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Proc Natl Acad Sci U S A. 2017 Mar 28;114(13):E2709-E2718. doi: 10.1073/pnas.1619326114. Epub 2017 Mar 14.

Hormone and receptor interplay in the regulation of mosquito lipid metabolism.

Wang X1,2, Hou Y1,2, Saha TT3, Pei G1,2, Raikhel AS4,5, Zou Z6,2.

Author information

1
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China.
2
University of Chinese Academy of Sciences, Beijing 100049, People's Republic of China.
3
Department of Entomology, University of California, Riverside, CA 92521.
4
Department of Entomology, University of California, Riverside, CA 92521; alexander.raikhel@ucr.edu zouzhen@ioz.ac.cn.
5
Institute for Integrative Genome Biology, University of California, Riverside, CA 92521.
6
State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, People's Republic of China; alexander.raikhel@ucr.edu zouzhen@ioz.ac.cn.

Abstract

Mosquitoes transmit devastating human diseases because they need vertebrate blood for egg development. Metabolism in female mosquitoes is tightly coupled with blood meal-mediated reproduction, which requires an extremely high level of energy consumption. Functional analysis has shown that major genes encoding for enzymes involved in lipid metabolism (LM) in the mosquito fat bodies are down-regulated at the end of the juvenile hormone (JH)-controlled posteclosion (PE) phase but exhibit significant elevation in their transcript levels during the post-blood meal phase (PBM), which is regulated mainly by 20-hydroxyecdysone (20E). Reductions in the transcript levels of genes encoding triacylglycerol (TAG) catabolism and β-oxidation enzymes were observed to correlate with a dramatic accumulation of lipids in the PE phase; in contrast, these transcripts were elevated significantly and lipid stores were diminished during the PBM phase. The RNAi depletion of Methoprene-tolerant (Met) and ecdysone receptor (EcR), receptors for JH and 20E, respectively, reversed the LM gene expression and the levels of lipid stores and metabolites, demonstrating the critical roles of these hormones in LM regulation. Hepatocyte nuclear factor 4 (HNF4) RNAi-silenced mosquitoes exhibited down-regulation of the gene transcripts encoding TAG catabolism and β-oxidation enzymes and an inability to use lipids effectively, as manifested by TAG accumulation. The luciferase reporter assay showed direct regulation of LM-related genes by HNF4. Moreover, HNF4 gene expression was down-regulated by Met and activated by EcR and Target of rapamycin, providing a link between nutritional and hormonal regulation of LM in female mosquitoes.

KEYWORDS:

20-hydroxyecdysone; beta-oxidation; hepatocyte nuclear factor 4; juvenile hormone; lipid

PMID:
28292900
PMCID:
PMC5380040
DOI:
10.1073/pnas.1619326114
[Indexed for MEDLINE]
Free PMC Article

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