Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection
During bloodfeeding, the presence of sand fly saliva in the hemorrhagic pool where Leishmania is also inoculated modulates the development of host immune mechanisms creating a favorable environment for disease progression. To date, information obtained through experimental models suggests that sand...
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Frontiers Media S.A.
2018-05-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00881/full |
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| author | Clarissa R. Teixeira Claire da S. Santos Deboraci B. Prates Deboraci B. Prates Rafael T. dos Santos Théo Araújo-Santos Sebastião M. de Souza-Neto Valéria M. Borges Manoel Barral-Netto Manoel Barral-Netto Manoel Barral-Netto Cláudia I. Brodskyn Cláudia I. Brodskyn Cláudia I. Brodskyn |
| author_facet | Clarissa R. Teixeira Claire da S. Santos Deboraci B. Prates Deboraci B. Prates Rafael T. dos Santos Théo Araújo-Santos Sebastião M. de Souza-Neto Valéria M. Borges Manoel Barral-Netto Manoel Barral-Netto Manoel Barral-Netto Cláudia I. Brodskyn Cláudia I. Brodskyn Cláudia I. Brodskyn |
| author_sort | Clarissa R. Teixeira |
| collection | DOAJ |
| description | During bloodfeeding, the presence of sand fly saliva in the hemorrhagic pool where Leishmania is also inoculated modulates the development of host immune mechanisms creating a favorable environment for disease progression. To date, information obtained through experimental models suggests that sand fly saliva induces cellular recruitment and modulates production of eicosanoids. However, the effect of sand fly saliva in the different steps of the inflammatory response triggered by Leishmania remains undefined. Here we further investigate if interaction of Lutzomyia longipalpis salivary gland sonicate (SGS) with different host cells present during the initial inflammatory events regulate Leishmania infantum infectivity. Initially, we observed that incubation of human peripheral blood mononuclear cells (PBMC) with Lu. longipalpis SGS in the presence of L. infantum significantly increased IL-10 but did not alter expression of IFN-γ and TNF-α by CD4+ T cells induced by the parasite alone. Interestingly, incubation of PBMC with Lu. longipalpis SGS alone or in the presence of L. infantum resulted in increased IL-17 production. The presence of IL-17 is related to neutrophil recruitment and plays an important role at the site of infection. Here, we also observed increased migration of neutrophil using an in vitro chemotactic assay following incubation with supernatants from PBMC stimulated with L. infantum and Lu. longipalpis SGS. Neutrophil migration was abrogated following neutralization of IL-17 with specific antibodies. Moreover, culture of human neutrophils with L. infantum in the presence of Lu. longipalpis SGS promoted neutrophil apoptosis resulting in increased parasite viability. Neutrophils operate as the first line of defense in the early stages of infection and later interact with different cells, such as macrophages. The crosstalk between neutrophils and macrophages is critical to determine the type of specific immune response that will develop. Here, we observed that co-culture of human macrophages with autologous neutrophils previously infected in the presence of Lu. longipalpis SGS resulted in a higher infection rate, accompanied by increased production of TGF-β and PGE2. Our results provide new insight into the contribution of Lu. longipalpis SGS to L. infantum-induced regulation of important inflammatory events, creating a favorable environment for parasite survival inside different host cells. |
| first_indexed | 2024-04-12T13:39:12Z |
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| last_indexed | 2024-04-12T13:39:12Z |
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| spelling | doaj.art-8d7f973e9df14c62be961033c8fffa632022-12-22T03:30:54ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2018-05-01910.3389/fmicb.2018.00881379623Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum InfectionClarissa R. Teixeira0Claire da S. Santos1Deboraci B. Prates2Deboraci B. Prates3Rafael T. dos Santos4Théo Araújo-Santos5Sebastião M. de Souza-Neto6Valéria M. Borges7Manoel Barral-Netto8Manoel Barral-Netto9Manoel Barral-Netto10Cláudia I. Brodskyn11Cláudia I. Brodskyn12Cláudia I. Brodskyn13Fundação Oswaldo Cruz, Teresina, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilInstituto de Ciências da Saúde da Universidade Federal da Bahia, Departamentos de Biomorfologia e Biointeração, Salvador, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilCentro de Ciências Biológicas e Saúde, Universidade Federal do Oeste da Bahia, Barreiras, BrazilFaculdade de Ciências da Saúde, Universidade Federal da Grande Dourados, Dourados, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilFaculdade de Medicina da Universidade Federal da Bahia, Departamento de Patologia e Medicina Legal, Salvador, BrazilInstituto de Investigação em Imunologia, iii-INCT, São Paulo, BrazilInstituto Gonçalo Moniz, Fundação Oswaldo Cruz, Salvador, BrazilInstituto de Ciências da Saúde da Universidade Federal da Bahia, Departamentos de Biomorfologia e Biointeração, Salvador, BrazilInstituto de Investigação em Imunologia, iii-INCT, São Paulo, BrazilDuring bloodfeeding, the presence of sand fly saliva in the hemorrhagic pool where Leishmania is also inoculated modulates the development of host immune mechanisms creating a favorable environment for disease progression. To date, information obtained through experimental models suggests that sand fly saliva induces cellular recruitment and modulates production of eicosanoids. However, the effect of sand fly saliva in the different steps of the inflammatory response triggered by Leishmania remains undefined. Here we further investigate if interaction of Lutzomyia longipalpis salivary gland sonicate (SGS) with different host cells present during the initial inflammatory events regulate Leishmania infantum infectivity. Initially, we observed that incubation of human peripheral blood mononuclear cells (PBMC) with Lu. longipalpis SGS in the presence of L. infantum significantly increased IL-10 but did not alter expression of IFN-γ and TNF-α by CD4+ T cells induced by the parasite alone. Interestingly, incubation of PBMC with Lu. longipalpis SGS alone or in the presence of L. infantum resulted in increased IL-17 production. The presence of IL-17 is related to neutrophil recruitment and plays an important role at the site of infection. Here, we also observed increased migration of neutrophil using an in vitro chemotactic assay following incubation with supernatants from PBMC stimulated with L. infantum and Lu. longipalpis SGS. Neutrophil migration was abrogated following neutralization of IL-17 with specific antibodies. Moreover, culture of human neutrophils with L. infantum in the presence of Lu. longipalpis SGS promoted neutrophil apoptosis resulting in increased parasite viability. Neutrophils operate as the first line of defense in the early stages of infection and later interact with different cells, such as macrophages. The crosstalk between neutrophils and macrophages is critical to determine the type of specific immune response that will develop. Here, we observed that co-culture of human macrophages with autologous neutrophils previously infected in the presence of Lu. longipalpis SGS resulted in a higher infection rate, accompanied by increased production of TGF-β and PGE2. Our results provide new insight into the contribution of Lu. longipalpis SGS to L. infantum-induced regulation of important inflammatory events, creating a favorable environment for parasite survival inside different host cells.http://journal.frontiersin.org/article/10.3389/fmicb.2018.00881/fullLutzomyia longipalpissand fly salivaLeishmania infantumIL-17neutrophilsmacrophages |
| spellingShingle | Clarissa R. Teixeira Claire da S. Santos Deboraci B. Prates Deboraci B. Prates Rafael T. dos Santos Théo Araújo-Santos Sebastião M. de Souza-Neto Valéria M. Borges Manoel Barral-Netto Manoel Barral-Netto Manoel Barral-Netto Cláudia I. Brodskyn Cláudia I. Brodskyn Cláudia I. Brodskyn Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection Frontiers in Microbiology Lutzomyia longipalpis sand fly saliva Leishmania infantum IL-17 neutrophils macrophages |
| title | Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection |
| title_full | Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection |
| title_fullStr | Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection |
| title_full_unstemmed | Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection |
| title_short | Lutzomyia longipalpis Saliva Drives Interleukin-17-Induced Neutrophil Recruitment Favoring Leishmania infantum Infection |
| title_sort | lutzomyia longipalpis saliva drives interleukin 17 induced neutrophil recruitment favoring leishmania infantum infection |
| topic | Lutzomyia longipalpis sand fly saliva Leishmania infantum IL-17 neutrophils macrophages |
| url | http://journal.frontiersin.org/article/10.3389/fmicb.2018.00881/full |
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