Penetration of the mosquito midgut wall by the ookinetes ofPlasmodium yoelii nigeriensis

Syafruddin, Syafruddin; Arakawa, Ryo; Kamimura, Kiyoshi; Kawamoto, Fumihiko

doi:10.1007/bf00930863

Cited by 24 publications

(18 citation statements)

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“…In previous TEM studies of midgut invasion by the human malaria parasite P. falciparum as well as other malaria parasites, the ookinetes were found both within and between midgut cells (3)(4)(5)(6)(7)(8). It has been proposed that the ookinete leaves the midgut cell after invasion and continues its migration intercellularly toward the basement membrane (8).…”

Section: Discussionmentioning

confidence: 99%

“…contrast, ookinetes within midgut cells are clearly free in the cytoplasm (3,4,7,8,26). The lack of a PV in ookinete invasion may explain the lack of rhoptry structures in ookinetes (4,(47)(48)(49)(50); rhoptries are associated with PV formation (51).…”

Section: Discussionmentioning

confidence: 99%

“…Before it can develop into an oocyst, however, the ookinete must escape from the blood meal and traverse the midgut epithelium to reach the midgut's basement membrane (1). Although several studies by light and transmission electron microscopy (TEM) have been directed at the ookinete's invasion of midgut cells (2)(3)(4)(5)(6)(7)(8), none have succeeded in producing a mechanistic description of the invasion process.…”

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confidence: 99%

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Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells

Zieler

Dvorak

2000

Proc. Natl. Acad. Sci. U.S.A.

137

126

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Using an in vitro culture system, we observed the migration of malaria ookinetes on the surface of the mosquito midgut and invasion of the midgut epithelium. Ookinetes display constrictions during migration to the midgut surface and a gliding motion once on the luminal midgut surface. Invasion of a midgut cell always occurs at its lateral apical surface. Invasion is rapid and is often followed by invasion of a neighboring midgut cell by the ookinete. The morphology of the invaded cells changes dramatically after invasion, and invaded cells die rapidly. Midgut cell death is accompanied by activation of a caspase-3-like protease, suggesting cell death is apoptotic. The events occurring during invasion were identical for two different species of Plasmodium and two different genera of mosquitoes; they probably represent a universal mechanism of mosquito midgut penetration by the malaria parasite.T he transmission of malaria to a new vertebrate host depends on the successful passage of the malaria ookinete through the mosquito midgut, transformation to an oocyst on the external midgut wall, and the multiplication and migration of sporozoites into the lumen of the insect's salivary gland. After ingestion by its vector mosquito in a blood meal taken from an infected vertebrate host, male and female gametes form a zygote, which transforms into an ookinete in the lumen of the midgut. Before it can develop into an oocyst, however, the ookinete must escape from the blood meal and traverse the midgut epithelium to reach the midgut's basement membrane (1). Although several studies by light and transmission electron microscopy (TEM) have been directed at the ookinete's invasion of midgut cells (2-8), none have succeeded in producing a mechanistic description of the invasion process.The development in the past of methods to culture various stages of Plasmodium or to observe their behavior in vitro has been of great importance in our ability to study the malaria parasite (9-15). With this history in mind, we developed an in vitro system to observe ookinete migration on the mosquito midgut surface and penetration of midgut cells. We here report the mechanism and kinetics of midgut cell invasion by the malaria ookinete. Materials and MethodsParasite and Mosquito Cultivation. The 8A strain of the avian malaria parasite Plasmodium gallinaceum and the Liverpool͞ black eye strain of Aedes aegypti were used throughout this study. Parasites were maintained in white Leghorn chickens by serial blood passages. In addition, a standard laboratory strain of Anopheles stephensi was used, as well as the ANKA strain of Plasmodium berghei, which was maintained in BALB͞c mice by serial blood passages. Mosquitoes were raised and fed by using standard techniques (16, 17).Invasion Assay. The midgut was removed from bloodfed A. aegypti mosquitoes and was cut longitudinally into two halves (18). The midgut epithelia were cleaned of the blood meal and gently spread out on a glass slide in M199 medium supplemented with 2 mM L-glutamine͞100 units͞ml peni...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells

Zieler

Dvorak

2000

Proc. Natl. Acad. Sci. U.S.A.

137

126

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“…There are conflicting reports about whether the ookinete migrates to the basal lamina through or between epithelial cells. For some parasites species, ookinetes have been observed both inter-and intracellularly (Syafruddin et al, 1991;Torii et al, 1992). Ookinetes of Plasmodium falciparum have been found in intercellular space and those of Plasmodium berghei within epithelial cells of the same vector, An.…”

Section: Midgut Epitheliummentioning

confidence: 99%

Molecular approaches to mosquito parasite interactions

Zheng

1997

Arch. Insect Biochem. Physiol.

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“…The ultrastructure of ookinetes within the mosquito midgut epithelium has been studied (4)(5)(6)(7). In these experiments, only a few parasites were observed because invasion and transit across the epithelial cells are asynchronous.…”

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Plasmodium gallinaceum preferentially invades vesicular ATPase-expressing cells in Aedes aegypti midgut

Shahabuddin

Pimenta

1998

Proc. Natl. Acad. Sci. U.S.A.

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Penetration of the mosquito midgut epithelium is obligatory for the further development of Plasmodium parasites. Therefore, blocking the parasite from invading the midgut wall disrupts the transmission of malaria. Despite such a pivotal role in malaria transmission, the cellular and molecular interactions that occur during the invasion are not understood. Here, we demonstrate that the ookinetes of Plasmodium gallinaceum, which is related closely to the human malaria parasite Plasmodium falciparum, selectively invade a cell type in the Aedes aegypti midgut. These cells, unlike the majority of the cells in the midgut, do not stain with a basophilic dye (toluidine blue) and are less osmiophilic. In addition, they contain minimal endoplasmic reticulum, lack secretory granules, and have few microvilli. Instead, these cells are highly vacuolated and express large amounts of vesicular ATPase. The enzyme is associated with the apical plasma membrane, cytoplasmic vesicles, and tubular extensions of the basal membrane of the invaded cells. The high cost of insecticide use in endemic areas and the emergence of drug resistant malaria parasites call for alternative approaches such as modifying the mosquito to block the transmission of malaria. One of the targets for such modification is the parasite receptor on midgut cells. A step toward the identification of this receptor is the realization that malaria parasites invade a special cell type in the mosquito midgut. This is the centennial of the discovery in 1897 by Ronald Ross that mosquitoes transmit malaria (1). In the 1890s, fertilization of malaria parasites to form zygotes, the first step of Plasmodium development in the mosquito, also was discovered. Zygotes develop into ookinetes within the midgut and penetrate the peritrophic matrix and the midgut epithelium. In the hemolymph, parasites develop as oocysts between the midgut epithelium and basal lamina. Sporozoites develop during the hemolymph stage and penetrate the salivary glands to be injected into the human during blood feeding (2, 3). One of the most crucial aspects of the sporogonic development of malaria parasites is the crossing of the mosquito midgut epithelium by the ookinetes. The ookinetes that fail to penetrate the midgut epithelium die in the gut lumen. Blocking ookinete penetration of mosquito midgut epithelium, therefore, is a potential strategy to block malaria transmission. To exploit this invasion process, however, a better understanding of ookinete interaction with the midgut is necessary. The molecular aspects of this penetration process currently are not known.The ultrastructure of ookinetes within the mosquito midgut epithelium has been studied (4-7). In these experiments, only a few parasites were observed because invasion and transit across the epithelial cells are asynchronous. To examine the invasion process more extensively, we have developed an in vitro invasion assay. This assay, along with an in vivo procedure, has allowed us to examine a large number of invaded cells and has pr...

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Penetration of the mosquito midgut wall by the ookinetes ofPlasmodium yoelii nigeriensis

Cited by 24 publications

References 10 publications

Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells

Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells

Molecular approaches to mosquito parasite interactions

Plasmodium gallinaceum preferentially invades vesicular ATPase-expressing cells in Aedes aegypti midgut

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