Transcriptional Coordination of Synaptogenesis and Neurotransmitter Signaling
Open accessAbstract
During nervous system development, postmitotic neurons face the challenge of generating and structurally organizing specific synapses with appropriate synaptic partners. An important unexplored question is whether the process of synaptogenesis is coordinated with the adoption of specific signaling properties of a neuron. Such signaling properties are defined by the neurotransmitter system that a neuron uses to communicate with postsynaptic partners, the neurotransmitter receptor type used to receive input from presynaptic neurons, and, potentially, other sensory receptors that activate a neuron. Elucidating the mechanisms that coordinate synaptogenesis, neuronal activation, and neurotransmitter signaling in a postmitotic neuron represents one key approach to understanding how neurons develop as functional units. Using the SAB class of Caenorhabditis elegans motor neurons as a model system, we show here that the phylogenetically conserved COE-type transcription factor UNC-3 is required for synaptogenesis. UNC-3 directly controls the expression of the ADAMTS-like protein MADD-4/Punctin, a presynaptically secreted synapse-organizing molecule that clusters postsynaptic receptors. UNC-3 also controls the assembly of presynaptic specializations and ensures the coordinated expression of enzymes and transporters that define the cholinergic neurotransmitter identity of the SAB neurons. Furthermore, synaptic output properties of the SAB neurons are coordinated with neuronal activation and synaptic input, as evidenced by UNC-3 also regulating the expression of ionotropic neurotransmitter receptors and putative stretch receptors. Our study shows how synaptogenesis and distinct, function-defining signaling features of a postmitotic neuron are hardwired together through coordinated transcriptional control.
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Prior functional studies link SMD to Ω-turn amplitude, SMB to sinusoidal movement amplitude, SAB to proprioception, and SIA to flipping behaviour during lethargus.
“Functional studies have shown that SMD encodes the amplitude of a deep ventral bend behaviour known as the Ω-turn; SMB influences the amplitude of sinusoidal movement; SAB is thought to act in proprioception; and the SIA neurons are involved in so-called ‘flipping behaviour’ during lethargus24,29,30.”
From Whole-animal connectomes of both Caenorhabditis elegans sexes (2019) · cites this paper as [29]
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Xu, C., Ramos, T. B., Rogers, E. M., Reiser, M. B., & Doe, C. Q. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.01.462699 · Cited by 1 · see citing works
Smith, J. J., Taylor, S. R., Destain, H., Kim, G., Hall, D., White, J. G., Miller, D. M., & Kratsios, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2025.12.23.696256 · Cited by 1 · see citing works
Self-citationDestain, H., Koh, A., Shin, H., Brown, A. E., & Kratsios, P. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.14.725191 · Cited by 1 · see citing works
Self-citationFate transitions in Drosophila neural lineages: a single cell road map to mature neurons.Preprint
Marques, G. S., Teles-Reis, J., Konstantinides, N., Brito, P. H., & Homem, C. C. F. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.22.449317
Control of Neuronal Terminal Differentiation Through Cell Context-Dependent CFI-1/ARID3 FunctionsPreprint
Li, Y., Smith, J. J., Marques, F., Osuma, A., Huang, H.-C., & Kratsios, P. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4156163
Self-citationHomeodomain proteins hierarchically specify neuronal diversity and synaptic connectivityPreprint
Xu, C., Ramos, T. B., Rogers, E. M., Reiser, M. B., & Doe, C. Q. (2023) · eLife · doi:10.7554/elife.90133.1
Homeodomain proteins hierarchically specify neuronal diversity and synaptic connectivity
Xu, C., Ramos, T. B., Rogers, E. M., Reiser, M. B., & Doe, C. Q. (2024) · eLife · doi:10.7554/elife.90133.3
Axon termination of the SAB motor neurons in C. elegans depends on pre- and postsynaptic activityPreprint
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Self-citationSpatiotemporal isoform profiling identifies a central activator of microexon splicing in C. elegansPreprint
Koterniak, B., Liang, E., Zoberman, M., He, C., Choudhary, B. C., Sadek, N. H., Pilaka, P. P., Norris, A. D., & Calarco, J. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.14.751627
- Authors
- Kratsios, P., Pinan-Lucarré, B., Kerk, S. Y., Weinreb, A., Bessereau, J.-L., & Hobert, O.
- Affiliations
- Howard Hughes Medical Institute (US)
- Lyon 1 Université (FR)
- Corresponding author
- Kratsios, Paschalis
- Hobert, Oliver
- Venue
- Current Biology
- Publisher
- Elsevier BV
- Published
- 2015-05
- Volume
- 25
- Issue
- 10
- Pages
- 1282-1295
- ISSN
- 0960-9822 (ISSN-L)
- PMC
- PMC4465358
- OpenAlex
- W2012467082
- Cited by
- 74
- References
- 38
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 10 · 2020: 9 · 2019: 6 · 2018: 5 · 2017: 4 · 2016: 8 · 2015: 3
- FWCI
- 3.11
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Current Biology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- Agence Nationale de la Recherche (ANR-11-BSV4-0019)
- National Institute of Neurological Disorders and Stroke (R01NS050266, K99NS084988, R01NS039996)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- 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
- Keywords
- synaptogenesis, neurotransmitter signaling, transcriptional regulation, presynaptic specialization, ligand-gated ion channels, stretch receptors, neuronal activation
- MeSH terms
- Animals, Motor Neurons, Mutation, Nerve Tissue Proteins, Synaptic Transmission, Synapses, Transcription Factors, Signal Transduction, Caenorhabditis elegans, Neurotransmitter Agents, Gene Expression Regulation, Developmental, Caenorhabditis elegans Proteins, Animals, Genetically Modified, Neurogenesis
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