1887

Abstract

Snakehead fish vesiculovirus (SHVV), a member of the family , has caused mass mortality in snakehead fish culture in China. Previous transcriptomic sequencing of SHVV-infected and non-infected striped snakehead fish cells (SSN-1) showed that glutaminase (GLS), the critical enzyme of glutamine metabolism, was upregulated upon SHVV infection. It therefore drew our attention to investigating the role of glutamine in SHVV propagation. Glutamine deprivation significantly reduced the expression of the mRNAs and proteins of SHVV, and the production of virus particles, indicating that glutamine was required for SHVV propagation. Glutamine can be converted to glutamate by GLS, and then be converted to α-ketoglutarate, to join in the tricarboxylic acid (TCA) cycle. Addition of the TCA cycle intermediate α-ketoglutarate, oxaloacetic acid or pyruvate significantly restored SHVV propagation, indicating that the requirement of glutamine for SHVV propagation was due to its replenishment of the TCA cycle. Inhibiting the activity of GLS in SSN-1 cells by an inhibitor, bis-2-(5-phenylacetamido-1,3,4-thiadiazol-2-yl)ethyl sulfide, decreased SHVV propagation, while overexpression of GLS increased SHVV propagation. Taken together, our data have revealed the relationship between glutamine metabolism and SHVV propagation.

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2016-11-10
2021-08-05
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References

  1. Betts A., Stone D., Way K., Torhy C., Chilmonczyk S., Benmansour A., de Kinkelin P. 2003; Emerging vesiculo-type virus infections of freshwater fishes in Europe. Dis Aquat Organ 57:201–212 [CrossRef]
    [Google Scholar]
  2. Chambers J. W., Maguire T. G., Alwine J. C. 2010; Glutamine metabolism is essential for human cytomegalovirus infection. J Virol 84:1867–1873 [View Article][PubMed]
    [Google Scholar]
  3. Crane M., Hyatt A. 2011; Viruses of fish: an overview of significant pathogens. Viruses 3:2025–2046 [View Article][PubMed]
    [Google Scholar]
  4. Curi R., Lagranha C. J., Doi S. Q., Sellitti D. F., Procopio J., Pithon-Curi T. C., Corless M., Newsholme P. 2005; Molecular mechanisms of glutamine action. Cell Physiol 204:392–401 [View Article]
    [Google Scholar]
  5. Dang C. V. 2012; Links between metabolism and cancer. Genes Dev 26:877–890 [View Article][PubMed]
    [Google Scholar]
  6. DeBerardinis R. J., Mancuso A., Daikhin E., Nissim I., Yudkoff M., Wehrli S., Thompson C. B. 2007; Beyond aerobic glycolysis: transformed cells can engage in glutamine metabolism that exceeds the requirement for protein and nucleotide synthesis. Proc Natl Acad Sci USA 104:19345–19350 [View Article][PubMed]
    [Google Scholar]
  7. Deberardinis R. J., Sayed N., Ditsworth D., Thompson C. B. 2008; Brick by brick: metabolism and tumor cell growth. Curr Opin Genet Dev 18:54–61 [View Article][PubMed]
    [Google Scholar]
  8. Delgado T., Sanchez E. L., Camarda R., Lagunoff M. 2012; Global metabolic profiling of infection by an oncogenic virus: KSHV induces and requires lipogenesis for survival of latent infection. PLoS Pathog 8:e1002866 [View Article][PubMed]
    [Google Scholar]
  9. Diamond D. L., Syder A. J., Jacobs J. M., Sorensen C. M., Walters K. A., Proll S. C., McDermott J. E., Gritsenko M. A., Zhang Q. et al. 2010; Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 6:e1000719 [View Article][PubMed]
    [Google Scholar]
  10. Edinger A. L., Thompson C. B. 2002; Akt maintains cell size and survival by increasing mTOR-dependent nutrient uptake. Mol Biol Cell 13:2276–2288 [View Article][PubMed]
    [Google Scholar]
  11. Fontaine K. A., Camarda R., Lagunoff M. 2014; Vaccinia virus requires glutamine but not glucose for efficient replication. J Virol 88:4366–4374 [View Article][PubMed]
    [Google Scholar]
  12. Hammerman P. S., Fox C. J., Thompson C. B. 2004; Beginnings of a signal-transduction pathway for bioenergetic control of cell survival. Trends Biochem Sci 29:586–592 [View Article][PubMed]
    [Google Scholar]
  13. Kim J. W., Dang C. V. 2006; Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 66:8927–8930 [View Article][PubMed]
    [Google Scholar]
  14. Kuzmin I. V., Novella I. S., Dietzgen R. G., Padhi A., Rupprecht C. E. 2009; The rhabdoviruses: biodiversity, phylogenetics, and evolution. Infect Genet Evol 9:541–553 [View Article][PubMed]
    [Google Scholar]
  15. Liu X., Wen Y., Hu X., Wang W., Liang X., Li J., Vakharia V., Lin L. 2015; Breaking the host range: mandarin fish is susceptible to a vesiculovirus derived from snakehead fish. J Gen Virol 96:775–781 [View Article][PubMed]
    [Google Scholar]
  16. Lu W., Pelicano H., Huang P. 2010; Cancer metabolism: is glutamine sweeter than glucose?. Cancer Cell 18:199–200 [View Article][PubMed]
    [Google Scholar]
  17. Lyles D. S., Rupprecht C. E. 2006; Rhabdoviridae. In Fields Virology, 5th edn. pp. 1364–1386. Philadelphia, PA:: Lippincott, Williams and Wilkins, and Wolters Kluwer;
    [Google Scholar]
  18. McFee R. B. 2007; Global infections – avian influenza and other significant emerging pathogens: an overview. Dis Mon 53:343–347 [View Article][PubMed]
    [Google Scholar]
  19. Newsholme E. A., Crabtree B., Ardawi M. S. M. 1985; The role of high rates of glycolysis and glutamine utilization in rapidly dividing cells. Biosci Rep 5:393–400 [View Article][PubMed]
    [Google Scholar]
  20. Shabert J. K., Wilmore D. W. 1996; Glutamine deficiency as a cause of human immunodeficiency virus wasting. Med Hypotheses 46:252–256 [View Article][PubMed]
    [Google Scholar]
  21. Shukla K., Ferraris D. V., Thomas A. G., Stathis M., Duvall B., Delahanty G., Alt J., Rais R., Rojas C. et al. 2012; Design, synthesis, and pharmacological evaluation of bis-2-(5-phenylacetamido-1,2,4-thiadiazol-2-yl)ethyl sulfide 3 (BPTES) analogs as glutaminase inhibitors. J Med Chem 55:10551–10563 [View Article][PubMed]
    [Google Scholar]
  22. Tang Y. K., Jia Y. Y. 2008; Method of processing real time PCR data. Biotechnology 18:89–91
    [Google Scholar]
  23. Tennant D. A., Durán R. V., Gottlieb E. 2010; Targeting metabolic transformation for cancer therapy. Nat Rev Cancer 10:267–277 [View Article][PubMed]
    [Google Scholar]
  24. Vastag L., Koyuncu E., Grady S. L., Shenk T. E., Rabinowitz J. D. 2011; Divergent effects of human cytomegalovirus and herpes simplex virus-1 on cellular metabolism. PLoS Pathog 7:e1002124 [View Article][PubMed]
    [Google Scholar]
  25. Wang W., Asim M., Yi L., Hegazy A. M., Hu X., Zhou Y., Ai T., Lin L. 2015; Abortive infection of snakehead fish vesiculovirus in ZF4 cells was associated with the RLRs pathway activation by viral replicative intermediates. Int J Mol Sci 16:6235–6250 [View Article][PubMed]
    [Google Scholar]
  26. Wise D. R., Thompson C. B. 2010; Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci 35:427–433 [View Article][PubMed]
    [Google Scholar]
  27. Wise D. R., DeBerardinis R. J., Mancuso A., Sayed N., Zhang X. Y., Pfeiffer H. K., Nissim I., Daikhin E., Yudkoff M. et al. 2008; Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci USA 105:18782–18787 [View Article][PubMed]
    [Google Scholar]
  28. Yuneva M., Zamboni N., Oefner P., Sachidanandam R., Lazebnik Y. 2007; Deficiency in glutamine but not glucose induces MYC-dependent apoptosis in human cells. J Cell Biol 178:93–105 [View Article][PubMed]
    [Google Scholar]
  29. Zuxun S. J. G. 1997; Advances of research on molecular biology of Rhabdoviridae. Genomic structure of Rhabdoviridae. Virol Sin 2:103–111
    [Google Scholar]
  30. Zuxun S. J. G. 1998; Advances of research on molecular biology of Rhabdoviridae. Viral structural protein, transcription, replication and capsidation. Virol Sin 4:281–291
    [Google Scholar]
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