Human bile acid transporter ASBT (SLC10A2) forms functional non-covalent homodimers and higher order oligomers

Biochim Biophys Acta Biomembr. 2018 Mar;1860(3):645-653. doi: 10.1016/j.bbamem.2017.11.016. Epub 2017 Dec 1.

Abstract

The human apical sodium-dependent bile acid transporter, hASBT/SLC10A2, plays a central role in cholesterol homeostasis via the efficient reabsorption of bile acids from the distal ileum. hASBT has been shown to self-associate in higher order complexes, but while the functional role of endogenous cysteines has been reported, their implication in the oligomerization of hASBT remains unresolved. Here, we determined the self-association architecture of hASBT by site-directed mutagenesis combined with biochemical, immunological and functional approaches. We generated a cysteine-less form of hASBT by creating point mutations at all 13 endogenous cysteines in a stepwise manner. Although Cysless hASBT had significantly reduced function correlated with lowered surface expression, it featured an extra glycosylation site that facilitated its differentiation from wt-hASBT on immunoblots. Decreased protein expression was associated with instability and subsequent proteasome-dependent degradation of Cysless hASBT protein. Chemical cross-linking of wild-type and Cysless species revealed that hASBT exists as an active dimer and/or higher order oligomer with apparently no requirement for endogenous cysteine residues. This was further corroborated by co-immunoprecipitation of differentially tagged (HA-, Flag-) wild-type and Cysless hASBT. Finally, Cysless hASBT exhibited a dominant-negative effect when co-expressed with wild-type hASBT which validated heterodimerization/oligomerization at the functional level. Combined, our data conclusively demonstrate the functional existence of hASBT dimers and higher order oligomers irrespective of cysteine-mediated covalent bonds, thereby providing greater understanding of its topological assembly at the membrane surface.

Keywords: Bile acid; Epitope tag; Intestinal absorption; Transporter.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Transport
  • COS Cells
  • Cell Membrane / metabolism
  • Chlorocebus aethiops
  • Cysteine / chemistry*
  • Cystine / chemistry
  • Genes, Dominant
  • Glycosylation
  • Humans
  • Immunoprecipitation
  • Mutagenesis, Site-Directed
  • Organic Anion Transporters, Sodium-Dependent / chemistry*
  • Organic Anion Transporters, Sodium-Dependent / genetics
  • Peptide Fragments / metabolism
  • Proteasome Endopeptidase Complex / metabolism
  • Protein Multimerization
  • Protein Processing, Post-Translational
  • Protein Stability
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Symporters / chemistry*
  • Symporters / genetics
  • Taurocholic Acid / metabolism

Substances

  • Organic Anion Transporters, Sodium-Dependent
  • Peptide Fragments
  • Recombinant Proteins
  • Symporters
  • sodium-bile acid cotransporter
  • Cystine
  • Taurocholic Acid
  • Proteasome Endopeptidase Complex
  • Cysteine