The immune response of the small interfering RNA pathway in the defense against bee viruses

Current Opinion in Insect Science

Volumn 6, Issue , 2014, Pages 22-27

  Niu, Jinzhi ^a   Meeus, Ivan ^a   Cappelle, Kaat ^a   Piot, Niels ^a   Smagghe, Guy ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

APOIDEA; DICISTROVIRIDAE; RNA VIRUSES;

EID: 84923763720     PISSN: 22145745     EISSN: 22145753     Source Type: Journal    
DOI: 10.1016/j.cois.2014.09.014     Document Type: Review

References (53)

1. D.J. Hosken Sex and death: microevolutionary trade-offs between reproductive and immune investment in dung flies Curr Biol 11 2001 R379 R380
2. A.P. Bascuñán-García, C. Lara, and A. Córdoba-Aguilar Immune investment impairs growth, female reproduction and survival in the house cricket, Acheta domesticus J Insect Physiol 56 2010 204 211
3. M.B. Kingsolver, Z.J. Huang, and R.W. Hardy Insect antiviral innate immunity: pathways, effectors, and connections J Mol Biol 425 2013 4921 4936
4. S.H. Merkling, and R.P. van Rij Beyond RNAi: antiviral defense strategies in Drosophila and mosquito J Insect Physiol 59 2013 159 170
5. D. Vijayendran, P.M. Airs, K. Dolezal, and B.C. Bonning Arthropod viruses and small RNAs J Invertebr Pathol 114 2013 186 195
6. R.C. Wilson, and J.A. Doudna Molecular mechanisms of RNA interference Annu Rev Biophys 42 2013 217 239
7. N. Gallai, J.-M. Salles, J. Settele, and B.E. Vaissière Economic valuation of the vulnerability of world agriculture confronted with pollinator decline Ecol Econ 68 2009 810 821
8. M.A. Fürst, D.P. McMahon, J.L. Osborne, R.J. Paxton, and M.J.F. Brown Disease associations between honeybees and bumblebees as a threat to wild pollinators Nature 506 2014 364 366
9. D.L. Cox-Foster, S. Conlan, E.C. Holmes, G. Palacios, J.D. Evans, N.A. Moran, P.-L. Quan, T. Briese, M. Hornig, and D.M. Geiser A metagenomic survey of microbes in honey bee colony collapse disorder Science 318 2007 283 287
10. A.L. Levitt, R. Singh, D.L. Cox-Foster, E. Rajotte, K. Hoover, N. Ostiguy, and E.C. Holmes Cross-species transmission of honey bee viruses in associated arthropods Virus Res 176 2013 232 240
11. R. Singh, A.L. Levitt, E.G. Rajotte, E.C. Holmes, N. Ostiguy, D. vanEngelsdorp, W.I. Lipkin, C.W. dePamphilis, A.L. Toth, and D.L. Cox-Foster RNA viruses in hymenopteran pollinators: evidence of inter-taxa virus transmission via pollen and potential impact on non-Apis hymenopteran species PLoS ONE 5 2010 e14357
12. L. De Smet, J. Ravoet, J.R. de Miranda, T. Wenseleers, M.Y. Mueller, R.F.A. Moritz, and D.C. de Graaf BeeDoctor, a versatile MLPA-based diagnostic tool for screening bee viruses PLoS ONE 7 2012 e47953
13. E.V. Ryabov, G.R. Wood, J.M. Fannon, J.D. Moore, J.C. Bull, D. Chandler, A. Mead, N. Burroughs, and D.J. Evans A virulent strain of deformed wing virus (DWV) of honeybees (Apis mellifera) prevails after Varroa destructor-mediated, or in vitro, transmission PLoS Pathog 10 2014 e1004230
14. R.M. Francis, S.L. Nielsen, and P. Kryger Varroa-virus interaction in collapsing honey bee colonies PLoS ONE 8 2013 e57540
15. G. Di Prisco, V. Cavaliere, D. Annoscia, P. Varricchio, E. Caprio, F. Nazzi, G. Gargiulo, and F. Pennacchio Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees Proc Natl Acad Sci U S A 110 2013 18466 18471
16. J.T. Marques, J.-P. Wang, X. Wang, K.P.V. de Oliveira, C. Gao, E.R.G.R. Aguiar, N. Jafari, and R.W. Carthew Functional specialization of the small interfering RNA pathway in response to virus infection PLoS Pathog 9 2013 e1003579
17. M.-C. Saleh, M. Tassetto, R.P. van Rij, B. Goic, V. Gausson, B. Berry, C. Jacquier, C. Antoniewski, and R. Andino Antiviral immunity in Drosophila requires systemic RNA interference spread Nature 458 2009 346 350
18. H. Huvenne, and G. Smagghe Mechanisms of dsRNA uptake in insects and potential of RNAi for pest control: a review J Insect Physiol 56 2010 227 235
19. J.G. Scott, K. Michel, L.C. Bartholomay, B.D. Siegfried, W.B. Hunter, G. Smagghe, K.Y. Zhu, and A.E. Douglas Towards the elements of successful insect RNAi J Insect Physiol 59 2013 1212 1221
20. A. Jarosch, and R.F.A. Moritz Systemic RNA-interference in the honeybee Apis mellifera: tissue dependent uptake of fluorescent siRNA after intra-abdominal application observed by laser-scanning microscopy J Insect Physiol 57 2011 851 857
21. N. Wynant, H. Verlinden, B. Breugelmans, G. Simonet, and J. Vanden Broeck Tissue-dependence and sensitivity of the systemic RNA interference response in the desert locust, Schistocerca gregaria Insect Biochem Mol Biol 42 2012 911 917
22. K. Aronstein, T. Pankiw, and E. Saldivar SID-I is implicated in systemic gene silencing in the honey bee J Apic Res 45 2006 20 24
23. S.D. Desai, Y.J. Eu, S. Whyard, and R.W. Currie Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion Insect Mol Biol 21 2012 446 455
24. E. Maori, N. Paldi, S. Shafir, H. Kalev, E. Tsur, E. Glick, and I. Sela IAPV, a bee-affecting virus associated with colony collapse disorder can be silenced by dsRNA ingestion Insect Mol Biol 18 2009 55 60
25. Y.P. Chen, J.S. Pettis, M. Corona, W.P. Chen, C.J. Li, M. Spivak, P.K. Visscher, G. DeGrandi-Hoffman, H. Boncristiani, and Y. Zhao Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health PLoS Pathog 10 2014 e1004261
26. N. Chejanovsky, R. Ophir, M.S. Schwager, Y. Slabezki, S. Grossman, and D. Cox-Foster Characterization of viral siRNA populations in honey bee colony collapse disorder Virology 454-455 2014 176 183
27. H. Wang, J. Xie, T.G. Shreeve, J. Ma, D.W. Pallett, L.A. King, and R.D. Possee Sequence recombination and conservation of varroa destructor virus-1 and deformed wing virus in field collected honey bees (Apis mellifera) PLoS ONE 8 2013 e74508
28. S.J. Martin, A.C. Highfield, L. Brettell, E.M. Villalobos, G.E. Budge, M. Powell, S. Nikaido, and D.C. Schroeder Global honey bee viral landscape altered by a parasitic mite Science 336 2012 1304 1306
29. J.T. van Mierlo, A.W. Bronkhorst, G.J. Overheul, S.A. Sadanandan, J.-O. Ekström, M. Heestermans, D. Hultmark, C. Antoniewski, and R.P. van Rij Convergent evolution of argonaute-2 slicer antagonism in two distinct insect RNA viruses PLoS Pathog 8 2012 e1002872
30. K. Azzami, W. Ritter, J. Tautz, and H. Beier Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses Arch Virol 157 2012 689 702
31. M.B. Kingsolver, and R.W. Hardy Making connections in insect innate immunity Proc Natl Acad Sci U S A 109 2012 18639 18640
32. P.N. Paradkar, L. Trinidad, R. Voysey, J.-B. Duchemin, and P.J. Walker Secreted vago restricts west nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway Proc Natl Acad Sci U S A 109 2012 18915 18920
33. M.L. Flenniken, and R. Andino Non-specific dsRNA-mediated antiviral response in the honey bee PLoS ONE 8 2013 e77263
34. X. Liu, Y. Zhang, X. Yan, and R. Han Prevention of chinese sacbrood virus infection in Apis cerana using RNA interference Curr Microbiol 61 2010 422 428
35. W. Hunter, J. Ellis, D. vanEngelsdorp, J. Hayes, D. Westervelt, E. Glick, M. Williams, I. Sela, E. Maori, J. Pettis, D. Cox-Foster, and N. Paldi Large-scale field application of RNAi technology reducing israeli acute paralysis virus disease in honey bees Apis mellifera, Hymenoptera: Apidae PLoS Pathog 6 2010 e1001160
36. Y. Garbian, E. Maori, H. Kalev, S. Shafir, and I. Sela Bidirectional transfer of RNAi between honey bee and Varroa destructor: Varroa gene silencing reduces Varroa population PLoS Pathog 8 2012 e1003035
37. B.Y. Kim, K.S. Lee, H.J. Yoon, I. Kim, J. Li, H.D. Sohn, and B.R. Jin Expression profile of the iron-binding proteins transferrin and ferritin heavy chain subunit in the bumblebee Bombus ignitus Comp Biochem Phys B 153 2009 165 170
38. H. You, H. Wan, J. Li, and B.R. Jin Molecular cloning and characterization of a short peptidoglycan recognition protein (PGRP-S) with antibacterial activity from the bumblebee Bombus ignitus Dev Comp Immunol 34 2010 977 985
39. Z. Hu, K.S. Lee, Y.M. Choo, H.J. Yoon, S.M. Lee, J.H. Lee, D.H. Kim, H.D. Sohn, and B.R. Jin Molecular cloning and characterization of 1-Cys and 2-Cys peroxiredoxins from the bumblebee Bombus ignitus Comp Biochem Phys B 155 2010 272 280
40. S. Deshwal, and E.B. Mallon Antimicrobial peptides play a functional role in bumblebee anti-trypanosome defense Dev Comp Immunol 42 2014 240 243
41. T. Farooqui, H. Vaessin, and B.H. Smith Octopamine receptors in the honeybee (Apis mellifera) brain and their disruption by RNA-mediated interference J Insect Physiol 50 2004 701 713
42. J.A. Mustard, P.M. Pham, and B.H. Smith Modulation of motor behavior by dopamine and the D1-like dopamine receptor AmDOP2 in the honey bee J Insect Physiol 56 2010 422 430
43. H.S. Gatehouse, L.N. Gatehouse, L.A. Malone, S. Hodges, E. Tregidga, and J. Todd Amylase activity in honey bee hypopharyngeal glands reduced by RNA interference J Apic Res 43 2004 9 13
44. H. Schlüns, and R.H. Crozier Relish regulates expression of antimicrobial peptide genes in the honeybee, Apis mellifera, shown by RNA interference Insect Mol Biol 16 2007 753 759
45. G. Amdam, Z. Simoes, K. Guidugli, K. Norberg, and S. Omholt Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA BMC Biotechnol 3 2003 1
46. G.V. Amdam, K. Norberg, R.E. Page Jr., J. Erber, and R. Scheiner Downregulation of vitellogenin gene activity increases the gustatory responsiveness of honey bee workers (Apis mellifera) Behav Brain Res 169 2006 201 205
47. C.M. Nelson, K.E. Ihle, M.K. Fondrk, R.E. Page Jr., and G.V. Amdam The gene vitellogenin has multiple coordinating effects on social organization PLoS Biol 5 2007 e62
48. D. Marco Antonio, K. Guidugli-Lazzarini, A. do Nascimento, Z. Simões, and K. Hartfelder RNAi-mediated silencing of vitellogenin gene function turns honeybee (Apis mellifera) workers into extremely precocious foragers Naturwissenschaften 95 2008 953 961
49. K.E. Ihle, R.E. Page Jr., K. Frederick, M.K. Fondrk, and G.V. Amdam Genotype effect on regulation of behaviour by vitellogenin supports reproductive origin of honeybee foraging bias Anim Behav 79 2010 1001 1006
50. Y. Wang, N. Baker, and G.V. Amdam RNAi-mediated double gene knockdown and gustatory perception measurement in honey bees (Apis mellifera) J Vis Exp 2013 e50446
51. L. Mussig, A. Richlitzki, R. Rossler, D. Eisenhardt, R. Menzel, and G. Leboulle Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation J Neurosci 30 2010 7817 7825
52. Y. Wang, N.S. Mutti, K.E. Ihle, A. Siegel, A.G. Dolezal, O. Kaftanoglu, and G.V. Amdam Down-regulation of honey bee IRS gene biases behavior toward food rich in protein PLoS Genet 6 2010 e1000896
53. K. Tamura, G. Stecher, D. Peterson, A. Filipski, and S. Kumar MEGA6: molecular evolutionary genetics analysis version 6.0 Mol Biol Evol 30 2013 2725 2729