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First published online 18 February 2004
doi: 10.1242/dev.01018

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Newborn horizontal cells migrate bi-directionally across the neuroepithelium during retinal development

Department of Neuroscience, Unit of Developmental Neuroscience, Biomedical Center, Uppsala Univeristy, S-751 23, Uppsala, Sweden

View larger version (119K): [in a new window]   Fig. 1. Fluorescence immunohistochemistry for Lim1 and Prox1 in stage 24-35 developing avian retina. Micrographs showing immunohistochemistry for (AH) Lim1 (green) in horizontal cells (HCs) and Ng-CAM (red) on ganglion cells in stage 24-35 retina. (I) Overview of Lim1 immunoreactivity in stage 35 retina. The gradual spatial maturation with corresponding developmental stages are indicated. (J-M) Prox1 (red) and Lim1 (green) immunoreactivity in (J, K) stage 28, (L) stage 33 and (M) stage 35 retinas. Arrows in I and J indicate the central region of the retina. st, stage. Scale bars: in A (for A-C), D (for D-H), K, L (for L-M) are 20 µm and I (for I-J) is 100 µm.

View larger version (55K): [in a new window]   Fig. 2. Micrographs showing Lim1 immunohistochemistry in BrdU-, cytochalasin D- and Colcemid-treated retinas. Fluorescence micrographs showing (A-E) Lim1 (green) and BrdU (red) labelling in retinas at different developmental stages. See also Table 1. Arrows in A and B indicate double labelled cells. (F-H) Micrographs showing Lim1 (green) and Ng-CAM (red) in (F) cytochalasin D-treated, (G) Colcemid-treated and (H) control-treated retinas. Embryos were analysed at stage 33. gcl, ganglion cell layer (always oriented down); inl, inner nuclear layer; st, stage. Scale bars: 20 µm.

View larger version (89K): [in a new window]   Fig. 5. Lamination of the stage 35 retina as shown by transcription factor immunoreactivity. Representative fluorescence micrographs showing transcription factor immunoreactivity in the central region of stage 35 retina. (A) Pax6, (B) Prox1, (D) Ap2, (E) Prox1, (G) Lim3, (H) Prox1, (J) Lim3, (K) Chx10, (M) Lim1 and (N) Chx10. (C,F,I,L,O) Merged image of the fluorescence micrographs presented in the top two rows. (P) Schematic summary of the immunoreactivity shown in A-O. (+) Moderate and (++) strong immunoreactivity. The results are representative of and were collected from more than three animals in each case. ONL/onl: outer nuclear layer, INL/inl: inner nuclear layer (a: outer external INL, b: inner external INL, c: outer internal INL, d: inner internal INL), GCL/glc: ganglion cell layer. Scale bar: A (for A-O) 20 µm.

View larger version (102K): [in a new window]   Fig. 3. GFP and Lim1 immunohistochemistry in biolistically transfected stage 31 retinas. (A-C) A time-lapse series of a retinal slice from a biolistically transfected stage 31 retina using a green fluorescent protein (GFP) expression vector. A cell indicated by a large arrowhead is migrating towards the ventricular side in relation to its starting point (small arrowhead). (D) Lim1 (red) and GFP (green) co-labelling in cells fixed and cryosectioned 24 hours after gene transfer. (E-H) GFP (green), and other markers (red) in fixed and cryosectioned retinas at different time points after transfection. White arrows indicate gold particles in the internal retina. Black arrows indicate GFP and antibody co-expression. (E) GFP and Prox1 22 hours after transfection. (F) Ganglion cell marker Ng-CAM (G4) expression and gold particle penetration 15 minutes after transfection. GFP is not yet expressed. (G) Ganglion cell marker Islet1 and GFP, 22 hours after transfection. (H) GFP and Ng-CAM (G4) in a retina 18 hours after transfection. Gold particles as well as cells expressing GFP are found on the ventricular side of the retina (white arrow). Scale bars: in A (for A-C), D,E (for E-H) 20 µm.

View larger version (71K): [in a new window]   Fig. 4. Lim1+ cells are also positive for GABA and calretinin. Fluorescence and differential interference micrographs of (A-D) GABA (red) and Lim1 (green) immunoreactivity in HCs of a stage 44 retina. (A) Merged image of B, C and D. (E-H) Calretinin (red) and Lim1 (green) immunoreactivity in stage 45 retina. (E) Merged image of F, G and H. Scale bars: in A,B (for B-D), E,F (for F-H) 10 µm.

View larger version (23K): [in a new window]   Fig. 6. Hypothetical models for cell differentiation and migration in chick embryo retina. (A) In the current model for retinal development cells migrate directly to their final lamina. (B) In the model suggested by this work, HCs migrate bi-directionally across the neuroepithelium before attaining their final position. Numbers denote developmental stages. PR: photoreceptors, HC, horizontal cells; BP, bipolar cells; AC, amacrine cells; RGC, retinal ganglion cells; GCL, ganglion cell layer.

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