The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase.
Aedes aegypti mosquitoes are the main vectors of arboviruses. The peritrophic matrix (PM) is an extracellular layer that surrounds the blood bolus. It acts as an immune barrier that prevents direct contact of bacteria with midgut epithelial cells during blood digestion. Here, we describe a heme-depe...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-02-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1011149 |
| _version_ | 1797848209515610112 |
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| author | Octavio A C Talyuli Jose Henrique M Oliveira Vanessa Bottino-Rojas Gilbert O Silveira Patricia H Alvarenga Ana Beatriz F Barletta Asher M Kantor Gabriela O Paiva-Silva Carolina Barillas-Mury Pedro L Oliveira |
| author_facet | Octavio A C Talyuli Jose Henrique M Oliveira Vanessa Bottino-Rojas Gilbert O Silveira Patricia H Alvarenga Ana Beatriz F Barletta Asher M Kantor Gabriela O Paiva-Silva Carolina Barillas-Mury Pedro L Oliveira |
| author_sort | Octavio A C Talyuli |
| collection | DOAJ |
| description | Aedes aegypti mosquitoes are the main vectors of arboviruses. The peritrophic matrix (PM) is an extracellular layer that surrounds the blood bolus. It acts as an immune barrier that prevents direct contact of bacteria with midgut epithelial cells during blood digestion. Here, we describe a heme-dependent peroxidase, hereafter referred to as heme peroxidase 1 (HPx1). HPx1 promotes PM assembly and antioxidant ability, modulating vector competence. Mechanistically, the heme presence in a blood meal induces HPx1 transcriptional activation mediated by the E75 transcription factor. HPx1 knockdown increases midgut reactive oxygen species (ROS) production by the DUOX NADPH oxidase. Elevated ROS levels reduce microbiota growth while enhancing epithelial mitosis, a response to tissue damage. However, simultaneous HPx1 and DUOX silencing was not able to rescue bacterial population growth, as explained by increased expression of antimicrobial peptides (AMPs), which occurred only after double knockdown. This result revealed hierarchical activation of ROS and AMPs to control microbiota. HPx1 knockdown produced a 100-fold decrease in Zika and dengue 2 midgut infection, demonstrating the essential role of the mosquito PM in the modulation of arbovirus vector competence. Our data show that the PM connects blood digestion to midgut immunological sensing of the microbiota and viral infections. |
| first_indexed | 2024-04-09T18:23:45Z |
| format | Article |
| id | doaj.art-e52e6055087042508fa2ad005c5dd9d3 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-04-09T18:23:45Z |
| publishDate | 2023-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-e52e6055087042508fa2ad005c5dd9d32023-04-12T05:31:34ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742023-02-01192e101114910.1371/journal.ppat.1011149The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase.Octavio A C TalyuliJose Henrique M OliveiraVanessa Bottino-RojasGilbert O SilveiraPatricia H AlvarengaAna Beatriz F BarlettaAsher M KantorGabriela O Paiva-SilvaCarolina Barillas-MuryPedro L OliveiraAedes aegypti mosquitoes are the main vectors of arboviruses. The peritrophic matrix (PM) is an extracellular layer that surrounds the blood bolus. It acts as an immune barrier that prevents direct contact of bacteria with midgut epithelial cells during blood digestion. Here, we describe a heme-dependent peroxidase, hereafter referred to as heme peroxidase 1 (HPx1). HPx1 promotes PM assembly and antioxidant ability, modulating vector competence. Mechanistically, the heme presence in a blood meal induces HPx1 transcriptional activation mediated by the E75 transcription factor. HPx1 knockdown increases midgut reactive oxygen species (ROS) production by the DUOX NADPH oxidase. Elevated ROS levels reduce microbiota growth while enhancing epithelial mitosis, a response to tissue damage. However, simultaneous HPx1 and DUOX silencing was not able to rescue bacterial population growth, as explained by increased expression of antimicrobial peptides (AMPs), which occurred only after double knockdown. This result revealed hierarchical activation of ROS and AMPs to control microbiota. HPx1 knockdown produced a 100-fold decrease in Zika and dengue 2 midgut infection, demonstrating the essential role of the mosquito PM in the modulation of arbovirus vector competence. Our data show that the PM connects blood digestion to midgut immunological sensing of the microbiota and viral infections.https://doi.org/10.1371/journal.ppat.1011149 |
| spellingShingle | Octavio A C Talyuli Jose Henrique M Oliveira Vanessa Bottino-Rojas Gilbert O Silveira Patricia H Alvarenga Ana Beatriz F Barletta Asher M Kantor Gabriela O Paiva-Silva Carolina Barillas-Mury Pedro L Oliveira The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. PLoS Pathogens |
| title | The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. |
| title_full | The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. |
| title_fullStr | The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. |
| title_full_unstemmed | The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. |
| title_short | The Aedes aegypti peritrophic matrix controls arbovirus vector competence through HPx1, a heme-induced peroxidase. |
| title_sort | aedes aegypti peritrophic matrix controls arbovirus vector competence through hpx1 a heme induced peroxidase |
| url | https://doi.org/10.1371/journal.ppat.1011149 |
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