Rapid adaptive evolution of avian leukosis virus subgroup J in response to biotechnologically induced host resistance

PLoS Pathog. 2024 Aug 15;20(8):e1012468. doi: 10.1371/journal.ppat.1012468. eCollection 2024 Aug.

Abstract

Genetic editing of the germline using CRISPR/Cas9 technology has made it possible to alter livestock traits, including the creation of resistance to viral diseases. However, virus adaptability could present a major obstacle in this effort. Recently, chickens resistant to avian leukosis virus subgroup J (ALV-J) were developed by deleting a single amino acid, W38, within the ALV-J receptor NHE1 using CRISPR/Cas9 genome editing. This resistance was confirmed both in vitro and in vivo. In vitro resistance of W38-/- chicken embryonic fibroblasts to all tested ALV-J strains was shown. To investigate the capacity of ALV-J for further adaptation, we used a retrovirus reporter-based assay to select adapted ALV-J variants. We assumed that adaptive mutations overcoming the cellular resistance would occur within the envelope protein. In accordance with this assumption, we isolated and sequenced numerous adapted virus variants and found within their envelope genes eight independent single nucleotide substitutions. To confirm the adaptive capacity of these substitutions, we introduced them into the original retrovirus reporter. All eight variants replicated effectively in W38-/- chicken embryonic fibroblasts in vitro while in vivo, W38-/- chickens were sensitive to tumor induction by two of the variants. Importantly, receptor alleles with more extensive modifications have remained resistant to the virus. These results demonstrate an important strategy in livestock genome engineering towards antivirus resistance and illustrate that cellular resistance induced by minor receptor modifications can be overcome by adapted virus variants. We conclude that more complex editing will be necessary to attain robust resistance.

MeSH terms

  • Animals
  • Avian Leukosis Virus* / genetics
  • Avian Leukosis Virus* / physiology
  • Avian Leukosis* / genetics
  • Avian Leukosis* / virology
  • CRISPR-Cas Systems
  • Chick Embryo
  • Chickens* / virology
  • Disease Resistance / genetics
  • Evolution, Molecular
  • Fibroblasts / metabolism
  • Fibroblasts / virology
  • Gene Editing
  • Poultry Diseases / genetics
  • Poultry Diseases / virology
  • Viral Envelope Proteins / genetics
  • Viral Envelope Proteins / metabolism

Substances

  • Viral Envelope Proteins

Grants and funding

J.H. received funds from the Czech Academy of Sciences (Praemium Academiae, and the program Strategy AV21, project Virology and Antiviral Therapy) and the National Institute of Virology and Bacteriology (Program EXCELLES, ID LX22NPO5103 - funded by the European Union - Next Generation EU). The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.