The Journey of Malaria Sporozoites in the Mosquito Salivary Gland

Abstract

The life cycle of malaria parasites in the mosquito vector is completed when the sporozoites infect the salivary gland and are ready to be injected into the vertebrate host. This paper describes the fine structure of the invasive process of mosquito salivary glands by malaria parasites. Plasmodium gallinaceum sporozoites start the invasion process by attaching to and crossing the basal lamina and then penetrating the host plasma membrane of the salivary cells. The penetration process appears to involve the formation of membrane junctions. Once inside the host cells, the sporozoites are seen within vacuoles attached by their anterior end to the vacuolar membrane. Mitochondria surround, and are closely associated with, the invading sporozoites. After the disruption of the membrane vacuole, the parasites traverse the cytoplasm, attach to, and invade the secretory cavity through the apical plasma membrane of the cells. Inside the secretory cavity, sporozoites are seen again inside vacuoles. Upon escaping from these vacuoles, sporozoites are positioned in parallel arrays forming large bundles attached by multilammelar membrane junctions. Several sporozoites are seen around and inside the secretory duct. Except for the penetration of the chitinous salivary duct, our observations have morphologically characterized the entire process of sporozoite passage through the salivary gland.

Anopheles stephensi salivary glands bear receptors for region I of the circumsporozoite protein of Plasmodium falciparum

“…A recent electron microscopic study demonstrates that salivary gland invasion by sporozoites is a multistep process involving sequential interac tions with the basal lamina and the plasma membrane of the target cell [20]. The first event in invasion is the adhesion of the sporozoite to the target cell.…”

Anopheles gambiae salivary gland proteins as putative targets for blocking transmission of malaria parasites

“…Ultrastructural studies have shown that sporozoites invading salivary glands may encounter one receptor at the basal lamina of the salivary glands and another at the plasma membrane of the secretory cells (15). Other studies have indicated that the salivary gland components are highly glycosylated (2) and that specific lectins can inhibit sporozoite invasion of the salivary glands (3).…”

“…The sporozoites recognize the female-specific lobes of the salivary glands (14,15). Both the 29-kDa and 100-kDa salivary gland proteins are expressed on these lobes and fit the logical parameters we considered for a putative salivary gland receptor for sporozoites.…”

Transgenic Plasmodium berghei sporozoites expressing β-galactosidase for quantification of sporozoite transmission

“…Although sporozoites are likely passively transported throughout the hemocoel, there is evidence that they specifically recognize the salivary glands through a receptor-mediated process [4][5][6][7]. Sporozoites breach the basal lamina and acinar gland cells and accumulate in the salivary duct [8]. When the infected mosquito takes another blood-meal, salivary gland sporozoites are injected into the avascular portion of the skin [9,10] where they start vigorous gliding locomotion in search of a capillary [11,12].…”