Motor innervation directs the correct development of the mouse sympathetic nervous system
The sympathetic nervous system controls bodily functions including vascular tone, cardiac rhythm, and the "fight-or-flight response". Sympathetic chain ganglia develop in parallel with preganglionic motor nerves extending from the neural tube, raising the question of whether axon targeting contributes to sympathetic chain formation. Using nerve-selective genetic ablations and lineage tracing in mouse, we reveal that motor nerve-associated Schwann cell precursors (SCPs) contribute sympathetic neurons and satellite glia after the initial seeding of sympathetic ganglia by neural crest. Motor nerve ablation causes mispositioning of SCP-derived sympathoblasts as well as sympathetic chain hypoplasia and fragmentation. Sympathetic neurons in motor-ablated embryos project precociously and abnormally towards dorsal root ganglia, eventually resulting in fusion of sympathetic and sensory ganglia. Cell interaction analysis identifies semaphorins as potential motor nerve-derived signaling molecules regulating sympathoblast positioning and outgrowth. Overall, central innervation functions both as infrastructure and regulatory niche to ensure the integrity of peripheral ganglia morphogenesis.
Authors
- Alessia Motta (ORCID: https://orcid.org/0000-0002-1008-8347)
- Emy Théoulle
- Maria Eleni Kastriti (ORCID: https://orcid.org/0000-0002-0563-7399)
- Giovanni Canu (ORCID: https://orcid.org/0000-0002-3349-4479)
- Kaj Fried (ORCID: https://orcid.org/0000-0002-9997-7078)
- Fanny Coulpier (ORCID: https://orcid.org/0000-0002-1558-0293)
- Dario Bonanomi (ORCID: https://orcid.org/0000-0003-4517-1244)
- Piotr Topilko (ORCID: https://orcid.org/0000-0001-7381-6770)
- Saïda Hadjab (ORCID: https://orcid.org/0000-0001-7953-8396)
- Alek G. Erickson (ORCID: https://orcid.org/0000-0001-7110-9386)
- Quenten Schwarz (ORCID: https://orcid.org/0000-0002-5958-4181)
- François Lallemend (ORCID: https://orcid.org/0000-0001-5484-0011)
- Steven R Edwards (ORCID: https://orcid.org/0000-0002-9866-0327)
- Igor I. Adameyko (ORCID: https://orcid.org/0000-0001-5471-0356)
- Jérémy Ganofsky (ORCID: https://orcid.org/0000-0002-2361-7869)
- А. Р. Муртазина
- Irina Poverennaya (ORCID: https://orcid.org/0000-0003-2562-5632)
- Christiana Ruhrberg (ORCID: https://orcid.org/0000-0002-3212-9381)
- Valérie Castellani (ORCID: https://orcid.org/0000-0001-9623-9312)
- Daniel Wies
Institutions
- Université Claude Bernard Lyon 1 (FR)
- Centre National de la Recherche Scientifique (FR)
- Vita-Salute San Raffaele University (IT)
- Inserm (FR)
- University of South Australia (AU)
- Karolinska Institutet (SE)
- Institut NeuroMyoGène (FR)
- IRCCS Ospedale San Raffaele (IT)
- Centre for Cancer Biology (AU)
- Istituti di Ricovero e Cura a Carattere Scientifico (IT)
- Institut Mondor de Recherche Biomédicale (FR)
- Istituto di Ricovero e Cura a Carattere Scientifico San Raffaele (IT)
- University College London (GB)
- Medical University of Vienna (AT)
- KTH Royal Institute of Technology (SE)
Publication Details
- Journal
- Nature Communications
- Published
- 2024-08-16
- DOI
- https://doi.org/10.1038/s41467-024-51290-0
- Citations
- 6
- Primary Topic
- Congenital heart defects research
- Type
- article
- Field-Weighted Citation Impact
- 1.40
Funders
- Giovanni Armenise-Harvard Foundation
- European Commission
- Austrian Science Fund
- Cancerfonden
- Karolinska Institutet
- Knut och Alice Wallenbergs Stiftelse
- Vetenskapsrådet
- Science for Life Laboratory
- National Institutes of Health
- National Institute of Dental and Craniofacial Research