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

Frontiers in Physiology

Physiology

Jeffrey A. Riffell¹  Grace Van Susteren¹  Hannah L. Kaylor²  Edwin E. Lewis²  Nora Céspedes²  Alexandria D. Adams²  Ronald E. Bentil²  Anna M. Briggs²  Taylor A. Coles²  Malayna G. Hambly²  Abigail M. Fellows²  Shirley Luckhart³  Michael A. Robert⁴ 

[1] Department of Biology, University of Washington, Seattle, WA, United States;Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Moscow, ID, United States;Department of Entomology, Plant Pathology, and Nematology, University of Idaho, Moscow, ID, United States;Department of Biological Sciences, University of Idaho, Moscow, ID, United States;Department of Mathematics, Center for Emerging, Zoonotic, and Arthropod-Borne Pathogens (CeZAP), Virginia Tech, Blacksburg, VA, United States;

关键词: histamine;    serotonin;    Anopheles stephensi;    flight behavior;    feeding behavior;    lifespan;    Plasmodium yoelii;    malaria;   

DOI  :  10.3389/fphys.2023.1247316

 received in 2023-06-25, accepted in 2023-07-17,  发布年份 2023

来源: Frontiers

【 摘 要 】

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.

【 授权许可】

Unknown   
Copyright © 2023 Coles, Briggs, Hambly, Céspedes, Fellows, Kaylor, Adams, Van Susteren, Bentil, Robert, Riffell, Lewis and Luckhart.