Role of a "Magic" Methyl: 2'-Deoxy-2'-α-F-2'-β- C-methyl Pyrimidine Nucleotides Modulate RNA Interference Activity through Synergy with 5'-Phosphate Mimics and Mitigation of Off-Target Effects

J Am Chem Soc. 2022 Aug 17;144(32):14517-14534. doi: 10.1021/jacs.2c01679. Epub 2022 Aug 3.

Abstract

Although 2'-deoxy-2'-α-F-2'-β-C-methyl (2'-F/Me) uridine nucleoside derivatives are a successful class of antiviral drugs, this modification had not been studied in oligonucleotides. Herein, we demonstrate the facile synthesis of 2'-F/Me-modified pyrimidine phosphoramidites and their subsequent incorporation into oligonucleotides. Despite the C3'-endo preorganization of the parent nucleoside, a single incorporation into RNA or DNA resulted in significant thermal destabilization of a duplex due to unfavorable enthalpy, likely resulting from steric effects. When located at the terminus of an oligonucleotide, the 2'-F/Me modification imparted more resistance to degradation than the corresponding 2'-fluoro nucleotides. Small interfering RNAs (siRNAs) modified at certain positions with 2'-F/Me had similar or better silencing activity than the parent siRNAs when delivered via a lipid nanoparticle formulation or as a triantennary N-acetylgalactosamine conjugate in cells and in mice. Modification in the seed region of the antisense strand at position 6 or 7 resulted in an activity equivalent to the parent in mice. Additionally, placement of the antisense strand at position 7 mitigated seed-based off-target effects in cell-based assays. When the 2'-F/Me modification was combined with 5'-vinyl phosphonate, both E and Z isomers had silencing activity comparable to the parent. In combination with other 2'-modifications such as 2'-O-methyl, the Z isomer is detrimental to silencing activity. Presumably, the equivalence of 5'-vinyl phosphonate isomers in the context of 2'-F/Me is driven by the steric and conformational features of the C-methyl-containing sugar ring. These data indicate that 2'-F/Me nucleotides are promising tools for nucleic acid-based therapeutic applications to increase potency, duration, and safety.

MeSH terms

  • Animals
  • Liposomes
  • Mice
  • Models, Molecular
  • Nanoparticles
  • Nucleic Acid Conformation
  • Nucleosides
  • Nucleotides
  • Oligonucleotides
  • Organophosphonates*
  • Phosphates
  • Pyrimidine Nucleotides*
  • RNA Interference
  • RNA, Small Interfering / genetics

Substances

  • Lipid Nanoparticles
  • Liposomes
  • Nucleosides
  • Nucleotides
  • Oligonucleotides
  • Organophosphonates
  • Phosphates
  • Pyrimidine Nucleotides
  • RNA, Small Interfering