A fate-map for cranial sensory ganglia in the sea lamprey

Abstract

Cranial neurogenic placodes and the neural crest make essential contributions to key adult characteristics of all vertebrates, including the paired peripheral sense organs and craniofacial skeleton. Neurogenic placode development has been extensively characterized in representative jawed vertebrates (gnathostomes) but not in jawless fishes (agnathans). Here, we use in vivo lineage tracing with DiI, together with neuronal differentiation markers, to establish the first detailed fate-map for placode-derived sensory neurons in a jawless fish, the sea lamprey Petromyzon marinus, and to confirm that neural crest cells in the lamprey contribute to the cranial sensory ganglia. We also show that a pan-Pax3/7 antibody labels ophthalmic trigeminal (opV, profundal) placode-derived but not maxillomandibular trigeminal (mmV) placode-derived neurons, mirroring the expression of gnathostome Pax3 and suggesting that Pax3 (and its single Pax3/7 lamprey ortholog) is a pan-vertebrate marker for opV placode-derived neurons. Unexpectedly, however, our data reveal that mmV neuron precursors are located in two separate domains at neurula stages, with opV neuron precursors sandwiched between them. The different branches of the mmV nerve are not comparable between lampreys and gnatho-stomes, and spatial segregation of mmV neuron precursor territories may be a derived feature of lampreys. Nevertheless, maxillary and mandibular neurons are spatially segregated within gnathostome mmV ganglia, suggesting that a more detailed investigation of gnathostome mmV placode development would be worthwhile. Overall, however, our results highlight the conservation of cranial peripheral sensory nervous system development across vertebrates, yielding insight into ancestral vertebrate traits.

Characterization of two neurogenin genes from the brook lamprey lampetra planeri and their expression in the lamprey nervous system

“…D). At stage 24, expression intensified in these placodes and was observed in both lobes of the trigeminal ganglion, the posterior lateral line ganglion, the geniculate/anterior lateral line ganglia (which are inferred to be adjacent at this stage as their ganglionic derivatives form a single complex at later stages of development) (Modrell et al, ), and in the petrosal and nodose placodes (Fig. E–G).…”

“…Expression of LpNgnA in the posterior lateral line ganglion parallels that of zebrafish ngn1 and Xenopus Ngn1 and Ngn2 in lateral line placodes (Schlosser and Northcutt, ; Andermann et al, ; Nieber et al, ). An anterior and a posterior lateral line ganglion have been previously identified in lamprey embryos (Kuratani et al, ; Takio et al, ; Modrell et al, ). In lamprey adults an additional ganglion, the intracapsular ganglion, has been observed associated with the anterior lateral line nerve (Ronan and Northcutt, ; Koyama et al, ).…”

“…While we did not detect LpNgnB expression in DRG, LpNgnA is clearly seen in these structures. Expression in the DRG starts at stage 25 and is observed until stage 27, that is before the observation of condensed DRG in P. marinus embryos at embryonic day 16 (approximately Tahara stage 26/27) by HuC/D immunostaining (Modrell et al, ). PmNgnA has also been described as expressed in the DRGs, although the temporal progression has not been defined (Uy et al, ).…”

“…In lamprey adults an additional ganglion, the intracapsular ganglion, has been observed associated with the anterior lateral line nerve (Ronan and Northcutt, ; Koyama et al, ). Given that the geniculate and anterior lateral line ganglia form a single complex as they develop (Modrell et al, ), it is likely that the geniculate and anterior lateral line placode also form a single cell population marked (at least in part) by LpNgnA in stage 24 embryos.…”

Developmental expression of Pitx2c in Xenopus trigeminal and profundal placodes

“…Our comparative analysis highlights a differential combinatorial expression of transcription factors in the profundal and trigeminal placodes and their derived ganglia (Fig 4; Table 1) suggesting that the formation of each placodal domain is independently regulated. In all vertebrates, including the lamprey, the profundal placode is characterized by Pax3 expression (Modrell et al, 2014). Moreover Pax3 is necessary for neurogenesis in the ophthalmic trigeminal placode in chicken (Dude et al, 2009).…”