Research Article: Polydnaviral Ankyrin Proteins Aid Parasitic Wasp Survival by Coordinate and Selective Inhibition of Hematopoietic and Immune NF-kappa B Signaling in Insect Hosts

Date Published: August 29, 2013

Publisher: Public Library of Science

Author(s): Gwenaelle Gueguen, Marta E. Kalamarz, Johnny Ramroop, Jeffrey Uribe, Shubha Govind, David S. Schneider.


Polydnaviruses are mutualists of their parasitoid wasps and express genes in immune cells of their Lepidopteran hosts. Polydnaviral genomes carry multiple copies of viral ankyrins or vankyrins. Vankyrin proteins are homologous to IκB proteins, but lack sequences for regulated degradation. We tested if Ichnoviral Vankyrins differentially impede Toll-NF-κB-dependent hematopoietic and immune signaling in a heterologous in vivo Drosophila, system. We first show that hematopoiesis and the cellular encapsulation response against parasitoid wasps are tightly-linked via NF-κB signaling. The niche, which neighbors the larval hematopoietic progenitors, responds to parasite infection. Drosophila NF-κB proteins are expressed in the niche, and non cell-autonomously influence fate choice in basal and parasite-activated hematopoiesis. These effects are blocked by the Vankyrin I2-vank-3, but not by P-vank-1, as is the expression of a NF-κB target transgene. I2-vank-3 and P-vank-1 differentially obstruct cellular and humoral inflammation. Additionally, their maternal expression weakens ventral embryonic patterning. We propose that selective perturbation of NF-κB-IκB interactions in natural hosts of parasitic wasps negatively impacts the outcome of hematopoietic and immune signaling and this immune deficit contributes to parasite survival and species success in nature.

Partial Text

Parasitic wasps develop within their insect hosts as they devour host bodies. Wasp oviposition in Drosophila larvae simultaneously activates humoral and cellular immune reactions. In a systemic acute inflammatory reaction, humoral antimicrobial secretions and cytokines from the fat body synergize with hematopoietic proliferation and differentiation, to encapsulate the wasp egg and protect host larvae [1], [2], [3]. Immune response against wasp eggs alters hematopoietic development in the larval lymph gland and in the hemolymph [4], [5], [6]. Genetic and molecular analysis of wasp-infected Drosophila hosts has revealed the fundamental role for the Toll-NF-κB pathway in both humoral and cellular immunity [2], [3], [7]. Toll signaling is also essential for basal hematopoiesis in the lymph gland [8], although the precise functions of the Toll effector proteins, the NF-κB family transcription factors Dorsal (dl) and Dorsal-related immunity factor (Dif), in either basal or activated hematopoiesis are not understood.

Despite common features, mutualistic polydnaviruses of Braconid and Ichneumonid wasps derive from different ancestral viruses [19], [20]. Yet, genomes from both families encode several copies of vankyrin genes. While high sequence similarity and multiple gene copies in the PDV genome may suggest similar localization or redundant biological effects, we observed surprising differences in localization of I3 and P1, and qualitative and quantitative differences of their effects on NF-κB signaling in hematopoiesis, immunity, and development.




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