Convergent downstream candidate mechanisms of independent intergenic polymorphisms between co-classified diseases implicate epistasis among noncoding elements

Jiali Han, Jianrong Li and Ikbel Achour†,[2]&

Center for Biomedical Informatics and Biostatistics (CB2)

Departments of Medicine and of Systems and Industrial Engineering,

The University of Arizona, Tucson, AZ 85721, USA
Email: jialih@email.arizona.edu, jianrong@email.arizona.edu,ikachour@gmail.com

 

Lorenzo Pesce and Ian Foster

Computation Institute, Argonne National Laboratory and University of Chicago, Chicago, IL 60637, USA
Email: lpesce
@cs.uchicago.edu, foster@cs.uchicago.edu

Haiquan Li* and Yves A. Lussier*

CB2, BIO5 Institute, UACC, and Dept of Medicine, The University of Arizona, Tucson, AZ 85721, USA
Email: haiquan@email.arizona.edu, yves@email.arizona.edu

Authors contributed equally to this work conducted at The Universities of Arizona and of Illinois

[1]& now employed at AstraZeneca MedImmune

* Corresponding authors contributed equally to this work

 

Eighty percent of DNA outside protein coding regions was shown biochemically functional by the ENCODE project, enabling studies of their interactions. Studies have since explored how convergent downstream mechanisms arise from independent genetic risks of one complex disease. However, the cross-talk and epistasis between intergenic risks associated with distinct complex diseases have not been comprehensively characterized. Our recent integrative genomic analysis unveiled downstream biological effectors of disease-specific polymorphisms buried in intergenic regions, and we then validated their genetic synergy and antagonism in distinct GWAS. We extend this approach to characterize convergent downstream candidate mechanisms of distinct intergenic SNPs across distinct diseases within the same clinical classification. We construct a multipartite network consisting of 467 diseases organized in 15 classes, 2,358 disease-associated SNPs, 6,301 SNP-associated mRNAs by eQTL, and mRNA annotations to 4,538 Gene Ontology mechanisms. Functional similarity between two SNPs (similar SNP pairs) is imputed using a nested information theoretic distance model for which p-values are assigned by conservative scale-free permutation of network edges without replacement (node degrees constant). At FDR≤5%, we prioritized 3,870 intergenic SNP pairs associated, among which, 755 that are associated with distinct diseases sharing the same disease class, implicating 167 intergenic SNPs, 14 classes, 230 mRNAs, and 134 GO terms. Co-classified SNP pairs were more likely to be prioritized as compared to those of distinct classes confirming a noncoding genetic underpinning to clinical classification (odds ratio ~3.8; p≤10-25). The prioritized pairs were also enriched in regions bound to the same/interacting transcription factors and/or interacting in long-range chromatin interactions suggestive of epistasis (odds ratio ~ 2,500; p≤10-25). This prioritized network implicates complex epistasis between intergenic polymorphisms of co-classified diseases and offers a roadmap for a novel therapeutic paradigm: repositioning medications that target proteins within downstream mechanisms of intergenic disease-associated SNPs. Supplementary information and software: http://lussiergroup.org/publications/disease_class

Keywords: SNP; Intergenic; Noncoding; Disease class; Biological similarity; Enrichment.

Supplements

Disease classes curated from disease/trait terms in the NHGRI GWAS catalog
Calculation of SNP ITS
permution of eQTL network