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Effect of chloroquine on gene expression of Plasmodium yoelii nigeriensis during its sporogonic development in the mosquito vector
Henrique Silveira, Susana Ramos, Patrícia Abrantes, Luís Lopes, Virgílio E do Rosario, Mitchell S Abrahamsen
Malaria Journal , 2007, DOI: 10.1186/1475-2875-6-84
Abstract: Differential display RT-PCR (DDRT-PCR) was used to identify genes expressed during the sporogonic cycle that are regulated by exposure to chloroquine. Anopheles stephensi mosquitoes were fed on Plasmodium yoelii nigeriensis-infected mice. Three days post-infection, mosquitoes were fed a non-infectious blood meal from mice treated orally with 50 mg/kg chloroquine. Two differentially expressed Plasmodium transcripts (Pyn_chl091 and Pyn_chl055) were further characterized by DNA sequencing and real-time PCR analysis.Both transcripts were represented in Plasmodium EST databases, but displayed no homology with any known genes. Pyn_chl091 was upregulated by day 18 post infection when the mosquito had a second blood meal. However, when the effect of chloroquine on that transcript was investigated during the erythrocytic cycle, no significant differences were observed. Although slightly upregulated by chloroquine exposure the expression of Pyn_chl055 was more affected by development, increasing towards the end of the sporogonic cycle. Transcript abundance of Pyn_chl055 was reduced when erythrocytic stages were treated with chloroquine.Chloroquine increased parasite load in mosquito salivary glands and interferes with the expression of at least two Plasmodium genes. The transcripts identified contain putative signal peptides and transmembrane domains suggesting that these proteins, due to their location, are targets of chloroquine (not as an antimalarial) probably through cell trafficking and recycling.Malaria transmission starts when the anopheline mosquito takes an infected blood meal, initiating the sporogonic cycle of the Plasmodium parasite. The full sporogonic cycle varies in length, depending on species and temperature, and can take up to two weeks [1]. It is speculated that since mosquitoes will have several blood meals during their life span, components of this meal can interfere with parasite development in the mosquito vector. In endemic areas anti-malarial drugs,
Phenotypic Dissection of a Plasmodium-Refractory Strain of Malaria Vector Anopheles stephensi: The Reduced Susceptibility to P. berghei and P. yoelii  [PDF]
Naoaki Shinzawa, Tomoko Ishino, Mayumi Tachibana, Takafumi Tsuboi, Motomi Torii
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0063753
Abstract: Anopheline mosquitoes are the major vectors of human malaria. Parasite-mosquito interactions are a critical aspect of disease transmission and a potential target for malaria control. Current investigations into parasite-mosquito interactions frequently assume that genetically resistant and susceptible mosquitoes exist in nature. Therefore, comparisons between the Plasmodium susceptibility profiles of different mosquito species may contribute to a better understanding of vectorial capacity. Anopheles stephensi is an important malaria vector in central and southern Asia and is widely used as a laboratory model of parasite transmission due to its high susceptibility to Plasmodium infection. In the present study, we identified a rodent malaria-refractory strain of A. stephensi mysorensis (Ehime) by comparative study of infection susceptibility. A very low number of oocysts develop in Ehime mosquitoes infected with P. berghei and P. yoelii, as determined by evaluation of developed oocysts on the basal lamina. A stage-specific study revealed that this reduced susceptibility was due to the impaired formation of ookinetes of both Plasmodium species in the midgut lumen and incomplete crossing of the midgut epithelium. There were no apparent abnormalities in the exflagellation of male parasites in the ingested blood or the maturation of oocysts after the rounding up of the ookinetes. Overall, these results suggest that invasive-stage parasites are eliminated in both the midgut lumen and epithelium in Ehime mosquitoes by strain-specific factors that remain unknown. The refractory strain newly identified in this report would be an excellent study system for investigations into novel parasite-mosquito interactions in the mosquito midgut.
Cloning, characterization, and expression of microRNAs from the Asian malaria mosquito, Anopheles stephensi
Edward Mead, Zhijian Tu
BMC Genomics , 2008, DOI: 10.1186/1471-2164-9-244
Abstract: We report the cloning and characterization of 27 distinct miRNAs from 17-day old An. stephensi female mosquitoes. Seventeen of the 27 miRNAs matched previously predicted An. gambiae miRNAs, offering the first experimental verification of miRNAs from mosquito species. Ten of the 27 are miRNAs previously unknown to mosquitoes, four of which did not match any known miRNAs in any organism. Twenty-five of the 27 Anopheles miRNAs had conserved sequences in the genome of a divergent relative, the yellow fever mosquito Aedes aegypti. Two clusters of miRNAs were found within introns of orthologous genes in An. gambiae, Ae. aegypti, and Drosophila melanogaster. Mature miRNAs were detected in An. stephensi for all of the nine selected miRNAs, including the four novel miRNAs (miR-x1- miR-x4), either by northern blot or by Ribonuclease Protection Assay. Expression profile analysis of eight of these miRNAs revealed distinct expression patterns from early embryo to adult stages in An. stephensi. In both An. stephensi and Ae. aegypti, the expression of miR-x2 was restricted to adult females and predominantly in the ovaries. A significant reduction of miR-x2 level was observed 72 hrs after a blood meal. Thus miR-x2 is likely involved in female reproduction and its function may be conserved among divergent mosquitoes. A mosquito homolog of miR-14, a regulator of longevity and apoptosis in D. melanogaster, represented 25% of all sequenced miRNA clones from 17-day old An. stephensi female mosquitoes. An. stephensi miR-14 displayed a relatively strong signal from late embryonic to adult stages. miR-14 expression is consistent during the adult lifespan regardless of age, sex, and blood feeding status. Thus miR-14 is likely important across all mosquito life stages.This study provides experimental evidence for 23 conserved and four new microRNAs in An. stephensi mosquitoes. Comparisons between miRNA gene clusters in Anopheles and Aedes mosquitoes, and in D. melanogaster suggest the loss o
Relative Toxicity of Leaf Extracts of Eucalyptus globulus and Centella asiatica against Mosquito Vectors Aedes aegypti and Anopheles stephensi  [PDF]
Savitha Sekhar Nair,Vinaya Shetty,Nadikere Jaya Shetty
Journal of Insects , 2014, DOI: 10.1155/2014/985463
Abstract: The larvicidal activity of different solvent leaf extracts (hexane, diethyl ether, dichloromethane, and methanol) of Eucalyptus globulus and Centella asiatica against two geographically different strains of Aedes aegypti and Anopheles stephensi was investigated. The extracts were tested against the late third instar larvae of Aedes aegypti and Anopheles stephensi, and larval mortality was observed after 24 hours of treatment. LC50 and LC90 were calculated. The LC50 values of hexane extract of Eucalyptus globulus against the late third instar larvae of the BSN and JPN strains of Aedes aegypti and the DLC and KNG strains of Anopheles stephensi were 225.2, 167.7, 118.8, and 192.8?ppm, while those of the hexane extract of Centella asiatica were 246.5, 268.7, 50.6, and 243.5?ppm, respectively. The LC50 values of diethyl ether extract of Centella asiatica were 339.6, 134.5, 241, and 14.7?ppm. The hexane extracts of both plants and the diethyl ether extract of C. asiatica presented the highest potential for the control of Aedes aegypti and Anopheles stephensi. The present findings also reveal the necessity of assaying multiple strains of a species to fully comprehend the larvicidal efficacy of a compound. 1. Introduction Apart from being a social nuisance, mosquitoes pose serious health threats to both men and animals considering that they are the principal vectors for many vector borne diseases including malaria, dengue, yellow fever, and Chikungunya [1, 2] in men and equine encephalitis, haemorrhagic septicaemia of buffaloes, and enzootic hepatitis in animals [3]. In some individuals, mosquito bites also result in acute systemic allergic reactions defined by the presence of one or more of the following: urticaria, angioedema, wheezing, dyspnea, hypotension, and decrease or loss of consciousness [4]. The mosquito, Aedes (Stegomyia) aegypti (Linn.), (Diptera: Culicidae) is the primary vector of dengue, yellow fever, and Chikungunya [2]. According to WHO, over 40% of the world’s population is now at risk of dengue and there are 200?000 estimated cases of yellow fever, causing 30?000 deaths, worldwide each year. Malaria, on the other hand, a life threatening disease which caused an estimated 627?000 deaths in 2012 is transmitted exclusively through the bites of Anopheles mosquitoes [5]. Anopheles stephensi Liston (Diptera: Culicidae) is a major vector in India as well as in some of the West Asian countries and has been shown to be directly responsible for about 40–50% of the annual malarial incidence [6, 7]. Mosquito control is an extensively researched topic
Mosquito immune responses and compatibility between Plasmodium parasites and anopheline mosquitoes
Giovanna Jaramillo-Gutierrez, Janneth Rodrigues, Georges Ndikuyeze, Michael Povelones, Alvaro Molina-Cruz, Carolina Barillas-Mury
BMC Microbiology , 2009, DOI: 10.1186/1471-2180-9-154
Abstract: Four new An. gambiae (G3) genes were identified that, when silenced, have a different effect on P. berghei (Anka 2.34) and P. falciparum (3D7) infections. Orthologs of these genes, as well as LRIM1 and CTL4, were also silenced in An. stephensi (Nijmegen Sda500) females infected with P. yoelii (17XNL). For five of the six genes tested, silencing had the same effect on infection in the P. falciparum-An. gambiae and P. yoelii-An. stephensi parasite-vector combinations. Although silencing LRIM1 or CTL4 has no effect in An. stephensi females infected with P. yoelii, when An. gambiae is infected with the same parasite, silencing these genes has a dramatic effect. In An. gambiae (G3), TEP1, LRIM1 or LRIM2 silencing reverts lysis and melanization of P. yoelii, while CTL4 silencing enhances melanization.There is a broad spectrum of compatibility, the extent to which the mosquito immune system limits infection, between different Plasmodium strains and particular mosquito strains that is mediated by TEP1/LRIM1 activation. The interactions between highly compatible animal models of malaria, such as P. yoelii (17XNL)-An. stephensi (Nijmegen Sda500), is more similar to that of P. falciparum (3D7)-An. gambiae (G3).Mosquitoes transmit many infectious diseases, including malaria, lymphatic filariasis, yellow fever, and dengue. Among these diseases, malaria is by far the most costly in terms of human health. It is endemic to more than 100 countries and causes 550 million cases per year, with the highest mortality in children from sub-Saharan Africa. Malaria transmission to humans requires a competent mosquito species, as Plasmodium parasites must undergo a complex developmental cycle and survive the defense responses of their insect host. In Africa, Anopheles gambiae is the major vector of Plasmodium falciparum infection, which causes the most aggressive form of human malaria.The Plasmodium berghei (murine malaria) model is one of the most widely used experimental systems to study ma
Larvicidal and repellent properties of Adansonia digitata against medically important human malarial vector mosquito Anopheles stephensi (Diptera: Culicidae)  [PDF]
K. Krishnappa , K. Elumalai , S. Dhanasekaran & J. Gokulakrishnan
Journal of Vector Borne Diseases , 2012,
Abstract: Background & objectives: Development of plant-based alternative compounds for mosquito control has gainedimportance now-a-days, in view of increasing resistance in mosquito vectors to existing insecticides. The larvicidaland repellent activities of benzene, chloroform, hexane and methanol leaf extracts of Indian medicinal plant,Adansonia digitata were investigated against malarial vector, Anopheles stephensi.Methods: In all, 25 III instar larvae of An. stephensi were exposed to various concentrations (30–180 mg/l) in thelaboratory by using the standard protocol described by WHO (2005). The larvae were exposed for 24 h andmortalities were subjected to log-probit analysis. Repellent activity of crude leaf extract at the dosages of 2, 4and 6 mg/cm2 was evaluated in a net cage (45 × 30 × 45 cm) containing 100 blood starved female mosquitoes ofAn. stephensi using the protocol of WHO (1996).Results: Preliminary phytochemical analysis of A. digitata showed the presence of triterpenoids and saponins.The LC50 and LC90 values of hexane, benzene, chloroform, and methanol extracts of A. digitata against An.stephensi larvae in 24 h were 111.32, 97.13, 88.55, 78.18 and 178.63, 176.19, 168.14, 155.42 mg/l, respectively.The repellent activity of methanol extract was found to be most effective and at higher concentration of 6mg/cm2 benzene, chloroform hexane and methanol extracts provided 100% protection up to 150, 180, 120 and210 min against An. stephensi, respectively.Conclusion: The preliminary study indicated that A. digitata showed larvicidal and repellent activities againstAn. stephensi and could be used for controlling mosquitoes. Further studies are indicated to purify the activecompounds from these plants for developing larvicide and repellents.
Enterobacter-Activated Mosquito Immune Responses to Plasmodium Involve Activation of SRPN6 in Anopheles stephensi  [PDF]
Abraham G. Eappen, Ryan C. Smith, Marcelo Jacobs-Lorena
PLOS ONE , 2013, DOI: 10.1371/journal.pone.0062937
Abstract: Successful development of Plasmodium in the mosquito is essential for the transmission of malaria. A major bottleneck in parasite numbers occurs during midgut invasion, partly as a consequence of the complex interactions between the endogenous microbiota and the mosquito immune response. We previously identified SRPN6 as an immune component which restricts Plasmodium berghei development in the mosquito. Here we demonstrate that SRPN6 is differentially activated by bacteria in Anopheles stephensi, but only when bacteria exposure occurs on the lumenal surface of the midgut epithelium. Our data indicate that AsSRPN6 is strongly induced following exposure to Enterobacter cloacae, a common component of the mosquito midgut microbiota. We conclude that AsSRPN6 is a vital component of the E. cloacae-mediated immune response that restricts Plasmodium development in the mosquito An. stephensi.
Effects of Anti-Mosquito Salivary Glands and Deglycosylated Midgut Antibodies of Anopheles stephensi on Fecundity and Longevity
H Mohammadzadeh Hajipirloo,GhH Edrissian,M Nateghpour,H Basseri
Iranian Journal of Public Health , 2005,
Abstract: With the aim of controlling malaria by reducing vector population, the effects of antibodies produced against salivary glands and deglycosylated midgut antigens of Anopheles stephensi mosquitoes on fecundity and longevity of the same species were tested. Three deglycosylated preparations of midgut and two preparations of salivary glands were produced, conjugated with aluminum hydroxide gel, and subcutaneously injected to shoulders of TO (Turner Out-bred) mice. After 4 immunizations and assurance of enough antibody production against utilized antigenic suspensions, effects of blood feeding on immunized and control mice were assayed. Insoluble preparation of midgut showed the strongest effect with 23.5% reduction in egg laying, and increasing death rate of vectors in third day after feeding. No significant reduction in fecundity or survivorship was seen with other preparations. Anopheles midgut insoluble antigens are potential candidates for designing vaccines against malaria vectors and further investigations need to be done to find effective antigens and the best way of their use.
Mitochondrial NAD+-dependent malic enzyme from Anopheles stephensi: a possible novel target for malaria mosquito control
Jennifer Pon, Eleonora Napoli, Shirley Luckhart, Cecilia Giulivi
Malaria Journal , 2011, DOI: 10.1186/1475-2875-10-318
Abstract: To characterize the mitochondrial ME from immortalized ASE cells (Mos. 43; ASE), mass spectrometry analyses of trypsin fragments of ME, genomic sequence analysis and biochemical assays were performed to identify the enzyme and evaluate its activity in terms of cofactor dependency and inhibitor preference.The encoding gene sequence and primary sequences of several peptides from mitochondrial ME were found to be highly homologous to the mitochondrial ME from Anopheles gambiae (98%) and 59% homologous to the mitochondrial NADP+-dependent ME isoform from Homo sapiens. Measurements of ME activity in mosquito mitochondria isolated from ASE cells showed that (i) Vmax with NAD+ was 3-fold higher than that with NADP+, (ii) addition of Mg2+ or Mn2+ increased the Vmax by 9- to 21-fold, with Mn2+ 2.3-fold more effective than Mg2+, (iii) succinate and fumarate increased the activity by 2- and 5-fold, respectively, at sub-saturating concentrations of malate, (iv) among the analogs of L-malate tested as inhibitors of the NAD+-dependent ME catalyzed reaction, small (2- to 3-carbons) organic diacids carrying a 2-hydroxyl/keto group behaved as the most potent inhibitors of ME activity (e.g., oxaloacetate, tartronic acid and oxalate).The biochemical characterization of Anopheles stephensi ME is of critical relevance given its important role in bioenergetics, suggesting that it is a suitable target for insecticide development.Recently, several pathways for energy production have been identified in mitochondria from Anopheles stephensi [1], a well-studied Anopheles species in the investigation of malaria transmission [2]. The mitochondria-dependent energy pathways mainly use proline, pyruvate, α-glycerophosphate, and acyl-carnitine derivatives as suitable substrates. Proline is also the main substrate for flight metabolism in the tsetse fly [3], the mosquito Aedes aegypti [4] as well as other insects [5]. About 20% of the glutamate produced by proline oxidation is in turn oxidized by gl
Plasmodium yoelii-Infected A. stephensi Inefficiently Transmit Malaria Compared to Intravenous Route  [PDF]
Solomon Conteh,Rana Chattopadhyay,Charles Anderson,Stephen L. Hoffman
PLOS ONE , 2012, DOI: 10.1371/journal.pone.0008947
Abstract: It was recently reported that when mosquitoes infected with P. berghei sporozoites feed on mice, they deposit approximately 100–300 sporozoites in the dermis. When we inoculate P. yoelii (Py) sporozoites intravenously (IV) into BALB/c mice, the 50% infectious dose (ID50) is often less than 3 sporozoites, indicating that essentially all Py sporozoites in salivary glands are infectious. Thus, it should only take the bite of one infected mosquito to infect 100% of mice. In human subjects, it takes the bite of at least 5 P. falciparum-infected mosquitoes to achieve 100% blood stage infection. Exposure to 1–2 infected mosquitoes only leads to blood stage infection in approximately 50% of subjects. If mosquitoes carrying Py sporozoites inoculate 100–300 sporozoites per bite, and 1 to 2 mosquito bites achieve 50% blood stage infection rates, then this would suggest that the majority of sporozoites inoculated by mosquitoes into the dermis are not responsible for a productive infection, or that a significant number of sporozoite-infected mosquitoes do not inoculate any sporozoites. The objective of this study was to determine if this is the case. We therefore studied the infectivity to mice of the bites of 1, 2, 4, or 5–8 Py-infected mosquitoes. The bite of one Py sporozoite-infected mosquito caused blood stage infection in 41.4% (12/29) of mice, two bites infected 66.7% (22/33), four bites infected 75% (18/24), and five to eight bites infected 100% (21/21). These findings demonstrate that inoculation of sporozoites by mosquito bite is much less efficient than IV inoculation of Py sporozoites by needle and syringe. Such data may have implications for determining the best route and dose of administration to humans of our attenuated P. falciparum sporozoite vaccine, the scientific basis of which is immunity by bites from irradiated infected mosquitoes, and suggest that the challenge is to develop a method of administration that approximates IV inoculation, not one that mimics mosquito bite.
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