Vesicular ATPase-overexpressing Cells Determine the Distribution of Malaria Parasite Oocysts on the Midguts of Mosquitoes*

Abstract

In Plasmodium-infected mosquitoes, oocysts are preferentially located at the posterior half of the posterior midgut. Because mosquitoes rest vertically after feeding, the effect of gravity on the ingested blood has been proposed as the cause of such a biased distribution. In this paper, we examined the oocyst distribution on the midguts of mosquitoes that were continuously rotated to nullify the effect of gravity and found that the typical pattern of oocyst distribution did not change. Invasion of the midgut epithelium by ookinetes was similarly found to be biased toward the posterior part of the posterior midgut. We examined whether the distribution of oocysts depends on the distribution of vesicular ATPase (V-ATPase)-overexpressing cells that Plasmodium ookinetes preferentially use to cross the midgut epithelium. An antiserum raised against recombinant Aedes aegypti V-ATPase B subunit indicated that the majority of V-ATPase-overexpressing cells inAe. aegypti and Anopheles gambiae are localized at the posterior part of the posterior midgut. We propose that the typical distribution of oocysts on the mosquito midgut is attributable to the presence and the spatial distribution of the V-ATPase-overexpressing cells in the midgut epithelium.

Footnotes

  • * This work was supported, in part, by Grant 950476 (to Louis H. Miller) from the United Nations Developmental Program/World Bank/World Health Organization Special Program for Research and Training in Tropical Diseases.The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

    The nucleotide sequence(s) reported in this paper has been submitted to the GenBank™/EMBL Data Bank with accession number(s) AF092934.

  • § Supported by the Vector Biology Network of the John D. and Catherine T. MacArthur Foundation.

  • To whom correspondence should be addressed: Laboratory of Parasitic Diseases, NIAID, National Institutes of Health, Bldg. 4, Rm. B2-39, 9000 Rockville Pike, Bethesda, MD 20892-0425. Tel.: 301-496-9389; Fax: 301-402-8536; E-mail:mohammed_shahabuddin{at}nih.gov.

  • 2 S. O. Cociancich and M. Shahabuddin, unpublished observations.

  • Abbreviations:
    V-ATPase

    vesicular ATPase

    PCR

    polymerase chain reaction

    PBS

    phosphate-buffered saline

    PIPES

    1,4-piperazinediethanesulfonic acid

    • Received December 4, 1998.
    • Revision received January 29, 1999.
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