Abstract
Some long noncoding RNAs (lncRNAs) are specifically expressed in brain cells, implying their neural and behavioural functions. However, how lncRNAs contribute to neural regulatory networks governing the precise behaviour of animals is less explored. Here, we report the regulatory mechanism of the nuclear-enriched lncRNA PAHAL for dopamine biosynthesis and behavioural adjustment in migratory locusts (Locusta migratoria), a species with extreme behavioral plasticity. PAHAL is transcribed from the sense (coding) strand of the gene encoding phenylalanine hydroxylase (PAH), which is responsible for the synthesis of dopamine from phenylalanine. PAHAL positively regulates PAH expression resulting in dopamine production in the brain. In addition, PAHAL modulates locust behavioral aggregation in a population density-dependent manner. Mechanistically, PAHAL mediates PAH transcriptional activation by recruiting serine/arginine-rich splicing factor 2 (SRSF2), a transcription/splicing factor, to the PAH proximal promoter. The co-activation effect of PAHAL requires the interaction of the PAHAL/SRSF2 complex with the promoter-associated nascent RNA of PAH. Thus, the data support a model of feedback modulation of animal behavioural plasticity by an lncRNA. In this model, the lncRNA mediates neurotransmitter metabolism through orchestrating a local transcriptional loop.
Highlights
Long noncoding RNAs are transcripts comprising > 200 nucleotides and possessing minimal or non-existent protein-coding capacity [1] and are increasingly recognised as key players in numerous cellular processes [2,3]
We discovered a nuclear-enriched Long noncoding RNAs (lncRNAs) PAH-activating lncRNA (PAHAL) that is transcribed from the coding strand of the phenylalanine hydroxylase (PAH) gene in the locust
Sense lncRNA PAHAL is expressed from the intron/exon of the PAH gene locus
Summary
Long noncoding RNAs (lncRNAs) are transcripts comprising > 200 nucleotides and possessing minimal or non-existent protein-coding capacity [1] and are increasingly recognised as key players in numerous cellular processes [2,3]. The brain and neuronal specificity of lncRNA expression has prompted the exploration of the potential roles of lncRNAs in neuronal development and cognitive and behavioural regulation [10,15,16,17,18,19,20,21]. The lncRNA CRG exhibits spatiotemporal specific expression patterns within the central nervous system; in addition, CRG affects the locomotor behaviour of Drosophila by positively regulating a neighbouring gene that encodes a Ca2+/calmodulin-dependent protein kinase [23]. Despite the recognised roles of lncRNAs in the neuronal system and behaviour, how neuronal and behavioural responses to environmental stimuli are modulated at the cellular and organismal levels by lncRNAs remains incompletely understood
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