1887

Journal of General Virology header logo

Volume 97, Issue 6

Impact of ERK activation on fly survival and -mediated protection during virus infection Free

Abstract

Elevated levels of reactive oxygen species (ROS) provide protection against virus-induced mortality in . In addition to contributing to oxidative stress, ROS are known to activate a number of signalling pathways including the extracellular signal-regulated kinases (ERK) signalling cascade. It was recently shown that ERK signalling is important for resistance against viral replication and invasion in cultured cells and the gut epithelium of adult flies. Here, using a loss-of-function ERK () mutant we demonstrated that ERK is important for fly survival during virus infection. ERK mutant flies subjected to Drosophila C virus (DCV) oral and systemic infection were more susceptible to virus-induced mortality as compared with wild-type flies. We have demonstrated experimentally that ERK activation is important for fly survival during oral and systemic virus infection. Given that elevated ROS correlates with -mediated antiviral protection, we also investigated the involvement of ERK in antiviral protection in flies infected by . The results indicate that ERK activation is increased in the presence of but this does not appear to influence -mediated antiviral protection, at least during systemic infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): Dicistroviridae , Drosophila virus , ERK , Rolled , ROS and Wolbachia
© 2016 The Authors
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000456
2016-06-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/6/1446.html?itemId=/content/journal/jgv/10.1099/jgv.0.000456&mimeType=html&fmt=ahah

References

  1. Abe M. K., Chao T. S., Solway J., Rosner M. R., Hershenson M. B. 1994; Hydrogen peroxide stimulates mitogen-activated protein kinase in bovine tracheal myocytes: Implications for human airway disease. Am J Respir Cell Mol Biol 11:577–585 [View Article][PubMed]
     [Google Scholar]
  2. Abid M. R., Spokes K. C., Shih S. C., Aird W. C. 2007; NADPH oxidase activity selectively modulates vascular endothelial growth factor signaling pathways. J Biol Chem 282:35373–35385 [View Article][PubMed]
     [Google Scholar]
  3. Arbiser J. L., Petros J., Klafter R., Govindajaran B., McLaughlin E. R., Brown L. F., Cohen C., Moses M., Kilroy S., other authors. 2002; Reactive oxygen generated by Nox1 triggers the angiogenic switch. Proc Natl Acad Sci U S A 99:715–720 [View Article][PubMed]
     [Google Scholar]
  4. Arnold P. A., Johnson K. N., White C. R. 2013; Physiological and metabolic consequences of viral infection in Drosophila melanogaster . J Exp Biol 216:3350–3357 [View Article][PubMed]
     [Google Scholar]
  5. Bae G. U., Seo D. W., Kwon H. K., Lee H. Y., Hong S., Lee Z. W., Ha K. S., Lee H. W., Han J. W. 1997; Epidermal growth factor (EGF-induced generation of hydrogen peroxide. Role in EGF receptor-mediated tyrosine phosphorylation. J Biol Chem 272:217–221[PubMed]
     [Google Scholar]
  6. Chrostek E., Marialva M. S., Yamada R., O'Neill S. L., Teixeira L. 2014; High anti-viral protection without immune upregulation after interspecies Wolbachia transfer. PLoS One 9:e99025 [View Article][PubMed]
     [Google Scholar]
  7. Chtarbanova S., Lamiable O., Lee K. Z., Galiana D., Troxler L., Meignin C., Hetru C., Hoffmann J. A., Daeffler L., other authors. 2014; Drosophila C virus systemic infection leads to intestinal obstruction. J Virol 88:14057–14069 [View Article][PubMed]
     [Google Scholar]
  8. Covarrubias L., Hernández-García D., Schnabel D., Salas-Vidal E., Castro-Obregón S. 2008; Function of reactive oxygen species during animal development: passive or active?. Dev Biol 320:1–11 [View Article][PubMed]
     [Google Scholar]
  9. Ferreira G., Naylor H., Esteves S. S., Pais I. S., Martins N. E., Teixeira L. 2014; The Toll-Dorsal pathway is required for resistance to viral oral infection in Drosophila . PLoS Pathog 10:e1004507 [View Article][PubMed]
     [Google Scholar]
  10. Futran A. S., Link A. J., Seger R., Shvartsman S. Y. 2013; ERK as a model for systems biology of enzyme kinetics in cells. Curr Biol 23:R972–R979 [View Article][PubMed]
     [Google Scholar]
  11. Guyton K. Z., Liu Y., Gorospe M., Xu Q., Holbrook N. J. 1996; Activation of mitogen-activated protein kinase by H2O2 . J Biol Chem 271:4138–4142[PubMed]
     [Google Scholar]
  12. Hedges L. M., Brownlie J. C., O'Neill S. L., Johnson K. N. 2008; Wolbachia and virus protection in insects. Science 322:702 [View Article]
     [Google Scholar]
  13. Hedges L. M., Johnson K. N. 2008; Induction of host defence responses by Drosophila C virus. J Gen Virol 89:1497–1501 [View Article][PubMed]
     [Google Scholar]
  14. Hoffmann A. A., Turelli M., Simmons G. M. 1986; Unidirectional incompatibility between populations of Drosophila simulans. Evolution 40:692–701 [View Article]
     [Google Scholar]
  15. Johnson K. N. 2015a; Bacteria and antiviral immunity in insects. Curr Opin Insect Sci 8:97–103 [View Article]
     [Google Scholar]
  16. Johnson K.N. 2015b; The impact of Wolbachia on virus infection in mosquitoes. Viruses 7:5705–5717 [View Article]
     [Google Scholar]
  17. Johnson K. N., Christian P. D. 1998; The novel genome organization of the insect picorna-like virus Drosophila C virus suggests this virus belongs to a previously undescribed virus family. J Gen Virol 79:191–203 [View Article][PubMed]
     [Google Scholar]
  18. Johnson K. N., Christian P. D. 1999; Molecular characterization of Drosophila C virus isolates. J Invertebr Pathol 73:248–254 [View Article][PubMed]
     [Google Scholar]
  19. Katz M., Amit I., Yarden Y. 2007; Regulation of MAPKs by growth factors and receptor tyrosine kinases. Biochim Biophys Acta 1773:1161–1176 [View Article][PubMed]
     [Google Scholar]
  20. Martinez J., Longdon B., Bauer S., Chan Y. S., Miller W. J., Bourtzis K., Teixeira L., Jiggins F. M. 2014; Symbionts commonly provide broad spectrum resistance to viruses in insects: A comparative analysis of Wolbachia strains. PLoS Pathog 10:e1004369 [View Article][PubMed]
     [Google Scholar]
  21. Martins N. E., Faria V. G., Teixeira L., Magalhães S., Sucena É. 2013; Host adaptation is contingent upon the infection route taken by pathogens. PLoS Pathog 9:e1003601 [View Article][PubMed]
     [Google Scholar]
  22. Milligan S. A., Owens M. W., Grisham M. B. 1998; Differential regulation of extracellular signal-regulated kinase and nuclear factor-kappa B signal transduction pathways by hydrogen peroxide and tumor necrosis factor. Arch Biochem Biophys 352:255–262 [View Article][PubMed]
     [Google Scholar]
  23. Molloy J. C., Sinkins S. P. 2015; Wolbachia do not induce reactive oxygen species-dependent immune pathway activation in Aedes albopictus . Viruses 7:4624–4639 [View Article][PubMed]
     [Google Scholar]
  24. Muller J. M., Cahill M. A., Rupec R. A., Baeuerle P. A., Nordheim A. 1997; Antioxidants as well as oxidants activate c-fos via Ras-dependent activation of extracellular-signal-regulated kinase 2 and Elk-1. Eur J Biochem 244:45–52 [View Article][PubMed]
     [Google Scholar]
  25. Osborne S. E., Leong Y. S., O'Neill S. L., Johnson K. N. 2009; Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 5:e1000656 [View Article][PubMed]
     [Google Scholar]
  26. Pan X., Zhou G., Wu J., Bian G., Lu P., Raikhel A. S., Xi Z. 2012; Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control Dengue virus in the mosquito Aedes aegypti . Proc Natl Acad Sc U S A 109:E23–E31 [View Article]
     [Google Scholar]
  27. Rainey S. M., Shah P., Kohl A., Dietrich I. 2014; Understanding the Wolbachia-mediated inhibition of arboviruses in mosquitoes: Progress and challenges. J Gen Virol 95:517–530 [View Article][PubMed]
     [Google Scholar]
  28. Raman M., Chen W., Cobb M. H. 2007; Differential regulation and properties of MAPKs. Oncogene 26:3100–3112 [View Article][PubMed]
     [Google Scholar]
  29. Rances E., Johnson T. K., Popovici J., Iturbe-Ormaetxe I., Zakir T., Warr C. G., O'Neill S. L. 2013; The Toll and Imd pathways are not required for Wolbachia-mediated Dengue virus interference. J Virol 87:11945–11949 [View Article][PubMed]
     [Google Scholar]
  30. Rances E., Ye Y. X. H., Woolfit M., McGraw E. A., O'Neill S. L. 2012; The relative importance of innate immune priming in Wolbachia-mediated Dengue interference. PLoS Pathog 8:e1002548 [View Article][PubMed]
     [Google Scholar]
  31. Riegler M., Sidhu M., Miller W. J., O'Neill S. L. 2005; Evidence for a global Wolbachia replacement in Drosophila melanogaster. Curr Biol 15:1428–1433 [View Article][PubMed]
     [Google Scholar]
  32. Rubinfeld H., Seger R. 2005; The ERK cascade: a prototype of MAPK signaling. Mol Biotechnol 31:151–174 [View Article]
     [Google Scholar]
  33. Sansone C. L., Cohen J., Yasunaga A., Xu J., Osborn G., Subramanian H., Gold B., Buchon N., Cherry S. 2015; Microbiota-dependent priming of antiviral intestinal immunity in Drosophila . Cell Host & Microbe 18:571–581 [View Article][PubMed]
     [Google Scholar]
  34. Shaul Y. D., Seger R. 2007; The MEK/ERK cascade: from signaling specificity to diverse functions. Biochim Biophys Acta 1773:1213–1226 [View Article][PubMed]
     [Google Scholar]
  35. Stevanovic A. L., Johnson K. N. 2015; Wolbachia-mediated antiviral protection in Drosophila larvae and adults following oral infection. Appl Environ Microbiol 81:8215–8223 [View Article][PubMed]
     [Google Scholar]
  36. Stevenson M. A., Pollock S. S., Coleman C. N., Calderwood S. K. 1994; X-irradiation, phorbol esters, and H2O2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res 52:12–15
     [Google Scholar]
  37. Teixeira L., Ferreira Álvaro., Ashburner M. 2008; The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster . PLoS Biol 6:e1000002–1002763 [View Article]
     [Google Scholar]
  38. Thannickal V. J., Fanburg B. L. 2000; Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279:L1005–1028[PubMed]
     [Google Scholar]
  39. Werren J. H., Baldo L., Clark M. E. 2008; Wolbachia: Master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751 [View Article][PubMed]
     [Google Scholar]
  40. Wong Z. S., Brownlie J. C., Johnson K. N. 2015; Oxidative stress correlates with Wolbachia-mediated antiviral protection in Wolbachia–Drosophila associations. Appl Environ Microbiol 81:3001–3005 [View Article][PubMed]
     [Google Scholar]
  41. Wong Z. S., Hedges L. M., Brownlie J. C., Johnson K. N. 2011; Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila . PLoS One 6:e25430 [View Article][PubMed]
     [Google Scholar]
  42. Wortzel I., Seger R. 2011; The ERK cascade: distinct functions within various subcellular organelles. Genes & Cancer 2:195–209 [View Article][PubMed]
     [Google Scholar]
  43. Xia C., Meng Q., Liu L. Z., Rojanasakul Y., Wang X. R., Jiang B. H. 2007; Reactive oxygen species regulate angiogenesis and tumor growth through vascular endothelial growth factor. Cancer Res 67:10823–10830 [View Article][PubMed]
     [Google Scholar]
  44. Xu J., Hopkins K., Sabin L., Yasunaga A., Subramanian H., Lamborn I., Gordesky-Gold B., Cherry S. 2013; ERK signaling couples nutrient status to antiviral defense in the insect gut. Proc Natl Acad Sci U S A 110:15025–15030 [View Article]
     [Google Scholar]
  45. Zhang M., Brewer A. C., Schröder K., Santos C. X., Grieve D. J., Wang M., Anilkumar N., Yu B., Dong X., other authors. 2010; NADPH oxidase-4 mediates protection against chronic load-induced stress in mouse hearts by enhancing angiogenesis. Proc Natl Acad Sci U S A 107:18121–18126 [View Article][PubMed]
     [Google Scholar]
  46. Zhou W. G., Rousset F., O'Neill S. 1998; Phylogeny and PCR-based classification of Wolbachia strains using wsp gene sequences. Proceedings of the Royal Society B: Biological Sciences 265:509–515 [View Article]
     [Google Scholar]
  47. Zug R., Hammerstein P. 2015; Wolbachia and the insect immune system: what reactive oxygen species can tell us about the mechanisms of Wolbachia–host interactions. Front Microbiol 6:1201 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000456
Loading
Impact of ERK activation on fly survival and Wolbachia-mediated protection during virus infection
J. Gen. Virol. 97, 1446 (2016); https://doi.org/10.1099/jgv.0.000456
/content/journal/jgv/10.1099/jgv.0.000456
/content/journal/jgv/10.1099/jgv.0.000456
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error