ArticlePloS one2013
Retinoic acid upregulates ret and induces chain migration and population expansion in vagal neural crest cells to colonise the embryonic gut.
Article in PloS one, 2013. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 40 papers.
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Who cites it
40 citing papers in PubMed, 70 citations in OpenAlex.
- Retinol dehydrogenase 10-mediated retinoic acid signaling regulates the neural crest cell microenvironment during enteric nervous system formation.Human molecular genetics · 2026Article
- Perlecan, CollagenXVIII, and Agrin Expression in Normo-, Hypo-, and Aganglionic Segments in Hirschsprung's Disease.Neurogastroenterology and motility · 2026Article
- Retinoic Acid Inhibition Alters Intestinal Composition in Zebrafish: A Non-genetic Model to Study Hirschsprung Disease?Neurogastroenterology and motility · 2025Article
- Intestinal neuron-associated macrophages in health and disease.Nature immunology · 2025Review
- Ancient emergence of neuronal heterogeneity in the enteric nervous system of jawless vertebrates.Developmental biology · 2025Article
- Genetic regulation of enteric nervous system development in zebrafish.Biochemical Society transactions · 2024Review
- Virus-Triggered Autoimmunity Was Associated With Hirschsprung's Disease Through Activation of Innate Immunity.Journal of immunology research · 2024Article
- Dendritic Inhibition by Shh Signaling-Dependent Stellate Cell Pool Is Critical for Motor Learning.The Journal of neuroscience : the official journal of the Society for Neuroscience · 2022Article
- Innervation in organogenesis.Current topics in developmental biology · 2022Article
- Defining Pathological Activities of ALK in Neuroblastoma, a Neural Crest-Derived Cancer.International journal of molecular sciences · 2021Review
- Cell-autonomous retinoic acid receptor signaling has stage-specific effects on mouse enteric nervous system.JCI insight · 2021Article
- Hirschsprung's Disease-Recent Understanding of Embryonic Aspects, Etiopathogenesis and Future Treatment Avenues.Medicina (Kaunas, Lithuania) · 2020Review
- Extrinsic innervation of the pelvic organs in the lesser pelvis of human embryos.Journal of anatomy · 2020Article
- Development of the Autonomic Nervous System: Clinical Implications.Seminars in neurology · 2020Review
- Retinoic Acid Accelerates the Specification of Enteric Neural Progenitors from In-Vitro-Derived Neural Crest.Stem cell reports · 2020Article
- Large intestine embryogenesis: Molecular pathways and related disorders (Review).International journal of molecular medicine · 2020Review
- Neurogenesis From Neural Crest Cells: Molecular Mechanisms in the Formation of Cranial Nerves and Ganglia.Frontiers in cell and developmental biology · 2020Review
- Induced pluripotent stem cells for disease modeling, cell therapy and drug discovery in genetic autonomic disorders: a review.Clinical autonomic research : official journal of the Clinical Autonomic Research Society · 2019Review
- Abnormal serum vitamin A levels and retinoic acid receptor α expression patterns in children with anorectal malformation.Pediatric surgery international · 2019Article
- The molecular basis of neural crest axial identity.Developmental biology · 2018Review
Corrections and comments
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Authors and funding
4 authors at 2 institutions in 1 country.
Funding
No grant is acknowledged in the PubMed record.
Abstract
Vagal neural crest cells (VNCCs) arise in the hindbrain, and at (avian) embryonic day (E) 1.5 commence migration through paraxial tissues to reach the foregut as chains of cells 1-2 days later. They then colonise the rest of the gut in a rostrocaudal wave. The chains of migrating cells later resolve into the ganglia of the enteric nervous system. In organ culture, E4.5 VNCCs resident in the gut (termed enteric or ENCC) which have previously encountered vagal paraxial tissues, rapidly colonised aneural gut tissue in large numbers as chains of cells. Within the same timeframe, E1.5 VNCCs not previously exposed to paraxial tissues provided very few cells that entered the gut mesenchyme, and these never formed chains, despite their ability to migrate in paraxial tissue and in conventional cell culture. Exposing VNCCs in vitro to paraxial tissue normally encountered en route to the foregut conferred enteric migratory ability. VNCC after passage through paraxial tissue developed elements of retinoic acid signalling such as Retinoic Acid Binding Protein 1 expression. The paraxial tissue's ability to promote gut colonisation was reproduced by the addition of retinoic acid, or the synthetic retinoid Am80, to VNCCs (but not to trunk NCCs) in organ culture. The retinoic acid receptor antagonist CD 2665 strongly reduced enteric colonisation by E1.5 VNCC and E4.5 ENCCs, at a concentration suggesting RARα signalling. By FACS analysis, retinoic acid application to vagal neural tube and NCCs in vitro upregulated Ret; a Glial-derived-neurotrophic-factor receptor expressed by ENCCs which is necessary for normal enteric colonisation. This shows that early VNCC, although migratory, are incapable of migrating in appropriate chains in gut mesenchyme, but can be primed for this by retinoic acid. This is the first instance of the characteristic form of NCC migration, chain migration, being attributed to the application of a morphogen.
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