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Non-coding autoimmune risk variant accelerates T peripheral helper cell development via ICOS

Nigrovic, P. A.; Kim, T.; Martinez-Bonet, M.; Wang, Q.; Hackert, N.; Sparks, J. A.; Baglaenko, Y.; Koh, B.-H.; Darbousset, R.; Laza-Briviesca, R.; Chen, X.; Gutierrez-Arcelus, M.; Westra, H.-J.; Weirauch, M. T.; Raychaudhuri, S.; Rao, D. A.

2022-12-16 genetics
10.1101/2022.12.16.520733 bioRxiv
Show abstract

Fine-mapping and functional studies implicate rs117701653, a common non-coding variant in the CD28/CTLA4/ICOS locus, as a contributor to risk for rheumatoid arthritis and type 1 diabetes. Using DNA pulldown, mass spectrometry, genome editing and eQTL analysis, we establish that the disease-associated allele reduces affinity for the inhibitory chromosomal regulator SMCHD1 to drive expression of inducible T-cell costimulator (ICOS), enhancing memory CD4+ T cell ICOS expression in individuals bearing the risk allele. Higher ICOS expression is paralleled by an increase in circulating T peripheral helper (Tph) cells, and in rheumatoid arthritis patients, of blood and joint fluid Tph cells and circulating plasmablasts, suggesting a causal link. Indeed, ICOS ligation accelerates T cell differentiation into CXCR5-PD-1high Tph cells producing IL-21 and CXCL13, as does carriage of the rs117701653 risk allele. Thus, mechanistic dissection of a causal non-coding variant in human autoimmunity discloses a new pathway through which ICOS regulates Tph abundance.

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