Autoimmune diseases, including systemic lupus erythematosus (SLE), present a strong gender bias with 80% of patients being women. The second X chromosome in XX females is normally silenced by an epigenetic process, X chromosome inactivation (XCI). However, recent studies revealed that lncRNA XIST, a master-regulator of XCI, transiently dissociates from the epigenetically silenced X (Xi) during normal development of immune cells [1], implying the possibility of partial X-reactivation in females.
This suggests that increased X chromosome dosage could contribute to autoimmune disease susceptibility, however this phenomenon lacks mechanistic and functional evidence. We aim to determine if X-chromosome reactivation is enriched in autoreactive-B-cells and if it's required for normal female B-cell development.
To address this, we performed allele-specific long-read single-cell transcriptional profiling coupled with whole-genome sequencing and B-cell-receptor sequencing of B-lymphocytes isolated from bone marrow and peripheral blood of healthy controls and patients with SLE.
We found that the largest increase in reactivated Xi-genes during B-lymphocyte development occurred in pro and pre-B cells. This aligns with reported XIST dissociation at these developmental stages, which are characterised by VDJ-recombination, integral to antigen recognition. For example, CD99, involved in immune cell adhesion and migration, was expressed from the Xi in 99% of cells at the pro-B stage. In peripheral blood naïve and memory B-cells, we observed significantly increased Xi-reactivation in SLE patients versus healthy controls.
For the first time, allele-specific long-read profiling has quantitatively resolved Xi-reactivation at gene and developmental-stage by identifying expression directly from the Xi. Establishing Xi-reactivation as a regulated feature of immune cell development provides a framework to mechanistically explore X-dosage effects. We plan to further investigate the mechanism of Xi-reactivation using CRISPR screens in cell lines, and to determine the importance of reactivated genes in SLE using CRISPR activation in a mouse model.