Feeding, Flight Behavior, and Infection With Malaria Parasites Are Altered by Ingestion of Serotonin

Overview

Journal Front Physiol

Date 2022 Jun 24

PMID 35747317

Authors

Anna M Briggs

Malayna G Hambly

Raquel M Simao-Gurge

Sarah M Garrison

Zainab Khaku

Grace Van Susteren

Edwin E Lewis

Jeffrey A Riffell

Shirley Luckhart

Affiliations

Soon will be listed here.

Abstract

Approximately 3.4 billion people are at risk of malaria, a disease caused by infection with spp. parasites, which are transmitted by mosquitoes. Individuals with severe falciparum malaria often exhibit changes in circulating blood levels of biogenic amines, including reduced serotonin or 5-hydroxytryptamine (5-HT), and these changes are associated with disease pathology. In insects, 5-HT functions as an important neurotransmitter for many behaviors and biological functions. In , we show that 5-HT is localized to innervation in the head, thorax, and midgut, suggesting a gut-to-brain signaling axis that could support the effects of ingested 5-HT on mosquito biology and behavioral responses. Given the changes in blood levels of 5-HT associated with severe malaria and the key roles that 5-HT plays in insect neurophysiology, we investigated the impact of ingesting blood with healthy levels of 5-HT (1.5 µM) or malaria-associated levels of 5-HT (0.15 µM) on various aspects of biology. In these studies, we provisioned 5-HT and monitored fecundity, lifespan, flight behavior, and blood feeding of We also assessed the impact of 5-HT ingestion on infection of with the mouse malaria parasite 17XNL and the human malaria parasite . Our data show that ingestion of 5-HT associated with severe malaria increased mosquito flight velocity and investigation of visual objects in response to host odor (CO). 5-HT ingestion in blood at levels associated with severe malaria also increased the tendency to take a second blood meal 4 days later in uninfected . In mosquitoes infected with 17XNL, feeding tendency was decreased when midgut oocysts were present but increased when sporozoites were present. In addition to these effects, treatment of with 5-HT associated with severe malaria increased infection success with 17XNL compared to control, while treatment with healthy levels of 5-HT decreased infection success with These changes in mosquito behavior and infection success could be used as a basis to manipulate 5-HT signaling in vector mosquitoes for improved control of malaria parasite transmission.

Citing Articles

Hormones in malaria infection: influence on disease severity, host physiology, and therapeutic opportunities.

Das A, Suar M, Reddy K Biosci Rep. 2024; 44(11).

PMID: 39492784 PMC: 11581842. DOI: 10.1042/BSR20240482.

Dietary L-3,4-dihydroxyphenylalanine (L-DOPA) augments cuticular melanization in mosquitos while reducing their lifespan and malaria parasite burden.

Camacho E, Dong Y, Chrissian C, Cordero R, Saravia R, Anglero-Rodriguez Y Res Sq. 2024; .

PMID: 39483913 PMC: 11527263. DOI: 10.21203/rs.3.rs-5167892/v1.

Host 5-HT affects Plasmodium transmission in mosquitoes via modulating mosquito mitochondrial homeostasis.

Gao L, Zhang B, Feng Y, Yang W, Zhang S, Wang J PLoS Pathog. 2024; 20(10):e1012638.

PMID: 39405338 PMC: 11508672. DOI: 10.1371/journal.ppat.1012638.

Feeding Behavior and Detection in , a Malaria Vector in District Khyber, Khyber Pakhtunkhwa, Pakistan.

Arif M, Rasheed S, Ullah H, Shah T, Rehman F, Dawoud T Iran J Parasitol. 2024; 19(3):333-340.

PMID: 39318824 PMC: 11417983. DOI: 10.18502/ijpa.v19i3.16393.

The complexities of blood-feeding patterns in mosquitoes and sandflies and the burden of disease: A minireview.

Bursali F, Touray M Vet Med Sci. 2024; 10(5):e1580.

PMID: 39171609 PMC: 11339650. DOI: 10.1002/vms3.1580.

References

Sinka M, Pironon S, Massey N, Longbottom J, Hemingway J, Moyes C . A new malaria vector in Africa: Predicting the expansion range of and identifying the urban populations at risk. Proc Natl Acad Sci U S A. 2020; 117(40):24900-24908. PMC: 7547157. DOI: 10.1073/pnas.2003976117. View

Pakpour N, Riehle M, Luckhart S . Effects of ingested vertebrate-derived factors on insect immune responses. Curr Opin Insect Sci. 2014; 3:1-5. PMC: 4228800. DOI: 10.1016/j.cois.2014.07.001. View

Winn S, Scherer T, Thony B, Ying M, Martinez A, Weber S . Blood phenylalanine reduction corrects CNS dopamine and serotonin deficiencies and partially improves behavioral performance in adult phenylketonuric mice. Mol Genet Metab. 2018; 123(1):6-20. PMC: 5786171. DOI: 10.1016/j.ymgme.2017.10.009. View

Loo Y . Serotonin deficiency in experimental hyperphenylalaninemia. J Neurochem. 1974; 23(1):139-47. DOI: 10.1111/j.1471-4159.1974.tb06928.x. View

ODonnell A, Rund S, Reece S . Time-of-day of blood-feeding: effects on mosquito life history and malaria transmission. Parasit Vectors. 2019; 12(1):301. PMC: 6604169. DOI: 10.1186/s13071-019-3513-9. View

Chapman P, Burkland R, Bradley S, Houot B, Bullman V, Dacks A . Flight motor networks modulate primary olfactory processing in the moth . Proc Natl Acad Sci U S A. 2018; 115(21):5588-5593. PMC: 6003457. DOI: 10.1073/pnas.1722379115. View

Huser A, Eschment M, Gullu N, Collins K, Bopple K, Pankevych L . Anatomy and behavioral function of serotonin receptors in Drosophila melanogaster larvae. PLoS One. 2017; 12(8):e0181865. PMC: 5544185. DOI: 10.1371/journal.pone.0181865. View

Howard C, Chen C, Tabachnik T, Hormigo R, Ramdya P, Mann R . Serotonergic Modulation of Walking in Drosophila. Curr Biol. 2019; 29(24):4218-4230.e8. PMC: 6935052. DOI: 10.1016/j.cub.2019.10.042. View

Mukherjee S . Novel perspectives on the molecular crosstalk mechanisms of serotonin and melatonin in plants. Plant Physiol Biochem. 2018; 132:33-45. DOI: 10.1016/j.plaphy.2018.08.031. View

10.

Thomas J, Saleh E, Alammar N, Akroush A . The indole alkaloid tryptamine impairs reproduction in Drosophila melanogaster. J Econ Entomol. 1998; 91(4):841-6. DOI: 10.1093/jee/91.4.841. View

11.

Sze J, Victor M, Loer C, Shi Y, Ruvkun G . Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature. 2000; 403(6769):560-4. DOI: 10.1038/35000609. View

12.

Pakpour N, Akman-Anderson L, Vodovotz Y, Luckhart S . The effects of ingested mammalian blood factors on vector arthropod immunity and physiology. Microbes Infect. 2013; 15(3):243-54. PMC: 3602389. DOI: 10.1016/j.micinf.2013.01.003. View

13.

Pietri J, Pakpour N, Napoli E, Song G, Pietri E, Potts R . Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism. Biochem J. 2016; 473(20):3487-3503. PMC: 5508860. DOI: 10.1042/BCJ20160271. View

14.

Bradley S, Chapman P, Lizbinski K, Daly K, Dacks A . A Flight Sensory-Motor to Olfactory Processing Circuit in the Moth Manduca sexta. Front Neural Circuits. 2016; 10:5. PMC: 4754697. DOI: 10.3389/fncir.2016.00005. View

15.

Murakami H, Murakami S . Serotonin receptors antagonistically modulate Caenorhabditis elegans longevity. Aging Cell. 2007; 6(4):483-8. DOI: 10.1111/j.1474-9726.2007.00303.x. View

16.

Suzuki Y, Schenk J, Tan H, Gaudry Q . A Population of Interneurons Signals Changes in the Basal Concentration of Serotonin and Mediates Gain Control in the Drosophila Antennal Lobe. Curr Biol. 2020; 30(6):1110-1118.e4. PMC: 7133499. DOI: 10.1016/j.cub.2020.01.018. View

17.

Murotani T, Ishizuka T, Isogawa Y, Karashima M, Yamatodani A . Possible involvement of serotonin 5-HT2 receptor in the regulation of feeding behavior through the histaminergic system. Neuropharmacology. 2011; 61(1-2):228-33. DOI: 10.1016/j.neuropharm.2011.04.003. View

18.

Dobbie M, Crawley J, Waruiru C, Marsh K, Surtees R . Cerebrospinal fluid studies in children with cerebral malaria: an excitotoxic mechanism?. Am J Trop Med Hyg. 2000; 62(2):284-90. DOI: 10.4269/ajtmh.2000.62.284. View

19.

Alonso San Alberto D, Rusch C, Zhan Y, Straw A, Montell C, Riffell J . The olfactory gating of visual preferences to human skin and visible spectra in mosquitoes. Nat Commun. 2022; 13(1):555. PMC: 8816903. DOI: 10.1038/s41467-022-28195-x. View

20.

Ro J, Pak G, Malec P, Lyu Y, Allison D, Kennedy R . Serotonin signaling mediates protein valuation and aging. Elife. 2016; 5. PMC: 5005037. DOI: 10.7554/eLife.16843. View