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Cell migration in the postembryonic development of the fish lateral line

Dora Sapède^*, Nicolas Gompel^*, Christine Dambly-Chaudière and Alain Ghysen

Laboratoire de Neurogénétique, INSERM E0012, cc 103, Université Montpellier II, Place E. Bataillon, 34095 Montpellier, France
^* These two authors contributed equally to this work

View larger version (114K): [in a new window]   Fig. 1. Time-lapse video microscopy of primII. The cells pictured in A,C are outlined and numbered in B,D. Cells 1, 5, 19 and 35 have also been numbered in A,C to illustrate the change in the overall morphology of the primordium during its journey. The broken lines indicate intersomitic boundaries. The time lapse covered 2 hours 30 minutes between frames A and B, at a rate of one frame per minute. (E-H) Irregularity in the progression of primII cells. (E,F) Although most cells move to the tail (white arrows), cell 1 near the front of the primordium moves backwards for a short while (black arrow). This cell then resumed its caudal progression. (G,H) The cells labelled with black arrows (cells 3 and 5 in B,D) move sideways rather than along the main path (white arrows). Time separation between E and F, and G and H was 10 minutes. A cell at the metaphase/early telophase of mitosis is seen in G,H (outline). Anterior is towards the left.

View larger version (100K): [in a new window]   Fig. 2. Labelling primII cells. Zygotes were injected with caged-fluorescein and allowed to develop for 48 hours, and the primII cells were irradiated with a brief UV pulse while on somite 6 (A, arrowed circle). On the next day, fluorescein was detected in one secondary neuromast located at the junction between somites 9 and 10, as well as in the primordium which had moved caudally to somite 12 (B, corresponding to the framed region in A). The neuromast (NMII) and primordium (primII) are shown at a higher magnification in C,D. g, glial cell. (E-G) Uncaging the D0 group, which stays on the first somite for many hours (E), appears on the next day in the presence of fluorescent cells in D1, the first neuromast of the dorsal line (F), as well as in primII (G). Anterior is towards the left.

View larger version (124K): [in a new window]   Fig. 3. Video time lapse illustrating the splitting of D0, a large group of primordium-like cells that stays for many hours on somite 1, into primII (black-numbered cells) and D1 (white-numbered cells). Sister cells resulting from a mitosis are named a and b (e.g. 16a and 16b). Anterior is towards the left.

View larger version (71K): [in a new window]   Fig. 4. Expression of the gene CB701 in primII (A) as well as on secondary primordia of the ALL system (B,C). At 48 haf, primII migrating towards the tail (arrow) has reached the primary neuromast L1 (A). The expression in the primordium is more intense at the trailing edge, much as it was in primI (Gompel et al., 2001b), and presumably defines the cells that will form the first secondary neuromast. (B) A secondary primordium (arrowhead) of the supra-orbital branch of the ALL system, between the first neuromast of this line (SO1) and the olfactory bulb (ob). (C) A secondary primordium (arrowhead) of the infra-orbital branch as seen in a near ventral view of the head, with the ventral midline shown as the broken line. Asterisks indicate neuromasts of the infra-orbital line. Anterior is towards the left.

View larger version (112K): [in a new window]   Fig. 5. Neuromast migration. (A) A labelled clone of epidermal cells extends anteroposteriorly at the level of the horizontal myoseptum, where proneuromasts are deposited. Each labelled cell can be identified on the basis of its shape and position relative to neighbours, and traced for several days. Neuromasts (arrows) have differentiated at 48 haf just dorsal to the clone and are seen to move ventrally through the clone in B-F. Note that some cells in the clone are recruited as pore cells by one of the neuromasts (arrowheads in C-F). (G) 4-Di-2-Asp labelling reveals the presence of the neuromast hair cells. This view was combined to that of the clone and superimposed on a bright field view showing the line of melanocytes along the horizontal myoseptum. The recruitment of epidermal pore cells is shown in more detail in H-K. A clone similar to that in A-G was examined at higher magnification. The progeny of cells marked 2 and 3 in H will contribute to the annulus-like pore of neuromast L2 at 72 haf (J). The morphology of these epidermal cells changes from polygonal to crescent shape, thereby defining the pore through which the hairs will protrude (I). Later on, other cells of the same clone were recruited to form the pore of the third secondary neuromast (K). Anterior is towards the left.

View larger version (96K): [in a new window]   Fig. 6. The juvenile lateral line of Danio (A), Astyanax (B) and Oryzias (medaka; C). The general pattern is identical to that in the adults, except for the size of the stitches. In Danio adults the stitches comprise two or sometimes three parallel rows of neuromasts totalling up to 30 organs. (C) In the medaka juvenile shown here, stitch formation had not yet taken place; in the adults the stitches are much smaller than in Danio or Astyanax – two to three neuromasts at most. One untypical neuromast has remained close to the horizontal myoseptum (arrow), whereas the other organs of the L-PLL have migrated away from it. In medaka, where many superficial fluorescent cells obscure the pattern of neuromasts, we reduced the intensity of this fluorescence by a factor of two to make the lateral line pattern stand out. Anterior is towards the left.

View larger version (131K): [in a new window]   Fig. 7. Early development of the PLL in Astyanax. (A) At 53 haf, several neuromasts of the anterior lateral line (ALL) system have differentiated, as well as all the neuromasts of the L-PLL (L1-L7 and three terminal neuromasts). The white dots that alternate with the labelled neuromasts are the organs on the other side of the embryo. (B) At 72 haf, the anteriormost neuromasts L1 and L2 have migrated about half way to the ventral midline, whereas the first neuromast of the L' and D line have formed. (C) At 4 days, additional neuromasts have formed on the D and L' lines. This larva is slightly tilted so that the two D2 neuromasts can be seen side by side. (D) At 5 days, the L' line has further extended. The asterisk labels a neuromast of the L' line, which might belong to the same wave that produces L'1 to L'4, or be the first neuromast of a second L' wave. (E) Nomarski micrograph of an Astyanax primordium showing its prepatterning. P1, P2 and P3 prefigure three neuromasts where the internal chamber through which the hairs will extend is already formed. A fourth pre-neuromast, P4, can be detected on the basis of the radial organisation of primordium cells. Anterior is towards the left.

View larger version (152K): [in a new window]   Fig. 8. Early development of the PLL in Oryzias. (A) Labelling with 4-di-2-Asp at 10-12 days of development reveals one lateral and one ventral line comprising ten neuromasts each at most. No labelling can be observed at earlier times. (B) At 3 days, a primordium (outlined by arrowheads) migrates from head to tail along the horizontal myoseptum, leaving a nerve (arrows) in its wake. (C) Soon after being deposited, and much before differentiation, pro-neuromasts (outlined in white) begin to migrate ventrally, towing their innervating fibres (white arrowheads). The nerve (black arrowheads) remains on the myoseptum. Black arrow indicates a glial cell. (D) At the time the neuromasts capture 4-di-2-Asp, trans-synaptic labelling of the axons reveals the path followed by the neuromasts when they migrated away from the horizontal myoseptum. (E) Some of the caudal neuromasts migrate dorsally rather than ventrally. These neuromasts are observed in juvenile fish, and we have no way of ascertaining whether they come from the L or L'-PLL line present in larvae (A), or whether they arise as a later set. Anterior is towards the left.