Stability of the resistance to the thiosemicarbazone derived from 5,6-dimethoxy-1-indanone, a non-nucleoside polymerase inhibitor of bovine viral diarrhea virus

PLoS One. 2014 Jun 20;9(6):e100528. doi: 10.1371/journal.pone.0100528. eCollection 2014.

Abstract

Bovine viral diarrhea virus (BVDV) is the prototype Pestivirus. BVDV infection is distributed worldwide and causes serious problems for the livestock industry. The thiosemicarbazone of 5,6-dimethoxy-1-indanone (TSC) is a non-nucleoside polymerase inhibitor (NNI) of BVDV. All TSC-resistant BVDV variants (BVDV-TSCr T1-5) present an N264D mutation in the NS5B gene (RdRp) whereas the variant BVDV-TSCr T1 also presents an NS5B A392E mutation. In the present study, we carried out twenty passages of BVDV-TSCr T1-5 in MDBK cells in the absence of TSC to evaluate the stability of the resistance. The viral populations obtained (BVDV R1-5) remained resistant to the antiviral compound and conserved the mutations in NS5B associated with this phenotype. Along the passages, BVDV R2, R3 and R5 presented a delay in the production of cytopathic effect that correlated with a decrease in cell apoptosis and intracellular accumulation of viral RNA. The complete genome sequences that encode for NS2 to NS5B, Npro and Erns were analyzed. Additional mutations were detected in the NS5B of BVDV R1, R3 and R4. In both BVDV R2 and R3, most of the mutations found were localized in NS5A, whereas in BVDV R5, the only mutation fixed was NS5A V177A. These results suggest that mutations in NS5A could alter BVDV cytopathogenicity. In conclusion, the stability of the resistance to TSC may be due to the fixation of different compensatory mutations in each BVDV-TSCr. During their replication in a TSC-free medium, some virus populations presented a kind of interaction with the host cell that resembled a persistent infection: decreased cytopathogenicity and viral genome synthesis. This is the first report on the stability of antiviral resistance and on the evolution of NNI-resistant BVDV variants. The results obtained for BVDV-TSCr could also be applied for other NNIs.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Apoptosis / drug effects
  • Base Sequence
  • Cattle
  • Cell Line
  • Conserved Sequence
  • Cytopathogenic Effect, Viral / drug effects
  • DNA-Directed RNA Polymerases / antagonists & inhibitors*
  • Diarrhea Viruses, Bovine Viral / drug effects*
  • Diarrhea Viruses, Bovine Viral / enzymology*
  • Diarrhea Viruses, Bovine Viral / genetics
  • Diarrhea Viruses, Bovine Viral / physiology
  • Drug Resistance, Viral / drug effects*
  • Drug Resistance, Viral / genetics
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology
  • Indans / chemistry*
  • Molecular Sequence Data
  • Mutation
  • RNA, Viral / metabolism
  • Thiosemicarbazones / chemistry*
  • Thiosemicarbazones / pharmacology*
  • Viral Nonstructural Proteins / chemistry
  • Viral Nonstructural Proteins / genetics
  • Virus Replication / drug effects

Substances

  • 5,6-dimethoxy-1-indanone thiosemicarbazone
  • Enzyme Inhibitors
  • Indans
  • RNA, Viral
  • Thiosemicarbazones
  • Viral Nonstructural Proteins
  • DNA-Directed RNA Polymerases

Grants and funding

This research was supported by grants from Agencia Nacional para la Promoción Científica y Tecnológica (PICT 2012-2867) (http://www.agencia.mincyt.gob.ar/) and Universidad de Buenos Aires (UBACYT 2011-2014, N° 20020100100612) (http://www.uba.ar/secyt/) from Argentina. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.