Motor innervation directs the correct development of the mouse sympathetic nervous system

Alek G. Erickson, Alessia Motta, Maria Eleni Kastriti, Steven Edwards, Fanny Coulpier, Emy Théoulle, Aliia Murtazina, Irina Poverennaya, Daniel Wies, Jeremy Ganofsky, Giovanni Canu, Francois Lallemend, Piotr Topilko, Saida Hadjab, Kaj Fried, Christiana Ruhrberg, Quenten Schwarz, Valerie Castellani, Dario Bonanomi () and Igor Adameyko ()
Additional contact information
Alek G. Erickson: Karolinska Institutet
Alessia Motta: IRCCS San Raffaele Scientific Institute
Maria Eleni Kastriti: Karolinska Institutet
Steven Edwards: KTH Royal Institute of Technology
Fanny Coulpier: Mondor Institute for Biomedical Research (IMRB), INSERM
Emy Théoulle: NeuroMyoGene Institute
Aliia Murtazina: Karolinska Institute
Irina Poverennaya: Medical University Vienna
Daniel Wies: Karolinska Institutet
Jeremy Ganofsky: NeuroMyoGene Institute
Giovanni Canu: Department of Ophthalmology London
Francois Lallemend: Karolinska Institute
Piotr Topilko: Mondor Institute for Biomedical Research (IMRB), INSERM
Saida Hadjab: Karolinska Institute
Kaj Fried: Karolinska Institute
Christiana Ruhrberg: Department of Ophthalmology London
Quenten Schwarz: University of South Australia
Valerie Castellani: NeuroMyoGene Institute
Dario Bonanomi: IRCCS San Raffaele Scientific Institute
Igor Adameyko: Karolinska Institutet

Nature Communications, 2024, vol. 15, issue 1, 1-16

Abstract: Abstract 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.

Date: 2024
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DOI: 10.1038/s41467-024-51290-0

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