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Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health.

Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y, vanEngelsdorp D, Delaplane K, Solter L, Drummond F, Kramer M, Lipkin WI, Palacios G, Hamilton MC, Smith B, Huang SK, Zheng HQ, Li JL, Zhang X, Zhou AF, Wu LY, Zhou JZ, Lee ML, Teixeira EW, Li ZG, Evans JD - PLoS Pathog. (2014)

Bottom Line: The phenotypic differences in pathology among different strains of IAPV found globally may be due to high levels of standing genetic variation.The expression of genes involved in immune pathways in adult bees indicates that IAPV infection triggers active immune responses.We believe that the knowledge and insights gained from this study will provide a new platform for continuing studies of the IAPV-host interactions and have positive implications for disease management that will lead to mitigation of escalating honey bee colony losses worldwide.

View Article: PubMed Central - PubMed

Affiliation: USDA-ARS Bee Research Laboratory, BARC-East Building, Beltsville, Maryland, United States of America.

ABSTRACT
Israeli acute paralysis virus (IAPV) is a widespread RNA virus of honey bees that has been linked with colony losses. Here we describe the transmission, prevalence, and genetic traits of this virus, along with host transcriptional responses to infections. Further, we present RNAi-based strategies for limiting an important mechanism used by IAPV to subvert host defenses. Our study shows that IAPV is established as a persistent infection in honey bee populations, likely enabled by both horizontal and vertical transmission pathways. The phenotypic differences in pathology among different strains of IAPV found globally may be due to high levels of standing genetic variation. Microarray profiles of host responses to IAPV infection revealed that mitochondrial function is the most significantly affected biological process, suggesting that viral infection causes significant disturbance in energy-related host processes. The expression of genes involved in immune pathways in adult bees indicates that IAPV infection triggers active immune responses. The evidence that silencing an IAPV-encoded putative suppressor of RNAi reduces IAPV replication suggests a functional assignment for a particular genomic region of IAPV and closely related viruses from the Family Dicistroviridae, and indicates a novel therapeutic strategy for limiting multiple honey bee viruses simultaneously and reducing colony losses due to viral diseases. We believe that the knowledge and insights gained from this study will provide a new platform for continuing studies of the IAPV-host interactions and have positive implications for disease management that will lead to mitigation of escalating honey bee colony losses worldwide.

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Related in: MedlinePlus

An overview of gene expression profiles in IAPV infected adults and brood.(A) Venn graph compares regulated genes between adult and brood. The intersecting circles indicate overlapping genes between adult and brood. Of 4615 genes with altered expression in IAPV-positive adult and 1350 genes with altered expression in IAPV-positive brood, the number of overlapping genes between adults and brood was 336. (B) A heat map illustrates differential expression profiles of up- and down- regulated genes for adults and brood. The number of genes with altered expression was significantly higher in IAPV infected adult than in IAPV infected brood. The relative levels of gene expression are depicted using a color scale where blue indicates the lowest and red indicates the highest level of expression. Significantly enriched Gene Ontology (GO) terms of up- and down regulated gene clusters inducted by IAPV infection (ρ≤0.05) appear on the right side of the heat map.
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ppat-1004261-g005: An overview of gene expression profiles in IAPV infected adults and brood.(A) Venn graph compares regulated genes between adult and brood. The intersecting circles indicate overlapping genes between adult and brood. Of 4615 genes with altered expression in IAPV-positive adult and 1350 genes with altered expression in IAPV-positive brood, the number of overlapping genes between adults and brood was 336. (B) A heat map illustrates differential expression profiles of up- and down- regulated genes for adults and brood. The number of genes with altered expression was significantly higher in IAPV infected adult than in IAPV infected brood. The relative levels of gene expression are depicted using a color scale where blue indicates the lowest and red indicates the highest level of expression. Significantly enriched Gene Ontology (GO) terms of up- and down regulated gene clusters inducted by IAPV infection (ρ≤0.05) appear on the right side of the heat map.

Mentions: Overall, the transcriptional response to IAPV infection was substantially different between adults and brood. There were 2,522 up-regulated and 2,093 down-regulated genes identified in IAPV-positive adults, but only 825 up-regulated and 525 down-regulated genes identified in IAPV-positive brood with a very small fraction of overlapping genes between the two groups (Figure 5A). Of the up-regulated and down-regulated genes, overlapping genes between adult and brood were 268 and 68, respectively. A heat map illustrates the differential expression of enriched functional genes between adults and brood (Figure 5B). Of the genes transcriptionally altered by IAPV infection, 2,150 genes identified in adults and 716 genes identified in brood could be assigned a putative function based on orthology to D. melanogaster genes. The GO-enriched analysis of the genes that displayed fold-changes of more than 1.5 (False Discovery Rate adjusted ρ value≤0.05) and had putative D. melanogaster orthologs by the Database for Annotation, Visualization and Integrated Discovery (DAVID) revealed major functional clusters including metabolism, host cell transcription, signal transduction, cell cycle, hormone synthesis, endocytosis, phagocytosis, autophagy, and innate immune response (Table S1 and S2). The majority of genes with up-regulated expression were related to the regulation of signaling transduction and immune response, while the majority of those with down-regulated expression were involved with metabolic energy generation. Of the top functional clusters, genes that were related to immune response functions were of particular interest in this study.


Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health.

Chen YP, Pettis JS, Corona M, Chen WP, Li CJ, Spivak M, Visscher PK, DeGrandi-Hoffman G, Boncristiani H, Zhao Y, vanEngelsdorp D, Delaplane K, Solter L, Drummond F, Kramer M, Lipkin WI, Palacios G, Hamilton MC, Smith B, Huang SK, Zheng HQ, Li JL, Zhang X, Zhou AF, Wu LY, Zhou JZ, Lee ML, Teixeira EW, Li ZG, Evans JD - PLoS Pathog. (2014)

An overview of gene expression profiles in IAPV infected adults and brood.(A) Venn graph compares regulated genes between adult and brood. The intersecting circles indicate overlapping genes between adult and brood. Of 4615 genes with altered expression in IAPV-positive adult and 1350 genes with altered expression in IAPV-positive brood, the number of overlapping genes between adults and brood was 336. (B) A heat map illustrates differential expression profiles of up- and down- regulated genes for adults and brood. The number of genes with altered expression was significantly higher in IAPV infected adult than in IAPV infected brood. The relative levels of gene expression are depicted using a color scale where blue indicates the lowest and red indicates the highest level of expression. Significantly enriched Gene Ontology (GO) terms of up- and down regulated gene clusters inducted by IAPV infection (ρ≤0.05) appear on the right side of the heat map.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4117608&req=5

ppat-1004261-g005: An overview of gene expression profiles in IAPV infected adults and brood.(A) Venn graph compares regulated genes between adult and brood. The intersecting circles indicate overlapping genes between adult and brood. Of 4615 genes with altered expression in IAPV-positive adult and 1350 genes with altered expression in IAPV-positive brood, the number of overlapping genes between adults and brood was 336. (B) A heat map illustrates differential expression profiles of up- and down- regulated genes for adults and brood. The number of genes with altered expression was significantly higher in IAPV infected adult than in IAPV infected brood. The relative levels of gene expression are depicted using a color scale where blue indicates the lowest and red indicates the highest level of expression. Significantly enriched Gene Ontology (GO) terms of up- and down regulated gene clusters inducted by IAPV infection (ρ≤0.05) appear on the right side of the heat map.
Mentions: Overall, the transcriptional response to IAPV infection was substantially different between adults and brood. There were 2,522 up-regulated and 2,093 down-regulated genes identified in IAPV-positive adults, but only 825 up-regulated and 525 down-regulated genes identified in IAPV-positive brood with a very small fraction of overlapping genes between the two groups (Figure 5A). Of the up-regulated and down-regulated genes, overlapping genes between adult and brood were 268 and 68, respectively. A heat map illustrates the differential expression of enriched functional genes between adults and brood (Figure 5B). Of the genes transcriptionally altered by IAPV infection, 2,150 genes identified in adults and 716 genes identified in brood could be assigned a putative function based on orthology to D. melanogaster genes. The GO-enriched analysis of the genes that displayed fold-changes of more than 1.5 (False Discovery Rate adjusted ρ value≤0.05) and had putative D. melanogaster orthologs by the Database for Annotation, Visualization and Integrated Discovery (DAVID) revealed major functional clusters including metabolism, host cell transcription, signal transduction, cell cycle, hormone synthesis, endocytosis, phagocytosis, autophagy, and innate immune response (Table S1 and S2). The majority of genes with up-regulated expression were related to the regulation of signaling transduction and immune response, while the majority of those with down-regulated expression were involved with metabolic energy generation. Of the top functional clusters, genes that were related to immune response functions were of particular interest in this study.

Bottom Line: The phenotypic differences in pathology among different strains of IAPV found globally may be due to high levels of standing genetic variation.The expression of genes involved in immune pathways in adult bees indicates that IAPV infection triggers active immune responses.We believe that the knowledge and insights gained from this study will provide a new platform for continuing studies of the IAPV-host interactions and have positive implications for disease management that will lead to mitigation of escalating honey bee colony losses worldwide.

View Article: PubMed Central - PubMed

Affiliation: USDA-ARS Bee Research Laboratory, BARC-East Building, Beltsville, Maryland, United States of America.

ABSTRACT
Israeli acute paralysis virus (IAPV) is a widespread RNA virus of honey bees that has been linked with colony losses. Here we describe the transmission, prevalence, and genetic traits of this virus, along with host transcriptional responses to infections. Further, we present RNAi-based strategies for limiting an important mechanism used by IAPV to subvert host defenses. Our study shows that IAPV is established as a persistent infection in honey bee populations, likely enabled by both horizontal and vertical transmission pathways. The phenotypic differences in pathology among different strains of IAPV found globally may be due to high levels of standing genetic variation. Microarray profiles of host responses to IAPV infection revealed that mitochondrial function is the most significantly affected biological process, suggesting that viral infection causes significant disturbance in energy-related host processes. The expression of genes involved in immune pathways in adult bees indicates that IAPV infection triggers active immune responses. The evidence that silencing an IAPV-encoded putative suppressor of RNAi reduces IAPV replication suggests a functional assignment for a particular genomic region of IAPV and closely related viruses from the Family Dicistroviridae, and indicates a novel therapeutic strategy for limiting multiple honey bee viruses simultaneously and reducing colony losses due to viral diseases. We believe that the knowledge and insights gained from this study will provide a new platform for continuing studies of the IAPV-host interactions and have positive implications for disease management that will lead to mitigation of escalating honey bee colony losses worldwide.

Show MeSH
Related in: MedlinePlus