Differential Gene Transcription in Honeybee (Apis cerana) Larvae Challenged by Chinese Sacbrood Virus (CSBV)

Yi Zhang, Xiu Huang, ZaiFu Xu, RiChou Han, JingHua Chen

Abstract


Honey bees are economically important social insect. They are suffering from all kinds of pathogens, especially the virus. In response to pathogens, different immune pathways such as Toll, Imd, Jak-Stat and RNAi are involved. In the present study, the transcription analysis of 32 immune-related genes from Apis cerana challenged by Chinese sacbrood virus (CSBV), the most widely distributed virus in A. cerana, was carried out by qRT-PCR to provide cues for the antiviral mechanism and the effective control of bee viruses. The expression level of 22 genes were statistically changed, including 11 up-regulated genes (catus-2, lys-2, vir, s3a, mta1, faa, vhdl, co-1-iv, ago-1, ago-3, aub) in which 3 (ago-1, ago-3, aub) were related to RNAi pathway, and 11 down-regulated genes (kenny, pgrp-lc, pgrp-s2, abaecin, lys-1, lys-3, domeless, tepa, mlc, dscam, rpl8) related to Toll, Imd, and Jak-Stat pathways. The results indicated CSBV infection in A. cerana may activate a RNA-based antiviral immunity system. This work constituted the first report, under laboratory conditions, about induction of immune related genes in response to CSBV.

Keywords


Apis cerana, qRT – PCR, antiviral immunity, RNAi

Full Text:

PDF

References


Ai, H.X., Yan, X., & Han, R.C. (2012). Occurrence and prevalence of seven bee viruses in Apis mellifera and Apis cerana apiaries in China. J. Invertebr. Pathol., 109: 160-164. doi: org/10.1016/j.jip.2011.10.006

Antúnez, K., Martín-Hernández, R., Prieto, L., Meana, A., Zunino, P., & Higes, M. (2009). Immune suppression in the honey bee (Apis mellifera) following infection by Nosema ceranae (Microsporidia). Environ. Microbiol., 11: 2284 - 90. doi: 10.1111/j.1462-2920.2009.01953.x

Aronstein, K.A., Murray, K.D., & Saldivar, E. (2010). Transcriptional responses in honey bee larvae infected with chalkbrood fungus. BMC Genomics, 11: 391. doi: 10.1186/1471-2164-11-391.

Azzami K., Ritter, W., Tautz, J., & 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. doi: 10.1007/s00705-012-1223-0

Boutros, M., Agaisse, H. & Perrimon, N. (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell, 3: 711 - 722. doi: org/10.1016/S1534-5807(02)00325-8

Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., & Pettis, J.S. (2012) Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. J. Insect Physiol. 58: 1090 - 1095. doi: org/10.1016/j.jinsphys.2012.04.016

Chan, Q.W., Melathopoulos, A.P., Pernal, S.F., & Foster, L.J. (2009). The innate immune and systemic response in honey bees to a bacterial pathogen, Paenibacillus larvae. BMC Genomics, 10: 387. doi:10.1186/1471-2164-10-387

Chen. Y., Zhao, Y., Hammond, J., Hsu, H.T., Evans, J., & Feldlaufer, M. (2004). Multiple virus infections in the honey bee and genome divergence of honey bee viruses. J. Invertebr. Pathol., 87: 84 - 93. doi: org/10.1016/j.jip.2004.07.005

Chen, Y.P., Pettis, J.S., Collins, A., & Feldlaufer, M.F. (2006). Prevalence and transmission of honeybee viruses. Appli. Environm. Microbiol., 72: 606 - 611. doi: 10.1128/AEM.72.1.606-611.2006

Christophides, G.K., Vlachou, D., & Kafatos, F.C. (2004). Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev., 198: 127 - 148. doi: 10.1111/j.0105-2896.2004.0127.x

Clem, R.J. (2005). The role of apoptosis in defense against baculovirus infection in insects. Curr. Top. Microbiol. Immunol., 289: 113 - 29. doi: 10.1007/3-540-27320-4_5

Ding, S.W. (2010). RNA-based antiviral immunity. Nat. Rev. Immunol., 10: 632 - 644. doi:10.1038/nri2824

Dostert, C., Jouanguy, E., Irving, P., Troxler, L., Galiana-Arnoux, D., Hetru, C., Hoffmann, J.A., & Imler, J.L. (2005). The jak-stat signaling pathway is required but not sufficient for the antiviral response of drosophila. Nat. Immunol., 6: 946 - 953. doi:10.1038/ni1237

Dussaubat, C., Brunet, J.L., Higes, M., Colbourne, J.K., & Lopez, J. (2012). Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS ONE 7(5): e37017. doi:10.1371/journal.pone.0037017

Evans, J.D., Aronstein, K., Chen, Y.P., Hetru, C., Imler, J.L., Jiang, H., Kanost, M., Thompson, G.J., Zou, Z., & Hultmark, D. (2006). Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol., 15: 645 - 656. doi: 10.1111/j.1365-2583.2006.00682.x

Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J.A., & Imler, J.L. (2006). Essential function in vivo for dicer-2 in host defense against RNA viruses in drosophila. Nat. Immunol., 7: 590 - 597. doi:10.1038/ni1335

Galiana-Arnoux, D., Deddouche, S., & Imler, J.L. (2007). Antiviral immunity in drosophila. J. Soc. Biol., 201: 359 - 365. doi: org/10.1016/j.coi.2009.01.007

Gallai, N., Salles, J.M., Settele, J., & Vaissière, B.E. (2009). Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ., 68: 810 - 821. doi: org/10.1016/j.ecolecon.2008.06.014

Garibaldi, L.A., Steffan-Dewenter, I., Kremen, C., Morales, J.M., Bommarco, R., Cunningham, S.A., Carvalheiro, L.G., Chacoff, N.P., Dudenhoffer, J.H., Greenleaf, S.S., Holzschuh, A., Isaacs, R., Krewenka, K., Mandelik, Y., Mayfield, M.M., Morandin, L.A., Potts, S.G., Ricketts, T.H., Szentgyorgyi, H., Viana, B.F., Westphal, C., Winfree, R., & Klein, A.M. (2011). Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol. Lett., 14: 1062-1072. doi: 10.1111/j.1461-0248.2011.01669.x

Garrido, P.M., Antúnez, K., Martín, M., Porrini, M.P., Zunino, P., & Eguaras, M.J. (2013). Immune-related gene expression in nurse honey bees (Apis mellifera) exposed to synthetic acaricides. J. Insect Physiol., 59: 113-119. doi: org/10.1016/j.jinsphys.2012.10.019

Ghosh, R.C., Ball, B.V., Willcocks, M.M., & Carter, M.J. (1999). The nucleotide sequence of sacbrood virus of the honey bee: an insect picorna-like virus. J. Gen. Virol., 80: 1541-1549.

Gorg, A., Postel, W., Domscheit, A., & Günther, S. (1988). Two-dimensional electrophoresis with immobilized pH gradients of leaf proteins from barley (Hordeum vulgare): method, reproducibility and genetic aspects. Electrophoresis. 9: 681- 692.

Gregorc, A., Evans, J.D., Scharf, M., & 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. doi: org/10.1016/j.jinsphys.2012.03.015

Gregory, P.G., Evans, J.D., Rinderer, T. & De Guzman, L. (2005) Conditional immune-gene suppression of honeybees parasitized by Varroa mites. J. Insect Sci., 5: 1 - 5.

Hamiduzzaman, M.M., Sinia, A., Guzman-Novoa, E., Guzman-Novoa, E., & Goodwin, P.H. (2012). Entomopatho genic fungi as potential biocontrol agents of the ecto-parasitic mite, Varroa destructor, and their effect on the immune response of honey bees (Apis mellifera L.). J. Invertebr. Pathol., 111: 237 - 243. doi: org/10.1016/j.jip.2012.09.001

Han, B., Zhang, L., Feng, M., Fang, Y., & Li, J.K. (2013). An integrated proteomics reveals pathological mechanism of honeybee (Apis cerena) sacbrood disease. J. Proteome Res., 12: 1881-1897. doi: 10.1021/pr301226d

Hoffmann, J.A. (2003). The immune response of Drosophila. Nature, 426: 33 - 38. doi:10.1038/nature02021

Honey Bee Genome Sequencing Consortium. (2006). Insights into social insects from the genome of the honeybee Apis mellifera. Nature, 443: 931 - 949. doi: 10.1038/nature05260

Hultmark, D. (2003). Drosophila immunity: Paths and patterns. Curr. Opin. Immunol., 15: 12 - 19. doi: org/10.1016/S0952-7915(02)00005-5

Keene, K.M., Foy, B.D., Sanchez-Vargas, I., Beaty, B.J., Blair, C.D., & Olson, K.E. (2004). RNA interference acts as a natural antiviral response to o’nyong-nyong virus (alphavirus; Togaviridae) infection of anopheles gambiae. Proc. Natl. Acad Sci. USA, 101: 17240 - 17245. doi: 10.1073/pnas.0406983101

Kemp, C., & Imler, J.L. (2009). Antiviral immunity in drosophila. Curr. Opin. Immunol., 21: 3 - 9. doi: org/10.1016/j.coi.2009.01.007

Liu, X.J., Zhang, Y., Yan, X., & Han, R.C. (2010). Prevention of chinese sacbrood virus infection in Apis cerana using RNA interference. Curr. Microbiol., 61: 422 - 428. doi: 10.1007/s00284-010-9633-2

Lourenço, A.P., Guidugli-Lazzarini, K.R., Freitas, F.C., Bitondi, M.M., Simões, Z.L., Parker, R., Guarna, M.M., Melathopoulos, A.P., Moon, K.M., White, R., Huxter, E., Pernal, S.F., & Foster, L.J. (2013). Bacterial infection activates the immune system response and dysregulates microRNA expression in honey bees. Insect Biochem. Mol. Biol., 43: 474 - 482. doi: org/10.1016/j.ibmb.2013.03.001

Ma, M.X., Li, M., Cheng, J., Yang, S., Wang, S.D., & Li, P.F. (2011). Molecular and biological characterization of Chinese sacbrood virus LN isolate. Comp. Funct. Genomics, doi:10.1155/2011/409386

Patel, A., Fondrk, M.K., Kaftanoglu, O., Emore, C., Hunt, G., Frederick, K., & Amdam, G.V. (2007). The making of a queen: TOR pathway is a key player in diphenic caste development. PLoS ONE, 2: e509. doi: 10.1371/journal.pone.0000509

Royet, J., Reichhart, J.-M., & HoVmann, J.A. (2005). Sensing and signaling during infection in Drosophila. Curr. Opin. Immunol., 17: 11 - 17. doi: org/10.1016/j.coi.2004.12.002

Scharlaken, B., de Graaf, D.C., & Goossens, K. (2008). Differential gene expression in the honeybee head after a bacterial challenge. Dev. Comp. Immunol., 32: 883 - 889. doi: org/10.1016/j.dci.2008.01.010

Stenbak, C.R., Ryu, J.H., Leulier, F., Pili-Floury, S., Parquet, C., Herve, M., Chaput, C., Boneca, I.G., Lee, W.J., Lemaitre, B. & Mengin-Lecreulx, D. (2004). Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway. J. Immunol., 173: 7339 - 7348. Retrived from: http://www.jimmunol.org/content/173/12/7339.short

van RiJ, R.P., Saleh, M.C., Berry, B., Foo, C., Houk, A., Antoniewski, C., & Andino, R. (2006). The RNA silencing endonuclease argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev., 20: 2985 - 2995. doi: 10.1101/gad.1482006

Werner, T., Borge-Renberg, K., Hultmark, D., Mellroth, P. & Steiner, H. (2003). Functional diversity of the Drosophila PGRP-LC gene cluster in the response to lipopolysaccharide and peptidoglycan. J. Biol. Chem., 278: 26319 - 26322. doi: 10.1074/jbc.C300184200

Xu, Y., Huang, L., Fu, S., Wu, J., & Zhou, X. (2012). Population diversity of rice stripe virus-derived siRNAs in three different hosts and RNAi-based antiviral immunity in Laodelphgax striatellus. PLoS One, 7: e46238. doi: 10.1371/journal.pone.0046238

Yan, X., Chen, J.H., & Han, R.C. (2009). Detection of Chinese sacbrood virus (CSBV) in Apis cerana by RT-PCR method. Sociobiology, 53: 687 - 694.

Yan, X., & Han, R.C. (2008). Diagnostic technologies of common pathogens of honeybees in China. Chin. Bull. Entomol., 45: 483 - 488. Retrived from: http://en.cnki.com.cn/Article_en/CJFDTOTAL-KCZS200803039.htm

Yang, X.L., & 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. doi: 10.1073/pnas.0501860102

Zhang, Y., Liu, X.J., Zhang, W.Q., & Han, R.C. (2010). Differential gene expression of the honey bees Apis mellifera and A. cerana induced by Varroa destructor infection. J. Insect Physiol., 56: 1207 - 1218. doi: org/10.1016/j.jinsphys.2010.03.019




DOI: http://dx.doi.org/10.13102/sociobiology.v60i4.413-420

Refbacks

  • There are currently no refbacks.


JCR Impact Factor 2018: 0.604