Proteolytic Enzyme Activity and Plasmodium falciparum Sporogonic Development in Three Species of Anopheles Mosquitoes

Abstract

If proteolytic enzymes affect the innate vector competence of Anopheles mosquitoes for Plasmodium infections, then mechanistic effects should be most pronounced at the zygote to ookinete developmental transition. Anopheles freeborni, Anopheles gambiae, and Anopheles albimanus exhibit excellent, good, and poor susceptibility to P. falciparum, respectively. Aminopeptidase and trypsin activity were determined relative to the kinetics of P. falciparum ookinete development in these 3 Anopheles species. Ookinetes in A. freeborni, A. gambiae, and A. albimanus were first observed at 18 hr postinfection. For separate infection experiments, peak parasite densities were observed at either 18, 24, or 30 hr for A. albimanus, at 24 or 30 hr for A. freeborni, and at either 24, 30, or 36 hr for A. gambiae. Although the 3 species supported ookinete development equally, they had significantly different oocyst infection rates. Similar patterns of aminopeptidase activity were observed for the most susceptible species, A. freeborni, and the least susceptible species, A. albimanus. Anopheles gambiae had the lowest levels of aminopeptidase. Anopheles freeborni also had higher levels of trypsin activity than either A. albimanus or A. gambiae. Irrespective of differences in innate vector competence, the 3 species showed peak levels of aminopeptidase and trypsin that were coincident with peak ookinete densities. Thus, the close correspondence between the kinetics of ookinetes and enzymes associated with bloodmeal digestion indicates that proteolytic enzymes alone do not limit the early stages of sporogonic development in vector species of Anopheles.