The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes
The immune and circulatory systems of animals are functionally integrated. In mammals, the spleen and lymph nodes filter and destroy microbes circulating in the blood and lymph, respectively. In insects, immune cells that surround the heart valves (ostia), called periostial haemocytes, destroy patho...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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The Royal Society
2022-09-01
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| Series: | Open Biology |
| Subjects: | |
| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.220111 |
| _version_ | 1797840297944678400 |
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| author | Yan Yan Leah T. Sigle David C. Rinker Tania Y. Estévez-Lao John A. Capra Julián F. Hillyer |
| author_facet | Yan Yan Leah T. Sigle David C. Rinker Tania Y. Estévez-Lao John A. Capra Julián F. Hillyer |
| author_sort | Yan Yan |
| collection | DOAJ |
| description | The immune and circulatory systems of animals are functionally integrated. In mammals, the spleen and lymph nodes filter and destroy microbes circulating in the blood and lymph, respectively. In insects, immune cells that surround the heart valves (ostia), called periostial haemocytes, destroy pathogens in the areas of the body that experience the swiftest haemolymph (blood) flow. An infection recruits additional periostial haemocytes, amplifying heart-associated immune responses. Although the structural mechanics of periostial haemocyte aggregation have been defined, the genetic factors that regulate this process remain less understood. Here, we conducted RNA sequencing in the African malaria mosquito, Anopheles gambiae, and discovered that an infection upregulates multiple components of the immune deficiency (IMD) and c-Jun N-terminal kinase (JNK) pathways in the heart with periostial haemocytes. This upregulation is greater in the heart with periostial haemocytes than in the circulating haemocytes or the entire abdomen. RNA interference-based knockdown then showed that the IMD and JNK pathways drive periostial haemocyte aggregation and alter phagocytosis and melanization on the heart, thereby demonstrating that these pathways regulate the functional integration between the immune and circulatory systems. Understanding how insects fight infection lays the foundation for novel strategies that could protect beneficial insects and harm detrimental ones. |
| first_indexed | 2024-04-09T16:12:40Z |
| format | Article |
| id | doaj.art-b96bac3478e84ecab7ca82a3ac8016eb |
| institution | Directory Open Access Journal |
| issn | 2046-2441 |
| language | English |
| last_indexed | 2024-04-09T16:12:40Z |
| publishDate | 2022-09-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj.art-b96bac3478e84ecab7ca82a3ac8016eb2023-04-24T09:14:29ZengThe Royal SocietyOpen Biology2046-24412022-09-0112910.1098/rsob.220111The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoesYan Yan0Leah T. Sigle1David C. Rinker2Tania Y. Estévez-Lao3John A. Capra4Julián F. Hillyer5Department of Biological Sciences, Vanderbilt University, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University, Nashville, TN, USADepartment of Biological Sciences, Vanderbilt University, Nashville, TN, USAThe immune and circulatory systems of animals are functionally integrated. In mammals, the spleen and lymph nodes filter and destroy microbes circulating in the blood and lymph, respectively. In insects, immune cells that surround the heart valves (ostia), called periostial haemocytes, destroy pathogens in the areas of the body that experience the swiftest haemolymph (blood) flow. An infection recruits additional periostial haemocytes, amplifying heart-associated immune responses. Although the structural mechanics of periostial haemocyte aggregation have been defined, the genetic factors that regulate this process remain less understood. Here, we conducted RNA sequencing in the African malaria mosquito, Anopheles gambiae, and discovered that an infection upregulates multiple components of the immune deficiency (IMD) and c-Jun N-terminal kinase (JNK) pathways in the heart with periostial haemocytes. This upregulation is greater in the heart with periostial haemocytes than in the circulating haemocytes or the entire abdomen. RNA interference-based knockdown then showed that the IMD and JNK pathways drive periostial haemocyte aggregation and alter phagocytosis and melanization on the heart, thereby demonstrating that these pathways regulate the functional integration between the immune and circulatory systems. Understanding how insects fight infection lays the foundation for novel strategies that could protect beneficial insects and harm detrimental ones.https://royalsocietypublishing.org/doi/10.1098/rsob.220111haemocytesheartinsectmelanizationphagocytosis |
| spellingShingle | Yan Yan Leah T. Sigle David C. Rinker Tania Y. Estévez-Lao John A. Capra Julián F. Hillyer The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes Open Biology haemocytes heart insect melanization phagocytosis |
| title | The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| title_full | The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| title_fullStr | The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| title_full_unstemmed | The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| title_short | The immune deficiency and c-Jun N-terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| title_sort | immune deficiency and c jun n terminal kinase pathways drive the functional integration of the immune and circulatory systems of mosquitoes |
| topic | haemocytes heart insect melanization phagocytosis |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.220111 |
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