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J. Biol. Chem., Vol. 281, Issue 16, 11167-11176, April 21, 2006

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GATA Factor Translation Is the Final Downstream Step in the Amino Acid/Target-of-Rapamycin-mediated Vitellogenin Gene Expression in the Anautogenous Mosquito Aedes aegypti^*

From the Center for Disease-Vector Research, Department of Entomology and Institute for Integrative Genome Biology, University of California, Riverside, California 92521

Ingestion of blood is required for vector mosquitoes to initiate reproductive cycles determining their role as vectors of devastating human diseases. Nutritional signaling plays a pivotal role in regulating mosquito reproduction. Transcription of yolk protein precursor genes is repressed until mosquitoes take blood. Previously, we have shown that to signal the presence of blood in the gut, mosquitoes utilize the target-of-rapamycin (TOR) pathway. The TOR signaling pathway transduces the amino acid signal activating the major yolk protein precursor gene, vitellogenin (Vg). Here we report the identification of a GATA factor (AaGATAa) that is synthesized after a blood meal and acts as a transcriptional activator of Vg. We showed that AaGATAa bound specifically to GATA-binding sites present in the proximal promoter region of the Vg gene and positively regulated Vg expression in transfection assays. RNA interference-mediated knock down of AaGATAa transcript resulted in a significant inhibition of Vg expression in both fat-body tissue culture and blood-fed mosquitoes. AaGATAa mRNA accumulated in the fat body prior to blood feeding. However, translation of GATA was activated by blood feeding because the GATA protein increased dramatically in the fat body of blood-fed mosquitoes. This increase was also reproduced in the fat-body culture stimulated with amino acids. GATA translation was inhibited by rapamycin and cycloheximide as well as by RNA interference-mediated knock down of S6 kinase. These experiments have revealed that the TOR signaling pathway induced by nutritional signaling regulates the translation of a GATA factor, which is the specific transcriptional activator of the Vg gene.

Received for publication, February 16, 2006

^* This work was supported by National Institutes of Health Grant 5R37AI24716 (to A. S. R.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ These authors contributed equally to this paper.

² Present address: Dept. of Advanced Technology Fusion, Hwayang-dong, Gwangin-gu, Konkuk University, Seoul, 143-701, Korea.

³ Present address: Yale School of Public Health, Yale University, New Haven, CT 06520.

⁴ To whom correspondence should be addressed: Dept. of Entomology, University of California, 3401 Watkins Dr., Riverside, CA 92521. Tel.: 951-827-2129; Fax: 951-827-2140; E-mail: alexander.raikhel{at}ucr.edu.

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