Noninfectious sporozoites in the salivary glands of a minimally susceptible anopheline mosquito

Abstract

In studies to evaluate vector-malaria parasite relationships, we have found that Anopheles albimanus is minimally susceptible to the rodent malaria parasite Plasmodium yoelii. Normally, less than 10% of A. albimanus develop oocyst infections compared to 80-100% for Anopheles stephensi and Anopheles freeborni mosquitoes. Although sporozoites produced in A. albimanus invade the salivary glands, they are not infectious to BALB/c or ICR mice. In 11 experiments with sporozoites from A. albimanus, intravenous inoculations of up to 24,000 sporozoites in individual mice failed to produce host infections. In contrast, inoculation of 300 sporozoites obtained from the salivary glands of A. stephensi and A. freeborni always infected mice. The noninfectious sporozoites from A. albimanus were morphologically similar to the infectious sporozoites from A. stephensi and yielded 4+ circumsporozoite precipitin reactions when incubated with a monoclonal antibody against the circumsporozoite protein of P. yoelii. The presence of noninfectious sporozoites in the salivary glands of A. albimanus suggests that this minimally susceptible vector either possesses a toxic factor that abolishes sporozoite infectiousness or lacks a critical substance needed by the sporozoite to become infectious. Sporozoite infectiousness was neither attenuated by incubation of infectious sporozoites with A. albimanus salivary glands nor restored when noninfectious sporozoites were incubated with A. stephensi salivary glands. These studies provide a starling point for defining the biological basis of sporozoite infectivity.