Infectious Spleen and Kidney Necrosis Virus ORF093R and ORF102R Regulate Glutamate Metabolic Reprogramming to Support Virus Proliferation by Interacting with c-Myc

Int J Mol Sci. 2025 Jan 16;26(2):718. doi: 10.3390/ijms26020718.

Abstract

Glutamine metabolism is essential for infectious spleen and kidney necrosis virus (ISKNV) replication. Glutaminase 1 (GLS1), the key enzyme of the glutamine metabolism, and c-Myc positively regulate ISKNV infection, while c-Myc is closely correlated with GLS1. However, the regulatory mechanism among ISKNV, c-Myc and glutamine metabolism remains unclear. Here, we indicated that c-Myc increased glutamine uptake by increasing the GLS1, glutamate dehydrogenase (GDH) and isocitrate dehydrogenase (IDH2) expression of glutamine metabolism. ISKNV ORF102R, ORF093R and ORF118L co-located with c-Myc in CPB cells. Co-IP results showed that ISKNV ORF102R and ORF093R interacted with c-Myc, while ORF118L did not interact with c-Myc. The expression levels of c-Myc, GLS1 and IDH2 were increased in ISKNV ORF093R expression cells, and the mRNA and protein levels of GLS1 were upregulated in ISKNV 102R-expressing cells. These results indicated that ISKNV reconstructed glutamine metabolism to satisfy the energy and macromolecule requirements for virus proliferation by ORF093R and ORF102R interacting with c-Myc, which provides the foundation for innovative antiviral strategies.

Keywords: ISKNV; c-Myc; glutamine metabolism.

MeSH terms

  • Animals
  • DNA Virus Infections / metabolism
  • DNA Virus Infections / virology
  • Glutamate Dehydrogenase / genetics
  • Glutamate Dehydrogenase / metabolism
  • Glutamic Acid / metabolism
  • Glutaminase* / genetics
  • Glutaminase* / metabolism
  • Glutamine / metabolism
  • Iridoviridae* / genetics
  • Iridoviridae* / physiology
  • Metabolic Reprogramming
  • Proto-Oncogene Proteins c-myc* / genetics
  • Proto-Oncogene Proteins c-myc* / metabolism
  • Viral Proteins / genetics
  • Viral Proteins / metabolism
  • Virus Replication*

Substances

  • Proto-Oncogene Proteins c-myc
  • Glutaminase
  • Glutamine
  • Glutamic Acid
  • Viral Proteins
  • Glutamate Dehydrogenase

Supplementary concepts

  • Infectious spleen and kidney necrosis virus

Grants and funding

This study was supported by the National Key Research and Development Program of China (2023YFD2400701), the National Natural Science Fund (No. 32273181), the Key Research and Development Program of Guangzhou City (2024B03J1263), and the Central Public-interest Scientific Institution Basal Research Fund, CAFS (No. 2023TD48).