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Polydnaviral ankyrin proteins aid parasitic wasp survival by coordinate and selective inhibition of hematopoietic and immune NF-kappa B signaling in insect hosts.

Gueguen G, Kalamarz ME, Ramroop J, Uribe J, Govind S - PLoS Pathog. (2013)

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, The City College of the City University of New York, New York, New York, United States of America.

ABSTRACT
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.

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Effect of wasp infection on D4-lacZ expression.A–A′. Uninfected Antp>GFP animals. D4-lacZ is expressed mostly in the niche (A′, arrowhead) where it colocalizes with Antp>GFP (A, yellow). B–B′. L. boulardi infection triggers four-fold increase in the expression of D4-lacZ (23.06±4.22 versus 89.65±41.4; t = −6.37, df = 14.7, p<0.001; N = 4 glands for uninfected and 8 for infected). D4-lacZ is also activated in cells of the anterior lobes. C–D′. Niche expression of D4-lacZ is abolished in glands lacking a functional dl gene (D, D′), but is observed in controls (C–C′). The reporter is expressed ectopically in the mutant but not control lobe cortex.
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ppat-1003580-g002: Effect of wasp infection on D4-lacZ expression.A–A′. Uninfected Antp>GFP animals. D4-lacZ is expressed mostly in the niche (A′, arrowhead) where it colocalizes with Antp>GFP (A, yellow). B–B′. L. boulardi infection triggers four-fold increase in the expression of D4-lacZ (23.06±4.22 versus 89.65±41.4; t = −6.37, df = 14.7, p<0.001; N = 4 glands for uninfected and 8 for infected). D4-lacZ is also activated in cells of the anterior lobes. C–D′. Niche expression of D4-lacZ is abolished in glands lacking a functional dl gene (D, D′), but is observed in controls (C–C′). The reporter is expressed ectopically in the mutant but not control lobe cortex.

Mentions: We utilized a D4-lacZ reporter, which contains four Dorsal/Dif binding sites [27]. In uninfected larvae, D4-lacZ expression (Fig. 2A–A′) co-localizes with Antp>GFP expression. This basal D4-lacZ expression suggests high Dorsal/Dif transcriptional activity in the niche even in uninfected animals. Upon L. boulardi infection, D4-lacZ expression is four times higher in infected compared to uninfected larvae (compare Fig. 2B′ to Fig. 2A′). Additionally, numerous cells of the anterior lobes are also positive for anti-β-galactosidase staining (Fig. 2B–B′). The basal D4-lacZ expression in the niche is not observed in glands from dl8/Df119 animals (compare Fig. 2C to Fig. 2D), although, surprisingly, these mutant glands express the D4-lacZ reporter in many cortical cells (Fig. 2C–D′). Thus, it appears that (a) consistent with NF-κB function in anti-wasp response, the D4-lacZ reporter is sensitive to and is differentially activated (in distinct cell populations) by parasitization; (b) transcriptional activity of Dorsal in the niche is essential for D4-lacZ expression; and (c) Dorsal possibly represses transcription of gene targets in the lobe cortex.


Polydnaviral ankyrin proteins aid parasitic wasp survival by coordinate and selective inhibition of hematopoietic and immune NF-kappa B signaling in insect hosts.

Gueguen G, Kalamarz ME, Ramroop J, Uribe J, Govind S - PLoS Pathog. (2013)

Effect of wasp infection on D4-lacZ expression.A–A′. Uninfected Antp>GFP animals. D4-lacZ is expressed mostly in the niche (A′, arrowhead) where it colocalizes with Antp>GFP (A, yellow). B–B′. L. boulardi infection triggers four-fold increase in the expression of D4-lacZ (23.06±4.22 versus 89.65±41.4; t = −6.37, df = 14.7, p<0.001; N = 4 glands for uninfected and 8 for infected). D4-lacZ is also activated in cells of the anterior lobes. C–D′. Niche expression of D4-lacZ is abolished in glands lacking a functional dl gene (D, D′), but is observed in controls (C–C′). The reporter is expressed ectopically in the mutant but not control lobe cortex.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3757122&req=5

ppat-1003580-g002: Effect of wasp infection on D4-lacZ expression.A–A′. Uninfected Antp>GFP animals. D4-lacZ is expressed mostly in the niche (A′, arrowhead) where it colocalizes with Antp>GFP (A, yellow). B–B′. L. boulardi infection triggers four-fold increase in the expression of D4-lacZ (23.06±4.22 versus 89.65±41.4; t = −6.37, df = 14.7, p<0.001; N = 4 glands for uninfected and 8 for infected). D4-lacZ is also activated in cells of the anterior lobes. C–D′. Niche expression of D4-lacZ is abolished in glands lacking a functional dl gene (D, D′), but is observed in controls (C–C′). The reporter is expressed ectopically in the mutant but not control lobe cortex.
Mentions: We utilized a D4-lacZ reporter, which contains four Dorsal/Dif binding sites [27]. In uninfected larvae, D4-lacZ expression (Fig. 2A–A′) co-localizes with Antp>GFP expression. This basal D4-lacZ expression suggests high Dorsal/Dif transcriptional activity in the niche even in uninfected animals. Upon L. boulardi infection, D4-lacZ expression is four times higher in infected compared to uninfected larvae (compare Fig. 2B′ to Fig. 2A′). Additionally, numerous cells of the anterior lobes are also positive for anti-β-galactosidase staining (Fig. 2B–B′). The basal D4-lacZ expression in the niche is not observed in glands from dl8/Df119 animals (compare Fig. 2C to Fig. 2D), although, surprisingly, these mutant glands express the D4-lacZ reporter in many cortical cells (Fig. 2C–D′). Thus, it appears that (a) consistent with NF-κB function in anti-wasp response, the D4-lacZ reporter is sensitive to and is differentially activated (in distinct cell populations) by parasitization; (b) transcriptional activity of Dorsal in the niche is essential for D4-lacZ expression; and (c) Dorsal possibly represses transcription of gene targets in the lobe cortex.

Bottom Line: 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.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.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, The City College of the City University of New York, New York, New York, United States of America.

ABSTRACT
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.

Show MeSH
Related in: MedlinePlus