Characterization of the IkappaB-like gene family in polydnaviruses associated with wasps belonging to different Braconid subfamilies

Abstract

Polydnaviruses (PDVs) are obligate symbionts of hymenopteran parasitoids of lepidopteran larvae that induce host immunosuppression and physiological redirection. PDVs include bracoviruses (BVs) and ichnoviruses (IVs), which are associated with braconid and ichneumonid wasps, respectively. In this study, the gene family encoding IkappaB-like proteins in the BVs associated with Cotesia congregata (CcBV) and Toxoneuron nigriceps (TnBV) was analysed. PDV-encoded IkappaB-like proteins (ANK) are similar to insect and mammalian IkappaB, an inhibitor of the transcription factor nuclear factor kappaB (NF-kappaB), but display shorter ankyrin domains and lack the regulatory domains for signal-mediated degradation and turnover. Phylogenetic analysis of ANK proteins indicates that those of IVs and BVs are closely related, even though these two taxa are believed to lack a common ancestor. Starting from a few hours after parasitization, the transcripts of BV ank genes were detected, at different levels, in several host tissues. The structure of the predicted proteins suggests that they may stably bind NF-kappaB/Rel transcription factors of the tumour necrosis factor (TNF)/Toll immune pathway. Accordingly, after bacterial challenge of Heliothis virescens host larvae parasitized by T. nigriceps, NF-kappaB immunoreactive material failed to enter the nucleus of host haemocytes and fat body cells. Moreover, transfection experiments in human HeLa cells demonstrated that a TnBV ank1 gene product reduced the efficiency of the TNF-alpha-induced expression of a reporter gene under NF-kappaB transcriptional control. Altogether, these results suggest strongly that TnBV ANK proteins cause retention of NF-kappaB/Rel factors in the cytoplasm and may thus contribute to suppression of the immune response in parasitized host larvae.