CRISPR/Cas9-mediated genome editing of the thymidine kinase gene in a clinical HSV-1 isolate identifies F289S as novel acyclovir-resistant mutation

Antiviral Res. 2024 Aug:228:105950. doi: 10.1016/j.antiviral.2024.105950. Epub 2024 Jun 27.

Abstract

Herpes simplex virus type 1 (HSV-1) is a neurotropic alphaherpesvirus that establishes a lifelong infection in sensory neurons of infected individuals, accompanied with intermittent reactivation of latent virus causing (a)symptomatic virus shedding. Whereas acyclovir (ACV) is a safe and highly effective antiviral to treat HSV-1 infections, long-term usage can lead to emergence of ACV resistant (ACVR) HSV-1 and subsequently ACV refractory disease. Here, we isolated an HSV-1 strain from a patient with reactivated herpetic eye disease that did not respond to ACV treatment. The isolate carried a novel non-synonymous F289S mutation in the viral UL23 gene encoding the thymidine kinase (TK) protein. Because ACV needs conversion by viral TK and subsequently cellular kinases to inhibit HSV-1 replication, the UL23 gene is commonly mutated in ACVR HSV-1 strains. The potential role of the F289S mutation causing ACVR was investigated using CRISPR/Cas9-mediated HSV-1 genome editing. Reverting the F289S mutation in the original clinical isolate to the wild-type sequence S289F resulted in an ACV-sensitive (ACVS) phenotype, and introduction of the F289S substitution in an ACVS HSV-1 reference strain led to an ACVR phenotype. In summary, we identified a new HSV-1 TK mutation in the eye of a patient with ACV refractory herpetic eye disease, which was identified as the causative ACVR mutation with the aid of CRISPR/Cas9-mediated genome engineering technology. Direct editing of clinical HSV-1 isolates by CRISPR/Cas9 is a powerful strategy to assess whether single residue substitutions are causative to a clinical ACVR phenotype.

Keywords: Acyclovir resistance; CRISPR/Cas9; Herpes simplex virus 1; Recurrent herpetic eye disease; Thymidine kinase.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acyclovir* / pharmacology
  • Acyclovir* / therapeutic use
  • Antiviral Agents* / pharmacology
  • Antiviral Agents* / therapeutic use
  • CRISPR-Cas Systems*
  • Drug Resistance, Viral* / genetics
  • Gene Editing*
  • Herpes Simplex / drug therapy
  • Herpes Simplex / virology
  • Herpesvirus 1, Human* / drug effects
  • Herpesvirus 1, Human* / enzymology
  • Herpesvirus 1, Human* / genetics
  • Humans
  • Mutation*
  • Thymidine Kinase* / genetics

Substances

  • Thymidine Kinase
  • Acyclovir
  • Antiviral Agents