ABCB4 missense mutations D243A, K435T, G535D, I490T, R545C, and S978P significantly impair the lipid floppase and likely predispose to secondary pathologies in the human population

Cell Mol Life Sci. 2017 Jul;74(13):2513-2524. doi: 10.1007/s00018-017-2472-6. Epub 2017 Feb 20.

Abstract

Bile salts are natural detergents required to solubilise dietary fat and lipid soluble vitamins. They are synthesised in hepatocytes and secreted into the luminal space of the biliary tree by the bile salt export pump (BSEP), an ATP-binding cassette (ABC) transporter in the canalicular membrane. BSEP deficiency causes cytotoxic accumulation of bile salts in the hepatocyte that results in mild-to-severe forms of cholestasis. The resulting inflammation can also progress to hepatocellular cancer via a novel mechanism involving upregulation of proliferative signalling pathways. A second ABC transporter of the canalicular membrane is also critical for bile formation. ABCB4 flops phosphatidylcholine into the outer leaflet of the membrane to be extracted by bile salts in the canalicular space. These mixed micelles reduce the detergent action of the bile salts and protect the biliary tree from their cytotoxic activity. ABCB4 deficiency also causes cholestasis, and might be expected to cause cholangitis and predispose to liver cancer. Non-synonymous SNPs in ABCB4 have now been described in patients with liver cancer or with inflammatory liver diseases that are known to predispose to cancer, but data showing that the SNPs are sufficiently deleterious to be an etiological factor are lacking. Here, we report the first characterisation at the protein level of six ABCB4 variants (D243A, K435T, G535D, I490T, R545C, and S978P) previously found in patients with inflammatory liver diseases or liver cancer. All significantly impair the transporter with a range of phenotypes exhibited, including low abundance, intracellular retention, and reduced floppase activity, suggesting that ABCB4 deficiency is the root cause of the pathology in these cases.

Keywords: Bile flow; Biliary cirrhosis; Cholestasis; Inflammatory liver disease; Liver cancer; MDR3; Sclerosing cholangitis.

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B / genetics*
  • Adenosine Triphosphatases / metabolism*
  • Amino Acid Substitution / genetics*
  • Cell Membrane / metabolism
  • Cyclosporine / pharmacology
  • Genetic Predisposition to Disease*
  • Glycosylation
  • HEK293 Cells
  • Humans
  • Intracellular Space / metabolism
  • Lipids / chemistry*
  • Molecular Chaperones / metabolism
  • Mutant Proteins / metabolism
  • Mutation, Missense / genetics*
  • Phosphatidylcholines / metabolism
  • Polymorphism, Single Nucleotide / genetics
  • Protein Stability / drug effects
  • Protein Transport / drug effects
  • Subcellular Fractions / metabolism

Substances

  • ATP Binding Cassette Transporter, Subfamily B
  • Lipids
  • Molecular Chaperones
  • Mutant Proteins
  • Phosphatidylcholines
  • Cyclosporine
  • multidrug resistance protein 3
  • Adenosine Triphosphatases
  • ATP8B1 protein, human