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[Preprint]. 2024 Jul 9:2024.07.06.602336. [Version 1] doi: 10.1101/2024.07.06.602336

ESRP2-microRNA-122 axis directs the postnatal onset of liver polyploidization and maturation

Sushant Bangru, Jackie Chen, Nicholas Baker, Diptatanu Das, Ullas V Chembazhi, Jessica M Derham, Sandip Chorghade, Waqar Arif, Frances Alencastro, Andrew W Duncan, Russ P Carstens, Auinash Kalsotra
PMCID: PMC11257421  PMID: 39026848

SUMMARY

Hepatocyte polyploidy and maturity are critical to acquiring specialized liver functions. Multiple intra- and extracellular factors influence ploidy, but how they cooperate temporally to steer liver polyploidization and maturation or how post-transcriptional mechanisms integrate into these paradigms is unknown. Here, we identified an important regulatory hierarchy in which postnatal activation of Epithelial-Splicing-Regulatory-Protein-2 (ESRP2) stimulates biogenesis of liver-specific microRNA (miR-122), thereby facilitating polyploidization, maturation, and functional competence of hepatocytes. By determining transcriptome-wide protein-RNA interactions in vivo and integrating them with single-cell and bulk hepatocyte RNA-seq datasets, we delineate an ESRP2-driven RNA processing program that drives sequential replacement of fetal-to-adult transcript isoforms. Specifically, ESRP2 binds the primary miR-122 host gene transcript to promote its processing/biogenesis. Combining constitutive and inducible ESRP2 gain- and loss-of-function mice models with miR-122 rescue experiments, we demonstrate that timed activation of ESRP2 augments miR-122-driven program of cytokinesis failure, ensuring proper onset and extent of hepatocyte polyploidization.

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