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Alteration of the phagocytosis and antimicrobial defense of Octodonta nipae (Coleoptera: Chrysomelidae) pupae to Escherichia coli following parasitism by Tetrastichus brontispae (Hymenoptera: Eulophidae)

  • E. Meng (a1) (a2), J. Li (a1) (a2), B. Tang (a1) (a2), Y. Hu (a1) (a2), T. Qiao (a1) (a2), Y. Hou (a1) (a2), Y. Lin (a1) (a2), J. Li (a1) (a2) and Z. Chen (a3)...


Although parasites and microbial pathogens are both detrimental to insects, little information is currently available on the mechanism involved in how parasitized hosts balance their immune responses to defend against microbial infections. We addressed this in the present study by comparing the immune response between unparasitized and parasitized pupae of the chrysomelid beetle, Octodonta nipae (Maulik), to Escherichia coli invasion. In an in vivo survival assay, a markedly reduced number of E. coli colony-forming units per microliter was detected in parasitized pupae at 12 and 24 h post-parasitism, together with decreased phagocytosis and enhanced bactericidal activity at 12 h post-parasitism. The effects that parasitism had on the mRNA expression level of selected antimicrobial peptides (AMPs) of O. nipae pupae showed that nearly all transcripts of AMPs examined were highly upregulated during the early and late parasitism stages except defensin 2B, whose mRNA expression level was downregulated at 24 h post-parasitism. Further elucidation on the main maternal fluids responsible for alteration of the primary immune response against E. coli showed that ovarian fluid increased phagocytosis at 48 h post-injection. These results indicated that the enhanced degradation of E. coli in parasitized pupae resulted mainly from the elevated bactericidal activity without observing the increased transcripts of target AMPs. This study contributes to a better understanding of the mechanisms involved in the immune responses of a parasitized host to bacterial infections.


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Akira, S. (2009) Innate immunity to pathogens diversity in receptors for microbial recognition. Immunological Reviews 227, 58.
Aung, K.M., Boldbaatar, D., Umemiya-Shirafuji, R., Liao, M., Tsuji, N., Xuenan, X., Suzuki, H., Kume, A., Galay, R.L., Tanaka, T. & Fujisaki, K. (2012) HlSRB, a class B scavenger receptor, is key to the granulocyte-mediated microbial phagocytosis in ticks. PLoS ONE 7, e33504.
Bang, K., Park, S., Yoo, J.Y. & Cho, S. (2012) Characterization and expression of attacin, an antibacterial protein-encoding gene, from the beet armyworm, Spodoptera exigua, (Hübner) (insecta: lepidoptera: noctuidae). Molecular Biology Reports 39, 51515159.
Bell, A. (2011) Antimalarial peptides-the long and the short of it. Current Pharmaceutical Design 17, 27192731.
Bicker, H., Höflich, C., Vogt, K.W., Volk, H.-D. & Katrin, R.S. (2008) A simple assay to measure phagocytosis of live bacteria. Clinical Chemistry 54, 911915.
Chernysh, S., Gordya, N. & Suborova, T. (2015) Insect antimicrobial peptide complexes prevent resistance development in bacteria. PLoS ONE 10, e0130788.
Cotter, S.C., Kruuk, L.E.B. & Wilson, K. (2004) Costs of resistance: genetic correlations and potential trade-offs in an insect immune system. Journal of Evolutionary Biology 17, 421429.
Dani, M.P., Richards, E.H., Isaac, R.E. & Edwards, J.P. (2003) Antibacterial and proteolytic activity in venom from the endoparasitic wasp Pimpla hypochondriaca (Hymenoptera: Ichneumonidae). Journal of Insect Physiology 49, 945954.
Dubovskiy, I.M., Krukova, N.A. & Glupov, V.V. (2008) Phagocytic activity and encapsulation rate of Galleria mellonella larval haemocytes during bacterial infection by Bacillus thuringiensis. Journal of Invertebrate Pathology 98, 360362.
Er, A., Uçkan, F., Rivers, D.B. & Sak, O. (2011) Cytotoxic effects of parasitism and application of venom from the endoparasitoid Pimpla turionellae on hemocytes of the host Galleria mellonella. Journal of Applied Entomology 135, 225236.
Fang, Q., Wang, F., Gatehouse, J.A., Gatehouse, A.M.R., Chen, X.-X., Hu, C. & Ye, G.-Y. (2011 a) Venom of parasitoid, Pteromalus puparum, suppresses host, Pieris rapae, immune promotion by decreasing host C-type lectin gene expression. PLoS ONE 6, e26888.
Fang, Q., Wang, L., Zhu, Y., Stanley, D.W., Chen, X., Hu, C. & Ye, G. (2011 b) Pteromalus puparum venom impairs host cellular immune responses by decreasing expression of its scavenger receptor gene. Insect Biochemistry and Molecular Biology 41, 852862.
Fieck, A., Hurwitz, I., Kang, A. & Durvasula, R. (2010) Trypanosoma cruzi: synergistic cytotoxicity of multiple amphipathic anti-microbial peptides to T. cruzi and potential bacterial hosts. Experimental Parasitology 125, 342347.
Giglio, A., Battistella, S., Talarico, F.F., Brandmayr, T.Z. & Giulianini, P.G. (2008) Circulating hemocytes from larvae and adults of Carabus (chaetocarabus) lefebvrei dejean 1826 (Coleoptera, Carabidae): cell types and their role in phagocytosis after in vivo artificial non-self-challenge. Micron 39, 552558.
Gillespie, J.P. & Kanost, M.R. (1997) Biological mediators of insect immunity. Annual Review of Entomology 42, 611643.
Giulianini, P.G., Bertolo, F., Battistella, S. & Amirante, G.A. (2003) Ultrastructure of the hemocytes of Cetonischema aeruginosa larvae (Coleoptera, Scarabaeidae): involvement of both granulocytes and oenocytoids in in vivo phagocytosis. Tissue and Cell 35, 243251.
Glupov, V.V. & Kryukova, N.A. (2016) Physiological and biochemical aspects of interactions between insect parasitoids and their hosts. Entomological Review 96, 513524.
Han, L.-B., Huang, L.-Q. & WANG, C.-Z. (2013) Host preference and suitability in the endoparasitoid Campoletis chlorideae is associated with its ability to suppress host immune responses. Ecological Entomology 38, 173182.
Haine, E.R., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008 a) Antimicrobial defense and persistent infection in insects. Science 322, 12571259.
Haine, E.R., Pollitt, L.C., Moret, Y., Siva-Jothy, M.T. & Rolff, J. (2008 b) Temporal patterns in immune responses to a range of microbial insults (Tenebrio molitor). Journal of Insect Physiology 54, 10901097.
Hou, Y.M. & Weng, Z.Q. (2010) Temperature-dependent development and life table parameters of Octodonta nipae (Coleoptera: Chrysomelidae). Environmental Entomology 39, 16761684.
Hou, Y.M., Wu, Z.J. & Wang, C.F. (2011) The status and harm of invasive insects in Fujian, China. pp. 111114 in Xie, L.H., You, M.S. & Hou, Y.M. (Eds) Biological Invasions: Problems and Countermeasures. Beijing, Science Press.
Hou, Y.M., Miao, Y.X. & Zhang, Z.Y. (2014 a) Leaf consumption capacity and damage projection of Octodonta nipae (Coleoptera: Chrysomelidae) on three palm species. Annals of the Entomological Society of America 107, 10101017.
Hou, Y.M., Miao, Y.X. & Zhang, Z.Y. (2014 b) Study on life parameters of the invasive species Octodonta nipae (Coleoptera: Chrysomelidae) on different palm species, under laboratory conditions. Journal of Economic Entomology 107, 14861495.
Huang, F., Yang, Y.Y., Shi, M., Li, J.Y., Chen, Z.Q., Chen, F.S. & Chen, X.X. (2010) Ultrastructural and functional characterization of circulating hemocytes from Plutella xylostella larva: cell types and their role in phagocytosis. Tissue and Cell 42, 360364.
Huang, F., Shi, M., Chen, X. & Zhang, J. (2011) Effect of parasitism by Diadegma semiclausum (Hymenoptera: Ichneumonidae) and its venom on the phagocytic ability of hemocytes from Plutella xylostella (Lepidoptera: Plutellidae) larvae. Acta Entomologica Sinica 54, 989996.
Hultmark, D., Engström, A., Andersson, K., Steiner, H., Bennich, H. & Boman, H.G. (1983) Insect immunity. Attacins, a family of antibacterial proteins from Hyalophora cecropia. EMBO Journal 2, 571576.
Ishihara, T., Maruyama, Y. & Furukawa, S. (2017) Gene expression and molecular characterization of a novel C-type lectin, encapsulation promoting lectin (EPL), in the rice armyworm, Mythimna separata. Insect Biochemistry and Molecular Biology 89, 5157.
Jan, S.L. & Shieh, G. (2013) Sample size determinations for Welch's test in one-way heteroscedastic ANOVA. British Journal of Mathematical and Statistical Psychology 67, 7293.
Kacsoh, B.Z. & Schlenke, T.A. (2012) High hemocyte load is associated with increased resistance against parasitoids in Drosophila suzukii, a relative of D. melanogaster. PLoS ONE 7, e34721.
Laughton, A.M., Garcia, J.R., Altincicek, B., Strand, M.R. & Gerardo, N.M. (2011) Characterisation of immune responses in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 57, 830839.
Lavine, M.D., Chen, G. & Strand, M.R. (2005) Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochemistry and Molecular Biology 35, 13351346.
Lesser, K.J., Paiusi, I.C. & Leips, J. (2006) Naturally occurring genetic variation in the age-specific immune response of Drosophila melanogaster. Aging Cell 5, 293295.
Li, L.F., Xu, Z.W., Liu, N.Y., Wu, G.X., Ren, X.M. & Zhu, J.Y. (2018) Parasitism and venom of ectoparasitoid Scleroderma guani impairs host cellular immunity. Archives of Insect Biochemistry and Physiology 98, e21451.
Ling, E.J. & Yu, X.Q. (2006) Hemocytes from the tobacco hornworm Manduca sexta have distinct functions in phagocytosis of foreign particles and self dead cells. Developmental and Comparative Immunology 30, 301309.
Mabiala-Moundoungou, A.D.N., Doury, G., Eslin, P., Cherqui, A. & Prévost, G. (2010) Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. Journal of Insect Physiology 56, 3541.
Madanagopal, N. & Kim, Y. (2006) Parasitism by Cotesia glomerata induces immunosuppression of Pieris rapae: effects of ovarian protein and polydnavirus. Journal of Asia-Pacific Entomology 9, 339346.
Mahmoud, A.M.A., De Luna-Santillana, E.J. & Rodríguez-Perez, M.A. (2012) Parasitism by the endoparasitoid wasp Cotesia flavipes induces cellular immunosuppression and enhances the susceptibility. Journal of Insect Science 11, 19.
Makarova, O., Rodriguez-Rojas, A., Eravci, M., Weise, C., Dobson, A., Johnston, P. & Rolff, J. (2016) Antimicrobial defence and persistent infection in insects revisited. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 371, 12571259.
McGwire, B., Olson, C., Tack, B. & Engman, D. (2003) Killing of African trypanosomes by antimicrobial peptides. Journal of Infectious Disease 188, 146152.
Meng, E., Tang, B., Hou, Y., Chen, X., Chen, J. & Yu, X. (2016) Altered immune function of Octodonta nipae (Maulik) to its pupal endoparasitoid, Tetrastichus brontispae Ferrière. Comparative Biochemistry and Physiology, Part B Biochemistry and Molecular Biology 198, 100109.
Moreau, S.J.M. (2013) ‘It stings a bit but it cleans well’: venoms of Hymenoptera and their antimicrobial potential. Journal of Insect Physiology 59, 186204.
Moret, Y. & Schmid-Hempel, P. (2001) Immune defence in bumble-bee offspring. Nature 414, 506.
Nalini, M., Ibrahim, A.M.A., Hwang, I. & Kim, Y. (2009) Altered actin polymerization of Plutella xylostella (L.) in response to ovarian calyx components of an endoparasitoid Cotesia plutellae (Kurdjumov). Physiological Entomology 34, 110118.
Namba, O., Nakamatsu, Y., Miura, K. & Tanaka, T. (2008) Autographa nigrisigna looper (Lepidoptera: Noctuidae) excludes parasitoid egg using cuticular encystment induced by parasitoid ovarian fluid. Applied Entomology and Zoology 43, 359367.
Nazario-Toole, A. & Wu, L. (2017) Phagocytosis in insect immunity. Advances in Insect Physiology 52, 3582.
Perron, G.G., Zasloff, M. & Bell, G. (2006) Experimental evolution of resistance to an antimicrobial peptide. Proceedings Biological Sciences 273, 251256.
Pfaffl, W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research 29, e45.
Richards, E.H. & Parkinson, N.M. (2000) Venom from the endoparasitic wasp Pimpla hypochondriaca adversely affects the morphology, viability, and immune function of hemocytes from larvae of the tomato moth, Lacanobia oleracea. Journal of Invertebrate Pathology 76, 3342.
Rohloff, L., Wiesner, A. & Götz, P. (1994) A fluorescence assay demonstrating stimulation of phagocytosis by haemolymph molecules of Gallerta mellonella. Journal of Insect Physiology 40, 10451049.
Rosales, C. (2017). Cellular and molecular mechanisms of insect immunity. pp. 179212 in Vonnie, S. (Ed.) Insect Physiology and Ecology. London, InTech.
Seufi, A.M., Hafez, E.E. & Galal, F.H. (2011) Identification, phylogenetic analysis and expression profile of an anionic insect defensin gene, with antibacterial activity, from bacterial-challenged cotton leafworm, Spodoptera littoralis. BMC Molecular Biology 12, 47.
Shen, X., Ye, G., Cheng, X., Yu, C., Yao, H. & Hu, C. (2010) Novel antimicrobial peptides identified from an endoparasitic wasp cDNA library. Journal of Peptide Science 16, 5864.
Shi, Z.H. & Sun, J.H. (2010) Immunocompetence of the red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Curculionidae, Scolytinae): variation between developmental stages and sexes in populations in China. Journal of Insect Physiology 56, 16961701.
Shiratsuchi, A., Nitta, M., Kuroda, A., Komiyama, C., Gawasawa, M., Shimamoto, N., Tuan, T.Q., Morita, T., Aiba, H. & Nakanishi, Y. (2016) Inhibition of phagocytic killing of Escherichia coli in Drosophila hemocytes by RNA Chaperone Hfq. Journal of Immunology 197, 12981307.
Smilanich, A.M., Dyer, L.A. & Gentry, G.L. (2009) The insect immune response and other putative defenses as effective predictors of parasitism. Ecology 90, 14341440.
Stoehr, A.M. (2007) Inter- and intra-sexual variation in immune defence in the cabbage white butterfly, Pieris rapae L. (Lepidoptera: Pieridae). Ecological Entomology 32, 188193.
Strand, M.R. (2008) The insect cellular immune response. Insect Science 15, 114.
Strand, M.R. & Pech, L.L. (1995) Immunological basis for compatibility in parasitoid-host relationships. Annual Review of Entomology 40, 3156.
Strand, M.R., Beck, M.H., Lavine, M.D. & Clark, K.D. (2006) Microplitis demolitor bracovirus inhibits phagocytosis by hemocytes from Pseudoplusia includens. Archives of Insect Biochemistry and Physiology 61, 134145.
Tang, B.Z. & Hou, Y.M. (2017) Nipa palm hispid beetle Octodonta nipae (Maulik). pp. 257266 in Wan, F.H., Jiang, M.X. & Zhan, A.B. (Eds) Biological Invasions and Its Management in China, Volume 11 of the Series Invading Nature – Springer Series in Invasion Ecology. The Netherlands, Springer.
Tang, B.Z., Xu, L. & Hou, Y.M. (2014 a) Effects of rearing conditions on the parasitism of Tetrastichus brontispae on its pupal host Octodonta nipae. Biocontrol 59, 647657.
Tang, B.Z., Chen, J., Hou, Y.M. & Meng, E. (2014 b) Transcriptome immune analysis of the invasive beetle Octodonta nipae (Maulik) (Coleoptera: Chrysomelidae) parasitized by Tetrastichus brontispae Ferrière (Hymenoptera: Eulophidae). PLoS ONE 9, 112.
Teng, Z., Xu, G., Gan, S., Chen, X., Fang, Q. & Ye, G.Y. (2016) Effects of the endoparasitoid Cotesia chilonis (Hymenoptera: Braconidae) parasitism, venom, and calyx fluid on cellular and humoral immunity of its host Chilo suppressalis (Lepidoptera: Crambidae) larvae. Journal of Insect Physiology 85, 4656.
Tsuzuki, S., Matsumoto, H., Furihata, S., Ryuda, M., Tanaka, H., Sung, E.J., Bird, G.S., Zhou, Y., Shears, S.B. & Hayakawa, Y. (2014) Switching between humoral and cellular and humoral responses in Drosophila is guided by the cytokine CBP. Nature Communications 5, 111.
Vogelweith, F., Korner, M., Foitzik, S. & Meunier, J. (2017) Age, pathogen exposure, but not maternal care shape offspring immunity in an insect with facultative family life. BMC Evolutionary Biology 17, 69.
Wan, F.H., Hou, Y.M. & Jiang, M.X. (2015) Invasion Biology. Beijing, China, Science Press, pp. 240244.
Xi, B., Zhang, Z.Y., Hou, Y.M. & Shi, Z.H. (2013) Effects of host plants on the developmental duration, feeding and reproduction of the nipa palm hispid, Octodonta nipae (Coleoptera: Chrysomelidae). Acta Entomologica Sinica 56, 799806.
Xu, L., Lan, J.L., Hou, Y.M., Chen, Y.S., Chen, Z.X. & Weng, Z.Q. (2011) Molecular identification and pathogenicity assay on Metarhizium against Octodonta nipae (Coleoptera: Chrysomelidae). Chinese Journal of Applied Entomology 48, 922927.
Ye, J., Zhao, H., Wang, H., Bian, J. & Zheng, R. (2010) A defensin antimicrobial peptide from the venoms of Nasonia vitripennis. Toxicon 56, 101106.
Yi, H., Chowdhury, M., Huang, Y. & Yu, X. (2014) Insect antimicrobial peptides and their applications. Applied Microbiology Biotechnology 98, 58075822.
Zhang, Q., Huang, J., Zhu, J. & Ye, G. (2012) Parasitism of Pieris rapae (Lepidoptera: Pieridae) by the endoparasitic wasp Pteromalus puparum (Hymenoptera: Pteromalidae): effects of parasitism on differential hemocyte counts, micro- and ultra-structures of host hemocytes. Insect Science 19, 485497.
Zhong, K., Liu, Z., Wang, J. & Liu, X. (2017) The entomopathogenic fungus Nomuraea rileyi impairs cellular immunity of its host Helicoverpa armigera. Archives of Insect Biochemistry and Physiology 96, e21402.


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Alteration of the phagocytosis and antimicrobial defense of Octodonta nipae (Coleoptera: Chrysomelidae) pupae to Escherichia coli following parasitism by Tetrastichus brontispae (Hymenoptera: Eulophidae)

  • E. Meng (a1) (a2), J. Li (a1) (a2), B. Tang (a1) (a2), Y. Hu (a1) (a2), T. Qiao (a1) (a2), Y. Hou (a1) (a2), Y. Lin (a1) (a2), J. Li (a1) (a2) and Z. Chen (a3)...


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