Drinking a hot blood meal elicits a protective heat shock response in mosquitoes

Benoit, Joshua B.; López‐Martínez, Giancarlo; Patrick, Kevin R.; Phillips, Zachary P.; Krause, Tyler B.; Denlinger, David L.

doi:10.1073/pnas.1105195108

Cited by 138 publications

(126 citation statements)

References 31 publications

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“…An increased accumulation of heat shock protein 70 (HSP70) was detected as early as 1 hPBM and its presence is attributed to protection from the stress of warm blood ingestion (Benoit et al 2011). HSPs are encoded by a gene family that has expanded in the Ae.…”

Section: Resultsmentioning

confidence: 99%

Strain Variation in the Transcriptome of the Dengue Fever Vector,Aedes aegypti

Bonizzoni¹,

Dunn

Campbell³

et al. 2012

G3 Genes|Genomes|Genetics

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Studies of transcriptome dynamics provide a basis for understanding functional elements of the genome and the complexity of gene regulation. The dengue vector mosquito, Aedes aegypti, exhibits great adaptability to diverse ecological conditions, is phenotypically polymorphic, and shows variation in vectorial capacity to arboviruses. Previous genome sequencing showed richness in repetitive DNA and transposable elements that can contribute to genome plasticity. Population genetic studies revealed a varying degree of worldwide genetic polymorphism. However, the extent of functional genetic polymorphism across strains is unknown. The transcriptomes of three Ae. aegypti strains, Chetumal (CTM), Rexville D-Puerto Rico (Rex-D) and Liverpool (LVP), were compared. CTM is more susceptible than Rex- D to infection by dengue virus serotype 2. A total of 4188 transcripts exhibit either no or small variation (<2-fold) among sugar-fed samples of the three strains and between sugar- and blood-fed samples within each strain, corresponding most likely to genes encoding products necessary for vital functions. Transcripts enriched in blood-fed mosquitoes encode proteins associated with catalytic activities, molecular transport, metabolism of lipids, carbohydrates and amino acids, and functions related to blood digestion and the progression of the gonotropic cycle. Significant qualitative and quantitative differences were found in individual transcripts among strains including differential representation of paralogous gene products. The majority of immunity-associated transcripts decreased in accumulation after a bloodmeal and the results are discussed in relation to the different susceptibility of CTM and Rex-D mosquitoes to DENV2 infection.

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Section: Resultsmentioning

confidence: 99%

Strain Variation in the Transcriptome of the Dengue Fever Vector,Aedes aegypti

Bonizzoni¹,

Dunn

Campbell³

et al. 2012

G3 Genes|Genomes|Genetics

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show abstract

“…Interestingly, the increased mortality induced by the ingestion of CXM appears to be due to the ingestion of a warm blood meal, as CXM-fed mosquitoes that were not blood-fed had mortality rates similar to those of sucrose-fed (control) mosquitoes (16% of mortality). These results suggest that the drug might also impair their ability to deal with the heat stress generated by the ingestion of warm blood (Benoit et al, 2011).…”

Section: Memory Characterisationmentioning

confidence: 89%

Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Vinauger

Lutz

Riffell

2014

Journal of Experimental Biology

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Olfactory learning in blood-feeding insects, such as mosquitoes, could play an important role in host preference and disease transmission. However, standardised protocols allowing testing of their learning abilities are currently lacking, and how different olfactory stimuli are learned by these insects remains unknown. Using a Pavlovian conditioning paradigm, we trained individuals and groups of Aedes aegypti mosquitoes to associate an odorant conditioned stimulus (CS) with a blood-reinforced thermal stimulus (unconditioned stimulus; US). Results showed, first, that mosquitoes could learn the association between L-lactic acid and the US, and retained the association for at least 24 h. Second, the success of olfactory conditioning was dependent upon the CS -some odorants that elicited indifferent responses in naïve mosquitoes, such as L-lactic acid and 1-octen-3-ol, were readily learned, whereas others went from aversive to attractive after training (Z-3-hexen-1-ol) or were untrainable (β-myrcene and benzyl alcohol). Third, we examined whether mosquitoes' ability to learn could interfere with the action of the insect repellent DEET. Results demonstrated that pre-exposure and the presence of DEET in the CS reduced the aversive effects of DEET. Last, the nature of the formed memories was explored. Experiments using cold-shock treatments within the first 6 h posttraining (for testing anaesthesia-resistant memory) and a protein synthesis inhibitor (cycloheximide; to disrupt the formation of longterm memory) both affected mosquitoes' performances. Together, these results show that learning is a crucial component in odour responses in A. aegypti, and provide the first evidence for the functional role of different memory traces in these responses.

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“…There is some indication that adult anopheline mosquitoes can avoid the warmest locations [45], but there is little evidence for precise behavioural thermoregulation [46]. Additionally, it has been shown that expression of mosquito heat-shock proteins increase in response to thermal stress [47] and these proteins have been shown to interact with Plasmodium development [48]. The extent to which these interactions would affect EIP in these environments is unclear, but should be considered in future studies.…”

Section: Discussionmentioning

confidence: 99%

Characterizing microclimate in urban malaria transmission settings: a case study from Chennai, India

Cator

Thomas

Paaijmans

et al. 2013

Malar J

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BackgroundEnvironmental temperature is an important driver of malaria transmission dynamics. Both the parasite and vector are sensitive to mean ambient temperatures and daily temperature variation. To understand transmission ecology, therefore, it is important to determine the range of microclimatic temperatures experienced by malaria vectors in the field.MethodsA pilot study was conducted in the Indian city of Chennai to determine the temperature variation in urban microclimates and characterize the thermal ecology of the local transmission setting. Temperatures were measured in a range of probable indoor and outdoor resting habitats of Anopheles stephensi in two urban slum malaria sites. Mean temperatures and daily temperature fluctuations in local transmission sites were compared with standard temperature measures from the local weather station. The biological implications of the different temperatures were explored using temperature-dependent parasite development models to provide estimates of the extrinsic incubation period (EIP) of Plasmodium vivax and Plasmodium falciparum.ResultsMean daily temperatures within the urban transmission sites were generally warmer than those recorded at the local weather station. The main reason was that night-time temperatures were higher (and hence diurnal temperature ranges smaller) in the urban settings. Mean temperatures and temperature variation also differed between specific resting sites within the transmission environments. Most differences were of the order of 1-3°C but were sufficient to lead to important variation in predicted EIPs and hence, variation in estimates of transmission intensity.ConclusionsStandard estimates of environmental temperature derived from local weather stations do not necessarily provide realistic measures of temperatures within actual transmission environments. Even the small differences in mean temperatures or diurnal temperature ranges reported in this study can lead to large variations in key mosquito and/or parasite life history traits that determine transmission intensity. Greater effort should be directed at quantifying adult mosquito resting behaviour and determining the temperatures actually experienced by mosquitoes and parasites in local transmission environments. In the absence of such highly resolved data, the approach used in the current study provides a framework for improved thermal characterization of transmission settings.

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Drinking a hot blood meal elicits a protective heat shock response in mosquitoes

Cited by 138 publications

References 31 publications

Strain Variation in the Transcriptome of the Dengue Fever Vector,Aedes aegypti

Strain Variation in the Transcriptome of the Dengue Fever Vector,Aedes aegypti

Olfactory learning and memory in the disease vector mosquito,Aedes aegypti

Characterizing microclimate in urban malaria transmission settings: a case study from Chennai, India

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