Biotin-responsive basal ganglia disease-linked mutations inhibit thiamine transport via hTHTR2: biotin is not a substrate for hTHTR2

Am J Physiol Cell Physiol. 2006 Nov;291(5):C851-9. doi: 10.1152/ajpcell.00105.2006. Epub 2006 Jun 21.

Abstract

The water-soluble micronutrient thiamine is required for normal tissue growth and development in humans. Thiamine is accumulated into cells through the activity of two cell surface thiamine transporters (hTHTR1 and hTHTR2), which are differentially targeted in polarized tissues. Mutational dysfunction of hTHTR1 is associated with the clinical condition of thiamine-responsive megaloblastic anemia: the symptoms of which are alleviated by thiamine supplementation. Recently, two hTHTR2 mutants (G23V, T422A) have been discovered in clinical kindreds manifesting biotin-responsive basal ganglia disease (BBGD): the symptoms of which are alleviated by biotin administration. Why then does mutation of a specific thiamine transporter isoform precipitate a disorder correctable by exogenous biotin? To investigate the suggestion that hTHTR2 can physiologically function as a biotin transporter, we examined 1) the cell biological basis of hTHTR2 dysfunction associated with the G23V and T422A mutations and 2) the substrate specificity of hTHTR2 and these clinically relevant mutants. We show that the G23V and T422A mutants both abrogate thiamine transport activity rather than targeting of hTHTR2 to the cell surface. Furthermore, biotin accumulation was not detectable in cells overexpressing either the full length hTHTR2 or the clinically relevant hTHTR2 mutants, yet was demonstrable in the same assay using cells overexpressing the human sodium-dependent multivitamin transporter, a known biotin transporter. These results cast doubt on the most parsimonious explanation for the BBGD phenotype, namely that hTHTR2 is a physiological biotin transporter.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Basal Ganglia Diseases / genetics*
  • Basal Ganglia Diseases / metabolism*
  • Biological Transport / drug effects
  • Biotin / metabolism*
  • Biotin / pharmacology*
  • Caco-2 Cells
  • Conserved Sequence
  • Dogs
  • Gene Expression Regulation
  • Glutamic Acid / chemistry
  • Glycosylation
  • Humans
  • Membrane Transport Proteins / chemistry
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism*
  • Models, Biological
  • Molecular Sequence Data
  • Mutant Proteins / metabolism
  • Point Mutation / genetics*
  • Protein Transport
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Substrate Specificity
  • Thiamine / metabolism*
  • Tritium

Substances

  • Membrane Transport Proteins
  • Mutant Proteins
  • RNA, Messenger
  • SLC19A3 protein, human
  • Tritium
  • Glutamic Acid
  • Biotin
  • Thiamine