1887

Abstract

Although it is known that Israeli acute paralysis virus (IAPV) can cause bee mortality, the symptoms of paralysis and the distribution of the virus in different body tissues and their potential to respond with an increase of the siRNA antiviral immune system have not been studied. In this project we worked with , which is one of the most numerous bumblebee species in Europe and an important pollinator for wild flowers and many crops in agriculture. Besides the classic symptoms of paralysis and trembling prior to death, we report a new IAPV-related symptom, crippled/immobilized forelegs. Reverse-transcriptase quantitative PCR showed that IAPV accumulates in different body tissues (midgut, fat body, brain and ovary). The highest levels of IAPV were observed in the fat body. With fluorescence hybridization (FISH) we detected IAPV in the Kenyon cells of mushroom bodies and neuropils from both antennal and optic lobes of the brain in IAPV-infected workers. Finally, we observed an induction of a core gene of the RNAi antiviral immune response, in the IAPV-infected tissues of workers. According to our results, tissue tropism and the induction strength of could not be correlated with virus-related paralysis symptoms.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000516
2016-08-01
2021-07-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/8/1981.html?itemId=/content/journal/jgv/10.1099/jgv.0.000516&mimeType=html&fmt=ahah

References

  1. Bailey L., Woods R. D. 1974; Three previously undescribed viruses from the honey bee. J Gen Virol 25:175–186 [View Article][PubMed]
    [Google Scholar]
  2. Bailey L., Gibbs A. J., Woods R. D. 1963; Two viruses from adult honey bees (Apis mellifera Linnaeus). Virology 21:390–395 [View Article]
    [Google Scholar]
  3. Boncristiani H. F., Evans J. D., Chen Y., Pettis J., Murphy C., Lopez D. L., Simone-Finstrom M., Strand M., Tarpy D. R., Rueppell O. 2013; In vitro infection of pupae with Israeli acute paralysis virus suggests disturbance of transcriptional homeostasis in honey bees (Apis mellifera). PLoS One 8:e73429 [View Article][PubMed]
    [Google Scholar]
  4. Brutscher L. M., Daughenbaugh K. F., Flenniken M. L. 2015; Antiviral defense mechanisms in honey bees. Curr Opin Insect Sci 10:71–82 [View Article][PubMed]
    [Google Scholar]
  5. Chen Y. P., Pettis J. S., Corona M., Chen W. P., Li C. J., Spivak M., Visscher P. K., DeGrandi-Hoffman G., Boncristiani H. et al. 2014; Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health. PLoS Pathog 10:e1004261 [View Article][PubMed]
    [Google Scholar]
  6. Cox-Foster D. L., Conlan S., Holmes E. C., Palacios G., Evans J. D., Moran N. A., Quan P. L., Briese T., Hornig M. et al. 2007; A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318:283–287 [View Article][PubMed]
    [Google Scholar]
  7. de Brito Sanchez M. G., Lorenzo E., Su S., Liu F., Zhan Y., Giurfa M. 2014; The tarsal taste of honey bees: behavioral and electrophysiological analyses. Front Behav Neurosci 8:25 [View Article][PubMed]
    [Google Scholar]
  8. de Miranda J. R., Cordoni G., Budge G. 2010; The Acute bee paralysis virus-Kashmir bee virus-Israeli acute paralysis virus complex. J Invertebr Pathol 103:S30–47 [View Article][PubMed]
    [Google Scholar]
  9. Deddouche S., Matt N., Budd A., Mueller S., Kemp C., Galiana-Arnoux D., Dostert C., Antoniewski C., Hoffmann J. A., Imler J. L. 2008; The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nat Immunol 9:1425–1432 [View Article][PubMed]
    [Google Scholar]
  10. DeGrandi-Hoffman G., Chen Y. 2015; Nutrition, immunity and viral infections in honey bees. Curr Opin Insect Sci 10:170–176 [View Article]
    [Google Scholar]
  11. Fujiyuki T., Matsuzaka E., Nakaoka T., Takeuchi H., Wakamoto A., Ohka S., Sekimizu K., Nomoto A., Kubo T. 2009; Distribution of Kakugo virus and its effects on the gene expression profile in the brain of the worker honeybee Apis mellifera L. J Virol 83:11560–11568 [View Article][PubMed]
    [Google Scholar]
  12. Fürst M. A., McMahon D. P., Osborne J. L., Paxton R. J., Brown M. J. 2014; Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506:364–366 [View Article][PubMed]
    [Google Scholar]
  13. Galbraith D. A., Yang X., Niño E. L., Yi S., Grozinger C. 2015; Parallel epigenomic and transcriptomic responses to viral infection in honey bees (Apis mellifera). PLoS Pathog 11:e1004713 [View Article][PubMed]
    [Google Scholar]
  14. Genersch E., Yue C., Fries I., de Miranda J. R. 2006; Detection of Deformed wing virus, a honey bee viral pathogen, in bumble bees (Bombus terrestris and Bombus pascuorum) with wing deformities. J Invertebr Pathol 91:61–63 [View Article][PubMed]
    [Google Scholar]
  15. Hakim R. S., Baldwin K., Smagghe G. 2010; Regulation of midgut growth, development, and metamorphosis. Annu Rev Entomol 55:593–608 [View Article][PubMed]
    [Google Scholar]
  16. Hellemans J., Mortier G., De Paepe A., Speleman F., Vandesompele J. 2007; qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19 [View Article][PubMed]
    [Google Scholar]
  17. Kingsolver M. B., Huang Z., Hardy R. W. 2013; Insect antiviral innate immunity: pathways, effectors, and connections. J Mol Biol 425:4921–4936 [View Article][PubMed]
    [Google Scholar]
  18. Lanzi G., de Miranda J. R., Boniotti M. B., Cameron C. E., Lavazza A., Capucci L., Camazine S. M., Rossi C. 2006; Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). J Virol 80:4998–5009 [View Article][PubMed]
    [Google Scholar]
  19. Levitt A. L., Singh R., Cox-Foster D. L., Rajotte E., Hoover K., Ostiguy N., Holmes E. C. 2013; Cross-species transmission of honey bee viruses in associated arthropods. Virus Res 176:232–240 [View Article][PubMed]
    [Google Scholar]
  20. Li Z., Chen Y., Zhang S., Chen S., Li W., Yan L., Shi L., Wu L., Sohr A., Su S. 2013; Viral infection affects sucrose responsiveness and homing ability of forager honey bees, Apis mellifera L. PLoS One 8:e77354 [View Article][PubMed]
    [Google Scholar]
  21. Locke B., Forsgren E., Fries I., de Miranda J. R. 2012; Acaricide treatment affects viral dynamics in Varroa destructor-infested honey bee colonies via both host physiology and mite control. Appl Environ Microb 78:227–235 [View Article]
    [Google Scholar]
  22. Maori E., Lavi S., Mozes-Koch R., Gantman Y., Peretz Y., Edelbaum O., Tanne E., Sela I. 2007; Isolation and characterization of Israeli acute paralysis virus, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra- and inter-species recombination. J Gen Virol 88:3428–3438 [View Article][PubMed]
    [Google Scholar]
  23. Maori E., Paldi N., Shafir S., Kalev H., Tsur E., Glick E., Sela I. 2009; IAPV, a bee-affecting virus associated with Colony Collapse Disorder can be silenced by dsRNA ingestion. Insect Mol Biol 18:55–60 [View Article][PubMed]
    [Google Scholar]
  24. Martin S. J., Highfield A. C., Brettell L., Villalobos E. M., Budge G. E., Powell M., Nikaido S., Schroeder D. C. 2012; Global honey bee viral landscape altered by a parasitic mite. Science 336:1304–1306 [View Article][PubMed]
    [Google Scholar]
  25. Martinson V. G., Moy J., Moran N. A. 2012; Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol 78:2830–2840 [View Article][PubMed]
    [Google Scholar]
  26. McMahon D. P., Fürst M. A., Caspar J., Theodorou P., Brown M. J., Paxton R. J. 2015; A sting in the spit: widespread cross-infection of multiple RNA viruses across wild and managed bees. J Anim Ecol 84:615–624 [View Article][PubMed]
    [Google Scholar]
  27. McMenamin A. J., Genersch E. 2015; Honey bee colony losses and associated viruses. Curr Opin Insect Sci 8:121–129 [View Article]
    [Google Scholar]
  28. Meeus I., de Miranda J. R., de Graaf D. C., Wäckers F., Smagghe G. 2014; Effect of oral infection with Kashmir bee virus and Israeli acute paralysis virus on bumblebee (Bombus terrestris) reproductive success. J Invertebr Pathol 121:64–69 [View Article][PubMed]
    [Google Scholar]
  29. Mommaerts V., Reynders S., Boulet J., Besard L., Sterk G., Smagghe G. 2010; Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19:207–215 [View Article][PubMed]
    [Google Scholar]
  30. Mommaerts V., Wäckers F., Smagghe G. 2013; Assessment of gustatory responses to different sugars in harnessed and free-moving bumblebee workers (Bombus terrestris). Chem Senses 38:399–407 [View Article][PubMed]
    [Google Scholar]
  31. Möckel N., Gisder S., Genersch E. 2011; Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. J Gen Virol 92:370–377 [View Article][PubMed]
    [Google Scholar]
  32. Müller. S., Matthiesen. S. H., Nielsen. K. V 2009; Preparation of FFPE tissue slides for solid tumor FISH analysis. In Immunohistochemical (IHC) Staining Methods, 5th edn. pp. 67–74 Edited by Kumar G. L., Rudbeck L. California Dako North America:
    [Google Scholar]
  33. Niu J., Cappelle K., de Miranda J. R., Smagghe G., Meeus I. 2014a; Analysis of reference gene stability after Israeli acute paralysis virus infection in bumblebees Bombus terrestris. J Invertebr Pathol 115:76–79 [View Article]
    [Google Scholar]
  34. Niu J., Meeus I., Cappelle K., Piot N., Smagghe G. 2014b; The immune response of the small interfering RNA pathway in the defense against bee viruses. Curr Opin Insect Sci 6:22–27 [View Article]
    [Google Scholar]
  35. Niu J., Smagghe G., Coninck D., Nieuwerburgh F., Deforce D., Meeus I. 2016; In vivo study of Dicer-2-mediated immune response of the small interfering RNA pathway upon systemic infections of virulent and avirulent viruses in Bombus terrestris. Insect Biochem Mol Biol 70:127–137 [View Article][PubMed]
    [Google Scholar]
  36. Otterstatter M. C., Thomson J. D. 2007; Contact networks and transmission of an intestinal pathogen in bumble bee (Bombus impatiens) colonies. Oecologia 154:411–421 [View Article][PubMed]
    [Google Scholar]
  37. Palacios G., Hui J., Quan P. L., Kalkstein A., Honkavuori K. S., Bussetti A. V., Conlan S., Evans J., Chen Y. P. et al. 2008; Genetic analysis of Israel acute paralysis virus: distinct clusters are circulating in the United States. J Virol 82:6209–6217 [View Article][PubMed]
    [Google Scholar]
  38. Parmentier L., Smagghe G., de Graaf D. C., Meeus I. 2016; Varroa destructor Macula-like virus, Lake Sinai virus and other new RNA viruses in wild bumblebee hosts (Bombus pascuorum, Bombus lapidarius and Bombus pratorum). J Invertebr Pathol 134:6–11 [View Article][PubMed]
    [Google Scholar]
  39. Peng W., Li J., Boncristiani H., Strange J. P., Hamilton M., Chen Y. 2011; Host range expansion of honey bee Black Queen Cell Virus in the bumble bee, Bombus huntii. Apidologie 42:650–658 [View Article]
    [Google Scholar]
  40. Piot N., Snoeck S., Vanlede M., Smagghe G., Meeus I. 2015; The effect of oral administration of dsRNA on viral replication and mortality in Bombus terrestris. Viruses 7:3172–3185 [View Article][PubMed]
    [Google Scholar]
  41. Sabin L. R., Hanna S. L., Cherry S. 2010; Innate antiviral immunity in Drosophila. Curr Opin Immunol 22:4–9 [View Article][PubMed]
    [Google Scholar]
  42. Shah K. S., Evans E. C., Pizzorno M. C. 2009; Localization of deformed wing virus (DWV) in the brains of the honeybee, Apis mellifera Linnaeus. Virol J 6:182 [View Article][PubMed]
    [Google Scholar]
  43. Singh R., Levitt A. L., Rajotte E. G., Holmes E. C., Ostiguy N., Vanengelsdorp D., Lipkin W., Depamphilis C. W., Toth A. L. et al. 2010; RNA viruses in hymenopteran pollinators: evidence of inter-Taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species. PLoS One 5:e14357 [View Article][PubMed]
    [Google Scholar]
  44. Velthuis H. H. W., van Doorn A. 2006; A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37:421–451 [View Article]
    [Google Scholar]
  45. Yue D., Nordhoff M., Wieler L. H., Genersch E. 2008; Fluorescence in situ hybridization (FISH) analysis of the interactions between honeybee larvae and Paenibacillus larvae, the causative agent of American foulbrood of honeybees (Apis mellifera). Environ Microbiol 10:1612–1620 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000516
Loading
/content/journal/jgv/10.1099/jgv.0.000516
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF

Supplementary File 2

Most cited this month 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