Immunogene and viral transcript dynamics during parasitic Varroa destructor mite infection of developing honey bee (Apis mellifera) pupae

Journal of Experimental Biology

Volumn 217, Issue 10, 2014, Pages 1710-1718

  Kuster, Ryan D ^a   Boncristiani, Humberto F ^a   Rueppell, Olav ^a  

^a UNIVERSITY OF NORTH CAROLINA AT GREENSBORO   (United States)

Author keywords

Apis mellifera; Arthropod virus interactions; Deformed wing virus; Development; DWV; Honey bee health; Immunity; Reproduction; Stress

Indexed keywords

ACARI; APIS MELLIFERA; APOIDEA; ARTHROPODA; DEFORMED WING VIRUS; VARROA; VARROA DESTRUCTOR;

TRANSCRIPTOME;

ANIMAL; BEE; GENETICS; HOST PARASITE INTERACTION; IMMUNITY; IMMUNOLOGY; PARASITOLOGY; PHYSIOLOGY; PUPA; VARROIDAE; VIROLOGY;

ANIMALS; BEES; HOST-PARASITE INTERACTIONS; IMMUNITY; PUPA; TRANSCRIPTOME; VARROIDAE;

EID: 84910683587     PISSN: 00220949     EISSN: 14779145     Source Type: Journal    
DOI: 10.1242/jeb.097766     Document Type: Article

References (57)

1. Andersen, C. L., Jensen, J. L. and O rntoft, T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245-5250.
2. Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P. and Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol. 11, 2284-2290.
3. Aronstein, K., Saldivar, E., Vega, R., Westmiller, S. and Douglas, A. E. (2012). How Varroa parasitism affects the immunological and nutritional status of the honey bee, Apis mellifera. Insects 3, 601-615.
4. Aumeier, P. and Rosenkranz, P. (2001). Sc ent or movement of Varroa destructor mites does not elicit hygienic behaviour by Africanized and Carniolan honey bees. Apidologie (Celle) 32, 253-263.
5. Azzami, K., Ritter, W., Tautz, J. and Beier, H. (2012). Infection of honey bees with acute bee paralysis virus does not trigger humoral or cellular immune responses. Arch. Virol. 157, 689-702.
6. Boecking, O. and Ritter, W. (1993). Grooming and r emoval behavior of Apis mellifera intermissa in Tunisia against Varroa jacobsoni. J. Apic. Res. 32, 127-134.
7. Boncristiani, H., Underwood, R., Schwarz, R., Evans, J. D., Pettis, J. and vanEngelsdorp, D. (2012). Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J. Insect Physiol. 58, 613-620.
8. Boncristiani, H. F., Evans, J. D., Chen, Y., Pettis, J., Murphy, C., Lopez, D. L., Simone-Finstrom, M. D., Strand, M., Tarpy, D. R. and Rueppell, O. (2013). In-vitro infection of pupae with Israeli acute paralysis virus suggests variation for susceptibility and disturbance of transcriptional homeost asis in honey bees (Apis mellifera). PLoS ONE 8, e73429.
9. Calderone, N. W. (2012). Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009. PLoS ONE 7, e37235.
10. Cameron, R. C., Duncan, E. J. and Dearden, P. K. (2013). Stable reference genes for the measurement of transcript abundance during larval caste development in the honeybee. Apidologie (Celle) 44, 357-366.
11. Casteels, P., Ampe, C., Riviere, L., Van Damme, J., Elicone, C., Fleming, M., Jacobs, F. and Tempst, P. (1990). Isolation and characterization of abaecin, a major antibacteria l response peptide in the honeybee (Apis mellifera). Eur. J. Biochem. 187, 381-386.
12. Chen, Y. P. and Siede, R. (2007). Honey bee viruses. Adv. Virus Res. 70, 33-80.
13. Cornman, R. S., Tarpy, D. R., Chen, Y., Jeffreys, L., Lopez, D., Pettis, J. S., vanEngelsdorp, D. and Evans, J. D. (2012). Pathogen webs in collapsing honey bee colonies. PLoS ONE 7, e43562.
14. Costa, A., Jan, E., Sarnow, P. and Schneider, D. (2009). The Imd pathway is involved in antiviral immune responses in Drosophila. PLoS ONE 4, e7436.
15. Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. and Neumann, P. (2012a). Dead or alive: deformed wing virus and Varroa destructor reduce the life span of winter honeybees. Appl. Environ. Microbiol. 78, 981-987.
16. Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. and Neumann, P. (2012b). Predictive markers of honey bee colony collapse. PLoS ONE 7, e32151.
17. De Gregorio, E., Spellman, P. T., Rubin, G. M. and Lemaitre, B. (2001). Genomewide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 98, 12590-12595.
18. De Ruijter, A. (1987). Reproduction of Varroa jacobsoni during successive brood cycles of the honeybee. Apidologie (Celle) 18, 321-326.
19. Donzé, G.,Guerin, P.M. 1994). Behavioral attributes and parental care of Varroa mites parasitizing honeybee brood. Behav. Ecol. Sociobiol. 34 305-319.
20. Ellis, J. D., Evans, J. D. and Pettis, J. S. (2010). Colony losses, managed colony population decline and colony collapse disorder in the United States. J. Apic. Res. 49, 134-136.
21. Erler, S., Popp, M. and Lattorff, H. M. (2011). Dynamics of immune system gene expression upon bacterial challenge and wounding in a social insect (Bombus terrestris). PLoS ONE 6, e18126.
22. Evans, J. D. (2004). Transcriptional immune responses by honey bee larvae during invasion by the bacterial pathogen, Paenibacillus larvae. J. Invertebr. Pathol. 85, 105-111.
23. Evans, J. D. (2006). Beepath: an o rdered quantitative-PCR array for exploring honey bee immunity and disease. J. Invertebr. Pathol. 93, 135-139.
24. Evans, J. D. and Schwarz, R. S. (2011). Bees brought to their knees: microbes affecting honey bee health. Trends Microbiol. 19, 614-620.
25. Evans, J. D., Aronstein, K., Chen, Y. P., Hetru, C., Imler, J. L., Jiang, H., Kanost, M., Thompson, G. J., Zou, Z. and Hultmark, D. (2006). Immune pathway s and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 15, 645-656.
26. Flenniken, M. L. and Andino, R. (2013). Non-specific dsRNA-mediated antiviral response in the honey bee. PLoS ONE 8, e77263.
27. Francis, R. M., Nielsen, S. L. and Kryger, P. (2013). Varroa-virus interaction in collapsing honey bee colonies. PLoS ONE 8, e57540.
28. Fuchs, S. and Langenbach, K. (1989). Multiple infestation of Apis mellifera L brood cells and reproduction in Varroa jacobsoni Oud. Apidologie (Celle) 20, 257-266.
29. Gregorc, A., Evans, J. D., Scharf, M. and Ellis, J. D. (2012). Gene expression in honey bee (Apis mellifera) larvae exposed to pesticides and Varroa mites (Varroa destructor). J. Insect Physiol. 58, 1042-1049.
30. Gregory, P. G., Evans, J. D., Rinderer, T. and de Guzman, L. (2005). Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J. Insect Sci. 5, 7.
31. Herniou, E. A., Huguet, E., Thézé, J., Bézier, A., Periquet, G. and Drezen, J. M. (2013). When parasitic wasps hijacked viruses: genomic and functional evolution of polydnaviruses. Philos. Trans. R. Soc. B 368, 20130051.
32. Herrmann, M., Kanbar, G. and Engels, W. (2005). Survival of honey bee (Apis mellifera) pupae after trypan blue staining of wounds caused by Varroa destructor mites or artificial perforation. Apidologie (Celle) 36, 107-111.
33. Ifantidis, M. D. (1983). Ontogenesis of the mite Varroa jacobsoni in worker and drone honeybee brood cells. J. Apic. Res. 22, 200-206.
34. Kanbar, G. and Engels, W. (2003). Ultrastructure and bacterial infection of wounds in honey bee ( Apis mellifera) pupae punctured by Varroa mites. Parasitol. Res. 90, 349-354.
35. Kraus, B. (1993). Preferences of Varroa jacobsoni for honey bees (Apis mellifera L) of different ages. J. Apic. Res. 32, 57-64.
36. Laught on, A. M., Boots, M. and Siva-Jothy, M. T. (2011). The ontogeny of immunity in the honey bee, Apis mellifera L. following an immune challenge. J. Insect Physiol. 57, 1023-1032.
37. Le Conte, Y., Ellis, M. and Ritter, W. (2010). Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie (Celle) 41, 353-363.
38. Lourenç o, A. P., Mackert, A., Cristino, A. D. and Simoes, Z. L. P. (2008). Validation of reference genes for gene expression studies in the honey bee, Apis mellifera, by quantitative real-time RT-PCR. Apidologie (Celle) 39, 372-385.
39. Martin, S. J. (1994). Ontogeny of the mite Varroa jacobsoni (Oud) in worker brood of the honeybee Apis mellifera (L) under natural conditions. Exp. Appl. Acarol. 19, 199-210.
40. Martin S. J. 1995 Reproduction of Varroa jacobsoni in cells of Apis mellifera containing one or more mother mites and the distribution of these cells.J. Apic. Res. 34 187-196.
41. Martin, S. J., Highfield, A. C., Brettell, L., Villalobos, E. M., Budge, G. E., Powell, M., Nikaido, S. and Schroeder, D. C. (2012). Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304-1306.
42. Navajas, M., Migeon, A., Alaux, C., Martin-Magniette, M., Robinson, G., Evans, J., Cros-Arteil, S., Crauser, D. and Le Conte, Y. (2008). Differential gene expression of the honey bee Apis mellifera associated with Varroa destructor infection. BMC Genomics 9, 301.
43. Nazzi, F., Brown, S. P. , Annoscia, D., Del Piccolo, F., Di Prisco, G., Varricchio, P., Della Vedova, G., Cattonaro, F., Caprio, E. and Pennacchio, F. (2012). Synergistic parasite-pathogen interactions mediated by host immunity can drive the c ollapse of honeybee colonies. PLoS Pathog. 8, e1002735.
44. Neumann, P. and Carreck, N. L. (2010). Honey bee colony losses. J. Apic. Res. 49, 1-6.
45. Neumann, P., Yañez, O., Fries, I. and de Miranda, J. R. (2012). Varroa invasion and virus adaptation. Trends Parasitol. 28, 353-354.
46. Pettis, J. S., vanEngelsdorp, D., Johnson, J. and Dively, G. (2012). Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99, 153-158.
47. Podgwaite, J. D. and Mazzone, H. M. (1986). Latency of insect viruses. Adv. Virus Res. 31, 293-320.
48. Potts, S. G., Biesmeijer, J. C., Kremen, C., Neumann, P., Schweiger, O. and Kunin, W. E. (2010). Global pollinator declines: trends, impacts and drivers. Trends Ecol. Evol. 25, 345-353.
49. Reim, T., Thamm, M., Rolke, D., Blenau, W. and Scheiner, R. (2013). Suitability of three common reference genes for quantitative real-time PCR in honey bees. Apidologie (Celle) 44, 342-350.
50. Rosenkranz, P., Aumeier , P. and Ziegelmann, B. (2010). Biology and control of Varroa destructor. J. Invertebr. Pathol. 103 Suppl. 1, S96-S119.
51. Sammataro, D., Gerson, U. and Needham, G. (2000). Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 45, 519-548.
52. Steiner, J., Dittmann, F., Rosenkranz, P. and Engels, W. (1994). The first gonocycle of the parasitic mite (Varroa jacobsoni) in relation to preimaginal development of its host, the honey bee (Apis mellifera carnica). Invertebr. Reprod. Dev. 25, 175-183.
53. van D ooremalen, C., Gerritsen, L., Cornelissen, B., van der Steen, J. J. M., van Langevelde, F. and Blacquiére, T. (2012). Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation.PLoS ONE 7, e36285.
54. Wikel, S. K. (1999). Tick modulation of host immunity: an important factor in pathogen transmission. Int. J. Parasitol. 29, 851-859.
55. Williams, G. R., Tarpy, D. R., vanEngelsdorp, D., Chauzat, M. P., Cox-Foster, D. L., Delaplane, K. S., Neumann, P., Pettis, J. S., Rogers, R. E. and Shutler, D. (2010). Colony collapse disorder in context. Bioessays 32, 845-846.
56. Yang, X. and Cox-Foster, D. L. (2005). Impact of an ectoparasite on the immunity and pathology of an invertebrate: evidence for host immunosuppression and viral amplification. Proc. Natl. Acad. Sci. USA 102, 7470-7475.
57. Zhao, R., Yu, X., Yu, H., Han, W., Zhai, L., Han, J. and Liu, J. (2009). Immunoregulatory peptides from salivary glands of the horsefly, Tabanus pleskei. Comp. Biochem. Physiol. 154B, 1-5.