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

• Published in: Nature communications Vol. 15; no. 1; pp. 7065 - 16
• Main Authors: Erickson, Alek G., Motta, Alessia, Kastriti, Maria Eleni, Edwards, Steven, Coulpier, Fanny, Théoulle, Emy, Murtazina, Aliia, Poverennaya, Irina, Wies, Daniel, Ganofsky, Jeremy, Canu, Giovanni, Lallemend, Francois, Topilko, Piotr, Hadjab, Saida, Fried, Kaj, Ruhrberg, Christiana, Schwarz, Quenten, Castellani, Valerie, Bonanomi, Dario, Adameyko, Igor
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 16-08-2024; Nature Publishing Group; Nature Portfolio
• Subjects: 13/51; 14/19; 14/32; 14/35; 14/63; 38; 38/91; 42; 631/136/368/2430; 631/378/2571/1696; 64; 64/60; Ablation; Animals; Cell fusion; Cells (biology); Defensive behavior; Dorsal root ganglia; Embryos; Female; Ganglia; Ganglia, Spinal; Ganglia, Sympathetic - cytology; Glial stem cells; Humanities and Social Sciences; Hypoplasia; Innervation; Life Sciences; Medicin och hälsovetenskap; Mice; Mice, Transgenic; Morphogenesis; Motor Neurons - physiology; multidisciplinary; Nerves; Nervous system; Neural crest; Neural Crest - cytology; Neural Crest - metabolism; Neural stem cells; Neural tube; Neuroglia - metabolism; Neuronal-glial interactions; Neurons; Peripheral nervous system; Progenitor cells; Questions; Schwann Cells - metabolism; Science; Science (multidisciplinary); Semaphorins; Semaphorins - genetics; Semaphorins - metabolism; Sensory evaluation; Sensory neurons; Stress (physiology); Sympathetic ganglia; Sympathetic nerves; Sympathetic nervous system; Sympathetic Nervous System - embryology
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51290-0

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.
How tissues interact to help each other grow is a major question for biologists. Here, the authors show that motor innervation controls positioning of sympathetic progenitor cells to ensure correct shaping of ganglia in the peripheral nervous system.