A conserved long noncoding RNA affects sleep behavior in Drosophila

Alexey A Soshnev; Hiroshi Ishimoto; Bryant F McAllister; Xingguo Li; Misty D Wehling; Toshihiro Kitamoto; Pamela K Geyer

doi:10.1534/genetics.111.131706

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A conserved long noncoding RNA affects sleep behavior in Drosophila

Journal article

Open access

Peer reviewed

A conserved long noncoding RNA affects sleep behavior in Drosophila

Alexey A Soshnev, Hiroshi Ishimoto, Bryant F McAllister, Xingguo Li, Misty D Wehling, Toshihiro Kitamoto and Pamela K Geyer

Genetics (Austin), Vol.189(2), pp.455-468

10/2011

DOI: 10.1534/genetics.111.131706

PMCID: PMC3189806

PMID: 21775470

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Abstract

Metazoan genomes encode an abundant collection of mRNA-like, long noncoding (lnc)RNAs. Although lncRNAs greatly expand the transcriptional repertoire, we have a limited understanding of how these RNAs contribute to developmental regulation. Here, we investigate the function of the Drosophila lncRNA called yellow-achaete intergenic RNA (yar). Comparative sequence analyses show that the yar gene is conserved in Drosophila species representing 40-60 million years of evolution, with one of the conserved sequence motifs encompassing the yar promoter. Further, the timing of yar expression in Drosophila virilis parallels that in D. melanogaster, suggesting that transcriptional regulation of yar is conserved. The function of yar was defined by generating null alleles. Flies lacking yar RNAs are viable and show no overt morphological defects, consistent with maintained transcriptional regulation of the adjacent yellow (y) and achaete (ac) genes. The location of yar within a neural gene cluster led to the investigation of effects of yar in behavioral assays. These studies demonstrated that loss of yar alters sleep regulation in the context of a normal circadian rhythm. Nighttime sleep was reduced and fragmented, with yar mutants displaying diminished sleep rebound following sleep deprivation. Importantly, these defects were rescued by a yar transgene. These data provide the first example of a lncRNA gene involved in Drosophila sleep regulation. We find that yar is a cytoplasmic lncRNA, suggesting that yar may regulate sleep by affecting stabilization or translational regulation of mRNAs. Such functions of lncRNAs may extend to vertebrates, as lncRNAs are abundant in neural tissues.

Gene Expression

Mutation

Basic Helix-Loop-Helix Transcription Factors - genetics

Genes, Insect - genetics

Species Specificity

Conserved Sequence - drug effects

Molecular Sequence Data

Drosophila - classification

Sleep - genetics

DNA, Intergenic - genetics

Reverse Transcriptase Polymerase Chain Reaction

Drosophila melanogaster - genetics

RNA, Untranslated - genetics

Sequence Homology, Nucleic Acid

Blotting, Northern

Animals

Base Sequence

RNA, Long Noncoding

Cytoplasm - genetics

Drosophila Proteins - genetics

Drosophila - genetics

Evolution, Molecular

Details

Title: Subtitle: A conserved long noncoding RNA affects sleep behavior in Drosophila
Creators: Alexey A Soshnev - Program in Molecular and Cellular Biology, Department of Anesthesia, University of Iowa, Iowa City, IA 52242, USA
Hiroshi Ishimoto
Bryant F McAllister
Xingguo Li - University of Iowa
Misty D Wehling
Toshihiro Kitamoto
Pamela K Geyer
Resource Type: Journal article
Publication Details: Genetics (Austin), Vol.189(2), pp.455-468
Publisher: United States
DOI: 10.1534/genetics.111.131706
PMID: 21775470
PMCID: PMC3189806
ISSN: 0016-6731
eISSN: 1943-2631
Grant note: R01 MH085081 / NIMH NIH HHS R01 GM042539 / NIGMS NIH HHS GM42539 / NIGMS NIH HHS
Language: English
Date published: 10/2011
Academic Unit: Iowa Neuroscience Institute; Biology; Anesthesia; Obstetrics and Gynecology; Neuroscience and Pharmacology; Biochemistry and Molecular Biology
Record Identifier: 9983991996102771

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