Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo
Amblyomma sculptum is an important vector of Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever and the most lethal tick-borne pathogen affecting humans. To feed on the vertebrate host's blood, A. sculptum secretes a salivary mixture, which may interact with skin resident de...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-02-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fimmu.2019.00118/full |
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| author | Eliane Esteves Bruna Bizzarro Francisco Borges Costa Alejandro Ramírez-Hernández Ana Paula Ferranti Peti Allan Henrique Depieri Cataneo Pryscilla Fanini Wowk Rodolfo Pessato Timóteo Marcelo Bahia Labruna Pedro Ismael Silva Junior Célio Lopes Silva Lúcia Helena Faccioli Andréa Cristina Fogaça Andréa Cristina Fogaça Carlos Arterio Sorgi Anderson Sá-Nunes Anderson Sá-Nunes |
| author_facet | Eliane Esteves Bruna Bizzarro Francisco Borges Costa Alejandro Ramírez-Hernández Ana Paula Ferranti Peti Allan Henrique Depieri Cataneo Pryscilla Fanini Wowk Rodolfo Pessato Timóteo Marcelo Bahia Labruna Pedro Ismael Silva Junior Célio Lopes Silva Lúcia Helena Faccioli Andréa Cristina Fogaça Andréa Cristina Fogaça Carlos Arterio Sorgi Anderson Sá-Nunes Anderson Sá-Nunes |
| author_sort | Eliane Esteves |
| collection | DOAJ |
| description | Amblyomma sculptum is an important vector of Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever and the most lethal tick-borne pathogen affecting humans. To feed on the vertebrate host's blood, A. sculptum secretes a salivary mixture, which may interact with skin resident dendritic cells (DCs) and modulate their function. The present work was aimed at depicting the A. sculptum saliva-host DC network and the biochemical nature of the immunomodulatory component(s) involved in this interface. A. sculptum saliva inhibits the production of inflammatory cytokines by murine DCs stimulated with LPS. The fractionation of the low molecular weight salivary content by reversed-phase chromatography revealed active fractions eluting from 49 to 55% of the acetonitrile gradient. Previous studies suggested that this pattern of elution matches with that observed for prostaglandin E2 (PGE2) and the molecular identity of this lipid mediator was unambiguously confirmed by a new high-resolution mass spectrometry methodology. A productive infection of murine DCs by R. rickettsii was demonstrated for the first time leading to proinflammatory cytokine production that was inhibited by both A. sculptum saliva and PGE2, a result also achieved with human DCs. The adoptive transfer of murine DCs incubated with R. rickettsii followed by treatment with A. sculptum saliva or PGE2 did not change the cytokine profile associated to cellular recall responses while IgG2a-specific antibodies were decreased in the serum of these mice. Together, these findings emphasize the role of PGE2 as a universal immunomodulator of tick saliva. In addition, it contributes to new approaches to explore R. rickettsii-DC interactions both in vitro and in vivo. |
| first_indexed | 2024-12-11T15:29:35Z |
| format | Article |
| id | doaj.art-e68494d344cb4c92a3269190ed853216 |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-11T15:29:35Z |
| publishDate | 2019-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-e68494d344cb4c92a3269190ed8532162022-12-22T01:00:07ZengFrontiers Media S.A.Frontiers in Immunology1664-32242019-02-011010.3389/fimmu.2019.00118410563Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivoEliane Esteves0Bruna Bizzarro1Francisco Borges Costa2Alejandro Ramírez-Hernández3Ana Paula Ferranti Peti4Allan Henrique Depieri Cataneo5Pryscilla Fanini Wowk6Rodolfo Pessato Timóteo7Marcelo Bahia Labruna8Pedro Ismael Silva Junior9Célio Lopes Silva10Lúcia Helena Faccioli11Andréa Cristina Fogaça12Andréa Cristina Fogaça13Carlos Arterio Sorgi14Anderson Sá-Nunes15Anderson Sá-Nunes16Department of Immunology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilDepartment of Immunology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilDepartment of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, BrazilDepartment of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, BrazilDepartment of Clinical Analysis, Toxicology and Food Science, School of Pharmaceutical Sciences of Ribeirao Preto, University of São Paulo, Ribeirao Preto, BrazilLaboratory of Molecular Virology, Carlos Chagas Institute, Fundação Oswaldo Cruz, Curitiba, BrazilLaboratory of Molecular Virology, Carlos Chagas Institute, Fundação Oswaldo Cruz, Curitiba, BrazilInstitute of Natural and Biological Sciences, Federal University of Triângulo Mineiro, Uberaba, BrazilDepartment of Preventive Veterinary Medicine and Animal Health, School of Veterinary Medicine and Animal Science, University of São Paulo, São Paulo, BrazilSpecial Laboratory of Applied Toxinology, Butantan Institute, São Paulo, BrazilDepartment of Biochemistry and Immunology, School of Medicine of Ribeirao Preto, University of São Paulo, Ribeirao Preto, BrazilDepartment of Clinical Analysis, Toxicology and Food Science, School of Pharmaceutical Sciences of Ribeirao Preto, University of São Paulo, Ribeirao Preto, BrazilDepartment de Parasitology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilNational Institute of Science and Technology in Molecular Entomology, National Council of Scientific and Technological Development (INCT-EM/CNPq), Rio de Janeiro, BrazilDepartment of Clinical Analysis, Toxicology and Food Science, School of Pharmaceutical Sciences of Ribeirao Preto, University of São Paulo, Ribeirao Preto, BrazilDepartment of Immunology, Institute of Biomedical Sciences, University of São Paulo, São Paulo, BrazilNational Institute of Science and Technology in Molecular Entomology, National Council of Scientific and Technological Development (INCT-EM/CNPq), Rio de Janeiro, BrazilAmblyomma sculptum is an important vector of Rickettsia rickettsii, causative agent of Rocky Mountain spotted fever and the most lethal tick-borne pathogen affecting humans. To feed on the vertebrate host's blood, A. sculptum secretes a salivary mixture, which may interact with skin resident dendritic cells (DCs) and modulate their function. The present work was aimed at depicting the A. sculptum saliva-host DC network and the biochemical nature of the immunomodulatory component(s) involved in this interface. A. sculptum saliva inhibits the production of inflammatory cytokines by murine DCs stimulated with LPS. The fractionation of the low molecular weight salivary content by reversed-phase chromatography revealed active fractions eluting from 49 to 55% of the acetonitrile gradient. Previous studies suggested that this pattern of elution matches with that observed for prostaglandin E2 (PGE2) and the molecular identity of this lipid mediator was unambiguously confirmed by a new high-resolution mass spectrometry methodology. A productive infection of murine DCs by R. rickettsii was demonstrated for the first time leading to proinflammatory cytokine production that was inhibited by both A. sculptum saliva and PGE2, a result also achieved with human DCs. The adoptive transfer of murine DCs incubated with R. rickettsii followed by treatment with A. sculptum saliva or PGE2 did not change the cytokine profile associated to cellular recall responses while IgG2a-specific antibodies were decreased in the serum of these mice. Together, these findings emphasize the role of PGE2 as a universal immunomodulator of tick saliva. In addition, it contributes to new approaches to explore R. rickettsii-DC interactions both in vitro and in vivo.https://www.frontiersin.org/article/10.3389/fimmu.2019.00118/fullAmblyomma sculptumtick salivaPGE2dendritic cellsRickettsia rickettsiiimmunomodulation |
| spellingShingle | Eliane Esteves Bruna Bizzarro Francisco Borges Costa Alejandro Ramírez-Hernández Ana Paula Ferranti Peti Allan Henrique Depieri Cataneo Pryscilla Fanini Wowk Rodolfo Pessato Timóteo Marcelo Bahia Labruna Pedro Ismael Silva Junior Célio Lopes Silva Lúcia Helena Faccioli Andréa Cristina Fogaça Andréa Cristina Fogaça Carlos Arterio Sorgi Anderson Sá-Nunes Anderson Sá-Nunes Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo Frontiers in Immunology Amblyomma sculptum tick saliva PGE2 dendritic cells Rickettsia rickettsii immunomodulation |
| title | Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo |
| title_full | Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo |
| title_fullStr | Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo |
| title_full_unstemmed | Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo |
| title_short | Amblyomma sculptum Salivary PGE2 Modulates the Dendritic Cell-Rickettsia rickettsii Interactions in vitro and in vivo |
| title_sort | amblyomma sculptum salivary pge2 modulates the dendritic cell rickettsia rickettsii interactions in vitro and in vivo |
| topic | Amblyomma sculptum tick saliva PGE2 dendritic cells Rickettsia rickettsii immunomodulation |
| url | https://www.frontiersin.org/article/10.3389/fimmu.2019.00118/full |
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