Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera)
Abstract Background Deformed wing virus (DWV) is a major honey bee pathogen that is actively transmitted by the parasitic mite Varroa destructor and plays a primary role in Apis mellifera winter colony losses. Despite intense investigation on this pollinator, which has a unique environmental and eco...
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2025-01-01
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| Online Access: | https://doi.org/10.1186/s12915-025-02117-x |
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| author | Andrea Becchimanzi Giovanna De Leva Rosanna Mattossovich Serena Camerini Marialuisa Casella Giovanni Jesu Ilaria Di Lelio Sabrina Di Giorgi Joachim R. de Miranda Anna Valenti Silvia Gigliotti Francesco Pennacchio |
| author_facet | Andrea Becchimanzi Giovanna De Leva Rosanna Mattossovich Serena Camerini Marialuisa Casella Giovanni Jesu Ilaria Di Lelio Sabrina Di Giorgi Joachim R. de Miranda Anna Valenti Silvia Gigliotti Francesco Pennacchio |
| author_sort | Andrea Becchimanzi |
| collection | DOAJ |
| description | Abstract Background Deformed wing virus (DWV) is a major honey bee pathogen that is actively transmitted by the parasitic mite Varroa destructor and plays a primary role in Apis mellifera winter colony losses. Despite intense investigation on this pollinator, which has a unique environmental and economic importance, the mechanisms underlying the molecular interactions between DWV and honey bees are still poorly understood. Here, we report on a group of honey bee proteins, identified by mass spectrometry, that specifically co-immunoprecipitate with DWV virus particles. Results Most of the proteins identified are involved in fundamental metabolic pathways. Among the co-immunoprecipitated proteins, one of the most interesting was arginine kinase (ArgK), a conserved protein playing multiple roles both in physiological and pathological processes and stress response in general. Here, we investigated in more detail the relationship between DWV and this protein. We found that argK RNA level positively correlates with DWV load in field-collected honey bee larvae and adults and significantly increases in adults upon DWV injection in controlled laboratory conditions, indicating that the argK gene was upregulated by DWV infection. Silencing argK gene expression in vitro, using RNAi, resulted in reduced DWV viral load, thus confirming that argK upregulation facilitates DWV infection, likely through interfering with the delicate balance between metabolism and immunity. Conclusions In summary, these data indicate that DWV modulates the host ArgK through transcriptional regulation and cooptation to enhance its fitness in honey bees. Our findings open novel perspectives on possible new therapies for DWV control by targeting specific host proteins. |
| format | Article |
| id | doaj-art-4781ee86be124df084ea81c00a7e967c |
| institution | Kabale University |
| issn | 1741-7007 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Biology |
| spelling | doaj-art-4781ee86be124df084ea81c00a7e967c2025-01-19T12:38:46ZengBMCBMC Biology1741-70072025-01-0123111510.1186/s12915-025-02117-xDeformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera)Andrea Becchimanzi0Giovanna De Leva1Rosanna Mattossovich2Serena Camerini3Marialuisa Casella4Giovanni Jesu5Ilaria Di Lelio6Sabrina Di Giorgi7Joachim R. de Miranda8Anna Valenti9Silvia Gigliotti10Francesco Pennacchio11Department of Agricultural Sciences, University of Naples Federico IIDepartment of Agricultural Sciences, University of Naples Federico IIInstitute of Biosciences and BioResources, National Council of Research of ItalyCore Facilities, Istituto Superiore di Sanità (ISS)Core Facilities, Istituto Superiore di Sanità (ISS)Department of Agricultural Sciences, University of Naples Federico IIDepartment of Agricultural Sciences, University of Naples Federico IIMinistero della SaluteDepartment of Ecology, Swedish University of Agricultural SciencesInstitute of Biosciences and BioResources, National Council of Research of ItalyInstitute of Biosciences and BioResources, National Council of Research of ItalyDepartment of Agricultural Sciences, University of Naples Federico IIAbstract Background Deformed wing virus (DWV) is a major honey bee pathogen that is actively transmitted by the parasitic mite Varroa destructor and plays a primary role in Apis mellifera winter colony losses. Despite intense investigation on this pollinator, which has a unique environmental and economic importance, the mechanisms underlying the molecular interactions between DWV and honey bees are still poorly understood. Here, we report on a group of honey bee proteins, identified by mass spectrometry, that specifically co-immunoprecipitate with DWV virus particles. Results Most of the proteins identified are involved in fundamental metabolic pathways. Among the co-immunoprecipitated proteins, one of the most interesting was arginine kinase (ArgK), a conserved protein playing multiple roles both in physiological and pathological processes and stress response in general. Here, we investigated in more detail the relationship between DWV and this protein. We found that argK RNA level positively correlates with DWV load in field-collected honey bee larvae and adults and significantly increases in adults upon DWV injection in controlled laboratory conditions, indicating that the argK gene was upregulated by DWV infection. Silencing argK gene expression in vitro, using RNAi, resulted in reduced DWV viral load, thus confirming that argK upregulation facilitates DWV infection, likely through interfering with the delicate balance between metabolism and immunity. Conclusions In summary, these data indicate that DWV modulates the host ArgK through transcriptional regulation and cooptation to enhance its fitness in honey bees. Our findings open novel perspectives on possible new therapies for DWV control by targeting specific host proteins.https://doi.org/10.1186/s12915-025-02117-xDWVIflaviridaeProtein–protein interactionMass spectrometryATP phosphotransferaseHoney bee cells |
| spellingShingle | Andrea Becchimanzi Giovanna De Leva Rosanna Mattossovich Serena Camerini Marialuisa Casella Giovanni Jesu Ilaria Di Lelio Sabrina Di Giorgi Joachim R. de Miranda Anna Valenti Silvia Gigliotti Francesco Pennacchio Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) BMC Biology DWV Iflaviridae Protein–protein interaction Mass spectrometry ATP phosphotransferase Honey bee cells |
| title | Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) |
| title_full | Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) |
| title_fullStr | Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) |
| title_full_unstemmed | Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) |
| title_short | Deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees (Apis mellifera) |
| title_sort | deformed wing virus coopts the host arginine kinase to enhance its fitness in honey bees apis mellifera |
| topic | DWV Iflaviridae Protein–protein interaction Mass spectrometry ATP phosphotransferase Honey bee cells |
| url | https://doi.org/10.1186/s12915-025-02117-x |
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