Rheumatoid arthritis (RA) is an autoimmune disease which disproportionately affects females. In concert with sex hormones, X-linked genes perturb key signalling pathways in immune cell types and may contribute towards sex bias in autoimmune disease. It has been proposed that incomplete or escape from X chromosome inactivation (XCI) contributes towards heightened immune responses and breakdown of self-tolerance.
To test the influence of X-linked genes on RA, we analysed single-cell RNA-sequencing data from PBMCs on a subset of female individuals with RA (n=10) from the OneK1K dataset. We first assessed differences in cell-type proportion, and then performed differential expression analysis in a cell-type specific manner with an age matched set of controls (n=23). We subsequently tested for the overlap of significantly differentially expressed and X-linked genes to measure enrichment for X-escapers, immune genes and signalling pathways.
Approximately 1,300 cells were sequenced per individual, and 30 immune cell-types and subtypes identified. We observed significant differences in cell-type proportions of CD14+ Monocytes and CD4 CTL (T-cells) between cases and controls, suggesting roles for these cell- types in RA aetiology. Pseudobulking and applying edgeR-LRT returned fewer significant genes per cell-type (FDR<0.05, mean=2.7±3.8 DEGs) compared to the single-cell approach (FDR<0.05, mean=24.2±49.8 DEGs) but with high concordance (>0.98%). By ranking genes by FDR and log2 fold change, we see chromosome X gene enrichment in B memory cells (Wilcoxon p = 0.05). Interestingly, we found enrichment of X escape genes in RA relevant cells including, B memory cells (Wilcoxon p = 0.009) and T regulatory (Treg) cells (Wilcoxon p = 0.039). These RA DEGs were enriched for immune functions (p = 1.53x10-9), suggesting a role in activating RA pro-inflammatory signalling pathways.
Through analysing the transcriptome at a single cell resolution, we have identified inflammatory pathways which are unbalanced by X-linked genes, in particular XCI escape genes.