scholarly journals Kinetics of Plasmodium midgut invasion in Anopheles mosquitoes

Author(s):  
Gloria Volohonsky ◽  
Perrine Paul-Gilloteaux ◽  
Jitka Štáfková ◽  
Julien Soichot ◽  
Jean Salamero ◽  
...  

AbstractMalaria-causing Plasmodium parasites traverse the mosquito midgut cells to establish infection at the basal side of the midgut. This dynamic process is a determinant of mosquito vector competence, yet the kinetics of the parasite migration is not well understood. Here we used transgenic mosquitoes of two Anopheles species and a Plasmodium berghei fluorescence reporter line to track parasite passage through the mosquito tissues at high spatial resolution. We provide new quantitative insight into malaria parasite invasion in African and Indian Anopheles species and demonstrate that species-specific kinetics of Plasmodium invasion is shaped by the mosquito complement-like system.Author SummaryThe traversal of the mosquito midgut cells is one of the critical stages in the life cycle of malaria parasites. Motile parasite forms, called ookinetes, traverse the midgut epithelium in a dynamic process which is not fully understood.Here, we harnessed transgenic reporters to track invasion of Plasmodium parasites in African and Indian mosquito species. We found important differences in parasite dynamics between the two anopheline species and demonstrated an unexpected role of mosquito complement-like system in regulation of parasite invasion.

2019 ◽  
Author(s):  
Jorian Prudhomme ◽  
Albin Fontaine ◽  
Guillaume Lacour ◽  
Jean-Charles Gantier ◽  
Laure Diancourt ◽  
...  

AbstractEurope is the world’s leading tourism destination and is receiving every year travelers from areas with active arbovirus transmission. There is thus a threat of mosquito-borne virus emergence in Europe due to the presence of the invasive mosquito vector Aedes albopictus. Little attention has been paid about the possible role of indigenous mosquito species as vectors of emerging arboviruses. Here, we assessed the vector competence dynamic of Ae. geniculatus, a European anthropophilic mosquito species, for chikungunya virus (CHIKV) in comparison with Ae. albopictus.We revealed that Ae. geniculatus was highly susceptible to CHIKV infection and could transmit the virus. By specifically exploring the vector competence dynamic in both mosquito species, we revealed that the cumulative distribution of CHIKV incubation period in Ae. geniculatus was delayed by several days as compared to Ae. albopictus.Our results strengthen the importance of considering indigenous species as potential vectors for emerging arboviruses. They also revealed the importance of considering variation in arbovirus dissemination or transmission dynamics in mosquitoes when performing vector competence assays. We will discuss the implications of our results on a CHIKV outbreak dynamic in a theoretical framework.Sentence summaryThe European mosquito Aedes geniculatus is highly susceptible to CHIKV infection but disseminate and transmit the virus several days later than Ae. albopictus.


2019 ◽  
Vol 56 (5) ◽  
pp. 1377-1383
Author(s):  
Wiem Ben Ayed ◽  
Fadila Amraoui ◽  
Youmna M’ghirbi ◽  
Francis Schaffner ◽  
Adel Rhaim ◽  
...  

Abstract The present study aimed to update the list of Aedes mosquito species occurring in Tunisia and to test the vector competence of Aedes (Ochlerotatus) caspius (Pallas) and Ae. (Ochlerotatus) detritus (Haliday), the locally most abundant and widespread species, to transmit Zika virus (ZIKV). In 2017–2018, mosquito larvae were collected from 39 different larval habitats in seven bioclimatic zones of Tunisia. The salinity and pH of each breeding site were measured. The survey revealed the presence of 10 Aedes species in Tunisia: Ae. (Stegomyia) albopictus (Skuse), Ae. (Ochlerotatus) berlandi (Séguy), Ae. caspius, Ae. detritus, Ae. (Finlaya) echinus (Edwards), Ae. (Finlaya) geniculatus (Olivier), Ae. (Acartomyia) mariae (Sergent and Sergent), Ae. (Ochlerotatus) pulcritarsis (Rondani), Ae. (Aedimorphus) vexans (Meigen), and Ae. (Fredwardsius) vittatus (Bigot). Of these 10 species, Ae. caspius and Ae. detritus were the most abundant in Tunisia. Aedes detritus and Ae. caspius larvae were reared until the imago stage under insectary conditions to test autogeny. The study showed that Ae. detritus is autogenous and stenogamous and Ae. caspius, anautogenous and eurygamous. Finally, the collected strains of these two species were experimentally infected with the Asian genotype of ZIKV, originally isolated from a patient in April 2014 in New Caledonia, to test their vector competence. Neither of these species was able to transmit ZIKV at 7 and 14 d postexposure. Further investigations are needed to test the competence of other Tunisian mosquito species that may be associated with ZIKV transmission.


2015 ◽  
Vol 112 (10) ◽  
pp. E1152-E1161 ◽  
Author(s):  
Katelyn O’Neill ◽  
Bradley J. S. C. Olson ◽  
Ning Huang ◽  
Dave Unis ◽  
Rollie J. Clem

Millions of people are infected each year by arboviruses (arthropod-borne viruses) such as chikungunya, dengue, and West Nile viruses, yet for reasons that are largely unknown, only a relatively small number of mosquito species are able to transmit arboviruses. Understanding the complex factors that determine vector competence could facilitate strategies for controlling arbovirus infections. Apoptosis is a potential antiviral defense response that has been shown to be important in other virus–host systems. However, apoptosis is rarely seen in arbovirus-infected mosquito cells, raising questions about its importance as an antiviral defense in mosquitoes. We tested the effect of stimulating apoptosis during arbovirus infection by infectingAedes aegyptimosquitoes with a Sindbis virus (SINV) clone called MRE/Rpr, in which the MRE-16 strain of SINV was engineered to express the proapoptotic genereaperfromDrosophila. MRE/Rpr exhibited an impaired infection phenotype that included delayed midgut infection, delayed virus replication, and reduced virus accumulation in saliva. Nucleotide sequencing of thereaperinsert in virus populations isolated from individual mosquitoes revealed evidence of rapid and strong selection against maintenance of Reaper expression in MRE/Rpr-infected mosquitoes. The impaired phenotype of MRE/Rpr, coupled with the observed negative selection against Reaper expression, indicates that apoptosis is a powerful defense against arbovirus infection in mosquitoes and suggests that arboviruses have evolved mechanisms to avoid stimulating apoptosis in mosquitoes that serve as vectors.


2018 ◽  
Author(s):  
Marco Brustolin ◽  
Sujit Pujhari ◽  
Cory A. Henderson ◽  
Jason L. Rasgon

AbstractThe Togavirus (Alphavirus) Mayaro virus (MAYV) was initially described in 1954 from Mayaro County (Trinidad) and has been responsible for outbreaks in South America and the Caribbean. Imported MAYV cases are on the rise, leading to invasion concerns similar to Chikungunya and Zika viruses. Little is known about the range of mosquito species that are competent MAYV vectors. We tested vector competence of 2 MAYV genotypes for six mosquito species (Aedes aegypti, Anopheles gambiae, An. stephensi, An. quadrimaculatus, An. freeborni, Culex quinquefasciatus). Ae. aegypti and Cx. quinquefasciatus were poor MAYV vectors, and either were poorly infected or poorly transmitted. In contrast, all Anopheles species were able to transmit MAYV, and 3 of the 4 species transmitted both genotypes. The Anopheles species tested are divergent and native to widely separated geographic regions, suggesting that Anopheles may be important in the invasion and spread of MAYV across diverse regions of the world.


2019 ◽  
Author(s):  
H. Patil ◽  
K.R. Hughes ◽  
L. Lemgruber ◽  
N. Philip ◽  
N. Dickens ◽  
...  

AbstractPlasmodium species are apicomplexan parasites whose zoites are polarized cells with a marked apical organisation where the organelles associated with host cell invasion and colonization reside. Plasmodium gametes mate in the mosquito midgut to form the spherical and presumed apolar zygote that morphs during the following 24 hours into a polarized, elongated and motile zoite form, the ookinete. Endocytosis-mediated protein transport is generally necessary for the establishment and maintenance of polarity in epithelial cells and neurons, and the small GTPase RAB11A is an important regulator of protein transport via recycling endosomes. PbRAB11A is essential in blood stage asexual of Plasmodium. Therefore, a promoter swap strategy was employed to down-regulate PbRAB11A expression in gametocytes and zygotes of the rodent malaria parasite, Plasmodium berghei which demonstrated the essential role of RAB11A in ookinete development. The approach revealed that lack of PbRAB11A had no effect on gamete production and fertility rates however, the zygote to ookinete transition was almost totally inhibited and transmission through the mosquito was prevented. Lack of PbRAB11A did not prevent meiosis and mitosis, nor the establishment of polarity as indicated by the correct formation and positioning of the Inner Membrane Complex (IMC) and apical complex. However, morphological maturation was prevented and parasites remained spherical and immotile and furthermore, they were impaired in the secretion and distribution of microneme cargo. The data are consistent with the previously proposed model of RAB11A endosome mediated delivery of plasma membrane in Toxoplasma gondii if not its role in IMC formation and implicate it in microneme function.Author SummaryAccording to the WHO there was estimated to be over 200 million cases of malaria in 2017 and nearly half a million deaths. The disease is caused by specific species of Plasmodium which are passed between human hosts by a mosquito vector. In order to transmit through the mosquito the single-celled parasite undergoes many developmental changes as it morphs from non-motile blood forms to become a polarised and motile ookinete in the mosquito midgut. Transport of proteins within the cell during these critical morphological transitions relies on specific endosome vesicles to correctly target proteins within the parasite. We investigated the role of the RAB11A protein which is known to be involved in endosomal vesicle targeting to generate cellular polarity in other organisms. Because RAB11A is also essential for parasite growth in the mammalian host we used a promoter swap system to specifically switch off RAB11A in the sexual transmission stages. In the absence of RAB11A parasites were unable to form elongated, motile ookinetes and were unable to pass through the mosquito. Interestingly the parasites were able to form some of the (polarising) structures specific to ookinetes however full morphological transformation did not occur and the parasites were not motile. We show that although proteins are still delivered to the parasite surface, secretion is impaired and that the mutant parasites are smaller despite obvious microtubule formation implying that there is a deficit in delivery of membrane to the surface.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Rebekah A. Reynolds ◽  
Hyeogsun Kwon ◽  
Thiago Luiz Alves e Silva ◽  
Janet Olivas ◽  
Joel Vega-Rodriguez ◽  
...  

AbstractMosquito physiology and immunity are integral determinants of malaria vector competence. This includes the principal role of hormonal signaling in Anopheles gambiae initiated shortly after blood-feeding, which stimulates immune induction and promotes vitellogenesis through the function of 20-hydroxyecdysone (20E). Previous studies demonstrated that manipulating 20E signaling through the direct injection of 20E or the application of a 20E agonist can significantly impact Plasmodium infection outcomes, reducing oocyst numbers and the potential for malaria transmission. In support of these findings, we demonstrate that a 20E agonist, halofenozide, is able to induce anti-Plasmodium immune responses that limit Plasmodium ookinetes. We demonstrate that halofenozide requires the function of ultraspiracle (USP), a component of the canonical heterodimeric ecdysone receptor, to induce malaria parasite killing responses. Additional experiments suggest that the effects of halofenozide treatment are temporal, such that its application only limits malaria parasites when applied prior to infection. Unlike 20E, halofenozide does not influence cellular immune function or AMP production. Together, our results further demonstrate the potential of targeting 20E signaling pathways to reduce malaria parasite infection in the mosquito vector and provide new insight into the mechanisms of halofenozide-mediated immune activation that differ from 20E.


2020 ◽  
Author(s):  
Rebekah A. Reynolds ◽  
Hyeogsun Kwon ◽  
Thiago Luiz Alves e Silva ◽  
Janet Olivas ◽  
Joel Vega-Rodriguez ◽  
...  

AbstractMosquito physiology and immunity are integral determinants of malaria vector competence. This includes the principal role of hormonal signaling in Anopheles gambiae initiated shortly after blood-feeding, which stimulates immune induction and promotes vitellogenesis through the function of 20-hydroxyecdysone (20E). Previous studies demonstrated that manipulating 20E signaling through the direct injection of 20E or the application of a 20E agonist can significantly impact Plasmodium infection outcomes, reducing oocyst numbers and the potential for malaria transmission. In support of these findings, we demonstrate that a 20E agonist, halofenozide, is able to induce anti-Plasmodium immune responses that limit Plasmodium ookinetes. We demonstrate that halofenozide requires the function of ultraspiracle (USP), a component of the canonical heterodimeric ecdysone receptor, to induce malaria parasite killing responses. Additional experiments suggest that the effects of halofenozide treatment are temporal, such that its application only limits malaria parasites when applied prior to infection. Unlike 20E, halofenozide does not influence cellular immune function or AMP production. Together, our results further demonstrate the potential of targeting 20E signaling pathways to reduce malaria parasite infection in the mosquito vector and provide new insight into the mechanisms of halofenozide-mediated immune activation that differ from 20E.


Viruses ◽  
2021 ◽  
Vol 13 (6) ◽  
pp. 1154
Author(s):  
Heidi Auerswald ◽  
Pierre-Olivier Maquart ◽  
Véronique Chevalier ◽  
Sebastien Boyer

Japanese encephalitis virus (JEV) is a zoonotic pathogen mainly found in East and Southeast Asia and transmitted by mosquitoes. The objective of this review is to summarize the knowledge on the diversity of JEV mosquito vector species. Therefore, we systematically analyzed reports of JEV found in field-caught mosquitoes as well as experimental vector competence studies. Based on the investigated publications, we classified 14 species as confirmed vectors for JEV due to their documented experimental vector competence and evidence of JEV found in wild mosquitoes. Additionally, we identified 11 mosquito species, belonging to five genera, with an experimentally confirmed vector competence for JEV but lacking evidence on their JEV transmission capacity from field-caught mosquitoes. Our study highlights the diversity of confirmed and potential JEV vector species. We also emphasize the variety in the study design of vector competence investigations. To account for the diversity of the vector species and regional circumstances, JEV vector competence should be studied in the local context, using local mosquitoes with local virus strains under local climate conditions to achieve reliable data. In addition, harmonization of the design of vector competence experiments would lead to better comparable data, informing vector and disease control measures.


Pathogens ◽  
2021 ◽  
Vol 10 (5) ◽  
pp. 525
Author(s):  
Thiago Nunes Pereira ◽  
Fabiano Duarte Carvalho ◽  
Jerônimo Nunes Rugani ◽  
Vanessa Rafaela de Carvalho ◽  
Jaqueline Jarusevicius ◽  
...  

The Mayaro virus (MAYV) is an arbovirus that circulates mainly in tropical forests or rural areas in Latin America and is transmitted mainly by Haemagogus mosquitoes. The objective of this study was to evaluate the vector competence, microbiome, and the presence of Wolbachia in three Aedes albopictus populations infected with MAYV. The vector competence was assessed based on viral infection and transmission by RT-qPCR. In addition, the microbiome was evaluated by amplification of the 16S rRNA V4 region and PCR to detect the presence of Wolbachia (strain wAlbA/wAlbB). Our results show that all three populations were susceptible to MAYV infection. The potential transmission of the MAYV was consistent in all populations of naïve mosquitoes injected (more than 50%). The microbiome analysis revealed 118 OTUs (operational taxonomic unit) from the three populations, 8 phyla, 15 classes, 26 orders, 35 families, 65 genera, and 53 species. All populations had Pseudomonas and Wolbachia as predominant genera. There was no difference between the variables for MAYV and Wolbachia (wAlbA or wAlbB) in the abdomen. However, in the head + thorax samples at 14 dpi, there was a difference between the two populations, indicating a possible correlation between the presence of Wolbachia (wAlbB) and infection. Overall, we show evidence that Ae. albopictus displays significant infection and transmission competence for the MAYV in the laboratory, and its bacterial microbiota play an important role in the host, mainly the strains of Wolbachia. The influence of the intestinal microbiota of Ae. albopictus is poorly known, and a better understanding of these interactions would open new perspectives for disease control through the manipulation of microbial communities. The exact contribution of this mosquito species to the transmission of the MAYV in the field remains to be confirmed.


2019 ◽  
Vol 116 (28) ◽  
pp. 14119-14128 ◽  
Author(s):  
Hyeogsun Kwon ◽  
Ryan C. Smith

Mosquito immunity is composed of both cellular and humoral factors that provide protection from invading pathogens. Immune cells known as hemocytes, have been intricately associated with phagocytosis and innate immune signaling. However, the lack of genetic tools has limited hemocyte study despite their importance in mosquito anti-Plasmodiumimmunity. To address these limitations, we employ the use of a chemical-based treatment to deplete phagocytic immune cells inAnopheles gambiae,demonstrating the role of phagocytes in complement recognition and prophenoloxidase production that limit the ookinete and oocyst stages of malaria parasite development, respectively. Through these experiments, we also define specific subtypes of phagocytic immune cells inAn. gambiae, providing insights beyond the morphological characteristics that traditionally define mosquito hemocyte populations. Together, this study represents a significant advancement in our understanding of the roles of mosquito phagocytes in mosquito vector competence and demonstrates the utility of clodronate liposomes as an important tool in the study of invertebrate immunity.


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