Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-06-11T08:29:54.390Z Has data issue: false hasContentIssue false
  • English
  • Français

Immunosuppressive influence of parasitoid wasp Pimpla turionellae calyx fluid on host Galleria mellonella cell-mediated immune response and hemocyte viability

Published online by Cambridge University Press:  08 October 2021

Serhat Kaya Open the ORCID record for Serhat Kaya [Opens in a new window] ,
Fevzi Uçkan  and
Aylin Er
Serhat Kaya*
Affiliation:
Department of Biology, Faculty of Arts and Sciences, CanakkaleOnsekiz Mart University, Canakkale, Turkey
Fevzi Uçkan
Affiliation:
Department of Biology, Faculty of Arts and Sciences, Kocaeli University, İzmit, Kocaeli, Turkey
Aylin Er
Affiliation:
Department of Biology, Faculty of Arts and Sciences, Balikesir University, Balikesir, Turkey
*
Author for correspondence: Serhat Kaya, Email: serhatkaya@comu.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

Endoparasitoid species devoid of symbiotic viruses inject secretions derived from their reproductive glands into their hosts during parasitism in order to avoid various immune responses of their hosts. Pimpla turionellae L. (Hymenoptera: Ichneumonidae) is an endoparasitoid that lacks polydnaviruses, and its venom has previously been shown to paralyze the host Galleria mellonella (Lepidoptera: Pyralidae) and suppress its immune reactions to ensure the egg survival. The present study demonstrates that another female-injected factor calyx fluid extracted from the P. turionellae ovary is also responsible for the suppression of G. mellonella immunity. The total hemocyte counts of G. mellonella decrease after treatment with calyx fluid in a concentration-dependent manner. Significant reductions in cell viability are also observed at all calyx fluid doses both in vivo and in vitro. The analyses of the beads injected into the insects as encapsulation targets revealed that the number of encapsulated beads reduced significantly compared to controls post-calyx fluid injection. The injection of the highest calyx fluid dose (1 female equivalent calyx) is sufficient to completely inhibit the strong encapsulation and melanization reactions of the last instar larvae 24 h post-injection. These results demonstrate that P. turionellae calyx fluid is required to regulate host immunity for successful parasitization.

Keywords

ApoptosiscalyxencapsulationGalleria mellonellahemocytePimpla turionellae
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 3 , June 2022 , pp. 361 - 369
Check for updates
Copyright
Copyright © Çanakkale Onsekiz Mart University, 2021. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asgari, S (2012) Venoms from endoparasitoid spp. In Beckage, NE and Drezen, JM (eds), Parasitoid Viruses. Academic Press, pp. 217–231.CrossRefGoogle Scholar
Beckage, NE (1993) Games parasites play: the dynamic roles of proteins and peptides in the relationship between parasite and host. In Beckage, EN and Thompson, SN (eds), Parasites and Pathogens of Insects. CA: Academic Press, pp. 25–57.CrossRefGoogle Scholar
Blass, S and Ruthmann, A (1989) Fine structure of the accessory glands of the female genital tract of the ichneumonid Pimpla turionellae (Insecta, Hymenoptera). Zoomorphology 108, 367–377.CrossRefGoogle Scholar
Bronskill, J (1961) A cage to simplify the rearing of the greater wax moth, Galleria mellonella (Pyralidae). Journal of the Lepidopterists’ Society 15, 102–104.Google Scholar
Cai, J, Ye, GY and Hu, C (2004) Parasitism of Pieris rapae (Lepidoptera: Pieridae) by a pupal endoparasitoid, Pteromaluspuparum (Hymenoptera: Pteromalidae): effects of parasitization and venom on host hemocytes. Journal of Insect Physiology 50, 315–322.CrossRefGoogle Scholar
Er, A, Uçkan, F, Rivers, DB, Ergin, E and Sak, O (2010) Effects of parasitization and envenomation by the endoparasitic wasp Pimplaturionellae (Hymenoptera: Ichneumonidae) on hemocyte numbers, morphology, and viability of its host Galleria mellonella (Lepidoptera: Pyralidae). Annals of the Entomological Society of America 103, 273–282.CrossRefGoogle Scholar
Er, A, Uçkan, F, Rivers, DB and Sak, O (2011) Cytotoxic effects of parasitism and application of venom from the endoparasitoid Pimplaturionellae on hemocytes of the host Galleria mellonella. Journal of Applied Entomology 135, 225–236.CrossRefGoogle Scholar
Ergin, E, Uçkan, F, Rivers, DB and Sak, O (2006) In vivo and in vitro activity of venom from the endoparasitic wasp Pimplaturionellae (L.) (Hymenoptera: Ichneumonidae). Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America 61, 87–97.CrossRefGoogle Scholar
Ergin, E, Uçkan, F and Rivers, DB (2007). Biochemical characterization and mode of action of venom from the endoparasitoid wasp Pimplaturionellae. In Rivers, D and Yoder, J (eds), Recent Advances in the Biochemistry, Toxicity, and Mode of Action of Parasitic Wasp Venoms. Kerala, India: Research Signpost, pp. 129–160.Google Scholar
Eslin, P and Prevost, G (1996) Variation in Drosophila concentration of haemocytes associated with different ability to encapsulate Asobaratabida larval parasitoid. Journal of Insect Physiology 42, 549–555.CrossRefGoogle Scholar
Hu, J, Xu, Q, Hu, S, Yu, X, Liang, Z and Zhang, W (2014) Hemomucin, an O-glycosylated protein on embryos of the wasp Macrocentrus cingulum that protects it against encapsulation by hemocytes of the host Ostriniafurnacalis. Journal of Innate Immunity 6, 663–675.CrossRefGoogle Scholar
Kaya, S, Uçkan, F and Er, A (2021). Influence of Indole-3-Acetic Acid on Cellular Immune Responses of Galleria mellonella L. (Lepidoptera: Pyralidae) and Pimpla turionellae L. (Hymenoptera: Ichneumonidae) in a host-parasitoid system. International Journal of Tropical Insect Science 41, 169–179.CrossRefGoogle Scholar
Kosmider, B, Zyner, E, Osiecka, R and Ochocki, J (2004) Induction of apoptosis and necrosis in A549 cells by the cis-Pt (II) complex of 3-aminoflavone in comparison with cis-DDP. Mutation Research/Genetic Toxicology and Environmental Mutagenesis 563, 61–70.CrossRefGoogle ScholarPubMed
Lavine, MD and Strand, MR (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology 32, 1295–1309.CrossRefGoogle ScholarPubMed
Li, Y, Lu, JF, Feng, CJ, Ke, XIN and Fu, WJ (2007) Role of venom and ovarian proteins in immune suppression of Ostriniafurnacalis (Lepidoptera: Pyralidae) larvae parasitized by Macrocentrus cingulum (Hymenoptera: Braconidae), a polyembryonic parasitoid. Insect Science 14, 93–100.CrossRefGoogle Scholar
Luckhart, S and Webb, BA (1996) Interaction of a wasp ovarian protein and polydnavirus in host immune suppression. Developmental & Comparative Immunology 20, 1–21.CrossRefGoogle ScholarPubMed
Mabiala-Moundoungou, ADN, Doury, G, Eslin, P, Cherqui, A and Prevost, G (2010) Deadly venom of Asobara japonica parasitoid needs ovarian antidote to regulate host physiology. Journal of Insect Physiology 56, 35–41.CrossRefGoogle ScholarPubMed
Marmaras, VJ and Lampropoulou, M (2009) Regulators and signalling in insect haemocyte immunity. Cellular Signalling 21, 186–195.CrossRefGoogle ScholarPubMed
Meng, E, Qiao, T, Tang, B, Hou, Y, Yu, W and Chen, Z (2018) Effects of ovarian fluid, venom and egg surface characteristics of Tetrastichusbrontispae (Hymenoptera: Eulophidae) on the immune response of Octodontanipae (Coleoptera: Chrysomelidae). Journal of Insect Physiology 109, 125–137.CrossRefGoogle Scholar
Moreau, SJ and Asgari, S (2015) Venom proteins from parasitoid wasps and their biological functions. Toxins 7, 2385–2412.CrossRefGoogle ScholarPubMed
Moreau, SJ, Eslin, P, Giordanengo, P and Doury, G (2003) Comparative study of the strategies evolved by two parasitoids of the genus Asobara to avoid the immune response of the host, Drosophila melanogaster. Developmental & Comparative Immunology 27, 273–282.CrossRefGoogle ScholarPubMed
Nappi, AJ, Vass, E, Frey, F and Carton, Y (1995) Superoxide anion generation in Drosophila during melanotic encapsulation of parasites. European Journal of Cell Biology 68, 450–456.Google ScholarPubMed
Osman, SE (1978) Der Einfluß der Imaginalernährung und der Begattung auf die Sekretproduktion der weiblichen Genitalanhangdrüsen und auf die Eireifung von Pimpla turionellae L. (Hym., Ichneumonidae) 1. Zeitschrift für angewandte Entomologie 85, 113–122.CrossRefGoogle Scholar
Osman, SE and Führer, E (1979) Histochemical analysis of accessory genital gland secretions in female Pimpla turionellae L. (Hymenoptera: Ichneumonidae). International Journal of Invertebrate Reproduction 1, 323–332.CrossRefGoogle Scholar
Özbek, R, Wielsch, N, Vogel, H, Lochnit, G, Foerster, F, Vilcinskas, A and von Reumont, BM (2019) Proteo-transcriptomic characterization of the venom from the endoparasitoid wasp Pimplaturionellae with aspects on its biology and evolution. Toxins 11, 721.CrossRefGoogle ScholarPubMed
Parkinson, NM and Weaver, RJ (1999) Noxious components of venom from the pupa-specific parasitoid Pimpla hypochondriaca. Journal of Invertebrate Pathology 73, 74–83.CrossRefGoogle ScholarPubMed
Prescott, SC and Breed, RS (1910) The determination of the number of body cells in milk by a direct method. The Journal of Infectious Diseases 7, 632–640.CrossRefGoogle Scholar
Quicke, DL and Butcher, BA (2021) Review of venoms of non-polydnavirus carrying ichneumonoid wasps. Biology 10, 50.CrossRefGoogle ScholarPubMed
Ratcliffe, NA, Rowley, AF, Fitzgerald, SW and Rhodes, CP (1985) Invertebrate immunity: basic concepts and recent advances. In Bourne GH (ed.), International Review of Cytology. Academic Press, vol. 97, pp. 183–350.Google Scholar
Richards, EH and Dani, MP (2008) Biochemical isolation of an insect haemocyte anti-aggregation protein from the venom of the endoparasitic wasp, Pimpla hypochondriaca, and identification of its gene. Journal of Insect Physiology 54, 1041–1049.CrossRefGoogle ScholarPubMed
Richards, EH and Parkinson, NM (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, 33–42.CrossRefGoogle ScholarPubMed
Rivers, DB, Ruggiero, L and Hayes, M (2002) The ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) differentially affects cells mediating the immune response of its flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). Journal of Insect Physiology 48, 1053–1064.CrossRefGoogle Scholar
Rivers, DB, Uçkan, F, Ergin, E and Keefer, DA (2010) Pathological and ultrastructural changes in cultured cells induced by venom from the ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae). Journal of Insect Physiology 56, 1935–1948.CrossRefGoogle Scholar
Schmidt, O, Theopold, U and Strand, M (2001) Innate immunity and its evasion and suppression by hymenopteran endoparasitoids. BioEssays 23, 344–351.CrossRefGoogle ScholarPubMed
Strand, MR and Noda, T (1991) Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor. Journal of Insect Physiology 37, 839–850.CrossRefGoogle Scholar
Strand, MR and Pech, LL (1995) Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens. Journal of General Virology 76, 283–291.CrossRefGoogle ScholarPubMed
Suzuki, M and Tanaka, T (2006) Virus-like particles in venom of Meteorus pulchricornis induce host hemocyte apoptosis. Journal of Insect Physiology 52, 602–613.CrossRefGoogle ScholarPubMed
Teng, ZW, Xu, G, Gan, SY, Chen, X, Fang, Q and Ye, GY (2016) Effects of the endoparasitoid Cotesiachilonis (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, 46–56.CrossRefGoogle ScholarPubMed
Teramoto, T and Tanaka, T (2004) Mechanism of reduction in the number of the circulating hemocytes in the Pseudaletia separata host parasitized by Cotesia kariyai. Journal of Insect Physiology 50, 1103–1111.CrossRefGoogle ScholarPubMed
Thompson, SN (1999) Nutrition and culture of entomophagous insects. Annual Review of Entomology 44, 561–592.CrossRefGoogle ScholarPubMed
Tojo, S, Naganuma, F, Arakawa, K and Yoko, S (2000) Involvement of both granular cells and plasmatocytes in phagocytic reactions in the greater wax moth, Galleria mellonella. Journal of Insect Physiology 46, 1129–1135.CrossRefGoogle ScholarPubMed
Uçkan, F, Er, A and Ergin, E (2010) Levels of encapsulation and melanization in Galleria mellonella (Lepidoptera: Pyralidae) parasitized and envenomated by Pimplaturionellae (Hymenoptera: Ichneumonidae). Journal of Applied Entomology 134, 718–726.CrossRefGoogle Scholar
Webb, BA and Luckhart, S (1994) Evidence for an early immunosuppressive role for related Campoletis sonorensis venom and ovarian proteins in Heliothis virescens. Archives of Insect Biochemistry and Physiology 26, 147–163.CrossRefGoogle ScholarPubMed
Wu, ML, Ye, GY, Zhu, JY, Chen, XX and Hu, C (2008) Isolation and characterization of an immunosuppressive protein from venom of the pupa-specific endoparasitoid Pteromalus puparum. Journal of Invertebrate Pathology 99, 186–191.CrossRefGoogle ScholarPubMed
Yu, RX, Chen, YF, Chen, XX, Huang, F, Lou, YG and Liu, SS (2007) Effects of venom/calyx fluid from the endoparasitic wasp Cotesia plutellae on the hemocytes of its host Plutella xylostella in vitro. Journal of Insect Physiology 53, 22–29.CrossRefGoogle ScholarPubMed
Zhang, G, Schmidt, O and Asgari, S (2004) A novel venom peptide from an endoparasitoid wasp is required for expression of polydnavirus genes in host hemocytes. Journal of Biological Chemistry 279, 41580–41585.CrossRefGoogle ScholarPubMed