Alpha-carboxy nucleoside phosphonates as universal nucleoside triphosphate mimics

Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3475-80. doi: 10.1073/pnas.1420233112. Epub 2015 Mar 2.

Abstract

Polymerases have a structurally highly conserved negatively charged amino acid motif that is strictly required for Mg(2+) cation-dependent catalytic incorporation of (d)NTP nucleotides into nucleic acids. Based on these characteristics, a nucleoside monophosphonate scaffold, α-carboxy nucleoside phosphonate (α-CNP), was designed that is recognized by a variety of polymerases. Kinetic, biochemical, and crystallographic studies with HIV-1 reverse transcriptase revealed that α-CNPs mimic the dNTP binding through a carboxylate oxygen, two phosphonate oxygens, and base-pairing with the template. In particular, the carboxyl oxygen of the α-CNP acts as the potential equivalent of the α-phosphate oxygen of dNTPs and two oxygens of the phosphonate group of the α-CNP chelate Mg(2+), mimicking the chelation by the β- and γ-phosphate oxygens of dNTPs. α-CNPs (i) do not require metabolic activation (phosphorylation), (ii) bind directly to the substrate-binding site, (iii) chelate one of the two active site Mg(2+) ions, and (iv) reversibly inhibit the polymerase catalytic activity without being incorporated into nucleic acids. In addition, α-CNPs were also found to selectively interact with regulatory (i.e., allosteric) Mg(2+)-dNTP-binding sites of nucleos(t)ide-metabolizing enzymes susceptible to metabolic regulation. α-CNPs represent an entirely novel and broad technological platform for the development of specific substrate active- or regulatory-site inhibitors with therapeutic potential.

Keywords: (deoxy)nucleoside triphosphate mimic; HIV reverse transcriptase; allosteric inhibition; alpha-carboxy nucleoside phosphonate; herpes virus DNA polymerase.

Publication types

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

MeSH terms

  • Allosteric Regulation / drug effects
  • Base Sequence
  • Biocatalysis / drug effects
  • Cell Extracts
  • DNA-Directed DNA Polymerase / metabolism
  • Drug Resistance, Viral / drug effects
  • HIV Reverse Transcriptase / antagonists & inhibitors
  • HIV Reverse Transcriptase / chemistry
  • HIV Reverse Transcriptase / metabolism
  • HeLa Cells
  • Humans
  • Kinetics
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation / genetics
  • Nucleosides / chemistry
  • Nucleosides / pharmacology*
  • Nucleotides / chemistry
  • Nucleotides / pharmacology*
  • Organophosphonates / chemistry
  • Organophosphonates / pharmacology*
  • Reverse Transcriptase Inhibitors / chemistry
  • Reverse Transcriptase Inhibitors / pharmacology
  • Stereoisomerism

Substances

  • Cell Extracts
  • Nucleosides
  • Nucleotides
  • Organophosphonates
  • Reverse Transcriptase Inhibitors
  • reverse transcriptase, Human immunodeficiency virus 1
  • HIV Reverse Transcriptase
  • DNA-Directed DNA Polymerase

Associated data

  • PDB/4R5P