A chemotactic response facilitates mosquito salivary gland infection by malaria sporozoites

Abstract

SUMMARY Sporozoite invasion of mosquito salivary glands is critical for malaria transmission to vertebrate hosts. After release into the mosquito hemocoel,the means by which malaria sporozoites locate the salivary glands is unknown. We developed a Matrigel-based in vitro system to observe and analyze the motility of GFP-expressing Plasmodium berghei sporozoites in the presence of salivary gland products of Anopheles stephensi mosquitoes using temperature-controlled, low-light-level video microscopy. Sporozoites moved toward unheated salivary gland homogenate (SGH) but not to SGH that had been heated at 56°C for 30 min. We also investigated the origin of the attracted population. Attraction to SGH was restricted to hemolymph- and oocyst-derived sporozoites; salivary gland-derived sporozoites were not attracted to SGH. These data imply that sporozoites employ a chemotactic response to high molecular mass proteins or carbohydrate-binding proteins to locate salivary glands. This raises the possibility of utilizing anti-chemotactic factors for the development of mosquito transmission blocking agents.

Evidence That a Laminin-Like Insect Protein Mediates Early Events in the Interaction of a Phytoparasite with Its Vector's Salivary Gland

“…The hemolymph bathes all other insect organs besides the salivary glands, so the presence of specific surface receptors at the external face of salivary glands could be considered a target for Phytomonas species, which ultimately attach to and invade that organ [6], [7]. Correspondingly, malaria parasites locate mosquito salivary glands by chemotaxis, suggesting the possibility that chemical component(s) can be identified and synthesized to block or suppress mosquito salivary gland invasion as a malaria transmission blocking strategy [66]. It is noteworthy to mention that laminin-binding proteins have been found on the surface of a variety of pathogens, including the protozoan parasites L. donovani [21], [67], [68], T. cruzi [19], [69], Plasmodium [16], [24], [70], and Trichomonas [71], [72]; fungi, such as Candida albicans [73]–[75], Histoplasma capsulatum [76], and Paracoccidioides [77], as well as bacteria, like Staphylococcus [78], Streptococcus [78], [79], and Mycobacterium leprae [80], [81].…”

Active migration and passive transport of malaria parasites

“…Sporozoites develop in oocysts in the mosquito midgut wall, and must exit into the hemocoel and go to the salivary gland. In the hemocoel, sporozoites are passively transported by the movement of the mosquito hemolymph and, although they are carried throughout the open circulatory system of the mosquito, they appear to preferentially recognize and invade salivary glands [16,32,[45][46][47][48]. Similarly to the sporozoites that make it into the bloodstream, the parasites in the hemolymph have the capacity to actively migrate but do not do so in the open circulation of the mosquito.…”

Expression Profiling of Plasmodium berghei HSP70 Genes for Generation of Bright Red Fluorescent Parasites

“…6A). This finding prompted us to explore whether we could image individual sporozoites in whole mosquitoes, as previously achieved with transgenic parasites that express GFP or mCherry under the control of the circumsporozoite protein ( CSP ) promoter [35], [36]. Intriguingly, we could readily capture individual bright red fluorescent hemocoel sporozoites in wing veins and the maxillary palps of infected mosquitoes (Fig.…”