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

Simple item page
dc.contributor.authorColes, Taylor A.en
dc.contributor.authorBriggs, Anna M.en
dc.contributor.authorHambly, Malayna G.en
dc.contributor.authorCespedes, Noraen
dc.contributor.authorFellows, Abigail M.en
dc.contributor.authorKaylor, Hannah L.en
dc.contributor.authorAdams, Alexandria D.en
dc.contributor.authorVan Susteren, Graceen
dc.contributor.authorBentil, Ronald E.en
dc.contributor.authorRobert, Michael A.en
dc.contributor.authorRiffell, Jeffrey A.en
dc.contributor.authorLewis, Edwin E.en
dc.contributor.authorLuckhart, Shirleyen
dc.date.accessioned2024-02-13T19:53:17Zen
dc.date.available2024-02-13T19:53:17Zen
dc.date.issued2023-07-24en
dc.description.abstractBlood 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.en
dc.description.versionPublished versionen
dc.format.extent16 page(s)en
dc.format.mimetypeapplication/pdfen
dc.identifierARTN 1247316 (Article number)en
dc.identifier.doihttps://doi.org/10.3389/fphys.2023.1247316en
dc.identifier.eissn1664-042Xen
dc.identifier.issn1664-042Xen
dc.identifier.orcidRobert, Michael [0000-0003-3705-0952]en
dc.identifier.otherPMC10405175en
dc.identifier.other1247316 (PII)en
dc.identifier.pmid37555020en
dc.identifier.urihttps://hdl.handle.net/10919/117988en
dc.identifier.volume14en
dc.language.isoenen
dc.publisherFrontiersen
dc.relation.urihttps://www.ncbi.nlm.nih.gov/pubmed/37555020en
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjecthistamineen
dc.subjectserotoninen
dc.subjectAnopheles stephensien
dc.subjectflight behavioren
dc.subjectfeeding behavioren
dc.subjectlifespanen
dc.subjectPlasmodium yoeliien
dc.subjectmalariaen
dc.titleIngested histamine and serotonin interact to alter <i>Anopheles stephensi</i> feeding and flight behavior and infection with <i>Plasmodium</i> parasitesen
dc.title.serialFrontiers in Physiologyen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.otherArticleen
dc.type.otherJournalen
dcterms.dateAccepted2023-07-17en
pubs.organisational-group/Virginia Techen
pubs.organisational-group/Virginia Tech/Scienceen
pubs.organisational-group/Virginia Tech/Science/Mathematicsen
pubs.organisational-group/Virginia Tech/All T&R Facultyen
pubs.organisational-group/Virginia Tech/Science/COS T&R Facultyen

Files

Original bundle
Now showing 1 - 1 of 1
Thumbnail Image
Name:
Ingested histamine and serotonin interact to alter iAnopheles stephensii feeding and flight behavior and infection with iPla.pdf
Size:
2.68 MB
Format:
Adobe Portable Document Format
Description:
Published version
Download
License bundle
Now showing 1 - 1 of 1
Name:
license.txt
Size:
1.5 KB
Format:
Plain Text
Description:
Download

Collections

All Faculty Deposits
Scholarly Works, Center for Emerging, Zoonotic, and Arthropod-borne Pathogens (CeZAP)
Scholarly Works, Mathematics