Discovering thiamine transporters as targets of chloroquine using a novel functional genomics strategy

PLoS Genet. 2012;8(11):e1003083. doi: 10.1371/journal.pgen.1003083. Epub 2012 Nov 29.

Abstract

Chloroquine (CQ) and other quinoline-containing antimalarials are important drugs with many therapeutic benefits as well as adverse effects. However, the molecular targets underlying most such effects are largely unknown. By taking a novel functional genomics strategy, which employs a unique combination of genome-wide drug-gene synthetic lethality (DGSL), gene-gene synthetic lethality (GGSL), and dosage suppression (DS) screens in the model organism Saccharomyces cerevisiae and is thus termed SL/DS for simplicity, we found that CQ inhibits the thiamine transporters Thi7, Nrt1, and Thi72 in yeast. We first discovered a thi3Δ mutant as hypersensitive to CQ using a genome-wide DGSL analysis. Using genome-wide GGSL and DS screens, we then found that a thi7Δ mutation confers severe growth defect in the thi3Δ mutant and that THI7 overexpression suppresses CQ-hypersensitivity of this mutant. We subsequently showed that CQ inhibits the functions of Thi7 and its homologues Nrt1 and Thi72. In particular, the transporter activity of wild-type Thi7 but not a CQ-resistant mutant (Thi7(T287N)) was completely inhibited by the drug. Similar effects were also observed with other quinoline-containing antimalarials. In addition, CQ completely inhibited a human thiamine transporter (SLC19A3) expressed in yeast and significantly inhibited thiamine uptake in cultured human cell lines. Therefore, inhibition of thiamine uptake is a conserved mechanism of action of CQ. This study also demonstrated SL/DS as a uniquely effective methodology for discovering drug targets.

Publication types

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

MeSH terms

  • Antimalarials / pharmacology*
  • Biological Transport / drug effects
  • Biological Transport / genetics
  • Chloroquine / pharmacology*
  • Gene Expression
  • Genomics
  • Humans
  • Membrane Transport Proteins / genetics
  • Membrane Transport Proteins / metabolism
  • Mutation
  • Nucleoside Transport Proteins* / antagonists & inhibitors
  • Nucleoside Transport Proteins* / genetics
  • Nucleoside Transport Proteins* / metabolism
  • Saccharomyces cerevisiae / genetics
  • Saccharomyces cerevisiae / physiology
  • Saccharomyces cerevisiae Proteins* / antagonists & inhibitors
  • Saccharomyces cerevisiae Proteins* / genetics
  • Saccharomyces cerevisiae Proteins* / metabolism
  • Thiamine / metabolism*

Substances

  • Antimalarials
  • Membrane Transport Proteins
  • Nrt1 protein, S cerevisiae
  • Nucleoside Transport Proteins
  • SLC19A3 protein, human
  • Saccharomyces cerevisiae Proteins
  • Thi72 protein, S cerevisiae
  • Chloroquine
  • Thiamine