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Skin and lung fibrosis in systemic sclerosis (SSc) is driven by myofibroblasts, alpha-smooth muscle actin expressing cells. The number of myofibroblasts in SSc skin correlates with the modified Rodnan skin score, the most widely used clinical measure of skin disease severity. Murine fibrosis models indicate that myofibroblasts can arise from a variety of different cell types, but their origin in SSc skin has remained uncertain. Utilizing single cell RNA-sequencing, we define different dermal fibroblast populations and transcriptome changes, comparing SSc to healthy dermal fibroblasts. Here, we show that SSc dermal myofibroblasts arise in two steps from an  SFRP2  hi  /DPP4 -expressing progenitor fibroblast population. In the first step, SSc fibroblasts show globally upregulated expression of transcriptome markers, such as  PRSS23  and  THBS1 . A subset of these cells shows markers indicating that they are proliferating. Only a fraction of  SFRP2  hi  SSc fibroblasts differentiate into myofibroblasts, as shown by expression of additional markers,  SFRP4  and  FNDC1 . Bioinformatics analysis of the SSc fibroblast transcriptomes implicated upstream transcription factors, including  FOSL2 ,  RUNX1 ,  STAT1, FOXP1, IRF7  and  CREB3L1 , as well as  SMAD3 , driving SSc myofibroblast differentiation.

Myofibroblast transcriptome indicates SFRP2hi fibroblast progenitors in systemic sclerosis skin