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First published online 15 December 2008
doi: 10.1242/dev.026419

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Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system

¹ Department of Zoology, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502, Japan.
² Department of Molecular and Cellular Biology, Division of Genetics and Development, University of California, Berkeley, CA 94720, USA.

View larger version (49K): [in this window] [in a new window]   Fig. 1. Development of the A- and b-line central nervous system in the Ciona embryo. (A) Schematic representations of A- and b-line neuronal cell lineages of the bilaterally symmetrical embryos at the late gastrula stage. Cell names are shown in the lower panel. (B,C) A schematic representation of the CNS cells at the tailbud stage from the (B) dorsal and (C) lateral views, and their lineages. Arrows indicate cell lineages and the cells with the same colors are derived from the single cells at the late gastrula stage (enclosed by pink lines). Cells enclosed by thick black lines are post-mitotic cells destined to become motoneurons. At the early tailbud stage, three pairs of presumptive motoneurons are post-mitotic. Until the mid-tailbud stage, two pairs of post-mitotic presumptive motoneurons are differentiated from the remaining two pairs of the visceral ganglion (VG) cells after cell divisions, as shown in the upper part of B. (D) The central nervous system of a tailbud embryo developed from an egg electroporated with Fgf8/17/18>RFP/AchTP>GFP. (E) A late tailbud embryo developed from an egg electroporated with Fgf8/17/18>RFP and AchTP>GFP. Arrowheads indicate motoneurons. (F) The central nervous system of a tailbud embryo developed from an egg electroporated with Fgf8/17/18>RFP/FoxB>GFP. RFP marks the A9.30-descendants and GFP marks neurons. LNC, the lateral rows of the nerve cord; DNC, the dorsal row of the nerve cord; VNC, the ventral row of the nerve cord.

View larger version (77K): [in this window] [in a new window]   Fig. 2. Expression profiles of the regulatory genes. (A) A- and b-line neural cells at the late gastrula stage, (B) posterior sensory vesicle (PSV), neck, VG and nerve cord at the early tailbud stage, and (C) VG at the middle tailbud stage. Each expression is shown by a red rectangle. (D) A hierarchical clustering of the neural cells based on the expression profiles of transcription factor genes shown in B.

View larger version (65K): [in this window] [in a new window]   Fig. 3. Gene regulatory networks in the ascidian CNS. (A) Summary of these networks. (B-E) Diagrams of gene circuits in (B) A11.64 (PSV), (C) A11.62 (neck), (D) A11.118 (VG) and (E) A11.116 (caudal nerve cord) at the early tailbud stage. The color code for cells is the same as in Fig. 1. Transcription factor genes and signaling ligand genes are indicated by rectangles and ovals, respectively. Genes expressed in the ancestors of the cell but not expressed at this stage are enclosed by broken lines. Genes that are not expressed in either the specified cell or its ancestors are shown in gray. Arrows indicate transcriptionally regulatory interactions. The lines ending in a bar indicate repression. See the text for details.

View larger version (51K): [in this window] [in a new window]   Fig. 4. FgF8/17/18 delineates PSV and neck regions. (A-H) Expression of (A,B) Otx, (C,D) En, (E,F) Pax2/5/8-A and (G,H) Hox1 in A,C,E,G control embryos and (B,D,F,H) experimental embryos developed from eggs injected with Fgf8/17/18 MO. Cell identities were determined by DAPI staining of nuclei (inserts in A-H). Cells from the posterior end of the SV (A11.63) to the middle part of the VG (A11.118 or its descendants) are enclosed by red and light-blue lines, which show the expression or lack of expression of the indicated genes, respectively. Broken white lines indicate the boundaries of the PSV/neck and the neck/VG. Note that A11.119 is about to divide, or has recently divided, into two daughter cells in A,B,E,F. For simplicity, they are enclosed by single lines. The embryos shown in G and H are at a slightly later stage, when Hox1 gene expression is more prominent. (I,J) Schematic representations of the brain regionalization mechanism by Fgf8/17/18 in (I) the normal embryo and (J) Fgf8/17/18-morphant embryo. Note that Fgf8/17/18 is not expressed in the VG at the tailbud stage but is expressed in the progenitor cells (A9.30) in the neural plate.

View larger version (62K): [in this window] [in a new window]   Fig. 5. The Fgf signaling between the late gastrula stage and the neurula stage is required for Pax2/5/8-A expression. (A-D) Expression of Fgf8/17/18 from the 44-cell stage to the neurula stage. Expression in A7.6 is shown by black arrowheads and expression in the A9.30 is shown by white arrowheads. (E-H) Expression of Pax2/5/8-A following U0126 treatment at different time points. Numbers indicate the total number of embryos analyzed. The developmental time point when embryos were placed in sea water containing U0126 is shown in the top. Embryos treated with U0126 from the late gastrula stage when Fgf8/17/18 expression in A9.30 begins do not express Pax2/5/8-A, whereas embryos treated with U0126 from the neurula stage express Pax2/5/8-A.

View larger version (76K): [in this window] [in a new window]   Fig. 6. Snail directs localized expression of Fgf8/17/18. (A-C) Expression of (A,A') Snail and (B,B',C) Fgf8/17/18 was examined in (A,B) control unperturbed embryos, (A',B') Neurogenin-knockdown embryos and (C) Snail-knockdown embryos. Red and white arrowheads indicate A9.30 and A9.32, respectively. (Insets in A and A') High-magnification images of the left side of the embryos shown in A and A'. A9.30 and A9.32 are enclosed by red and white lines, respectively. Note that the embryos shown in B,B' and C are slightly older than those in A and A'. (D) A schematic diagram of regulation of Fgf8/17/18. See the text for details.

View larger version (96K): [in this window] [in a new window]   Fig. 7. Retinoic acid is required for Hox1 expression. (A) Radlh2 is expressed in the most anterior muscle cells at the tailbud stage (upper panel, a lateral view; lower panel, a dorsal view). (B) Hox1 is expressed in the neck region, the anterior part of the VG and the anterior part of the caudal nerve cord within the CNS of control unperturbed embryos. Red and yellow arrowheads indicate boundaries between the neck and the visceral ganglion and between the visceral ganglion and the caudal nerve cord, respectively. (C) Hox1 expression is not observed in RaldH1-knockdown embryos. (D) A schematic diagram of regulation of Hox1. FoxB represses Hox1, and this repression may be through Cyp26, which is expressed under the control of FoxB. See the text for details.

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