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

JANE A. HOPWOOD^1,2, ASHRAF M. AHMED¹, ANTHONY POLWART³, GWYN T. WILLIAMS³ and HILARY HURD^1,*

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 )

View larger version (17K): [in a new window]   Fig. 1. The effect of malaria infection on the occurrence of apoptosis and resorption of follicles in ovaries from Anopheles stephensi. Mean percentage of follicles per ovary stained with Neutral Red and thus resorbing; uninfected mosquitoes (filled squares), infected mosquitoes (filled columns) and/or containing apoptotic nuclei stained with Acridine Orange; uninfected mosquitoes (open squares), infected mosquitoes (open columns). Sample size, 20 in each case. Values are means + S.E.M. A significant difference occurred between resorption and apoptosis in infected females at one time point (*P<0.05).

View larger version (87K): [in a new window]   Fig. 3. Follicles from ovaries of malaria-infected Anopheles stephensi developing normally (left) or showing evidence of apoptosis (right). (A) Whole-mounts of individual follicles 24h post-bloodfeeding, viewed under ultraviolet light after staining with Acridine Orange. The follicle in the left-hand frame (Ai) is exhibiting autofluorescence, and condensed apoptotic nuclei are visible in the follicle on the right, stained orange (a) (Aii). Scale bars, 20 µm. (B) Sections of follicles from ovaries 16h post-bloodfeeding stained with Methyl Green and treated by TUNEL (see Materials and methods). DNA fragmentation (indicated by brown staining) can be observed in follicular epithelial (f) and nurse (n) cells in the right-hand frame (Bii). Scale bars, 10 µm. (C) Electron micrographs of a normal follicle 18 h post-bloodfeeding (Ci) and a resorbing follicle 22h post-bloodfeeding (Cii). Patency (p) has developed in follicular epithelial cells of the normal follicle, and yolk spheres (y) have been deposited, whereas in the resorbing follicle no yolk is visible, epithelial cells are not patent and their nuclei contain condensed chromatin (c). Scale bars, 2 µm.

View larger version (13K): [in a new window]   Fig. 2. The relationship between resorption and apoptosis for control and infected mosquitoes (open circles, control: 58 d.f.; r2=0.569; P<0.001; filled circles, infected: 58 d.f.; r2=0.807; P<0.001).

View larger version (34K): [in a new window]   Fig. 4. The effect of inhibiting apoptosis on follicle resorption in malaria-infected Anopheles stephensi. Immediately after feeding on a mouse containing Plasmodium yoelii nigeriensis gametocytes, mosquitoes were injected with saline (N=11), 1% DMSO in saline (N=25) or 0.5 mmoll-1 z-VAD.fmk/1%DMSO (N=20) or left uninjected (N=20). The mean number of resorbing follicles per ovary pair is shown. Values are means ± S.E.M. A Kruskal—Wallis test demonstrated overall significance (P<0.001) followed by Mann—Whitney U-tests where all comparisons against z-VAD.fmk were significant (P<0.001). There was no significant difference between non-injected, saline-injected and DMSO-injected females.