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Cited by 1Neurobiology and Insect Physiology ResearchDevelopmental Biology and Gene RegulationMicroRNA in disease regulation

A microRNA that controls the emergence of embryonic movement

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Menzies, Jonathan AC, Maia Chagas, André, Baden, Tom, Alonso, Claudio R·2024·eLife
DOI 10.7554/elife.95209.3

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Abstract

Movement is a key feature of animal systems, yet its embryonic origins are not fully understood. Here, we investigate the genetic basis underlying the embryonic onset of movement in Drosophila focusing on the role played by small non-coding RNAs (microRNAs, miRNAs). To this end, we first develop a quantitative behavioural pipeline capable of tracking embryonic movement in large populations of fly embryos, and using this system, discover that the Drosophila miRNA miR-2b-1 plays a role in the emergence of movement. Through the combination of spectral analysis of embryonic motor patterns, cell sorting and RNA in situs, genetic reconstitution tests, and neural optical imaging we define that miR-2b-1 influences the emergence of embryonic movement by exerting actions in the developing nervous system. Furthermore, through the combination of bioinformatics coupled to genetic manipulation of miRNA expression and phenocopy tests we identify a previously uncharacterised (but evolutionarily conserved) chloride channel encoding gene – which we term Mo vement Modula tor ( Motor ) – as a genetic target that mechanistically links miR-2b-1 to the onset of movement. Cell-specific genetic reconstitution of miR-2b-1 expression in a null miRNA mutant background, followed by behavioural assays and target gene analyses, suggest that miR-2b-1 affects the emergence of movement through effects in sensory elements of the embryonic circuitry, rather than in the motor domain. Our work thus reports the first miRNA system capable of regulating embryonic movement, suggesting that other miRNAs are likely to play a role in this key developmental process in Drosophila as well as in other species.

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Authors
Menzies, J. A., Maia Chagas, A., Baden, T., & Alonso, C. R.
Affiliations
  • University of Sussex (GB)
  • Department of Neuroscience, Sussex Neuroscience, School of Life Sciences, University of Sussex
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2024-06-13
Volume
13
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.95209.3
OpenAlex
W4399626001
Cited by
1
References
1
Citations by year
2026: 1
FWCI
0.18
Type
journal article
Language
en
Open access
Licence
Locations
eLife (publishedVersion, cc-by)
Funders
  • Wellcome Trust (10.35802/098410, 10.35802/220277)
  • Medical Research Council (MR/S011609/1)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Keywords
embryonic movement, microRNA, Drosophila embryo, small RNA, chloride channels, sensory neurons, embryonic nervous system development, motor circuitry, behavioral phenotyping, miRNA target genes

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