Space-time logic of liver gene expression at sub-lobular scale

Nat Metab. 2021 Jan;3(1):43-58. doi: 10.1038/s42255-020-00323-1. Epub 2021 Jan 11.

Abstract

The mammalian liver is a central hub for systemic metabolic homeostasis. Liver tissue is spatially structured, with hepatocytes operating in repeating lobules, and sub-lobule zones performing distinct functions. The liver is also subject to extensive temporal regulation, orchestrated by the interplay of the circadian clock, systemic signals and feeding rhythms. However, liver zonation has previously been analysed as a static phenomenon, and liver chronobiology has been analysed at tissue-level resolution. Here, we use single-cell RNA-seq to investigate the interplay between gene regulation in space and time. Using mixed-effect models of messenger RNA expression and smFISH validations, we find that many genes in the liver are both zonated and rhythmic, and most of them show multiplicative space-time effects. Such dually regulated genes cover not only key hepatic functions such as lipid, carbohydrate and amino acid metabolism, but also previously unassociated processes involving protein chaperones. Our data also suggest that rhythmic and localized expression of Wnt targets could be explained by rhythmically expressed Wnt ligands from non-parenchymal cells near the central vein. Core circadian clock genes are expressed in a non-zonated manner, indicating that the liver clock is robust to zonation. Together, our scRNA-seq analysis reveals how liver function is compartmentalized spatio-temporally at the sub-lobular scale.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Algorithms
  • Amino Acids / metabolism
  • Animals
  • Carbohydrate Metabolism / genetics
  • Circadian Clocks / genetics*
  • Gene Expression / physiology*
  • Gene Expression Profiling
  • Hepatocytes / metabolism
  • Lipid Metabolism / genetics
  • Liver / metabolism*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Molecular Chaperones / metabolism
  • Period Circadian Proteins / genetics
  • Periodicity*
  • RNA, Messenger / biosynthesis
  • RNA, Messenger / genetics
  • Wnt Signaling Pathway / genetics

Substances

  • Amino Acids
  • Molecular Chaperones
  • Period Circadian Proteins
  • RNA, Messenger