Immunoevasive protein (IEP)-containing surface layer covering polydnavirus particles is essential for viral infection

• Published in: Journal of invertebrate pathology Vol. 115; pp. 26 - 32
• Main Authors: Furihata, Shunsuke, Tanaka, Kohjiro, Ryuda, Masasuke, Ochiai, Masanori, Matsumoto, Hitoshi, Csikos, Gyorge, Hayakawa, Yoichi
• Format: Journal Article
• Language: English
• Published: Amsterdam Elsevier Inc 01.01.2014; Elsevier
• Subjects: Animals; Biological and medical sciences; Blotting, Western; Chromatography, High Pressure Liquid; Fundamental and applied biological sciences. Psychology; Host-Parasite Interactions - physiology; Immunoevasive protein; Insect Proteins - immunology; Insect Proteins - metabolism; Insecta; Invertebrates; Microbiology; Oviduct; Parasitoid wasp; Polydnaviridae - immunology; Polydnaviridae - pathogenicity; Polydnavirus; Replicative cycle, interference, host-virus relations, pathogenicity, miscellaneous strains; Reverse Transcriptase Polymerase Chain Reaction; Venom; Virion - immunology; Virion - metabolism; Virology; Wasps - immunology; Wasps - metabolism; Wasps - virology; Immunoevasive protein; Polydnavirus; Parasitoid wasp; Oviduct; Venom; Biochemical compound; Insecta; Surface layer; Protein; Infection; Particle; Virus; Parasitoid; Entomophagous; Arthropoda; Female genital system; Invertebrata; Hymenoptera
• ISSN: 0022-2011; 1096-0805
• DOI: 10.1016/j.jip.2013.10.013

•Cotesia kariyai parasitoid wasp utilizes polydnavirus (CkPDV) for successful parasitization.•CkPDV particle is covered by a previously unidentified thin surface layer containing immunoevasive protein (IEP).•The thin layer is easily separated from CkPDV particles by mechanical stressors such as shaking.•The thin layer is essential for CkPDV particles to infect the wasp’s host tissues.•One of IEP family proteins is expressed in the venom reservoirs of C. kariyai wasps. Polydnaviruses (PDVs) are unique symbiotic viruses associated with parasitoid wasps: PDV particles are injected into lepidopteran hosts along with the wasp eggs and express genes that interfere with aspects of host physiology such as immune defenses and development. Recent comparative genomic studies of PDVs have significantly improved our understanding of their origin as well as the genome organization. However, the structural features of functional PDV particles remain ambiguous. To clear up the structure of Cotesia kariyai PDV (CkPDV) particles, we focused on immunoevasive protein (IEP), which is a mediator of immunoevasion by the wasp from the encapsulation reaction of the host insect’s hemocytes, because it has been demonstrated to be present on the surface of the virus particle. We discovered that IEP tends to polymerize and constitutes a previously unidentified thin surface layer covering CkPDV particles. This outermost surface layer looked fragile and was easily removed from CkPVD particles by mechanical stressors such as shaking, which prevented CkPDV from expressing the encoded genes in the host target tissues such as fat body or hemocytes. Furthermore, we detected IEP homologue gene expression in the wasp’s venom reservoirs, implying IEP has another unknown biological function in the wasp or parasitized hosts. Taken together, the present results demonstrated that female C. kariyai wasps produce the fragile thin layer partly composed of IEP to cover the outer surfaces of CkPDV particles; otherwise, they cannot function as infectious agents in the wasp’s host. The fact that IEP family proteins are expressed in both venom reservoirs and oviducts suggests an intimate relationship between both tissues in the development of the parasitism strategy of the wasp.