Neural crest and placode roles in formation and patterning of cranial sensory ganglia in lamprey

• Published in: Genesis (New York, N.Y. : 2000) Vol. 58; no. 5; pp. e23356 - n/a
• Main Authors: Yuan, Tian, York, Joshua R., McCauley, David W.
• Format: Journal Article
• Language: English
• Published: Hoboken, USA John Wiley & Sons, Inc 01.05.2020; Wiley Subscription Services, Inc
• Subjects: Ablation; Animals; Cell differentiation; Cell lineage; Clusters; cranial ganglia; Cranial nerves; CRISPR; CRISPR/Cas9; Divergence; Embryos; Fish Proteins - genetics; Fish Proteins - metabolism; Forkhead Transcription Factors - genetics; Forkhead Transcription Factors - metabolism; Ganglia; Ganglia, Sensory - cytology; Ganglia, Sensory - growth & development; Ganglia, Sensory - metabolism; Gene expression; Genetic modification; lamprey; Lampreys - growth & development; Lampreys - metabolism; Morphology; Neural crest; Neural Crest - growth & development; Neurogenesis; Neuroglia - cytology; Neuroglia - metabolism; Neuronal-glial interactions; Neurons; Neurons - cytology; Neurons - metabolism; Pattern formation; Peripheral nervous system; Petromyzon marinus; placode; Population genetics; Sensory neurons; Skull; Skull - growth & development; SOX Transcription Factors - genetics; SOX Transcription Factors - metabolism; Vertebrates; placode; CRISPR/Cas9; lamprey; cranial ganglia; neural crest
• DOI: 10.1002/dvg.23356
• ISSN: 1526-954X

Summary Vertebrates possess paired cranial sensory ganglia derived from two embryonic cell populations, neural crest and placodes. Cranial sensory ganglia arose prior to the divergence of jawed and jawless vertebrates, but the developmental mechanisms that facilitated their evolution are unknown. Using gene expression and cell lineage tracing experiments in embryos of the sea lamprey, Petromyzon marinus, we find that in the cranial ganglia we targeted, development consists of placode‐derived neuron clusters in the core of ganglia, with neural crest cells mostly surrounding these neuronal clusters. To dissect functional roles of neural crest and placode cell associations in these developing cranial ganglia, we used CRISPR/Cas9 gene editing experiments to target genes critical for the development of each population. Genetic ablation of SoxE2 and FoxD‐A in neural crest cells resulted in differentiated cranial sensory neurons with abnormal morphologies, whereas deletion of DlxB in cranial placodes resulted in near‐total loss of cranial sensory neurons. Taken together, our cell‐lineage, gene expression, and gene editing results suggest that cranial neural crest cells may not be required for cranial ganglia specification but are essential for shaping the morphology of these sensory structures. We propose that the association of neural crest and placodes in the head of early vertebrates was a key step in the organization of neurons and glia into paired sensory ganglia.