Hormone-dependent activation and repression of microRNAs by the ecdysone receptor in the dengue vector mosquito Aedes aegypti

Female mosquitoes transmit numerous devastating human diseases because they require vertebrate blood meal for egg development. MicroRNAs (miRNAs) play critical roles across multiple reproductive processes in female mosquitoes. However, how miRNAs are controlled to coordinate their activity with the...

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Bibliographic Details
Published in:Proceedings of the National Academy of Sciences - PNAS 2021-06, Vol.118 (26)
Main Authors: He, Ya-Zhou, Aksoy, Emre, Ding, Yike, Raikhel, Alexander S
Format: Article
Language:English
Subjects:
Aedes - drug effects
Aedes - genetics
Aedes aegypti
Animals
Biological Sciences
Blood
Co-Repressor Proteins - genetics
Co-Repressor Proteins - metabolism
Culicidae
Dengue - parasitology
Dengue fever
Ecdysone
Ecdysterone - pharmacology
Eggs
Fat body
Fat Body - drug effects
Fat Body - metabolism
Feeding Behavior - drug effects
Female
Gene expression
Gene Expression Regulation - drug effects
Gene sequencing
Histone Deacetylases - metabolism
Insect Proteins - genetics
Insect Proteins - metabolism
Insects
MicroRNAs
MicroRNAs - genetics
MicroRNAs - metabolism
miRNA
Mosquito Vectors - drug effects
Mosquito Vectors - genetics
Mosquitoes
Open Reading Frames - genetics
Ovum - growth & development
Promoter Regions, Genetic - genetics
Receptors
Receptors, Steroid - metabolism
Reproduction
Ribonucleic acid
RNA
RNA-mediated interference
Sequence analysis
Signal transduction
Signaling
SMRT protein
Transcription Initiation Site
Transcription, Genetic - drug effects
Transcriptome - genetics
Vector-borne diseases
Vertebrates
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Summary:Female mosquitoes transmit numerous devastating human diseases because they require vertebrate blood meal for egg development. MicroRNAs (miRNAs) play critical roles across multiple reproductive processes in female mosquitoes. However, how miRNAs are controlled to coordinate their activity with the demands of mosquito reproduction remains largely unknown. We report that the ecdysone receptor (EcR)-mediated 20-hydroxyecdysone (20E) signaling regulates miRNA expression in female mosquitoes. EcR RNA-interference silencing linked to small RNA-sequencing analysis reveals that EcR not only activates but also represses miRNA expression in the female mosquito fat body, a functional analog of the vertebrate liver. EcR directly represses the expression of clustered and before blood feeding when the 20E titer is low, whereas it activates their expression in response to the increased 20E titer after a blood meal. Furthermore, we find that SMRTER, an insect analog of the vertebrate nuclear receptor corepressors SMRT and N-CoR, interacts with EcR in a 20E-sensitive manner and is required for EcR-mediated repression of miRNA expression in mosquitoes. In addition, we demonstrate that miR-275 and miR-305 directly target and , respectively, to facilitate egg development. This study reveals a mechanism for how miRNAs are controlled by the 20E signaling pathway to coordinate their activity with the demands of mosquito reproduction.
ISSN:0027-8424
1091-6490
1091-6490
DOI:10.1073/pnas.2102417118