Malaria load affects the activity of mosquito salivary apyrase

Thiévent, Kevin; Zilio, Giacomo; Hauser, Gaël; Koella, Jacob C.

doi:10.1016/j.jinsphys.2019.04.003

Cited by 21 publications

(8 citation statements)

References 39 publications

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“…We interpret, cellular disruption and altered expression of salivary proteins caused by HPX12 dysregulation, may have a direct influence on mosquito's salivary-chemosensory derived hostseeking abilities, affecting the blood meal acquisition process. These observations further corroborate and support the idea that the down-regulation of salivary apyrase is crucial to enhances host attraction of the Plasmodium-infected than un-infected mosquitoes (46). Recently, hemeperoxidase homolog HPX15, has been suggested to act as an agonist and likely favor the survival of endogenous gut-bacterial population as well as Plasmodium parasite, by the formation of crosslinked mucin barrier on the luminal side of the midgut (40).…”

Section: Discussionsupporting

confidence: 80%

SalivaryAsHPX12influence pre-blood meal associated behavioral properties in the mosquitoAnopheles stephensi

Kumari

Chauhan

et al. 2020

Preprint

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In the adult female mosquito, successful blood meal acquisition is accomplished by salivary glands, which releases a cocktail of proteins to counteract vertebrate host's immunehomeostasis. However, the biological relevance of many salivary proteins remains unknown. Here, we characterize a salivary specific Heme peroxidase family member HPX12, originally identified from Plasmodium vivax infected salivary RNAseq data of the mosquito Anopheles stephensi. We demonstrate that dsRNA silencing mediated mRNA depletion of salivary AsHPX12 (80-90%), causes enhanced host attraction but reduced blood-meal acquisition abilities, by increasing probing propensity (31%), as well as probing time (100-200s, P<0.0001) as compared to control (35-90s) mosquitoes group. Altered expression of the salivary secretory and antennal proteins may account for an unusual fast release of salivary cocktail proteins, but the slowing acquisition of blood meal, possibly due to salivary homeostasis disruption of AsHPX12 silenced mosquitoes. A parallel transcriptional modulation in response to blood feeding and P. vivax infection, further establish a possible functional correlation of AsHPX12 role in salivary immune-physiology and Plasmodium sporozoites survival/transmission. We propose that salivary HPX12 may have a vital role in the management of 'preand post'-blood meal associated physiological-homeostasis and parasite transmission. Graphical abstractFigure 1: Schematic representation of mosquito's blood meal acquisition and upshot on bloodfeeding after silencing of salivary gland HPX-12. (A) After landing over host skin, mosquito mouthparts (proboscis) actively engaged to search, probe, and pierce the skin followed by a rapid release of the pre-synthesized salivary cocktail, which counteracts the host homeostasis, inflammation, and immune responses, during blood meal uptake. (B) Silencing of HPX-12 disrupts salivary gland homeostasis, enhancing mosquito attraction, possibly by up-regulating odorant-binding proteins genes-OBP-7,10 and OBP-20 expression in the Olfactory System. However, HPX-12 disruption may also cause significant effects on pre-blood meal associated probing abilities, which may be due to fast down-regulation of salivary cocktail proteins such as Anopheline, Apyrase, D7L proteins.

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Section: Discussionsupporting

confidence: 80%

SalivaryAsHPX12influence pre-blood meal associated behavioral properties in the mosquitoAnopheles stephensi

Kumari

Chauhan

et al. 2020

Preprint

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“…Whether similar results are observable in mosquitoes infected with malaria parasites is unclear. It is known that malaria infection alters feeding rates and blood-seeking behaviors [ 37 , 38 ], but more research is needed to understand whether insecticide exposure impacts vector competence [ 39 – 42 ] and/or whether the presence of malaria parasites affects the expression of insecticide resistance [ 29 , 43 ].…”

Section: Discussionmentioning

confidence: 99%

Use of novel lab assays to examine the effect of pyrethroid-treated bed nets on blood-feeding success and longevity of highly insecticide-resistant Anopheles gambiae s.l. mosquitoes

et al. 2022

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Background There is a pressing need to improve understanding of how insecticide resistance affects the functional performance of insecticide-treated nets (ITNs). Standard WHO insecticide resistance monitoring assays are designed for resistance surveillance and do not necessarily provide insight into how different frequencies, mechanisms or intensities of resistance affect the ability of ITNs to reduce malaria transmission. Methods The current study presents some novel laboratory-based assays that attempt to better simulate realistic exposure of mosquitoes to ITNs and to quantify impact of exposure not only on instantaneous mortality, but also on blood-feeding and longevity, two traits that are central to transmission. The assays evaluated the performance of a standard ITN (Permanet® 2.0; Vestergaard Frandsen), a ‘next generation’ combination ITN with a resistance-breaking synergist (Permanet® 3.0) and an untreated net (UTN), against field-derived Anopheles gambiae sensu lato mosquitoes from Côte d’Ivoire exhibiting a 1500-fold increase in pyrethroid resistance relative to a standard susceptible strain. Results The study revealed that the standard ITN induced negligible instantaneous mortality against the resistant mosquitoes, whereas the resistance-breaking net caused high mortality and a reduction in blood-feeding. However, both ITNs still impacted long-term survival relative to the UTN. The impact on longevity depended on feeding status, with blood-fed mosquitoes living longer than unfed mosquitoes following ITN exposure. Exposure to both ITNs also reduced the blood-feeding success, the time spent on the net and blood-feeding duration, relative to the untreated net. Conclusion Although a standard ITN did not have as substantial instantaneous impact as the resistance-breaking net, it still had significant impacts on traits important for transmission. These results highlight the benefit of improved bioefficacy assays that allow for realistic exposure and consider sub- or pre-lethal effects to help assess the functional significance of insecticide resistance. Graphical Abstract

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“…Infection status with human pathogens influences mosquito behavior and changes the content of salivary gland and salivary secretions (Chisenhall et al, 2014a , b ). A previous study suggested that apyrase activity decreases as sporozoite load increases, rendering the infected mosquitoes more likely to probe and re-feed after an infectious first blood meal (Thievent et al, 2019 ). Each probing event increases the likelihood of injecting sporozoites into the skin, which increases the chance of infection.…”

Section: Discussionmentioning

confidence: 99%

Antibody Responses Against Anopheles darlingi Immunogenic Peptides in Plasmodium Infected Humans

Londoño-Rentería

Montiel

Calvo

et al. 2020

Front. Cell. Infect. Microbiol.

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Introduction: Malaria is still an important vector-borne disease in the New World tropics. Despite the recent decline in malaria due to Plasmodium falciparum infection in Africa, a rise in Plasmodium infections has been detected in several low malaria transmission areas in Latin America. One of the main obstacles in the battle against malaria is the lack of innovative tools to assess malaria transmission risk, and the behavioral plasticity of one of the main malaria vectors in Latin America, Anopheles darlingi . Methods: We used human IgG antibodies against mosquito salivary gland proteins as a measure of disease risk. Whole salivary gland antigen (SGA) from Anopheles darlingi mosquitoes was used as antigen in Western blot experiments, in which a ~65 kDa protein was visualized as the main immunogenic band and sent for sequencing by mass spectrometry. Apyrase and peroxidase peptides were designed and used as antigens in an ELISA-based test to measure human IgG antibody responses in people with different clinical presentations of malaria. Results: Liquid chromatography–mass spectrometry revealed 17 proteins contained in the ~65 kDa band, with an apyrase and a peroxidase as the two most abundant proteins. Detection of IgG antibodies against salivary antigens by ELISA revealed a significant higher antibody levels in people with malaria infection when compared to uninfected volunteers using the AnDar_Apy1 and AnDar_Apy2 peptides. We also detected a significant positive correlation between the anti-peptides IgG levels and antibodies against the Plasmodium vivax and P. falciparum antigens PvMSP1 and PfMSP1. Odd ratios suggest that people with higher IgG antibodies against the apyrase peptides were up to five times more likely to have a malaria infection. Conclusion: Antibodies against salivary peptides from An. darlingi salivary gland proteins may be used as biomarkers for malaria risk.

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Malaria load affects the activity of mosquito salivary apyrase

Cited by 21 publications

References 39 publications

SalivaryAsHPX12influence pre-blood meal associated behavioral properties in the mosquitoAnopheles stephensi

SalivaryAsHPX12influence pre-blood meal associated behavioral properties in the mosquitoAnopheles stephensi

Use of novel lab assays to examine the effect of pyrethroid-treated bed nets on blood-feeding success and longevity of highly insecticide-resistant Anopheles gambiae s.l. mosquitoes

Antibody Responses Against Anopheles darlingi Immunogenic Peptides in Plasmodium Infected Humans

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