Neural crest contributions to the lamprey head

Abstract

The neural crest is a vertebrate-specific cell population that contributes to the facial skeleton and other derivatives. We have performed focal DiI injection into the cranial neural tube of the developing lamprey in order to follow the migratory pathways of discrete groups of cells from origin to destination and to compare neural crest migratory pathways in a basal vertebrate to those of gnathostomes. The results show that the general pathways of cranial neural crest migration are conserved throughout the vertebrates, with cells migrating in streams analogous to the mandibular and hyoid streams. Caudal branchial neural crest cells migrate ventrally as a sheet of cells from the hindbrain and super-pharyngeal region of the neural tube and form a cylinder surrounding a core of mesoderm in each pharyngeal arch, similar to that seen in zebrafish and axolotl. In addition to these similarities, we also uncovered important differences. Migration into the presumptive caudal branchial arches of the lamprey involves both rostral and caudal movements of neural crest cells that have not been described in gnathostomes, suggesting that barriers that constrain rostrocaudal movement of cranial neural crest cells may have arisen after the agnathan/gnathostome split. Accordingly, neural crest cells from a single axial level contributed to multiple arches and there was extensive mixing between populations. There was no apparent filling of neural crest derivatives in a ventral-to-dorsal order, as has been observed in higher vertebrates, nor did we find evidence of a neural crest contribution to cranial sensory ganglia. These results suggest that migratory constraints and additional neural crest derivatives arose later in gnathostome evolution.

Development of the viscerocranial skeleton during embryogenesis of the sea lamprey,Petromyzon Marinus

“…Embryos were fixed at stages 25-30 in MEMFA as described (McCauley and Bronner-Fraser, 2003), dehydrated and stored in 100% methanol at À20 C. Embryos and pro-larvae were staged according to the developmental staging table described by Tahara (1988) for Lampetra reissneri. Animals used in this study were housed according to protocols approved by the University of Oklahoma Institutional Animal Care and Use Committee.…”

“…Neural crest cells were labeled with DiI (Molecular Probes, Invitrogen) by pressure injection at stage 22 when neural crest cells are undergoing migration, as described previously (McCauley and Bronner-Fraser, 2003). Labeled embryos were cultured at 18 C for 30 days, fixed in MEMFA, sectioned (20-100 mm) using a Vibratome (Pelco 101 Series 1000, St. Louis), and imaged for fluorescence (ExBP550/25;EmBP605/70).…”

“…Chondrogenesis of the lamprey branchial skeleton was characterized at cellular and ultrastructural levels by Morrison and her colleagues (2000) and development of the branchial basket was recently described using the Weigert staining method for elastin . The lamprey branchial basket is thought to be derived from the neural crest, as inferred from the results of ablation and cell labeling studies (Langille and Hall, 1988;McCauley and Bronner-Fraser, 2003). A pair of trabecular neurocranial cartilages supports the brain rostrally.…”

Comparative analysis of neural crest cell death, migration, and function during vertebrate embryogenesis

“…Shortly after at stage 20, neural crest cell migration commences, and by stage 22 (E7), the presumptive branchial arch region is populated with neural crest cells (Horigome et al, 1999). Similar to mouse, chick, frog, and fish, neural crest cells from the midbrain or immediately caudal to the mid-hindbrain boundary invade the first arch (McCauley and Bronner-Fraser, 2003). Transverse sections of stage 23 embryos have revealed that neural crest cells migrating into the first arch do so both subectodermally as well as along a medial pathway to surround the mesoderm.…”

“…One significant difference, however, is the degree of caudal migration exhibited by hindbrain-derived neural crest cells. Only limited migration of neural crest cells from individual rhombomeres to the adjacent rostral or caudal rhombomere has been observed in gnathostomes, whereas this is greatly exaggerated in the lamprey (McCauley and Bronner-Fraser, 2003). Another significant difference between basal vertebrates and gnathostomes is that the lamprey caudal branchial neural crest cell population is initially unsegmented, similar to urodeles and teleosts (Hö rstadius and Sellman, 1946;Schilling and Kimmel, 1994), and moves in a sheet-like manner.…”