Functional filter for whole genome sequence data identifies stress impact, non-coding alternate polyadenylation site variants >5kb from coding DNA

Author:

Xiao SihaoORCID,Kai ZhentianORCID,Murphy Daniel,Li DongyangORCID,Patel Dilip,Bielowka AdriannaORCID,Bernabeu-Herrero Maria E.,Abdulmogith Awatif,Mumford Andrew DORCID,Westbury SarahORCID,Aldred Micheala AORCID,Vargesson NeilORCID,Caulfield Mark JORCID,Shovlin Claire LORCID,

Abstract

AbstractDespite whole genome sequencing (WGS), why do many single gene disorder cases remain unsolved, impeding diagnosis and preventative care for people whose disease-causing variants escape detection? Early WGS data analytic steps prioritize protein-coding sequences. To simultaneously prioritise variants in non-coding regions rich in transcribed and critical regulatory sequences, we developed GROFFFY, an analytic tool which integrates coordinates for regions with experimental evidence of functionality. Applied to WGS data from solved and unsolved hereditary hemorrhagic telangiectasia (HHT) recruits to the 100,000 Genomes Project, GROFFFY-based filtration reduced the mean number of variants per DNA from 4,867,167 to 21,486, without deleting disease-causal variants. In three unsolved cases (two related), GROFFFY identified ultra-rare deletions within the 3’ untranslated region (UTR) of the proto-oncogeneSMAD4, where germline loss-of-function alleles cause combined HHT and colonic polyposis. Sited >5.4kb distal to coding DNA, the deletions did not modify or generate microRNA binding sites, but instead disrupted the sequence context of the final cleavage and polyadenylation site necessary for protein production: By iFoldRNA, an AAUAAA-adjacent 16 nucleotide deletion brought the cleavage site into inaccessible neighboring secondary structures, while a 4-nucleotide deletion unfolded the downstream RNA polymerase II roadblock. MonocyteSMAD4RNA expression differed between patients and controls in resting and cycloheximide-stressed states. Patterns predicted the mutational site for an unrelated case, where a complex insertion was subsequently identified. In conclusion, a new type of functional rare variant is described, exposing novel regulatory systems based on polyadenylation. Extension of coding sequence-focused gene panels is required to capture these variants.

Publisher

Cold Spring Harbor Laboratory

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