IkB genes encoded in Cotesia plutellae bracovirus suppress an antiviral response and enhance baculovirus pathogenicity against the diamondback moth, Plutella xylostella

Bae, Sungwoo; Kim, Yonggyun

doi:10.1016/j.jip.2009.06.007

Cited by 44 publications

(29 citation statements)

References 33 publications

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“…Indeed, the analysis of the promoter region of genes belonging to the BV5 multigenic family allowed us to detect important sequence differences, insertions, and deletions that might explain the different expression levels observed. These results are consistent with previous studies of other PDV gene families that suggested that promoters play an important role in gene regulation (59,69). However, in-depth promoter analyses are now required to delineate the most important regulatory elements in PDV promoters.…”

Section: Discussionsupporting

confidence: 90%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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Bracoviruses (BVs) from the Polydnaviridae family are symbiotic viruses used as biological weapons by parasitoid wasps to manipulate lepidopteran host physiology and induce parasitism success. BV particles are produced by wasp ovaries and injected along with the eggs into the caterpillar host body, where viral gene expression is necessary for wasp development. Recent sequencing of the proviral genome of Cotesia congregata BV (CcBV) identified 222 predicted virulence genes present on 35 proviral segments integrated into the wasp genome. To date, the expressions of only a few selected candidate virulence genes have been studied in the caterpillar host, and we lacked a global vision of viral gene expression. In this study, a large-scale transcriptomic analysis by 454 sequencing of two immune tissues (fat body and hemocytes) of parasitized Manduca sexta caterpillar hosts allowed the detection of expression of 88 CcBV genes expressed 24 h after the onset of parasitism. We linked the expression profiles of these genes to several factors, showing that different regulatory mechanisms control viral gene expression in the host. These factors include the presence of signal peptides in encoded proteins, diversification of promoter regions, and, more surprisingly, gene position on the proviral genome. Indeed, most genes for which expression could be detected are localized in particular proviral regions globally producing higher numbers of circles. Moreover, this polydnavirus (PDV) transcriptomic analysis also reveals that a majority of CcBV genes possess at least one intron and an arthropod transcription start site, consistent with an insect origin of these virulence genes. IMPORTANCEBracoviruses (BVs) are symbiotic polydnaviruses used by parasitoid wasps to manipulate lepidopteran host physiology, ensuring wasp offspring survival. To date, the expressions of only a few selected candidate BV virulence genes have been studied in caterpillar hosts. We performed a large-scale analysis of BV gene expression in two immune tissues of Manduca sexta caterpillars parasitized by Cotesia congregata wasps. Genes for which expression could be detected corresponded to genes localized in particular regions of the viral genome globally producing higher numbers of circles. Our study thus brings an original global vision of viral gene expression and paves the way to the determination of the regulatory mechanisms enabling the expression of BV genes in targeted organisms, such as major insect pests. In addition, we identify sequence features suggesting that most BV virulence genes were acquired from insect genomes.

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Section: Discussionsupporting

confidence: 90%

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Chevignon

Thézé

Cambier

et al. 2014

J Virol

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“…Parasitized larvae exhibit severe immunosuppression in both cellular and humoral immune responses (Ibrahim & Kim, 2006;Nalini & Kim, 2007;Bae & Kim, 2009). Among several parasitic factors, CpBV is regarded as a main parasitic factor in host regulation presumably with 157 encoded genes including viral histone H4 (Chen et al, 2011).…”

Section: Introductionmentioning

confidence: 99%

Suppressive activity of a viral histone H4 against two host chromatin remodelling factors: lysine demethylase and SWI/SNF

Kumar

Venkata

Kim

2016

Journal of General Virology

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Histone H4, a nucleosome subunit in eukaryotes, plays crucial roles in DNA package and regulation of gene expression through covalent modification. A viral histone H4 encoded in Cotesia plutellae bracovirus (CpBV), a polydnavirus, is called CpBV-H4. It is highly homologous to other histone H4 proteins excepting 38 extra amino acid residues in the N terminus. CpBV-H4 can form octamer with other histone subunits and alter host gene expression. In this study, CpBV-H4 was transiently expressed in a natural host (Plutella xylostella) and its suppressive activity on host gene expression was evaluated by the suppressive subtractive hybridization (SSH) technique. The SSH targets down-regulated by CpBV-H4 were read with the 454 pyrosequencing platform and annotated using the genome of P. xylostella. The down-regulated genes (610 contigs) were annotated in most functional categories based on gene ontology. Among these SSH targets, 115 genes were functionally distinct, including two chromatin remodelling factors: a lysine-specific demethylase (Px-KDM) and a chromatin remodelling complex [Px-SWI/SNF (SWItch/Sucrose Non-Fermentable)]. Px-KDM was highly expressed in all tested tissues during the entire larval period. Suppression of Px-KDM expression by specific RNA interference (RNAi) significantly (P<0.05) reduced haemocyte nodule formation in response to immune challenge and impaired both larval and pupal development. Px-SWI/SNF was expressed in all developmental stages. Suppression of Px-SWI/SNF expression by RNAi reduced cellular immune response and interfered with adult metamorphosis. These results suggest that CpBV-H4 can alter host gene expression by interfering with chromatin modification and remodelling factors in addition to its direct epigenetic control activity.

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“…CpBV-IkB, have been suspected to suppress host humoral immune response (Bae and Kim, 2009). A current EST database introduced a cecropin gene in P. xylostella (PxCec) but its expression was not confirmed in P. xylostella.…”

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confidence: 99%

Cotesia plutellae bracovirus suppresses expression of an antimicrobial peptide, cecropin, in the diamondback Moth, Plutella xylostella, challenged by bacteria

Barandoc

Kim

2010

J Microbiol.

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An endoparasitoid wasp, Cotesia plutellae, induces significant immunosuppression of host insect, Plutella xylostella. This study was focused on suppression in humoral immune response of P. xylostella parasitized by C. plutellae. An EST database of P. xylostella provided a putative cecropin gene (PxCec) which is 627 bp long and encodes 66 amino acids. A signal peptide (22 amino acids) is predicted and two putative O-glycosylation sites in threonine are located at positions 58 and 64. Without bacterial infection, PxCec was expressed in pupa and adult stages but not in the egg and larval stages. Upon bacterial challenge, however, the larvae expressed PxCec as early as 3 h post infection (PI) and maintained high expression levels at 12-24 h PI. By 48 h PI, its expression noticeably diminished. All tested tissues of bacteria-infected P. xylostella showed PxCec expression. However, other microbes, such as virus and fungus, did not induce the PxCec expression. Parasitization by C. plutellae suppressed the expression of PxCec in response to bacterial challenge. Among the parasitic factors of C. plutellae, its symbiotic virus (C. plutellae bracovirus: CpBV) alone was able to inhibit the expression of PxCec of P. xylostella challenged by bacteria. These results indicate that PxCec expression is regulated by both immune and developmental processes in P. xylostella. The parasitization by C. plutellae inhibited the expression of PxCec by the wasp's symbiotic virus.

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IkB genes encoded in Cotesia plutellae bracovirus suppress an antiviral response and enhance baculovirus pathogenicity against the diamondback moth, Plutella xylostella

Cited by 44 publications

References 33 publications

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Functional Annotation of Cotesia congregata Bracovirus: Identification of Viral Genes Expressed in Parasitized Host Immune Tissues

Suppressive activity of a viral histone H4 against two host chromatin remodelling factors: lysine demethylase and SWI/SNF

Cotesia plutellae bracovirus suppresses expression of an antimicrobial peptide, cecropin, in the diamondback Moth, Plutella xylostella, challenged by bacteria

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