A Virulent Strain of Deformed Wing Virus (DWV) of Honeybees () Prevails after -Mediated, or , Transmission

English version České info

Honeybees are the most important managed pollinating insect, contributing billions of dollars to annual global agricultural production. Over the last century a parasitic mite, Varroa, has spread worldwide, with significant impacts on honeybee colony health as a consequence of its transmission of a cocktail of viruses while feeding on honeybee ‘blood’. The most important virus for colony health is deformed wing virus (DWV), high levels of which cause developmental deformities and premature ageing resulting in high overwintering colony losses. In experiments on individual Varroa-exposed pupae we demonstrate that a single type of virulent DWV is amplified 1,000–10,000 times in the recipient pupae, despite the mite containing a high diversity of replicating DWV strains. We could recapitulate this by direct injection of pupae with mixed virus populations, showing the virulent strain is advantaged by the route of transmission. In parallel, we detected changes in the immune response and developmental gene expression of the honeybee and propose that these contribute to the characteristic pathogenesis of DWV. Identification of a virulent strain of DWV has implications for therapeutic or prophylactic interventions to improve honeybee colony health, as well as contributing to our understanding of the biology of this important honeybee viral pathogen.

Vyšlo v časopise: A Virulent Strain of Deformed Wing Virus (DWV) of Honeybees () Prevails after -Mediated, or , Transmission. PLoS Pathog 10(6): e32767. doi:10.1371/journal.ppat.1004230
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004230

Souhrn

Zdroje

1. SorrellI, WhiteA, PedersenAB, HailsRS, BootsM (2009) The evolution of covert, silent infection as a parasite strategy. Proceedings of the Royal Society B-Biological Sciences 276 : 2217–2226.

2. LambrechtsL, ScottTW (2009) Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proceedings of the Royal Society B-Biological Sciences 276 : 1369–1378.

3. WeissRA (2002) Virulence and pathogenesis. Trends in Microbiology 10 : 314–317.

4. BootsM, GreenmanJ, RossD, NormanR, HailsR, et al. (2003) The population dynamical implications of covert infections in host-microparasite interactions. Journal of Animal Ecology 72 : 1064–1072.

5. RigaudT, Perrot-MinnotM-J, BrownMJF (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proceedings of the Royal Society B-Biological Sciences 277 : 3693–3702.

6. WoolhouseMEJ, TaylorLH, HaydonDT (2001) Population biology of multihost pathogens. Science 292 : 1109–1112.

7. KleinA-M, VaissiereBE, CaneJH, Steffan-DewenterI, CunninghamSA, et al. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B-Biological Sciences 274 : 303–313.

8. MartinSJ (2001) The role of Varroa and viral pathogens in the collapse of honeybee colonies: a modelling approach. Journal of Applied Ecology 38 : 1082–1093.

9. GenerschE, AubertM (2010) Emerging and re-emerging viruses of the honey bee (Apis mellifera L.). Veterinary Research 41 : 54 doi 10.1051vetres2010027/vetres/2010027

10. DainatB, EvansJD, ChenYP, GauthierL, NeumannP (2012) Dead or Alive: Deformed Wing Virus and Varroa destructor Reduce the Life Span of Winter Honeybees. Applied and Environmental Microbiology 78 : 981–987.

11. VanbergenAJ, BaudeM, BiesmeijerJC, BrittonNF, BrownMJF, et al. (2013) Threats to an ecosystem service: pressures on pollinators. Frontiers in Ecology and the Environment 11 : 251–259.

12. LanziG, De MirandaJR, BoniottiMB, CameronCE, LavazzaA, et al. (2006) Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). Journal of Virology 80 : 4998–5009.

13. de MirandaJR, GenerschE (2010) Deformed wing virus. Journal of Invertebrate Pathology 103: S48–S61.

14. OngusJR, PetersD, BonmatinJM, BengschE, VlakJM, et al. (2004) Complete sequence of a picorna-like virus of the genus Iflavirus replicating in the mite Varroa destructor. Journal of General Virology 85 : 3747–3755.

15. MooreJ, JironkinA, ChandlerD, BurroughsN, EvansDJ, et al. (2011) Recombinants between Deformed wing virus and Varroa destructor virus-1 may prevail in Varroa destructor-infested honeybee colonies. The Journal of general virology 92 : 156–161.

16. ZioniN, SorokerV, ChejanovskyN (2011) Replication of Varroa destructor virus 1 (VDV-1) and a Varroa destructor virus 1-deformed wing virus recombinant (VDV-1-DWV) in the head of the honey bee. Virology 417 : 106–112.

17. FujiyukiT, TakeuchiH, OnoM, OhkaS, SasakiT, et al. (2004) Novel insect picorna-like virus identified in the brains of aggressive worker honeybees. Journal of Virology 78 : 1093–1100.

18. YangXL, Cox-FosterDL (2005) Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the United States of America 102 : 7470–7475.

19. GregoryPG, EvansJD, RindererT, de GuzmanL (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. Journal of Insect Science 5 : 7.

20. MartinSJ, HighfieldAC, BrettellL, VillalobosEM, BudgeGE, et al. (2012) Global Honey Bee Viral Landscape Altered by a Parasitic Mite. Science 336 : 1304–1306.

21. NavajasM, MigeonA, AlauxC, Martin-MagnietteML, RobinsonGE, et al. (2008) Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. Bmc Genomics 9 : 301 doi: 10.1186/1471-2164-9-301

22. JohnsonRM, EvansJD, RobinsonGE, BerenbaumMR (2009) Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America 106 : 14790–14795.

23. NazziF, BrownSP, AnnosciaD, Del PiccoloF, Di PriscoG, et al. (2012) Synergistic Parasite-Pathogen Interactions Mediated by Host Immunity Can Drive the Collapse of Honeybee Colonies. Plos Pathogens 8: e1002735 doi: 10.1371/journal.ppat.1002735

24. MerklingSH, van RijRP (2013) Beyond RNAi: Antiviral defense strategies in Drosophila and mosquito. Journal of Insect Physiology 59 : 159–170.

25. KempC, ImlerJ-L (2009) Antiviral immunity in drosophila. Current Opinion in Immunology 21 : 3–9.

26. GoicB, VodovarN, MondotteJA, MonotC, FrangeulL, et al. (2013) RNA-mediated interference and reverse transcription control the persistence of RNA viruses in the insect model Drosophila. Nature Immunology 14 : 396–403.

27. RosenkranzP, AumeierP, ZiegelmannB (2010) Biology and control of Varroa destructor. Journal of Invertebrate Pathology 103: S96–S119.

28. TentchevaD, GauthierL, JouveS, Canabady-RochelleL, DainatB, et al. (2004) Polymerase Chain Reaction detection of deformed wing virus (DWV) in Apis mellifera and Varroa destructor. Apidologie 35 : 431–439.

29. MartinSJ, BallBV, CarreckNL (2013) The role of deformed wing virus in the initial collapse of varroa infested honey bee colonies in the UK. Journal of Apicultural Research 52 : 251–258 doi 10.3896ibra.1.52.5.12/ibra.1.52.5.12

30. VinciottiV, KhaninR, D'AlimonteD, LiuX, CattiniN, et al. (2005) An experimental evaluation of a loop versus a reference design for two-channel microarrays. Bioinformatics 21 : 492–501.

31. BaileyRA (2007) Designs for two-colour microarray experiments. Journal of the Royal Statistical Society Series C-Applied Statistics 56 : 365–394.

32. WeinstockGM, RobinsonGE, GibbsRA, WorleyKC, EvansJD, et al. (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443 : 931–949.

33. AshburnerM, BallCA, BlakeJA, BotsteinD, ButlerH, et al. (2000) Gene Ontology: tool for the unification of biology. Nature Genetics 25 : 25–29.

34. EvansJD, AronsteinK, ChenYP, HetruC, ImlerJL, et al. (2006) Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Molecular Biology 15 : 645–656.

35. ZouZ, LopezDL, KanostMR, EvansJD, JiangH (2006) Comparative analysis of serine protease-related genes in the honey bee genome: possible involvement in embryonic development and innate immunity. Insect Molecular Biology 15 : 603–614.

36. ChenX, YuX, CaiY, ZhengH, YuD, et al. (2010) Next-generation small RNA sequencing for microRNAs profiling in the honey bee Apis mellifera. Insect Molecular Biology 19 : 799–805.

37. LangmeadB, TrapnellC, PopM, SalzbergSL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology 10: R25 doi: 10.1186/gb-2009-10-3-r25

38. YueC, GenerschE (2005) RT-PCR analysis of Deformed wing virus in honeybees (Apis mellifera) and mites (Varroa destructor). Journal of General Virology 86 : 3419–3424.

39. MoeckelN, GisderS, GenerschE (2011) Horizontal transmission of deformed wing virus: pathological consequences in adult bees (Apis mellifera) depend on the transmission route. Journal of General Virology 92 : 370–377.

40. WoodGR, RyabovE, FannonJ, MooreJD, EvansDJ, et al. (2014) MosaicSolver: a tool for determining recombinants of viral genomes from pileup data. Nucleic Acid Research 42 (in press).

41. WangZ, GersteinM, SnyderM (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Reviews Genetics 10 : 57–63.

42. AkhterS, BaileyBA, SalamonP, AzizRK, EdwardsRA (2013) Applying Shannon's information theory to bacterial and phage genomes and metagenomes. Scientific Reports 3 : 7.

43. QuailMA, SmithM, CouplandP, OttoTD, HarrisSR, et al. (2012) A tale of three next generation sequencing platforms: comparison of Ion Torrent, Pacific Biosciences and Illumina MiSeq sequencers. Bmc Genomics 13 : 341 doi:10.1186/1471-2164-13-341

44. vanEngelsdorpD, MeixnerMD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. Journal of Invertebrate Pathology 103: S80–S95.

45. FurstMA, McMahonDP, OsborneJL, PaxtonRJ, BrownMJF (2014) Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506 : 364–366.

46. HighfieldAC, El NagarA, MackinderLCM, NoelL, HallMJ, et al. (2009) Deformed Wing Virus Implicated in Overwintering Honeybee Colony Losses. Applied and Environmental Microbiology 75 : 7212–7220.

47. KoudritskyM, DomanyE (2008) Positional distribution of human transcription factor binding sites. Nucleic Acids Research 36 : 6795–6805.

48. DoukasT, SarnowP (2011) Escape from Transcriptional Shutoff during Poliovirus Infection: NF-kappa B-Responsive Genes I kappa Ba and A20. Journal of Virology 85 : 10101–10108.

49. RozovicsJM, ChaseAJ, CathcartAL, ChouW, GershonPD, et al. (2012) Picornavirus Modification of a Host mRNA Decay Protein. Mbio 3: e00431–12 doi: 10.1128/mBio.00431-12

50. GrindeB, GayorfarM, HoddevikG (2007) Modulation of gene expression in a human cell line caused by poliovirus, vaccinia virus and interferon. Virology Journal 4 : 24 doi: 10.1186/1743-422X-4-24

51. ValanneS, WangJ-H, RametM (2011) The Drosophila Toll Signaling Pathway. Journal of Immunology 186 : 649–656.

52. DeddoucheS, MattN, BuddA, MuellerS, KempC, et al. (2008) The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in drosophila. Nature Immunology 9 : 1425–1432.

53. ParadkarPN, TrinidadL, VoyseyR, DucheminJ-B, WalkerPJ (2012) Secreted Vago restricts West Nile virus infection in Culex mosquito cells by activating the Jak-STAT pathway. Proceedings of the National Academy of Sciences of the United States of America 109 : 18915–18920.

54. ZambonRA, NandakumarM, VakhariaVN, WuLP (2005) The Toll pathway is important for an antiviral response in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 102 : 7257–7262.

55. BassetA, KhushRS, BraunA, GardanL, BoccardF, et al. (2000) The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response. Proceedings of the National Academy of Sciences of the United States of America 97 : 3376–3381.

56. LevyS, ShohamT (2005) The tetraspanin web modulates immune-signalling complexes. Nature Reviews Immunology 5 : 136–148.

57. MinakhinaS, TanW, StewardR (2011) JAK/STAT and the GATA factor Pannier control hemocyte maturation and differentiation in Drosophila. Developmental Biology 352 : 308–316.

58. LebestkyT, JungSH, BanerjeeU (2003) A serrate-expressing signaling center controls Drosophila hematopoiesis. Genes & Development 17 : 348–353.

59. RichardsEH, JonesB, BowmanA (2011) Salivary secretions from the honeybee mite, Varroa destructor: effects on insect haemocytes and preliminary biochemical characterization. Parasitology 138 : 602–608.

60. LavineMD, StrandMR (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32 : 1295–1309.

61. HillyerJF, SchmidtSL, FuchsJF, BoyleJP, ChristensenBM (2005) Age-associated mortality in immune challenged mosquitoes (Aedes aegypti) correlates with a decrease in haemocyte numbers. Cellular Microbiology 7 : 39–51.

62. HillyerJF (2009) Transcription in mosquito hemocytes in response to pathogen exposure. Journal of Biology 8 : 51.

63. WilliamsMJ (2007) Drosophila hemopoiesis and cellular immunity. Journal of Immunology 178 : 4711–4716.

64. MeisterM, LagueuxM (2003) Drosophila blood cells. Cellular Microbiology 5 : 573–580.

65. McGinnisW, KrumlaufR (1992) Homeobox genes and axial patterning. Cell 68 : 283–302.

66. MylesKM, WileyMR, MorazzaniEM, AdelmanZN (2008) Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proceedings of the National Academy of Sciences of the United States of America 105 : 19938–19943.

67. WangH, XieJ, ShreeveTG, MaJ, PallettDW, et al. (2013) Sequence Recombination and Conservation of Varroa destructor Virus-1 and Deformed Wing Virus in Field Collected Honey Bees (Apis mellifera). Plos One 8: e74508 doi: 10.1371/journal.pone.0074508

68. ChejanovskyN, OphirR, SchwagerMS, SlabezkiY, GrossmanS, et al. (2014) Characterization of viral siRNA populations in honey bee colony collapse disorder. Virology 254–255 : 176–183.

69. DesaiSD, EuYJ, WhyardS, CurrieRW (2012) Reduction in deformed wing virus infection in larval and adult honey bees (Apis mellifera L.) by double-stranded RNA ingestion. Insect Molecular Biology 21 : 446–455.

70. BrackneyDE, BeaneJE, EbelGD (2009) RNAi Targeting of West Nile Virus in Mosquito Midguts Promotes Virus Diversification. Plos Pathogens 5: e1000502 doi: 10.1371/journal.ppat.1000502

71. NayakA, BerryB, TassettoM, KunitomiM, AcevedoA, et al. (2010) Cricket paralysis virus antagonizes Argonaute 2 to modulate antiviral defense in Drosophila. Nature Structural & Molecular Biology 17 : 547–U541.

72. AmdamGV, SimoesZLP, GuidugliKR, NorbergK, OmholtSW (2003) Disruption of vitellogenin gene function in adult honeybees by intra-abdominal injection of double-stranded RNA. Bmc Biotechnology 3 : 1 doi: 10.1186/1472-6750-3-1

73. WolschinF, MuttiNS, AmdamGV (2011) Insulin receptor substrate influences female caste development in honeybees. Biology Letters 7 : 112–115.

74. Whinston M (1987) The biology of the honeybee. Boston, MA: Harvard University Press.

75. BullJC, RyabovEV, PrinceG, MeadA, ZhangC, et al. (2012) A strong immune response in young adult honeybees masks their increased susceptibility to infection compared to older bees. PLoS pathogens 8: e1003083.

76. RusticiG, KolesnikovN, BrandiziM, BurdettT, DylagM, et al. (2013) ArrayExpress update-trends in database growth and links to data analysis tools. Nucleic Acids Research 41: D987–D990.

77. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Bioinformatics and Computational Biology Solutions using R and Bioconductor. New York: Springer 397–420 p.

78. KendziorskiCM, NewtonMA, LanH, GouldMN (2003) On parametric empirical Bayes methods for comparing multiple groups using replicated gene expression profiles. Statistics in Medicine 22 : 3899–3914.

79. NewtonMA, KendziorskiCM, RichmondCS, BlattnerFR, TsuiKW (2001) On differential variability of expression ratios: Improving statistical inference about gene expression changes from microarray data. Journal of Computational Biology 8 : 37–52.

80. RossellD (2009) GAGA: A parsimonious and flexible model for differential expression analysis. Annals of Applied Statistics 3 : 1035–1051.

81. ConesaA, GotzS (2008) Blast2GO: A comprehensive suite for functional analysis in plant genomics. International journal of plant genomics 2008 : 619832–619832.

82. MaereS, HeymansK, KuiperM (2005) BiNGO: a Cytoscape plugin to assess overrepresentation of Gene Ontology categories in Biological Networks. Bioinformatics 21 : 3448–3449.

83. Team RDC (2011) R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

84. ThompsonJD, GibsonTJ, PlewniakF, JeanmouginF, HigginsDG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25 : 4876–4882.

85. FelsensteinJ (1989) PHYLIP –⁠ Phylogeny inference package (version 3.2). Cladistics 5 : 164–166.

86. LeinonenR, SugawaraH, ShumwayM (2011) Int Nucleotide Sequence Database C (2011) The Sequence Read Archive. Nucleic Acids Research 39: D19–D21.