A structural determinant of mycophenolic acid resistance in eukaryotic inosine 5'-monophosphate dehydrogenases

Protein Sci. 2020 Mar;29(3):686-694. doi: 10.1002/pro.3766. Epub 2019 Nov 20.

Abstract

Mycophenolic acid (MPA) is a potent natural product inhibitor of fungal and other eukaryotic inosine 5'-monophosphate dehydrogenases (IMPDHs) originally isolated from spoiled corn silage. MPA is produced by the filamentous fungi Penicillium brevicompactum, which contains two IMPDHs, PbIMPDHA and PbIMPDHB, both of which are MPA-resistant. The MPA binding sites of these enzymes are identical to MPA-sensitive IMPDHs, so the structural determinants of resistance are unknown. Here we show that a single residue, Ser267, accounts for the MPA resistance of PbIMPDHA. Substitution of Ser267 with Ala, the residue most commonly found in this position in eukaryotic IMPDHs, makes PbIMPDHA sensitive to MPA. Conversely, Aspergillus nidulans IMPDH becomes MPA-resistant when the analogous Ala residue is substituted with Ser. These substitutions have little effect on the catalytic cycles of either enzyme, suggesting the fitness costs are negligible despite the strong conservation of Ala at this position. Intriguingly, while only 1% of fungal IMPDHs contain Ser or Thr at position 267, these residues are found in the IMPDHs from several Aspergillus species that grow at the low temperatures also favored by Penicillium. Perhaps Ser/Thr267 is an evolutionary signature of MPA exposure.

Keywords: Aspergillus; Penicillium; IMP dehydrogenase; IMPDH; guanine nucleotides.

Publication types

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

MeSH terms

  • Antifungal Agents / chemistry
  • Antifungal Agents / pharmacology*
  • Aspergillus / drug effects
  • Aspergillus / enzymology
  • Drug Resistance, Fungal / drug effects*
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology*
  • Eukaryotic Cells / drug effects*
  • Eukaryotic Cells / metabolism
  • IMP Dehydrogenase / antagonists & inhibitors*
  • IMP Dehydrogenase / metabolism
  • Microbial Sensitivity Tests
  • Models, Molecular
  • Molecular Structure
  • Mycophenolic Acid / chemistry
  • Mycophenolic Acid / pharmacology*
  • Penicillium / drug effects*
  • Penicillium / enzymology

Substances

  • Antifungal Agents
  • Enzyme Inhibitors
  • IMP Dehydrogenase
  • Mycophenolic Acid