Plasmodium Oocysts: Overlooked Targets of Mosquito Immunity

Smith, R. V.; Barillas‐Mury, Carolina

doi:10.1016/j.pt.2016.08.012

Cited by 54 publications

(69 citation statements)

References 97 publications

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“…We also examined the temporal nature of an additional feeding, where mosquitoes infected with either P. berghei or P. falciparum received an additional blood-meal eight days post-infection (Figure 1F), a time in which developing oocysts have initiated sporogony (Smith and Barillas-Mury, 2016). At this stage of oocyst development, an additional blood meal does not influence P. berghei (Figure 1G) or P. falciparum (Figure 1H) oocyst numbers, which suggests there is a temporal component that determines P. berghei losses.…”

Section: Resultsmentioning

confidence: 99%

“…Plasmodium oocysts develop in the space between the midgut epithelium and the midgut basal lamina (Smith and Barillas-Mury, 2016), providing protection from the cellular or humoral components of the mosquito immune system. To examine if an additional blood- or protein-meal could influence the integrity of the basal lamina, we utilized a collagen hybridizing peptide (CHP) that specifically binds unfolded collagen chains, to serve as an indicator of tissue damage (Hwang et al, 2017).…”

Section: Resultsmentioning

confidence: 99%

“…This may be due to differences in immune detection, or alternatively, mature oocysts may have reached a stage of development in which they become immune privileged. There is support for the former due to the turnover of oocyst capsule proteins at the onset of sporogony (Smith and Barillas-Mury, 2016), which could potentially remove protein(s) involved in mosquito complement recognition of developing oocysts.…”

Section: Discussionmentioning

confidence: 99%

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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: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

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

Self Cite

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show abstract

“…A possible explanation is that the majority of the immune response factors that have been described belong to the early innate immunity response that takes place between 2-24h post-infection, at the ookinete stage, where the most part of the parasite recognition and killing occur [44,45]. The samples analyzed in this study correspond to the oocyst stage, approximately six and seven days after an infective blood feeding, and the immune factors playing a role at this stage still remain poorly characterized [46].…”

Section: Discussionmentioning

confidence: 99%

Chromatin changes in Anopheles gambiae induced by a Plasmodium falciparum infection

Ruiz

Yerbanga

Lefèvre

et al. 2018

Preprint

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Infection by the human malaria parasite leads to important changes in phenotypic traits related to vector competence. However, we still lack a clear understanding of the underlying mechanisms and in particular, of the epigenetic basis for these changes. We have examined genome-wide distribution maps of H3K27ac, H3K9ac, H3K9me3 and H3K4me3 by ChIP-seq and the transcriptome by RNA-seq, of midguts from Anopheles gambiae mosquitoes infected by the human malaria parasite Plasmodium falciparum. We report 15,916 regions containing differential histone modification enrichment, of which 8,339 locate at promoters and/or intersect with genes. The functional annotation of these regions allowed us to identify infection responsive genes showing differential enrichment in various histone modifications such as CLIP proteases, anti-microbial peptides encoding genes and genes related to melanization responses and the complement system. Further, the motif analysis of differential histone enriched regions predicts binding sites that might be involved in the cis-regulation of this regions such as Deaf1, Pangolin and Dorsal transcription factors (TFs). Some of these TFs are known to regulate immunity gene expression in Drosophila and are involved in the Notch and JAK/STAT signaling pathways. The analysis of malaria infection-induced chromatin changes in mosquitoes is important not only to identify regulatory elements and genes underlying mosquito responses to a malaria infection but also for possible applications to the genetic manipulation of mosquitoes and extension to other mosquito-borne systems.fications of histones (hPTMs) impact the structure and/or function of chromatin, with different histone marks yielding distinct functional consequences [13]. For example, in Drosophila, as in other organisms, H3K27ac, H3K9ac and H3K4me3 are linked to gene activation and localize at promoters, whereas H3K9me3 is associated with silencing and occupies broader regions [14]. Various combinations of active and repressive histone modifications define chromatin states that are linked to gene function [15][16][17]. These modifications can remain, leaving a record of gene activity, i.e. epigenetic memory, that affect or prime the transcriptional response later in life [12,[18][19][20][21][22][23][24]. In mosquitoes, despite their relevance for human health, there is very little knowledge on chromatin regulation and its link to mosquito immunity, physiology and behavior [25]. In a previous study, we characterized genome-wide occupancy patterns of various histone modifications and established a link between hPTMs and gene expression profiles in midguts and salivary glands of the human malaria vector A. gambiae [26]. In addition, recent reports reveal the role of various transcription factors such as REL2, lola and Deaf1, in A. gambiae immune defenses [27, 28]. These findings have set the stage for additional studies aimed at understanding how the chromatin landscape is altered in P. falciparum infected mosquito tissues and which are the molecular pla...

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“…Studies have shown exquisite susceptibility of motile ookinete stage parasites to complement-like proteins produced by the mosquito innate immune cells (Molina-Cruz et al, 2015; Ramphul et al, 2015). Oocysts are likewise also vulnerable to mosquito defense mechanism (Smith and Barillas-Mury, 2016). …”

Section: Discussionmentioning

confidence: 99%

Modulation of transmission success of Plasmodium falciparum gametocytes (sexual stages) in various species of Anopheles by erythrocytic asexual stage parasites

Kumar

2017

Acta Tropica

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During malaria infection, a small proportion of erythrocytic asexual stages undergo sexual differentiation. Male and female gametocytes ingested in the blood meal initiate the sexual development of malaria parasites in the mosquito midgut. During blood feeding on a host, a mosquito ingests, in addition to mature gametocytes, host immune factors present in the blood, as well as large excess of erythrocytic asexual stages. In the current study we addressed the impact of the presence of large excess of asexual stages, hitherto not known or even suspected to influence, on the infectivity of gametocytes in the mosquito. Asexual stages resulted in a dose-dependent inhibition of infectiousness of gametocytes, and some of this could be explained by the presumed effect of hemozoin and other unknown asexual-stage components on the mosquito immune system, affecting survival and maturation of parasites in the mosquito midgut. Interactions between asexual and sexual stages, maturity and ratio of male and female gametocytes, host immune factors and mosquito innate immune factors are some of the variables that determine the infectiousness of gametocytes in the mosquitoes and ultimately malaria transmission success. Understanding of determinants affecting malaria transmission will be critical to approaches directly targeting the transmission process for malaria elimination.

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Plasmodium Oocysts: Overlooked Targets of Mosquito Immunity

Cited by 54 publications

References 97 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

Chromatin changes in Anopheles gambiae induced by a Plasmodium falciparum infection

Modulation of transmission success of Plasmodium falciparum gametocytes (sexual stages) in various species of Anopheles by erythrocytic asexual stage parasites

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