Cargando…

Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites

Blood levels of histamine and serotonin (5-HT) are altered in human malaria, and, at these levels, we have shown they have broad, independent effects on Anopheles stephensi following ingestion by this invasive mosquito. Given that histamine and 5-HT are ingested together under natural conditions and...

Descripción completa

Detalles Bibliográficos
Autores principales: Coles, Taylor A., Briggs, Anna M., Hambly, Malayna G., Céspedes, Nora, Fellows, Abigail M., Kaylor, Hannah L., Adams, Alexandria D., Van Susteren, Grace, Bentil, Ronald E., Robert, Michael A., Riffell, Jeffrey A., Lewis, Edwin E., Luckhart, Shirley
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405175/
https://www.ncbi.nlm.nih.gov/pubmed/37555020
http://dx.doi.org/10.3389/fphys.2023.1247316
_version_ 1785085466509312000
author Coles, Taylor A.
Briggs, Anna M.
Hambly, Malayna G.
Céspedes, Nora
Fellows, Abigail M.
Kaylor, Hannah L.
Adams, Alexandria D.
Van Susteren, Grace
Bentil, Ronald E.
Robert, Michael A.
Riffell, Jeffrey A.
Lewis, Edwin E.
Luckhart, Shirley
author_facet Coles, Taylor A.
Briggs, Anna M.
Hambly, Malayna G.
Céspedes, Nora
Fellows, Abigail M.
Kaylor, Hannah L.
Adams, Alexandria D.
Van Susteren, Grace
Bentil, Ronald E.
Robert, Michael A.
Riffell, Jeffrey A.
Lewis, Edwin E.
Luckhart, Shirley
author_sort Coles, Taylor A.
collection PubMed
description Blood levels of histamine and serotonin (5-HT) are altered in human malaria, and, at these levels, we have shown they have broad, independent effects on Anopheles stephensi following ingestion by this invasive mosquito. Given that histamine and 5-HT are ingested together under natural conditions and that histaminergic and serotonergic signaling are networked in other organisms, we examined effects of combinations of these biogenic amines provisioned to A. stephensi at healthy human levels (high 5-HT, low histamine) or levels associated with severe malaria (low 5-HT, high histamine). Treatments were delivered in water (priming) before feeding A. stephensi on Plasmodium yoelii-infected mice or via artificial blood meal. Relative to effects of histamine and 5-HT alone, effects of biogenic amine combinations were complex. Biogenic amine treatments had the greatest impact on the first oviposition cycle, with high histamine moderating low 5-HT effects in combination. In contrast, clutch sizes were similar across combination and individual treatments. While high histamine alone increased uninfected A. stephensi weekly lifetime blood feeding, neither combination altered this tendency relative to controls. The tendency to re-feed 2 weeks after the first blood meal was altered by combination treatments, but this depended on mode of delivery. For blood delivery, malaria-associated treatments yielded higher percentages of fed females relative to healthy-associated treatments, but the converse was true for priming. Female mosquitoes treated with the malaria-associated combination exhibited enhanced flight behavior and object inspection relative to controls and healthy combination treatment. Mosquitoes primed with the malaria-associated combination exhibited higher mean oocysts and sporozoite infection prevalence relative to the healthy combination, with high histamine having a dominant effect on these patterns. Compared with uninfected A. stephensi, the tendency of infected mosquitoes to take a second blood meal revealed an interaction of biogenic amines with infection. We used a mathematical model to project the impacts of different levels of biogenic amines and associated changes on outbreaks in human populations. While not all outbreak parameters were impacted the same, the sum of effects suggests that histamine and 5-HT alter the likelihood of transmission by mosquitoes that feed on hosts with symptomatic malaria versus a healthy host.
format Online
Article
Text
id pubmed-10405175
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-104051752023-08-08 Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites Coles, Taylor A. Briggs, Anna M. Hambly, Malayna G. Céspedes, Nora Fellows, Abigail M. Kaylor, Hannah L. Adams, Alexandria D. Van Susteren, Grace Bentil, Ronald E. Robert, Michael A. Riffell, Jeffrey A. Lewis, Edwin E. Luckhart, Shirley Front Physiol Physiology Blood levels of histamine and serotonin (5-HT) are altered in human malaria, and, at these levels, we have shown they have broad, independent effects on Anopheles stephensi following ingestion by this invasive mosquito. Given that histamine and 5-HT are ingested together under natural conditions and that histaminergic and serotonergic signaling are networked in other organisms, we examined effects of combinations of these biogenic amines provisioned to A. stephensi at healthy human levels (high 5-HT, low histamine) or levels associated with severe malaria (low 5-HT, high histamine). Treatments were delivered in water (priming) before feeding A. stephensi on Plasmodium yoelii-infected mice or via artificial blood meal. Relative to effects of histamine and 5-HT alone, effects of biogenic amine combinations were complex. Biogenic amine treatments had the greatest impact on the first oviposition cycle, with high histamine moderating low 5-HT effects in combination. In contrast, clutch sizes were similar across combination and individual treatments. While high histamine alone increased uninfected A. stephensi weekly lifetime blood feeding, neither combination altered this tendency relative to controls. The tendency to re-feed 2 weeks after the first blood meal was altered by combination treatments, but this depended on mode of delivery. For blood delivery, malaria-associated treatments yielded higher percentages of fed females relative to healthy-associated treatments, but the converse was true for priming. Female mosquitoes treated with the malaria-associated combination exhibited enhanced flight behavior and object inspection relative to controls and healthy combination treatment. Mosquitoes primed with the malaria-associated combination exhibited higher mean oocysts and sporozoite infection prevalence relative to the healthy combination, with high histamine having a dominant effect on these patterns. Compared with uninfected A. stephensi, the tendency of infected mosquitoes to take a second blood meal revealed an interaction of biogenic amines with infection. We used a mathematical model to project the impacts of different levels of biogenic amines and associated changes on outbreaks in human populations. While not all outbreak parameters were impacted the same, the sum of effects suggests that histamine and 5-HT alter the likelihood of transmission by mosquitoes that feed on hosts with symptomatic malaria versus a healthy host. Frontiers Media S.A. 2023-07-24 /pmc/articles/PMC10405175/ /pubmed/37555020 http://dx.doi.org/10.3389/fphys.2023.1247316 Text en Copyright © 2023 Coles, Briggs, Hambly, Céspedes, Fellows, Kaylor, Adams, Van Susteren, Bentil, Robert, Riffell, Lewis and Luckhart. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Coles, Taylor A.
Briggs, Anna M.
Hambly, Malayna G.
Céspedes, Nora
Fellows, Abigail M.
Kaylor, Hannah L.
Adams, Alexandria D.
Van Susteren, Grace
Bentil, Ronald E.
Robert, Michael A.
Riffell, Jeffrey A.
Lewis, Edwin E.
Luckhart, Shirley
Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title_full Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title_fullStr Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title_full_unstemmed Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title_short Ingested histamine and serotonin interact to alter Anopheles stephensi feeding and flight behavior and infection with Plasmodium parasites
title_sort ingested histamine and serotonin interact to alter anopheles stephensi feeding and flight behavior and infection with plasmodium parasites
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10405175/
https://www.ncbi.nlm.nih.gov/pubmed/37555020
http://dx.doi.org/10.3389/fphys.2023.1247316
work_keys_str_mv AT colestaylora ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT briggsannam ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT hamblymalaynag ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT cespedesnora ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT fellowsabigailm ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT kaylorhannahl ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT adamsalexandriad ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT vansusterengrace ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT bentilronalde ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT robertmichaela ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT riffelljeffreya ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT lewisedwine ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites
AT luckhartshirley ingestedhistamineandserotonininteracttoalteranophelesstephensifeedingandflightbehaviorandinfectionwithplasmodiumparasites