Experiments upon the feeding of <i>Aëdes aegypti</i> through animal membranes with a view to applying this method to the chemotherapy of malaria

Bishop, Ann; Gilchrist, Barbara M.

doi:10.1017/s0031182000013202

Cited by 66 publications

(25 citation statements)

References 17 publications

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“…In an early study, infected mosquitoes fed on medium through a membrane and sporozoites were collected from the medium after the feeding but no attempt was made to count the sporozoites delivered (7). Subsequent studies counted sporozoites released by mosquitoes into fluid-filled capillary tubes or through membranes into fluid-filled vessels (4,5,14,19) or onto a glass slide (12).…”

Section: Discussionmentioning

confidence: 99%

Direct Microscopic Quantification of Dynamics of Plasmodium berghei Sporozoite Transmission from Mosquitoes to Mice

2007

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The number of malaria sporozoites delivered to a host by mosquitoes is thought to have a significant influence on the subsequent course of the infection in the mammalian host. We did studies with Anopheles stephensi mosquitoes with salivary gland infections of Plasmodium berghei sporozoites expressing a red fluorescent protein. After individual mosquitoes fed on an ear pinna or the ventral abdomen of a mouse, fluorescence microscopy was used to count numbers of sporozoites. Mosquitoes allowed to feed on the ear for periods of 3 versus 15 min deposited means of 281 versus 452 sporozoites, respectively, into the skin; this may have epidemiological implications because mosquitoes can feed for longer periods of time on sleeping hosts. Mosquitoes feeding on the ventral abdomen injected sporozoites not only into the skin but also into the underlying peritoneal musculature. Although mosquitoes injected fewer sporozoites into the abdominal tissues, more of these were reingested into the mosquito midgut, probably a consequence of easier access to blood intake from the abdominal area. The most consistent parameter of sporozoite transmission dynamics under all conditions of mosquito probing and feeding was the relatively slow release rate of sporozoites (ϳ1 to 2.5 per second) from the mosquito proboscis. The numbers of sporozoites introduced into the host by mosquitoes and the transmission efficiencies of sporozoite delivery are multifactorial phenomena that vary with length of probing time, skin site being fed upon, and numbers of sporozoites within the salivary glands. Malaria infection is initiated by anAnopheles stephensi mosquito injecting sporozoites into the skin of its mammalian host while probing for a blood meal (1,15,16,21,25,28). Continuation of the malaria infection depends upon these sporozoites leaving the skin via dermal blood vessels and then traveling to the liver and developing into exoerythrocytic forms (EEF). The relatively large number of studies attempting to quantify the dynamics of this process attests to the importance with which it has been viewed by malariologists; the history and rationale for such attempts have been reviewed previously (6,24,26). The approaches used have included assessment of numbers of sporozoites released by mosquitoes into liquid media (reviewed in reference 6) or onto glass slides (12), counting of EEF after mosquito feeding on rodent hosts (26), and determination of sporozoite 18S rRNA (16) or ␤-galactosidase expressed by transgenic sporozoites (8) within the skin of a mouse after sporozoite introduction by mosquitoes.Each of these approaches has had both advantages and limitations. We believe that the most biologically appropriate approach requires direct feeding of infected mosquitoes on a living host and that the most accurate and precise means of quantification is direct microscopic observation and counting of injected sporozoites. Aside from the unequivocal nature of direct counts of morphologically recognizable sporozoites, this method allows correlation of specifi...

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Section: Discussionmentioning

confidence: 99%

Direct Microscopic Quantification of Dynamics of Plasmodium berghei Sporozoite Transmission from Mosquitoes to Mice

2007

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“…For SMFAs, mature gametocytes of WT NF54 and the 7-Helix-1-KO line 2E6, which were positively tested for exflagellation activity, were enriched and the parasitemia was adjusted to 0.25% by the addition of human erythrocytes in A+ serum. The mosquitoes were allowed to feed on the cell suspension via glass feeders for 20 min [93]. For ookinete quantification, samples of the midgut were prepared at 24 h p.i.…”

Section: Methodsmentioning

confidence: 99%

A seven-helix protein constitutes stress granules crucial for regulating translation during human-to-mosquito transmission of Plasmodium falciparum

et al. 2018

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The complex life-cycle of the human malaria parasite Plasmodium falciparum requires a high degree of tight coordination allowing the parasite to adapt to changing environments. One of the major challenges for the parasite is the human-to-mosquito transmission, which starts with the differentiation of blood stage parasites into the transmissible gametocytes, followed by the rapid conversion of the gametocytes into gametes, once they are taken up by the blood-feeding Anopheles vector. In order to pre-adapt to this change of host, the gametocytes store transcripts in stress granules that encode proteins needed for parasite development in the mosquito. Here we report on a novel stress granule component, the seven-helix protein 7-Helix-1. The protein, a homolog of the human stress response regulator LanC-like 2, accumulates in stress granules of female gametocytes and interacts with ribonucleoproteins, such as CITH, DOZI, and PABP1. Malaria parasites lacking 7-Helix-1 are significantly impaired in female gametogenesis and thus transmission to the mosquito. Lack of 7-Helix-1 further leads to a deregulation of components required for protein synthesis. Consistently, inhibitors of translation could mimic the 7-Helix-1 loss-of-function phenotype. 7-Helix-1 forms a complex with the RNA-binding protein Puf2, a translational regulator of the female-specific antigen Pfs25, as well as with pfs25-coding mRNA. In accord, gametocytes deficient of 7-Helix-1 exhibit impaired Pfs25 synthesis. Our data demonstrate that 7-Helix-1 constitutes stress granules crucial for regulating the synthesis of proteins needed for life-cycle progression of Plasmodium in the mosquito vector.

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“…To investigate transmission stages in the mosquito midgut, mature gametocyte cultures were mixed with packed uninfected erythrocytes and centrifuged. The supernatant was replaced by normal human serum, mixed and membrane fed to Anopheles stephensi mosquitoes [56]. The mosquitoes were allowed to gorge for 5 min.…”

Section: Methodsmentioning

confidence: 99%

Malaria parasites form filamentous cell-to-cell connections during reproduction in the mosquito midgut

et al. 2010

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Physical contact is important for the interaction between animal cells, but can represent a major challenge for protists like malaria parasites. Recently, novel filamentous cell-cell contacts have been identified in different types of eukaryotic cells and termed nanotubes due to their morphological appearance. Nanotubes represent small dynamic membranous extensions that consist of F-actin and are considered an ancient feature evolved by eukaryotic cells to establish contact for communication. We here describe similar tubular structures in the malaria pathogen Plasmodium falciparum, which emerge from the surfaces of the forming gametes upon gametocyte activation in the mosquito midgut. The filaments can exhibit a length of more than 100 µm and contain the F-actin isoform actin 2. They actively form within a few minutes after gametocyte activation and persist until the zygote transforms into the ookinete. The filaments originate from the parasite plasma membrane, are close-ended and express adhesion proteins on their surfaces that are typically found in gametes, like Pfs230, Pfs48/45 or Pfs25, but not the zygote surface protein Pfs28. We show that these tubular structures represent long-distance cell-to-cell connections between sexual stage parasites and demonstrate that they meet the characteristics of nanotubes. We propose that malaria parasites utilize these adhesive “nanotubes” in order to facilitate intercellular contact between gametes during reproduction in the mosquito midgut.

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Experiments upon the feeding of Aëdes aegypti through animal membranes with a view to applying this method to the chemotherapy of malaria

Cited by 66 publications

References 17 publications

Direct Microscopic Quantification of Dynamics of Plasmodium berghei Sporozoite Transmission from Mosquitoes to Mice

Direct Microscopic Quantification of Dynamics of Plasmodium berghei Sporozoite Transmission from Mosquitoes to Mice

A seven-helix protein constitutes stress granules crucial for regulating translation during human-to-mosquito transmission of Plasmodium falciparum

Malaria parasites form filamentous cell-to-cell connections during reproduction in the mosquito midgut

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