Impaired Bile Secretion Promotes Hepatobiliary Injury in Sickle Cell Disease

Hepatology. 2020 Dec;72(6):2165-2181. doi: 10.1002/hep.31239. Epub 2020 Nov 13.

Abstract

Background and aims: Hepatic crisis is an emergent complication affecting patients with sickle cell disease (SCD); however, the molecular mechanism of sickle cell hepatobiliary injury remains poorly understood. Using the knock-in humanized mouse model of SCD and SCD patient blood, we sought to mechanistically characterize SCD-associated hepato-pathophysiology applying our recently developed quantitative liver intravital imaging, RNA sequence analysis, and biochemical approaches.

Approach and results: SCD mice manifested sinusoidal ischemia, progressive hepatomegaly, liver injury, hyperbilirubinemia, and increased ductular reaction under basal conditions. Nuclear factor kappa B (NF-κB) activation in the liver of SCD mice inhibited farnesoid X receptor (FXR) signaling and its downstream targets, leading to loss of canalicular bile transport and altered bile acid pool. Intravital imaging revealed impaired bile secretion into the bile canaliculi, which was secondary to loss of canalicular bile transport and bile acid metabolism, leading to intrahepatic bile accumulation in SCD mouse liver. Blocking NF-κB activation rescued FXR signaling and partially ameliorated liver injury and sinusoidal ischemia in SCD mice.

Conclusions: These findings identify that NF-κB/FXR-dependent impaired bile secretion promotes intrahepatic bile accumulation, which contributes to hepatobiliary injury of SCD. Improved understanding of these processes could potentially benefit the development of therapies to treat sickle cell hepatic crisis.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Video-Audio Media

MeSH terms

  • Adolescent
  • Adult
  • Anemia, Sickle Cell / blood
  • Anemia, Sickle Cell / complications*
  • Anemia, Sickle Cell / drug therapy
  • Anemia, Sickle Cell / genetics
  • Animals
  • Bile / metabolism*
  • Bile Ducts, Intrahepatic / diagnostic imaging
  • Bile Ducts, Intrahepatic / pathology
  • Cholestasis / etiology*
  • Cholestasis / pathology
  • Cholestasis / prevention & control
  • Disease Models, Animal
  • Female
  • Gene Knock-In Techniques
  • Hemoglobin, Sickle / genetics
  • Hepatic Insufficiency / etiology*
  • Hepatic Insufficiency / pathology
  • Hepatic Insufficiency / prevention & control
  • Humans
  • Intravital Microscopy
  • Liver / diagnostic imaging
  • Liver / pathology*
  • Male
  • Mice
  • Middle Aged
  • NF-kappa B / antagonists & inhibitors
  • NF-kappa B / drug effects
  • NF-kappa B / metabolism
  • Receptors, Cytoplasmic and Nuclear / metabolism
  • Signal Transduction / drug effects
  • Young Adult

Substances

  • Hemoglobin, Sickle
  • NF-kappa B
  • Receptors, Cytoplasmic and Nuclear
  • farnesoid X-activated receptor