The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein
Abstract Background The tick Amblyomma sculptum is the major vector of Rickettsia rickettsii, the causative agent of the highly lethal Brazilian spotted fever. It has been shown that R. rickettsii inhibits apoptosis in both human endothelial cells and tick cells. Apoptosis is regulated by different...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
BMC
2023-03-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s13071-023-05701-8 |
| _version_ | 1797865424996532224 |
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| author | Marcelly Nassar Larissa A. Martins Josiane Betim de Assis Eliane Esteves Anderson Sá-Nunes Marcelo B. Labruna Sirlei Daffre Andrea C. Fogaça |
| author_facet | Marcelly Nassar Larissa A. Martins Josiane Betim de Assis Eliane Esteves Anderson Sá-Nunes Marcelo B. Labruna Sirlei Daffre Andrea C. Fogaça |
| author_sort | Marcelly Nassar |
| collection | DOAJ |
| description | Abstract Background The tick Amblyomma sculptum is the major vector of Rickettsia rickettsii, the causative agent of the highly lethal Brazilian spotted fever. It has been shown that R. rickettsii inhibits apoptosis in both human endothelial cells and tick cells. Apoptosis is regulated by different factors, among which inhibitors of apoptosis proteins (IAPs) play a central role. In the study reported here, we selected an IAP of A. sculptum that has not yet been characterized to assess its role in cell death and to determine the effects of its gene silencing on tick fitness and R. rickettsii infection. Methods An A. sculptum cell line (IBU/ASE-16) was treated with specific double-stranded RNA (dsRNA) for either IAP (dsIAP) or green fluorescent protein (dsGFP; as a control). The activity of caspase-3 and the exposure of phosphatidylserine were determined in both groups. In addition, unfed adult ticks, infected or not infected with R. rickettsii, were treated with either dsIAP or dsGFP and allowed to feed on noninfected rabbits. In parallel, noninfected ticks were allowed to feed on an R. rickettsii-infected rabbit. Ticks (infected or not with R. rickettsii) that remained unfed were used as a control. Results Caspase-3 activity and the externalization of phosphatidylserine were significantly higher in IBU/ASE-16 cells treated with dsIAP than in those treated with dsGFP. The mortality rates of ticks in the dsIAP group were much higher than those in the dsGFP group when they were allowed to feed on rabbits, independent of the presence of R. rickettsii. Conversely, lower mortality rates were recorded in unfed ticks. Conclusions Our results show that IAP negatively regulates apoptosis in A. sculptum cells. Moreover, IAP-silenced ticks experienced higher mortality rates following the acquisition of a blood meal, suggesting that feeding may trigger the activation of apoptosis in the absence of this physiological regulator. These findings indicate that IAP is a potential antigen for an anti-tick vaccine. Graphical Abstract |
| first_indexed | 2024-04-09T23:08:37Z |
| format | Article |
| id | doaj.art-a513d62939fe443b90da68592ea57945 |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-04-09T23:08:37Z |
| publishDate | 2023-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-a513d62939fe443b90da68592ea579452023-03-22T10:33:31ZengBMCParasites & Vectors1756-33052023-03-0116111010.1186/s13071-023-05701-8The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis proteinMarcelly Nassar0Larissa A. Martins1Josiane Betim de Assis2Eliane Esteves3Anderson Sá-Nunes4Marcelo B. Labruna5Sirlei Daffre6Andrea C. Fogaça7Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloNational Institute of Allergy and Infectious Diseases, National Institutes of Health, Rocky Mountain LaboratoriesDepartamento de Imunologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Imunologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Medicina Veterinária Preventiva e Saúde Animal, Faculdade de Medicina Veterinária e Zootecnia, Universidade de São PauloDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloDepartamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São PauloAbstract Background The tick Amblyomma sculptum is the major vector of Rickettsia rickettsii, the causative agent of the highly lethal Brazilian spotted fever. It has been shown that R. rickettsii inhibits apoptosis in both human endothelial cells and tick cells. Apoptosis is regulated by different factors, among which inhibitors of apoptosis proteins (IAPs) play a central role. In the study reported here, we selected an IAP of A. sculptum that has not yet been characterized to assess its role in cell death and to determine the effects of its gene silencing on tick fitness and R. rickettsii infection. Methods An A. sculptum cell line (IBU/ASE-16) was treated with specific double-stranded RNA (dsRNA) for either IAP (dsIAP) or green fluorescent protein (dsGFP; as a control). The activity of caspase-3 and the exposure of phosphatidylserine were determined in both groups. In addition, unfed adult ticks, infected or not infected with R. rickettsii, were treated with either dsIAP or dsGFP and allowed to feed on noninfected rabbits. In parallel, noninfected ticks were allowed to feed on an R. rickettsii-infected rabbit. Ticks (infected or not with R. rickettsii) that remained unfed were used as a control. Results Caspase-3 activity and the externalization of phosphatidylserine were significantly higher in IBU/ASE-16 cells treated with dsIAP than in those treated with dsGFP. The mortality rates of ticks in the dsIAP group were much higher than those in the dsGFP group when they were allowed to feed on rabbits, independent of the presence of R. rickettsii. Conversely, lower mortality rates were recorded in unfed ticks. Conclusions Our results show that IAP negatively regulates apoptosis in A. sculptum cells. Moreover, IAP-silenced ticks experienced higher mortality rates following the acquisition of a blood meal, suggesting that feeding may trigger the activation of apoptosis in the absence of this physiological regulator. These findings indicate that IAP is a potential antigen for an anti-tick vaccine. Graphical Abstracthttps://doi.org/10.1186/s13071-023-05701-8ApoptosisTickCaspaseIAPRickettsia |
| spellingShingle | Marcelly Nassar Larissa A. Martins Josiane Betim de Assis Eliane Esteves Anderson Sá-Nunes Marcelo B. Labruna Sirlei Daffre Andrea C. Fogaça The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein Parasites & Vectors Apoptosis Tick Caspase IAP Rickettsia |
| title | The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein |
| title_full | The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein |
| title_fullStr | The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein |
| title_full_unstemmed | The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein |
| title_short | The survival of Amblyomma sculptum ticks upon blood-feeding depends on the expression of an inhibitor of apoptosis protein |
| title_sort | survival of amblyomma sculptum ticks upon blood feeding depends on the expression of an inhibitor of apoptosis protein |
| topic | Apoptosis Tick Caspase IAP Rickettsia |
| url | https://doi.org/10.1186/s13071-023-05701-8 |
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