The Role of the Mosquito Peritrophic Membrane in Bloodmeal Digestion and Infectivity of Plasmodium Species

Abstract

Secretion and luminal formation of the peritrophic membrane (PM) were induced in female Anopheles stephensi and Aedes aegypti by feeding the mosquitoes on a warmed suspension of latex particles in Ringer's solution. The PM in A. stephensi was produced from apical secretion vesicles stored in the midgut epithelial cells and secreted into the lumen during feeding. In A. aegypti, the PM was formed de novo. When the latex feeding was followed 24 hr later by a meal of lyophilized pig blood, the 2 mosquito species exhibited very different modifications to their PM structure; in A. stephensi no PM was formed around the blood meal, whereas de novo synthesis of the PM in A. aegypti continued during the blood meal, with the resulting PM greatly thickened compared to the normal feeding. This artificial induction of PM formation was used as the basis to study the role of the PM in blood meal digestion and in infectivity of mosquitoes by the appropriate species of Plasmodium. The feeding of a latex suspension alone had no stimulatory effect on the 2 major midgut proteases, trypsin and aminopeptidase, in either species. After a blood meal alone, proteases rose to maximum activity at 30 hr and 24 hr after feeding in A. stephensi and A. aegypti, respectively. After double feeding, protease activities in both species were almost identical to those in blood-fed mosquitoes. Neither the absence of a PM (in A. stephensi) nor the presence of a thickened PM (in A. aegypti), therefore, has any effect on the ability of mosquitoes to digest a blood meal. Malaria infectivity, measured by oocyst counts, also was compared after normal and double feeding using infective blood meals. Infectivity of A. stephensi by Plasmodium berghei was unaffected by the presence or absence of the PM. The thickened PM produced by double feeding in A. aegypti caused a reduction of midgut infectivity by Plasmodium gallinaceum. These results suggest that the PM may act as a partial, but not an absolute, barrier to invasion of the midgut by the ookinete.

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

“…5). As noted previously (Billingsley and Rudin, 1992), the number of apical vesicles drops dramatically within the first 15 min of feeding ( Fig. 4C and D), indicating the release of stored molecules.…”

The early sporogonic cycle of Plasmodium falciparum in laboratory‐infected Anopheles gambiae: an estimation of parasite efficacy

“…These mechanisms are more or less important according to host immune state and might explain the extreme heterogeneity among gametocyte carriers (Mulder et al 1994). The low digestion speed and the destructive action of digestive enzymes on immature stages of the malaria parasite might also explain part of the observed parasite loss (Gass 1977;Ponnudurai et al 1988;Billingsley & Rudin 1992).…”

“…Host immune factors probably lose their effect after the ookinete migration through the midgut wall. It is established that the penetration of the peritrophic matrix and the midgut wall by the ookinete constitutes a rate-limiting step which can lead to the ookinete deterioration (Feldmann et al 1990;Billingsley & Rudin 1992;Medley et al 1992;Shahabuddin et al 1993). The intensity of inflammatory reactions in the midgut wall probably reduced the OOK/OOC2 density by blocking the crossing of numerous OOK through the midgut wall.…”

Dengue-2 Virus Artificial Infection of Brazilian Colonized Aedes Aegypti

“…Then, they were allowed to feed through a chick-skin membrane in a glass feeder apparatus heated by circulating water at 37ºC during 1 hour (Rutledge et al 1964, Billingsley & Rudin 1992. The infected blood meal was constituted of two-thirds of heat-inactivated heparinized mouse blood mixed with onethird of virus-infected C6/36 cells and adenosine triphosphate as a phagostimulant.…”