Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector
Despite the increasing number of studies concerning insect immunity, Lutzomyia longipalpis immune responses in the presence of Leishmania infantum chagasi infection has not been widely investigated. The few available studies analyzed the role of the Toll and IMD pathways involved in response against...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-03-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fcimb.2019.00071/full |
| _version_ | 1818190197940027392 |
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| author | Tatiana Di-Blasi Erich Loza Telleria Erich Loza Telleria Christiane Marques Rodrigo de Macedo Couto Monique da Silva-Neves Magdalena Jancarova Petr Volf Antonio Jorge Tempone Yara Maria Traub-Csekö |
| author_facet | Tatiana Di-Blasi Erich Loza Telleria Erich Loza Telleria Christiane Marques Rodrigo de Macedo Couto Monique da Silva-Neves Magdalena Jancarova Petr Volf Antonio Jorge Tempone Yara Maria Traub-Csekö |
| author_sort | Tatiana Di-Blasi |
| collection | DOAJ |
| description | Despite the increasing number of studies concerning insect immunity, Lutzomyia longipalpis immune responses in the presence of Leishmania infantum chagasi infection has not been widely investigated. The few available studies analyzed the role of the Toll and IMD pathways involved in response against Leishmania and microbial infections. Nevertheless, effector molecules responsible for controlling sand fly infections have not been identified. In the present study we investigated the role a signal transduction pathway, the Transforming Growth Factor-beta (TGF-β) pathway, on the interrelation between L. longipalpis and L. i. chagasi. We identified an L. longipalpis homolog belonging to the multifunctional cytokine TGF-β gene family (LlTGF-β), which is closely related to the activin/inhibin subfamily and potentially involved in responses to infections. We investigated this gene expression through the insect development and in adult flies infected with L. i. chagasi. Our results showed that LlTGF-β was expressed in all L. longipalpis developmental stages and was upregulated at the third day post L. i. chagasi infection, when protein levels were also higher as compared to uninfected insects. At this point blood digestion is finished and parasites are in close contact with the insect gut. In addition, we investigated the role of LlTGF-β on L. longipalpis infection by L. i. chagasi using either gene silencing by RNAi or pathway inactivation by addition of the TGF-β receptor inhibitor SB431542. The blockage of the LlTGF-β pathway increased significantly antimicrobial peptides expression and nitric oxide levels in the insect gut, as expected. Both methods led to a decreased L. i. chagasi infection. Our results show that inactivation of the L. longipalpis TGF-β signal transduction pathway reduce L. i. chagasi survival, therefore suggesting that under natural conditions the parasite benefits from the insect LlTGF-β pathway, as already seen in Plamodium infection of mosquitoes. |
| first_indexed | 2024-12-11T23:54:54Z |
| format | Article |
| id | doaj.art-9d5a1e88f6304379b4959e1cbdda9532 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-12-11T23:54:54Z |
| publishDate | 2019-03-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-9d5a1e88f6304379b4959e1cbdda95322022-12-22T00:45:23ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882019-03-01910.3389/fcimb.2019.00071442500Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the VectorTatiana Di-Blasi0Erich Loza Telleria1Erich Loza Telleria2Christiane Marques3Rodrigo de Macedo Couto4Monique da Silva-Neves5Magdalena Jancarova6Petr Volf7Antonio Jorge Tempone8Yara Maria Traub-Csekö9Laboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilParasitology Department, Faculty of Science, Charles University, Prague, CzechiaLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilParasitology Department, Faculty of Science, Charles University, Prague, CzechiaParasitology Department, Faculty of Science, Charles University, Prague, CzechiaLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilLaboratório de Biologia Molecular de Parasitas e Vetores, Instituto Oswaldo Cruz, Rio de Janeiro, BrazilDespite the increasing number of studies concerning insect immunity, Lutzomyia longipalpis immune responses in the presence of Leishmania infantum chagasi infection has not been widely investigated. The few available studies analyzed the role of the Toll and IMD pathways involved in response against Leishmania and microbial infections. Nevertheless, effector molecules responsible for controlling sand fly infections have not been identified. In the present study we investigated the role a signal transduction pathway, the Transforming Growth Factor-beta (TGF-β) pathway, on the interrelation between L. longipalpis and L. i. chagasi. We identified an L. longipalpis homolog belonging to the multifunctional cytokine TGF-β gene family (LlTGF-β), which is closely related to the activin/inhibin subfamily and potentially involved in responses to infections. We investigated this gene expression through the insect development and in adult flies infected with L. i. chagasi. Our results showed that LlTGF-β was expressed in all L. longipalpis developmental stages and was upregulated at the third day post L. i. chagasi infection, when protein levels were also higher as compared to uninfected insects. At this point blood digestion is finished and parasites are in close contact with the insect gut. In addition, we investigated the role of LlTGF-β on L. longipalpis infection by L. i. chagasi using either gene silencing by RNAi or pathway inactivation by addition of the TGF-β receptor inhibitor SB431542. The blockage of the LlTGF-β pathway increased significantly antimicrobial peptides expression and nitric oxide levels in the insect gut, as expected. Both methods led to a decreased L. i. chagasi infection. Our results show that inactivation of the L. longipalpis TGF-β signal transduction pathway reduce L. i. chagasi survival, therefore suggesting that under natural conditions the parasite benefits from the insect LlTGF-β pathway, as already seen in Plamodium infection of mosquitoes.https://www.frontiersin.org/article/10.3389/fcimb.2019.00071/fullLutzomyia longipalpisLeishmaniavector-parasite interactioninnate immunityTGF-βactivin |
| spellingShingle | Tatiana Di-Blasi Erich Loza Telleria Erich Loza Telleria Christiane Marques Rodrigo de Macedo Couto Monique da Silva-Neves Magdalena Jancarova Petr Volf Antonio Jorge Tempone Yara Maria Traub-Csekö Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector Frontiers in Cellular and Infection Microbiology Lutzomyia longipalpis Leishmania vector-parasite interaction innate immunity TGF-β activin |
| title | Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector |
| title_full | Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector |
| title_fullStr | Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector |
| title_full_unstemmed | Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector |
| title_short | Lutzomyia longipalpis TGF-β Has a Role in Leishmania infantum chagasi Survival in the Vector |
| title_sort | lutzomyia longipalpis tgf β has a role in leishmania infantum chagasi survival in the vector |
| topic | Lutzomyia longipalpis Leishmania vector-parasite interaction innate immunity TGF-β activin |
| url | https://www.frontiersin.org/article/10.3389/fcimb.2019.00071/full |
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