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doi: 10.1242/10.1242/dev.00451

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Neural crest contributions to the lamprey head

Division of Biology 139-74, California Institute of Technology, Pasadena, CA 91125, USA

View larger version (22K): [in a new window]   Fig. 1. DiI-labeling in the lamprey embryo. Embryos were injected focally with a single bolus of DiI. (A) Embryo fixed immediately after injection to show initial position of labeled cells. (B) Individual embryos were labeled at one of the four positions indicated along the anteroposterior (AP) axis (I, midbrain; II, rostral hindbrain; III, caudal hindbrain; IV, rostral neural tube). (C) Number of embryos labeled at each position and initial positions of labeled cells determined retrospectively after fixation.

View larger version (60K): [in a new window]   Fig. 2. Pax2 expression and DiI-labeling of cranial neural crest cells at the midbrain and rostral-most hindbrain. (A) Lamprey Pax2 expression at stage 23. Pax2 is expressed at the mid-hindbrain boundary (mhb) and within the otic vesicle (ov). (B) DiI-labeled cells originating from the midbrain region have migrated into the first (mandibular) arch of a stage 23 embryo. (C) Cells originating from the rostral hindbrain have migrated into the mandibular arch. d indicates plane of section shown in D. (D) transverse section through mandibular arch of embryo shown in C in which labeled cells are positioned both medial and lateral to the mesodermal core. (E) Pax2 expression continued in the mid-hindbrain boundary and otic vesicle at stage 25. (F) Stage 25 embryo labeled in the midbrain; DiI-labeled cells are found in the upper (ul) and lower (ll) lips; g,h indicate planes of section shown in G and H, respectively. (G) Horizontal section indicating labeled cells contributed to the ophthalmic (V1) and maxillomandibular (V2) lobes of the trigeminal ganglion. (H) Plane of section through developing lips indicates labeled cells present both medial and lateral to mesodermal core. (I) Stage 26 embryo in which cells originating from midbrain persist in the upper and lower lips. Scale bar: 200 µm.

View larger version (105K): [in a new window]   Fig. 3. Migration of cranial neural crest cells from hindbrain. (A) Lateral view of stage 23 embryo showing initial hindbrain position of DiI-labeled cells and migration into the hyoid arch (hy). b and c indicate horizontal planes of section shown in B and C, respectively. (B) Migration of cells caudal to the initial site of labeling in the dorsal pharyngeal region. Arrow indicates position of labeled cells caudal to the original position of the DiI label. (C) Ventral section through developing branchial arches. Two most rostral arches containing labeled cells, the hyoid and first branchial arch, have been segregated by the outpocketing of the pharyngeal endoderm in these regions. Labeled cells in the caudal presumptive branchial arch region (pbar) are in a contiguous stream. DiI-labeled cells surround the mesodermal core of the hyoid arch (arrow pointing from white asterisk). (D) Lateral view of stage 23 embryo shown in cross-section in E. (E) Cross-section through hyoid arch of D at position marked e. Labeled neural crest cells have migrated ventrally beneath the ectoderm. (F) Lateral view of stage 25 embryo labeled in the hindbrain region. Neural crest cells have migrated ventrally into the hyoid arch. g indicates plane of section shown in G. (G) Horizontal section of stage 25 embryo shows neural crest cells in the hyoid arch are located in a lateral position beneath the ectoderm (arrow). A few cells can still be seen adjacent to the endoderm. Yellow circle indicates the initial position of the DiI injection. Yellow arrow indicates the direction and distance of migration along the rostrocaudal axis. Scale bar: 200 µm.

View larger version (114K): [in a new window]   Fig. 4. Neural crest cell migration at hindbrain and rostral trunk levels. (A) Stage 23 embryo in which cells originating from the caudal hindbrain region are located rostral to the site of injection within the rostral branchial arches; b-d indicate planes of section in B-D, respectively. (B-D) Neural crest cells from the mid hindbrain region have migrated ventrally and rostrally to populate the rostral branchial arches. (E) Late stage 23 embryo labeled at the hindbrain and rostral trunk neural tube level; by stage 23, labeled cells have migrated ventrally towards the caudal presumptive branchial arches. (F) At stage 25, labeled cells from the caudal hindbrain region are located throughout two branchial arches, having completely filled both arches along the dorsoventral axis. (G) Neural crest cells originating from the caudal hindbrain to rostral trunk level migrated ventrally toward the most caudal presumptive arch and migrated dorsocaudally into the dorsal fin. fm, fin mesenchyme; white arrows, final position of labeled cells; yellow circle, initial position of DiI; yellow arrow, direction and distance of migration away from initial site. Scale bar: 200 µm.

View larger version (82K): [in a new window]   Fig. 5. Rostrocaudal movement of cells originating from the hindbrain. (A) Lateral view of stage 25 embryo. Neural crest cells populate arches ventral and caudal to the site of injection. b indicates horizontal plane of section in B in which neural crest (nc) cells are also found medial to the mesoderm (m). (C) Pan-Dlx immunolabel of section shown in B. Black arrow indicates Dlx expression co-localizes with DiI labeled cells surrounding the mesodermal core. (D) Stage 23 embryo in which neural crest cells labeled at the hindbrain level have migrated ventrally in both rostral and caudal directions. e indicates plane of section in E, in which rostal labeled cells are segregated into arches while caudal cells are still in a continuous stream; neural crest cells are found medial to the mesodermal core. (F) Section (10 µm) of boxed region in C; arrowhead indicates Dlx positive cells excluded from mesodermal core. Yellow circle, initial position of DiI dorsally; yellow arrows, direction and distance of migration of labeled cells. Scale bars: in B, 200 µm for A-C; in D, 200 µm for D,E.

View larger version (68K): [in a new window]   Fig. 6. Neural crest cells labeled at stage 22 and fixed for observation at stage 25. (A) Pax2 expression at stage 25. Expression at the mid-hindbrain boundary (mhb) and the otic vesicle (ov) is used to indicate the position of the DiI-labeled cells; (B) Embryo labeled at the hindbrain region near the otic vesicle. At stage 25, labeled cells are found throughout mid-branchial arches; (C) Embryo labeled at the caudal hindbrain region. Cells have migrated ventrally to populate the dorsalmost portion of the caudal branchial arches. Cells have also migrated from the site of origin caudally into the dorsal fin. fm, fin mesenchyme; mhb, mid-hindbrain boundary; ov, otic vesicle; yellow circle, initial position of DiI; yellow arrow, direction and distance of migration of labeled cells along the rostrocaudal axis. Scale bar: 200 µm.

View larger version (128K): [in a new window]   Fig. 7. Ablation of neural crest causes a reduction in pigment and loss of the dorsal fin. (A) Control stage 26 embryo. (B) Stage 26 embryo after neural crest ablation from hindbrain at stage 21. Pigment cells and dorsal fin are missing from the region dorsal to the site of ablation. Fewer pigment cells are seen ventrally when compared with the control (A). Pigment cells in the operated embryo are smaller and without the stellate morphology seen in pigment cells of the control embryo. arrow, area of reduced pigmentation; *, region missing dorsal fin. Scale bar: 250 µm.

View larger version (70K): [in a new window]   Fig. 8. (A,B) DiI-labeling of trigeminal ganglia. Ophthalmic (V1) and maxillomandibular (V2) lobes of the trigeminal ganglion contain DiI-labeled cells only when DiI also labeled cells of the ectoderm. (B) Horizontal section through plane b shown in A shows labeled cells in the trigeminal ganglion (V1,V2) rostral to the otic vesicle. (C-F) Sox10 immunopositive cells excluded from cranial ganglia. (C) Lateral view of stage 24 embryo immunolabeled with Sox10 antibody. Immunopositive cells are seen in the rostral pharyngeal arches and dorsally surrounding V1 and V2 lobes of the trigeminal ganglion, the eye and the otic vesicle (ov). d and f indicate horizontal planes of section shown in D and F, respectively. e indicates plane of transverse section shown in E taken from a stage 24 companion embryo. Sox10 immunopositive cells are seen between the otic vesicle and V2 of the trigeminal ganglion (arrow in D) and lie medial to, but are excluded from, the placode-derived ganglia V1, V2 and eye (ey) in E. (F) Immunopositive cells are found in the mandibular arch (arrow) and weakly throughout the mesenchyme of the caudal branchial arches. Scale bars: in B, 200 µm for A,B; in C, 200 µm for C-F.

View larger version (53K): [in a new window]   Fig. 9. Cranial neural crest cell migration in the lamprey. Orange arrows indicate migration from the midbrain region; blue arrows indicate migration from the rostral hindbrain (anterior to the otic vesicle) or middle hindbrain region; pink arrows indicate migration of cells from the caudalmost region of the hindbrain or the rostral neural tube. Neural crest cell migration from the midbrain and rostral hindbrain appear similar to other vertebrates. In the mid and caudal regions of the hindbrain and the rostral neural tube, migration appears to involve greater rostral to caudal movement of cells than has been described in other vertebrates. Rostral migration of neural crest is also seen in cells emigrating from the caudal hindbrain region. Although morphological markers and expression of a mid-hindbrain marker (Pax2) have allowed us to determine regions within the hindbrain, we are presently unable to determine the posterior limit of the hindbrain (indicated by?), and the boundary between the hindbrain and the neural tube, because of the lack of sufficient markers for this region and the transient nature of rhombomeric constrictions.

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