Peritrophic matrix formation and Brugia malayi microfilaria invasion of the midgut of a susceptible vector, Ochlerotatus togoi (Diptera: Culicidae)

Abstract

The mosquito midgut is the first site that vector-borne pathogens contact during their multiplication, differentiation, or migration from blood meal to other tissues before transmission. After blood feeding, the mosquitoes synthesize a chitinous structure called peritrophic matrix (PM) that envelops the blood meal and separates the food bolus from the midgut epithelium. In this study, a systematic investigation of the PM formation and the interaction of Brugia malayi within the midgut of a susceptible vector, Ochlerotatus togoi, were performed using scanning electron microscopy (SEM). SEM analysis of the midguts dissected at different time points post feeding on a B. malayi-infected blood meal (PIBM) revealed that the PM was formed from 45 min PIBM and gradually thickened and matured during 8-18 h PIBM. The PM degraded from 24 to 72 h PIBM, when digestion was completed. The invasion process of the microfilariae was observed between 3 and 4 h PIBM. In the beginning of the process, only sheathed microfilariae interacted with the internal face of the PM by its anterior part, and then the midgut epithelium before entering the hemocoel, after that they exsheathed. Microfilarial sheaths lying within the hemocoel were observed suggesting that they may serve as a decoy to induce the immune systems of the mosquitoes to respond to the antigens on the sheaths, thereby protecting the exsheathed microfilariae. These initial findings would lead to further study on the proteins, chemicals, and factors in the midgut that are involved in the susceptibility of O. togoi as a vector of filariasis.

Immune responses of Aedes togoi, Anopheles paraliae and Anopheles lesteri against nocturnally subperiodic Brugia malayi microfilariae during migration from the midgut to the site of development

“…aegypti (Black eye, Liverpool strain) but some sheathed mf reached the haemocoel and exsheathed there. However, our results contrast with some other studies that describe that mf exsheathed in the haemocoel [ 20 – 22 , 25 , 34 , 35 ]. Christensen & Sutherland [ 21 ] used in vitro midgut penetration techniques, light and electron microscopy to show that nearly all B .…”

“…paraliae . However, during 48–72 hours post-blood meal, all exsheathed microfilariae successfully migrated out of the midgut which supports the belief that PM does not serve as a physical barrier to nocturnally B. malayi in these three mosquito species and corresponds with previous studies [ 19 , 22 , 42 ]. Kato et al [ 42 ] used RNAi to knock-down chitin synthase and demonstrated that PM does not affect the development of B. pahangi or the dissemination of dengue virus as well as infectivity of Plasmodium gallinaceum in Ae .…”

“…The midgut is one of the first tissue barriers preventing pathogens from entering the body cavity. Numerous studies have suggested that the exsheathment of mf either occurred exclusively in the lumen of the midgut [ 17 – 19 ] or the haemocoel as well as the midgut lumen [ 20 – 22 ]. Likewise, the study by Chen & Shih [ 23 ] demonstrated that the exsheathment of B. pahangi microfilariae occurred in the lumen of midgut and haemocoel of susceptible and refractory strains of Aedes aegypti .…”

“…Likewise, the study by Chen & Shih [ 23 ] demonstrated that the exsheathment of B. pahangi microfilariae occurred in the lumen of midgut and haemocoel of susceptible and refractory strains of Aedes aegypti . Jariyapan et al [ 22 ] showed the exsheathment of NSP B . malayi microfilariae happens in the haemocoel of Ae.…”

An Investigation into the Protein Composition of the Teneral Glossina morsitans morsitans Peritrophic Matrix

“…This may be the critical time point of chitinase activity, thereby degrading the PM and allowing trypanosomes to break through. Other parasites like Brugia malayi , Leishmania spp and Plasmodium spp secrete chitinases and proteases to degrade the proteins within the chitin meshwork and allow penetration of the PM [78], [79], [80]. Although the quantity of chitin has yet to be measured in the G. m. morsitans PM, the lack of chitinase expression in trypanosomes suggests that the chitin content of the tsetse PM may be probably low as reported in Lucilia cuprina larvae (which also expresses a type II PM).…”