Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale
Abstract Background It is well known that reactive oxygen species (ROS) and reactive nitrogen species (RNS) are involved in the control of pathogens and microbiota in insects. However, the knowledge of the role of ROS and RNS in tick-pathogen and tick-microbiota interactions is limited. Here, we eva...
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| Format: | Article |
| Language: | English |
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BMC
2017-12-01
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| Series: | Parasites & Vectors |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s13071-017-2575-9 |
| _version_ | 1818303114180034560 |
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| author | Sandra Patricia Kalil Rafael Diego da Rosa Janaína Capelli-Peixoto Paula Cristiane Pohl Pedro Lagerblad de Oliveira Andrea Cristina Fogaça Sirlei Daffre |
| author_facet | Sandra Patricia Kalil Rafael Diego da Rosa Janaína Capelli-Peixoto Paula Cristiane Pohl Pedro Lagerblad de Oliveira Andrea Cristina Fogaça Sirlei Daffre |
| author_sort | Sandra Patricia Kalil |
| collection | DOAJ |
| description | Abstract Background It is well known that reactive oxygen species (ROS) and reactive nitrogen species (RNS) are involved in the control of pathogens and microbiota in insects. However, the knowledge of the role of ROS and RNS in tick-pathogen and tick-microbiota interactions is limited. Here, we evaluated the immune-related redox metabolism of the embryonic cell line BME26 from the cattle tick Rhipicephalus microplus in response to Anaplasma marginale infection. Methods A high-throughput qPCR approach was used to determine the expression profile of 16 genes encoding proteins involved in either production or detoxification of ROS and RNS in response to different microbial challenges. In addition, the effect of RNAi-mediated gene silencing of catalase, glutathione peroxidase, thioredoxin and protein oxidation resistance 1 in the control of infection with A. marginale was evaluated. Results Infection with A. marginale resulted in downregulation of the genes encoding ROS-generating enzymes dual oxidase and endoplasmic reticulum oxidase. In contrast, the genes encoding the antioxidant enzymes superoxide dismutase, catalase, glutathione peroxidase, glutathione S-transferase, thioredoxin, thioredoxin reductase and peroxiredoxin were upregulated. The gene expression pattern in response to infection with Rickettsia rickettsii and exposure to heat-killed microorganisms, Micrococcus luteus, Enterobacter cloacae or S. cerevisiae was the opposite of that triggered by A. marginale challenge. The simultaneous silencing of three genes, catalase, glutathione peroxidase, and thioredoxin as well as the oxidation resistance 1 gene by RNAi apparently favoured the colonization of BME26 cells by A. marginale, suggesting that the antioxidant response might play a role in the control of infection. Conclusions Taken together, our results suggest that a general response of tick cells upon microbial stimuli is to increase ROS/RNS production. In contrast, A. marginale infection triggers an opposite profile, suggesting that this pathogen might manipulate the tick redox metabolism to evade the deleterious effect of the oxidant-based innate immune response. |
| first_indexed | 2024-12-13T05:49:39Z |
| format | Article |
| id | doaj.art-587e244f826a463194f178731399d3fa |
| institution | Directory Open Access Journal |
| issn | 1756-3305 |
| language | English |
| last_indexed | 2024-12-13T05:49:39Z |
| publishDate | 2017-12-01 |
| publisher | BMC |
| record_format | Article |
| series | Parasites & Vectors |
| spelling | doaj.art-587e244f826a463194f178731399d3fa2022-12-21T23:57:35ZengBMCParasites & Vectors1756-33052017-12-0110111010.1186/s13071-017-2575-9Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginaleSandra Patricia Kalil0Rafael Diego da Rosa1Janaína Capelli-Peixoto2Paula Cristiane Pohl3Pedro Lagerblad de Oliveira4Andrea Cristina Fogaça5Sirlei Daffre6Department of Parasitology, Institute of Biomedical Sciences, University of São PauloDepartment of Parasitology, Institute of Biomedical Sciences, University of São PauloDepartment of Parasitology, Institute of Biomedical Sciences, University of São PauloDepartment of Parasitology, Institute of Biomedical Sciences, University of São PauloLaboratory of Biochemistry of Hematophagous Arthropods, Institute of Medical Biochemistry Leopoldo de Meis, Federal University of Rio de JaneiroDepartment of Parasitology, Institute of Biomedical Sciences, University of São PauloDepartment of Parasitology, Institute of Biomedical Sciences, University of São PauloAbstract Background It is well known that reactive oxygen species (ROS) and reactive nitrogen species (RNS) are involved in the control of pathogens and microbiota in insects. However, the knowledge of the role of ROS and RNS in tick-pathogen and tick-microbiota interactions is limited. Here, we evaluated the immune-related redox metabolism of the embryonic cell line BME26 from the cattle tick Rhipicephalus microplus in response to Anaplasma marginale infection. Methods A high-throughput qPCR approach was used to determine the expression profile of 16 genes encoding proteins involved in either production or detoxification of ROS and RNS in response to different microbial challenges. In addition, the effect of RNAi-mediated gene silencing of catalase, glutathione peroxidase, thioredoxin and protein oxidation resistance 1 in the control of infection with A. marginale was evaluated. Results Infection with A. marginale resulted in downregulation of the genes encoding ROS-generating enzymes dual oxidase and endoplasmic reticulum oxidase. In contrast, the genes encoding the antioxidant enzymes superoxide dismutase, catalase, glutathione peroxidase, glutathione S-transferase, thioredoxin, thioredoxin reductase and peroxiredoxin were upregulated. The gene expression pattern in response to infection with Rickettsia rickettsii and exposure to heat-killed microorganisms, Micrococcus luteus, Enterobacter cloacae or S. cerevisiae was the opposite of that triggered by A. marginale challenge. The simultaneous silencing of three genes, catalase, glutathione peroxidase, and thioredoxin as well as the oxidation resistance 1 gene by RNAi apparently favoured the colonization of BME26 cells by A. marginale, suggesting that the antioxidant response might play a role in the control of infection. Conclusions Taken together, our results suggest that a general response of tick cells upon microbial stimuli is to increase ROS/RNS production. In contrast, A. marginale infection triggers an opposite profile, suggesting that this pathogen might manipulate the tick redox metabolism to evade the deleterious effect of the oxidant-based innate immune response.http://link.springer.com/article/10.1186/s13071-017-2575-9AnaplasmosisRedox metabolismRickettsiaeTick immunityROS |
| spellingShingle | Sandra Patricia Kalil Rafael Diego da Rosa Janaína Capelli-Peixoto Paula Cristiane Pohl Pedro Lagerblad de Oliveira Andrea Cristina Fogaça Sirlei Daffre Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale Parasites & Vectors Anaplasmosis Redox metabolism Rickettsiae Tick immunity ROS |
| title | Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale |
| title_full | Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale |
| title_fullStr | Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale |
| title_full_unstemmed | Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale |
| title_short | Immune-related redox metabolism of embryonic cells of the tick Rhipicephalus microplus (BME26) in response to infection with Anaplasma marginale |
| title_sort | immune related redox metabolism of embryonic cells of the tick rhipicephalus microplus bme26 in response to infection with anaplasma marginale |
| topic | Anaplasmosis Redox metabolism Rickettsiae Tick immunity ROS |
| url | http://link.springer.com/article/10.1186/s13071-017-2575-9 |
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