Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment
Background: Leishmaniasis results in a wide spectrum of clinical manifestations, ranging from skin lesions at the site of infection to disseminated lesions in internal organs, such as the spleen and liver. While the ability of Leishmania-infected host cells to migrate may be important to lesion dist...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-07-01
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| Series: | Frontiers in Cell and Developmental Biology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcell.2023.1206049/full |
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| author | Yasmin Luz Amanda Rebouças Carla Polyana O. S. Bernardes Erik A. Rossi Taíse S. Machado Bruno S. F. Souza Bruno S. F. Souza Bruno S. F. Souza Claudia Ida Brodskyn Patricia S. T. Veras Washington L. C. dos Santos Juliana P. B. de Menezes |
| author_facet | Yasmin Luz Amanda Rebouças Carla Polyana O. S. Bernardes Erik A. Rossi Taíse S. Machado Bruno S. F. Souza Bruno S. F. Souza Bruno S. F. Souza Claudia Ida Brodskyn Patricia S. T. Veras Washington L. C. dos Santos Juliana P. B. de Menezes |
| author_sort | Yasmin Luz |
| collection | DOAJ |
| description | Background: Leishmaniasis results in a wide spectrum of clinical manifestations, ranging from skin lesions at the site of infection to disseminated lesions in internal organs, such as the spleen and liver. While the ability of Leishmania-infected host cells to migrate may be important to lesion distribution and parasite dissemination, the underlying mechanisms and the accompanying role of host cells remain poorly understood. Previously published work has shown that Leishmania infection inhibits macrophage migration in a 2-dimensional (2D) environment by altering actin dynamics and impairing the expression of proteins involved in plasma membrane-extracellular matrix interactions. Although it was shown that L. infantum induces the 2D migration of dendritic cells, in vivo cell migration primarily occurs in 3-dimensional (3D) environments. The present study aimed to investigate the migration of macrophages and dendritic cells infected by Leishmania using a 3-dimensional environment, as well as shed light on the mechanisms involved in this process.Methods: Following the infection of murine bone marrow-derived macrophages (BMDM), human macrophages and human dendritic cells by L. amazonensis, L. braziliensis, or L. infantum, cellular migration, the formation of adhesion complexes and actin polymerization were evaluated.Results: Our results indicate that Leishmania infection inhibited 3D migration in both BMDM and human macrophages. Reduced expression of proteins involved in adhesion complex formation and alterations in actin dynamics were also observed in Leishmania-infected macrophages. By contrast, increased human dendritic cell migration in a 3D environment was found to be associated with enhanced adhesion complex formation and increased actin dynamics.Conclusion: Taken together, our results show that Leishmania infection inhibits macrophage 3D migration, while enhancing dendritic 3D migration by altering actin dynamics and the expression of proteins involved in plasma membrane extracellular matrix interactions, suggesting a potential association between dendritic cells and disease visceralization. |
| first_indexed | 2024-03-12T21:22:24Z |
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| institution | Directory Open Access Journal |
| issn | 2296-634X |
| language | English |
| last_indexed | 2024-03-12T21:22:24Z |
| publishDate | 2023-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cell and Developmental Biology |
| spelling | doaj.art-0e13ba035b914301a8266e37a33510b82023-07-28T13:02:20ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2023-07-011110.3389/fcell.2023.12060491206049Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environmentYasmin Luz0Amanda Rebouças1Carla Polyana O. S. Bernardes2Erik A. Rossi3Taíse S. Machado4Bruno S. F. Souza5Bruno S. F. Souza6Bruno S. F. Souza7Claudia Ida Brodskyn8Patricia S. T. Veras9Washington L. C. dos Santos10Juliana P. B. de Menezes11Laboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilCenter for Biotechnology and Cell Therapy, São Rafael Hospital, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilCenter for Biotechnology and Cell Therapy, São Rafael Hospital, Salvador, BrazilD’Or Institute for Research and Education, Salvador, BrazilLaboratory of Tissue Engineering and Immunopharmacology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Structural and Molecular Pathology, Gonçalo Moniz Institute, Salvador, BrazilLaboratory of Host—Parasite Interaction and Epidemiology, Gonçalo Moniz Institute, Salvador, BrazilBackground: Leishmaniasis results in a wide spectrum of clinical manifestations, ranging from skin lesions at the site of infection to disseminated lesions in internal organs, such as the spleen and liver. While the ability of Leishmania-infected host cells to migrate may be important to lesion distribution and parasite dissemination, the underlying mechanisms and the accompanying role of host cells remain poorly understood. Previously published work has shown that Leishmania infection inhibits macrophage migration in a 2-dimensional (2D) environment by altering actin dynamics and impairing the expression of proteins involved in plasma membrane-extracellular matrix interactions. Although it was shown that L. infantum induces the 2D migration of dendritic cells, in vivo cell migration primarily occurs in 3-dimensional (3D) environments. The present study aimed to investigate the migration of macrophages and dendritic cells infected by Leishmania using a 3-dimensional environment, as well as shed light on the mechanisms involved in this process.Methods: Following the infection of murine bone marrow-derived macrophages (BMDM), human macrophages and human dendritic cells by L. amazonensis, L. braziliensis, or L. infantum, cellular migration, the formation of adhesion complexes and actin polymerization were evaluated.Results: Our results indicate that Leishmania infection inhibited 3D migration in both BMDM and human macrophages. Reduced expression of proteins involved in adhesion complex formation and alterations in actin dynamics were also observed in Leishmania-infected macrophages. By contrast, increased human dendritic cell migration in a 3D environment was found to be associated with enhanced adhesion complex formation and increased actin dynamics.Conclusion: Taken together, our results show that Leishmania infection inhibits macrophage 3D migration, while enhancing dendritic 3D migration by altering actin dynamics and the expression of proteins involved in plasma membrane extracellular matrix interactions, suggesting a potential association between dendritic cells and disease visceralization.https://www.frontiersin.org/articles/10.3389/fcell.2023.1206049/fullmacrophagesdendritic cells3D migrationLeishmaniadissemination |
| spellingShingle | Yasmin Luz Amanda Rebouças Carla Polyana O. S. Bernardes Erik A. Rossi Taíse S. Machado Bruno S. F. Souza Bruno S. F. Souza Bruno S. F. Souza Claudia Ida Brodskyn Patricia S. T. Veras Washington L. C. dos Santos Juliana P. B. de Menezes Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment Frontiers in Cell and Developmental Biology macrophages dendritic cells 3D migration Leishmania dissemination |
| title | Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment |
| title_full | Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment |
| title_fullStr | Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment |
| title_full_unstemmed | Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment |
| title_short | Leishmania infection alters macrophage and dendritic cell migration in a three-dimensional environment |
| title_sort | leishmania infection alters macrophage and dendritic cell migration in a three dimensional environment |
| topic | macrophages dendritic cells 3D migration Leishmania dissemination |
| url | https://www.frontiersin.org/articles/10.3389/fcell.2023.1206049/full |
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