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Neuropilin-mediated neural crest cell guidance is essential to organise sensory neurons into segmented dorsal root ganglia

By Q Schwarz, CH Maden, K Davidson and C Ruhrberg

Abstract

The peripheral nervous system (PNS) of higher vertebrates is segmented to align the spinal nerve roots with the vertebrae. This co-patterning is set up during embryogenesis, when vertebrae develop from the sclerotome layer of the metameric somites, and PNS neurons and glia differentiate from neural crest cells (NCCs) that preferentially migrate into the anterior sclerotome halves. Previous analyses of mice deficient in the class 3 semaphorin (SEMA3) receptors neuropilin (NRP) 1 or 2 raised the possibility that each controlled a distinct aspect of trunk NCC migration. We now demonstrate that both pathways act sequentially in distinct NCC subpopulations and thereby cooperate to enforce segmental NCC migration. Specifically, SEMA3A/NRP1 signalling first directs one population of NCCs from the intersomitic path into the sclerotome, and SEMA3F/NRP2 signalling acts subsequently to restrict a second population to the anterior half of the sclerotome. NCC exclusion from either the posterior sclerotome or the intersomitic boundary is sufficient to enforce the separation of neighbouring NCC streams and the segregation of sensory NCC progeny into metameric dorsal root ganglia (DRG). By contrast, the combined loss of both guidance pathways leads to ectopic invasion of the intersomitic furrows and posterior sclerotome halves, disrupting metameric NCC streaming and DRG segmentation

Topics: Dorsal root ganglia, Neural crest cell, Neuropilin, Segmentation, Semaphorin, Sensory neurons, Mouse, AXON GUIDANCE, SYMPATHETIC NEURONS, NERVOUS-SYSTEM, PROXIMAL RIBS, SEMAPHORIN, REQUIREMENT, DIFFERENTIATION, EXPRESSION, PLEXIN-A3, MIGRATION
Publisher: COMPANY OF BIOLOGISTS LTD
Year: 2009
DOI identifier: 10.1242/dev.034322
OAI identifier: oai:eprints.ucl.ac.uk.OAI2:16373
Provided by: UCL Discovery

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Citations

  1. (1989). Consequences of somite manipulation on the pattern of dorsal root ganglion development.
  2. (2008). control cranial gangliogenesis and axon guidance through neural crest cells.
  3. (2004). Coordinated regulation of gene expression by Brn3a in developing sensory ganglia.
  4. (2002). Developmental regulation of somite derivatives: muscle, cartilage and tendon.
  5. Differential requirement for Plexin-A3 and -A4 in mediating responses of sensory and sympathetic neurons to distinct class 3 Semaphorins.
  6. (1997). Disruption of semaphorin III/D gene causes severe abnormality in peripheral nerve projection.
  7. (2005). Distinct roles for secreted semaphorin signaling in spinal motor axon guidance.
  8. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1.
  9. (2006). Guidance of trunk neural crest migration requires neuropilin 2/semaphorin 3F signaling.
  10. (1987). Interactions between somite cells: the formation and maintenance of segment boundaries in the chick embryo.
  11. (1998). Neural crest cell dynamics revealed by time-lapse video microscopy of whole embryo chick explant cultures.
  12. (2009). Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification.
  13. (2008). Plexin A3 and plexin A4 convey semaphorin signals during facial nerve development.
  14. (2008). Plexin-A3 and plexin-A4 restrict the migration of sympathetic neurons but not their neural crest precursors.
  15. (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation.
  16. (2002). Requirement of neuropilin 1-mediated Sema3A signals in patterning of the sympathetic nervous system.
  17. (2007). Selective requirements for neuropilin ligands in neurovascular development.
  18. (2003). Semaphorin 3F is critical for development of limbic system circuitry and is required in neurons for selective CNS axon guidance events.
  19. (2004). Somite polarity and segmental patterning of the peripheral nervous system.
  20. (1999). The Neural Crest. New York:
  21. (2000). The paired homeobox gene Uncx4.1 specifies pedicles, transverse processes and proximal ribs of the vertebral column.
  22. (2000). Uncx4.1 is required for the formation of the pedicles and proximal ribs and acts upstream of Pax9. Development

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