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The Journal of Experimental Biology 204, 2773-2780 (2001)
© 2001 The Company of Biologists Limited

MALARIA-INDUCED APOPTOSIS IN MOSQUITO OVARIES : A MECHANISM TO CONTROL VECTOR EGG PRODUCTION

JANE A. HOPWOOD1,2, ASHRAF M. AHMED1, ANTHONY POLWART3, GWYN T. WILLIAMS3 and HILARY HURD1,*

1 Centre for Applied Entomology and Parasitology, Keele University, Staffordshire ST5 5BG, UK
2 School of Biological Sciences, University of Manchester, 2.205 Stopford Building, Oxford Road, Manchester M13 9PT, UK
3 School of Life Sciences, Keele University, Staffordshire ST5 5BG, UK
* Author for correspondence (e-mail: h.hurd{at}keele.ac.uk )

Accepted May 29, 2001

Many insects are able to adjust their egg production according to physiological conditions such as nutrient supply and mating success. One way in which this is achieved is by resorption of some, or all, of the ovarian follicles at some stage during oogenesis. We have shown that the mosquito Anopheles stephensi responds in this manner when ookinetes of the malaria parasite Plasmodium yoelii nigeriensis first begin to invade the midgut. Little is known about the initiation and regulation of follicle resorption in any insect. Here, we demonstrate that there is a significant positive correlation between follicle resorption and the presence of follicular epithelial cells that are undergoing apoptosis. The parasite causes significantly more follicles to contain apoptotic cells from 16 h post-infection onwards. Injection of a caspase inhibitor immediately after feeding on an infective blood meal prevents parasite-induced resorption of follicles and thus demonstrates that apoptosis precedes resorption. Ultrastructural studies show that patches of follicular epithelial cells contain condensed nuclear chromatin, a characteristic of apoptosis, and that no patency develops in these cells. Our work suggests that apoptosis plays a role in malaria-initiated inhibition of mosquito oogenesis and that caspase is central to this process. Follicle resorption is one of the main factors contributing to malaria-induced fecundity reduction in mosquitoes.

Key words: mosquito, Anopheles stephensi, oogenesis, follicle resorption, apoptosis, caspase, Plasmodium yoelii nigeriensis, malaria, follicular epithelium, nurse cell






© The Company of Biologists Ltd 2001