Induction of actin gene expression in the mosquito midgut by blood ingestion correlates with striking changes of cell shape

Sodja, Ann; Fujioka, Hisashi; Lemos, Francisco José Alves; Donnelly-Doman, Marilyn; Jacobs-­Lorena, Marcelo

doi:10.1016/j.jinsphys.2007.03.017

Cited by 17 publications

(14 citation statements)

References 48 publications

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“…These results suggest that the effects of P. berghei killing are independent of the host blood meal, and more likely caused by the distention of the mosquito midgut following feeding. Ingestion of a blood- or protein-meal results in dramatic changes to midgut epithelium cell morphology, causing a flattening of the columnar cells, the loss of microvilli, and substantial degradation of the basal lamina (Dong et al, 2017; Sodja et al, 2007). This agrees with our CHP assays demonstrating the presence of degraded collagen shortly after taking a blood- or protein-meal, suggesting that the integrity of the basal lamina is compromised during distention, enabling the exposure of developing oocysts to components of the mosquito hemolymph.…”

Section: Discussionmentioning

confidence: 99%

Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals

Kwon

Reynolds

Simões

et al. 2019

Preprint

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14A minimum of two blood meals are required for a mosquito to acquire and transmit 15 malaria, yet Anopheles mosquitoes frequently obtain additional blood meals during their 16 adult lifespan. To determine the impact of subsequent blood-feeding on parasite 17 development in Anopheles gambiae, we examined rodent and human Plasmodium 18 parasite infection with or without an additional non-infected blood meal. We find that an 19 additional blood meal significantly reduces P. berghei immature oocyst numbers, yet does 20 not influence mature oocysts that have already begun sporogony. This is in contrast to 21 experiments performed with the human parasite, P. falciparum, where an additional blood 22 meal does not affect oocyst numbers. These observations are reproduced when 23 mosquitoes were similarly challenged with an artificial protein meal, suggesting that 24 parasite losses are due to the physical distension of the mosquito midgut. We provide 25 evidence that feeding compromises the integrity of the midgut basal lamina, enabling the 26 recognition and lysis of immature P. berghei oocysts by the mosquito complement 27 system. Moreover, we demonstrate that additional feeding promotes P. falciparum oocyst 28 growth, suggesting that human malaria parasites exploit host resources provided with 29 blood-feeding to accelerate their growth. This contrasts experiments with P. berghei, 30 where the size of surviving oocysts is independent of an additional blood meal. Together, 31 these data demonstrate differences in the ability of Plasmodium species to evade immune 32 detection and adapt to utilize host resources at the oocyst stage, representing an 33 additional, yet unexplored component of vectorial capacity that has important implications 34 for transmission of malaria. 36Blood-feeding is an inherent behavior of all hematophagous arthropods, providing 37 nutritional resources for development or reproduction, while enabling the acquisition and 38 transmission of a pathogen from one host to the next. This includes a number of 39 arthropod-borne diseases that influence human health, most notably malaria, which 40 causes more than 200 million infections and 400,000 deaths every year (WHO, 2018). 41Caused by Plasmodium parasites, malaria transmission requires the bite of an Anopheles 42 mosquito, such that understanding the factors that influence vectorial capacity are integral 43 to efforts to reduce malaria transmission. 44Following the ingestion of an infectious blood-meal, malaria parasites undergo substantial 45 development in the mosquito host as they transition from gametes to a fertilized zygote, 46 a motile ookinete, an oocyst, and a sporozoite capable of transmission to a new host 47 (Smith et al., 2014). During this approximate two week period of development (referred 48 to as the extrinsic incubation period, EIP), significant bottlenecks reduce parasite 49 numbers at each of these respective Plasmodium stages (Smith et al., 2014). These 50 losses are mediated in part by the mosquito innate immune system...

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Section: Discussionmentioning

confidence: 99%

Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals

Kwon

Reynolds

Simões

et al. 2019

Preprint

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“…Adults were collected 3 days after emerging from pupae. The adults fed with a blood meal were collected three hours later so that the genes responding to blood ingestion were sufficiently expressed [149]. Samples were homogenized with a dounce homogenizer and RNA was isolated from tissue homogenate with an RNeasy Midi kit (Qiagen).…”

Section: Methodsmentioning

confidence: 99%

Identification of New Protein Interactions between Dengue Fever Virus and Its Hosts, Human and Mosquito

et al. 2013

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The four divergent serotypes of dengue virus are the causative agents of dengue fever, dengue hemorrhagic fever and dengue shock syndrome. About two-fifths of the world's population live in areas where dengue is prevalent, and thousands of deaths are caused by the viruses every year. Dengue virus is transmitted from one person to another primarily by the yellow fever mosquito, Aedes aegypti. Recent studies have begun to define how the dengue viral proteins interact with host proteins to mediate viral replication and pathogenesis. A combined analysis of these studies, however, suggests that many virus-host protein interactions remain to be identified, especially for the mosquito host. In this study, we used high-throughput yeast two-hybrid screening to identify mosquito and human proteins that physically interact with dengue proteins. We tested each identified host protein against the proteins from all four serotypes of dengue to identify interactions that are conserved across serotypes. We further confirmed many of the interactions using co-affinity purification assays. As in other large-scale screens, we identified some previously detected interactions and many new ones, moving us closer to a complete host – dengue protein interactome. To help summarize and prioritize the data for further study, we combined our interactions with other published data and identified a subset of the host-dengue interactions that are now supported by multiple forms of evidence. These data should be useful for understanding the interplay between dengue and its hosts and may provide candidates for drug targets and vector control strategies.

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“…Importantly, upregulation of an actin-like gene was detected at 6h PBM. It was previously reported that increased levels of actin mRNA at 3-4h PBM correlates with epithelial remodeling to accommodate distention of the midgut upon blood ingestion [20]. As SCD1 KD causes rigidity of the epithelial cell membranes, this is suggestive of a stress response to overcome the mechanical pressure caused by the rigid cell membranes.…”

Section: Cytoskeleton Cell Adhesion and Structural Componentsmentioning

confidence: 85%

“…Noteworthily, cell membrane thickness in SCD1 KD midguts was only marginally reduced after bloodmeal (60 nm compared to 55 nm respectively). Reduction of cell membrane thickness is a known adjustment to the expansion of the epithelial cell surface in order to provide structural support to the engorged midgut epithelium [20]. We conclude that SCD1 loss-of-function alters the ability of midgut epithelial cells to undergo adjustments needed to offset the increased pressure within the lumen, causing rapturing of the epithelial cell layer upon blood feeding and blood perfusion of the thoracic cavity.…”

Section: Scd1 Silencing Affects Midgut Epithelial Integrity and Egg Dmentioning

confidence: 90%

Anopheles coluzziistearoyl-CoA desaturase is essential for adult female survival and reproduction upon blood feeding

Ferdous

Fuchs

Behrends

et al. 2020

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Vitellogenesis and oocyte maturation require anautogenous female Anopheles mosquitoes to obtain a bloodmeal from a vertebrate host. The bloodmeal is rich in proteins that are readily broken down into amino acids in the midgut lumen and absorbed by the midgut epithelial cells where they are converted into lipids and then transported to other tissues including ovaries. The stearoyl-CoA desaturase (SCD) plays a pivotal role in this process by converting saturated (SFAs) to unsaturated (UFAs) fatty acids; the latter being essential for maintaining cell membrane fluidity amongst other housekeeping functions. Here, we report the functional and phenotypic characterization of SCD1 in the malaria vector mosquito Anopheles coluzzii. We show that RNA interference (RNAi) silencing of SCD1 and administration of sterculic acid (SA), a small molecule inhibitor of SCD1, significantly impact on the survival and reproduction of female mosquitoes following blood feeding. Microscopic observations reveal that the mosquito thorax is quickly filled with blood, a phenomenon likely caused by the collapse of midgut epithelial cell membranes, and that epithelial cells are depleted of lipid droplets and oocytes fail to mature. Transcriptional profiling shows that genes involved in protein, lipid and carbohydrate metabolism and immunity-related genes are the most affected by SCD1 knock down (KD) in blood-fed mosquitoes. Metabolic profiling reveals that these mosquitoes exhibit increased amounts of saturated fatty acids and TCA cycle intermediates, highlighting the biochemical framework by which the SCD1 KD phenotype manifests as a result of a detrimental metabolic syndrome. Accumulation of SFAs is also the likely cause of the potent immune response observed in the absence of infection, which resembles an auto-inflammatory condition. These data provide insights into mosquito bloodmeal metabolism and lipid homeostasis and could inform efforts to develop novel interventions against mosquito-borne diseases.ClustalW and protein prediction was done using the SMART Package (http://smart.emblheidelberg.de/). Pathway analysis of transcriptomic and metabolomic data was performed using the Kyoto Encyclopedia of Genes and Genomes (KEGG). DsRNA preparation and gene silencingGene-specific double-stranded RNA (dsRNA) was synthesized and injected as described [12]. Briefly, SCD1-specific oligonucleotide primers flanked at their 5′ end by T7 RNA polymerase promoter sequence (SCD1-RNAi-F: taatacgactcactataggg-AAATGTGATTGCCTTCGGT; SCD1-RNAi-R: taatacgactcactataggg-GCGAGAAGAAGAAGCCAC) were used in PCR reactions on total RNA extracted from 10 sugar-fed adult female mosquitoes using the TRIzol reagent (Invitrogen). DsRNA was synthesized using the T7 MEGAscript kit (Invitrogen) and the PCR product was purified using the RNeasy kit (QIAGEN). DsRNA for the control LacZ gene was synthesized as reported [13]. Gene silencing was accomplished by injection of 69 nL (3 ug/uL) of dsRNA into the mesothoracic spiracle of each carbon dioxide-anesthetized 0-2-day old female mo...

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Induction of actin gene expression in the mosquito midgut by blood ingestion correlates with striking changes of cell shape

Cited by 17 publications

References 48 publications

Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals

Malaria parasite immune evasion and adaptation to its mosquito host is influenced by the acquisition of multiple blood meals

Identification of New Protein Interactions between Dengue Fever Virus and Its Hosts, Human and Mosquito

Anopheles coluzziistearoyl-CoA desaturase is essential for adult female survival and reproduction upon blood feeding

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