Interaction of Plasmodium gallinaceum ookinetes and oocysts with extracellular matrix proteins

Abstract

Plasmodium ookinetes are elongate, motile and invasive while inside the mosquito gut but promptly metamorphose into spherical immobile oocysts upon coming in contact with the basement membrane surrounding the midgut. There they begin a prolonged growth period characterized by massive DNA synthesis for the production of sporozoites. Living Plasmodium gallinaceum ookinetes attached avidly to the murine extracellular matrix proteins, laminin and collagen type IV. In ELISA-type assays, the main ookinete surface protein, Pgs28 was implicated as a mediator of parasite attachment to these basement membrane constituents. Laminin and collagen IV adhered to ookinete and oocyst lysates spotted onto nitrocellulose membranes. Receptor-ligand blot assays demonstrated that Pgs28 and an oocyst-specific antigen recognized by the mAb 10D6 interact with murine collagen IV and laminin. 10D6 antigen was also recognized by monospecific antiserum against the human epidermal growth factor receptor. Mosquito-derived laminin was incorporated into oocyst capsules of P. gallinaceum growing in Aedes aegypti. We hypothesize that contact with the mosquito basement membrane triggers the transformation of ookinetes into oocysts. Coalescence of basement membrane proteins onto the capsules masks developing oocysts from the mosquito's immune system and facilitates their prolonged extracellular development in the mosquito body cavity.

Functional Characterization of Anopheles Matrix Metalloprotease 1 Reveals Its Agonistic Role during Sporogonic Development of Malaria Parasites

“…Interaction of AgMMP1 with the growing oocyst can be direct, as in the case of laminin, which associates with the parasite at this developmental stage (67)(68)(69), or indirect through proteins of the extracellular matrix (70,71). Since AgMMP1 was not detected on the basal side of the epithelium (Fig.…”

Design and Activity of Antimicrobial Peptides against Sporogonic-Stage Parasites Causing Murine Malarias

“…Second, the activity of the peptide against oocysts was an unexpected bonus. Oocysts developing beneath the midgut basal lamina are thought to be in a privileged site and protected from the hemolymph antimicrobial peptides by a capsule composed, in part, of components of the basal lamina (1). Unlike the midgut and sporozoite stages, little parasite death occurs naturally at this stage (37,38).…”

Laminin and the malaria parasite's journey through the mosquito midgut

“…Several ookinete surface molecules, such as P25 and P28 (Siden-Kiamos et al, 2000), SOAP (secreted ookinete adhesive protein; Dessens et al, 2003) and CTRP (circumsporozoite protein and thrombospondin-related adhesive protein; Dessens et al, 1999), have been implicated in the process of midgut invasion but, to date, no putative receptor has been identified or proposed on the midgut epithelium. Direct or indirect binding to Plasmodium surface proteins has only been demonstrated for laminin (Vlachou et al, 2001;Arrighi and Hurd, 2002;Dessens et al, 2003;Adini and Warburg, 1999) and collagen IV (Arrighi and Hurd, 2002;Adini and Warburg, 1999), both components of all vertebrate (Miosge, 2001) and invertebrate (Hynes and Zhao, 2000) basal laminae, including the one surrounding the insect midgut on its haemocoel side.…”