065b1ad/pervasive-sharing-of-genetic-effects-in-autoimmune-disease-figure-1.jpg)
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“many loci were associated with multiple diseases and that the genes encoded in those loci fall into distinct immune pathways.69, 70”
From Genome‐wide association studies of multiple sclerosis (2018) · cites this paper as [70]
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“These results suggest that perturbations to key immune processes mediate risk to multiple diseases.”
From Genome‐wide association studies of multiple sclerosis (2018) · cites this paper as [70]
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“Some of these relationships are expected, such as the impact of obesity variants on risk of hepatic steatosis and type 2 diabetes84 or variants that influence multiple autoimmune conditions85.”
From A brief history of human disease genetics (2020) · cites this paper as [85]
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Metadata
- Authors
- Cotsapas, C., Voight, B. F., Rossin, E., Lage, K., Neale, B. M., Wallace, C., Abecasis, G. R., Barrett, J. C., Behrens, T., Cho, J., De Jager, P. L., Elder, J. T., Graham, R. R., Gregersen, P., Klareskog, L., Siminovitch, K. A., van Heel, D. A., Wijmenga, C., Worthington, J., Todd, J. A., Hafler, D. A., Rich, S. S., Daly, M. J., & on behalf of the FOCiS Network of Consortia
- Affiliations
- Massachusetts General Hospital (US)
- Broad Institute (US)
- University of Cambridge (GB)
- University of Michigan (US)
- Wellcome Sanger Institute (GB)
- Genentech (US)
- Yale University (US)
- Northwell Health (US)
- Karolinska Institutet (SE)
- Mount Sinai Hospital (CA)
- University Medical Center Groningen (NL)
- Manchester Academic Health Science Centre (GB)
- University of Virginia (US)
- Corresponding author
- Daly, Mark J.
- ORCID
- Cotsapas, Chris
- Voight, Benjamin F.
- Rossin, Elizabeth
- Lage, Kasper
- Neale, Benjamin M.
- Wallace, Chris
- Abecasis, Gonçalo R.
- Barrett, Jeffrey C.
- Behrens, Timothy
- Cho, Judy
- Elder, James T.
- Graham, Robert R.
- Gregersen, Peter
- Klareskog, Lars
- Wijmenga, Cisca
- Worthington, Jane
- Todd, John A.
- Hafler, David A.
- Rich, Stephen S.
- Daly, Mark J.
- Venue
- PLoS Genetics
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-08-10
- Volume
- 7
- Issue
- 8
- Pages
- e1002254
- ISSN
- 1553-7390 (ISSN-L)
- 1553-7404
- PMC
- PMC3154137
- OpenAlex
- W1859891932
- Cited by
- 606
- References
- 30
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 21 · 2023: 26 · 2022: 26 · 2021: 27 · 2020: 40 · 2019: 37 · 2018: 40 · 2017: 77 · 2016: 40 · 2015: 54 · 2014: 57 · 2013: 63 · 2012: 52
- FWCI
- 6.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS Genetics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Research Explorer (The University of Manchester) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Figshare (submittedVersion, cc-by)
- Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) (submittedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Queen Mary Research Online (Queen Mary University of London) (submittedVersion, cc-by)
- PLoS eBooks
- Funders
- Wellcome Trust (091157, 089989)
- National Institute for Health and Care Research (NF-SI-0508-10275)
- Versus Arthritis (/17552)
- National Institute of General Medical Sciences (T32GM007753)
- National Institute of Diabetes and Digestive and Kidney Diseases (P30DK043351)
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (R01AR050511, R01AR042742, R01AR054966)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Mapping and Diversity in Plants and Animals
- Keywords
- autoimmune disease, shared genetic risk, immune-mediated diseases, single nucleotide polymorphisms, celiac disease, Crohn's disease, multiple sclerosis, psoriasis, rheumatoid arthritis, systemic lupus erythematosus, type 1 diabetes, protein-protein interaction network, pathogenesis, MHC locus
- MeSH terms
- Autoimmune Diseases, Humans, Phenotype, Comorbidity, Cluster Analysis, Polymorphism, Single Nucleotide, Genome-Wide Association Study, Genetic Loci, Protein Interaction Maps
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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