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Adam, Rene C; Yang, Hanseul; Ge, Yejing; Infarinato, Nicole R; Gur-Cohen, Shiri; Miao, Yuxuan; Wang, Ping; Zhao, Yilin; Lu, Catherine P; Kim, Jeong E; Ko, Joo Y; Paik, Seung S; Gronostajski, Richard M; Kim, Jaehwan; Krueger, James G; Zheng, Deyou; Fuchs, Elaine
Nature cell biology, 06/2020, Volume: 22, Issue: 6Journal Article
Tissue homeostasis and regeneration rely on resident stem cells (SCs), whose behaviour is regulated through niche-dependent crosstalk. The mechanisms underlying SC identity are still unfolding. Here, using spatiotemporal gene ablation in murine hair follicles, we uncover a critical role for the transcription factors (TFs) nuclear factor IB (NFIB) and IX (NFIX) in maintaining SC identity. Without NFI TFs, SCs lose their hair-regenerating capability, and produce skin bearing striking resemblance to irreversible human alopecia, which also displays reduced NFIs. Through single-cell transcriptomics, ATAC-Seq and ChIP-Seq profiling, we expose a key role for NFIB and NFIX in governing super-enhancer maintenance of the key hair follicle SC-specific TF genes. When NFIB and NFIX are genetically removed, the stemness epigenetic landscape is lost. Super-enhancers driving SC identity are decommissioned, while unwanted lineages are de-repressed ectopically. Together, our findings expose NFIB and NFIX as crucial rheostats of tissue homeostasis, functioning to safeguard the SC epigenome from a breach in lineage confinement that otherwise triggers irreversible tissue degeneration.
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