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Early B-cell factors 2 and 3 (EBF2/3) regulate early migration of Cajal-Retzius cells from the cortical hem.

Chiara F, Badaloni A, Croci L, Yeh ML, Cariboni A, Hoerder-Suabedissen A, Consalez GG, Eickholt B, Shimogori T, Parnavelas JG, Rakić S - Dev. Biol. (2012)

Bottom Line: Here, we show that Ebf transcription factors are expressed in forebrain signalling centres-the septum, cortical hem and the pallial-subpallial boundary-known to generate CR cells.Accordingly, using in vitro preparations, we demonstrated that both Ebf2 and Ebf3, singly or together, control the migration of CR cells arising in the cortical hem.These findings provide evidence that Ebfs directly regulate CR cell development.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, University College London, UK.

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The distribution of CR cell subpopulations is affected in Ebf2−/− mice. At E12.5, Reelin and Dbx1 expressions are diminished in the septum and augmented in the CH and PSPB of Ebf2−/− mice, respectively (A–H). Cxcr4 expression was diminished in CH and in the dorsal pallium of Ebf2−/− mice compared to w-t littermates (I, J). Ebf3 in the CH and PSPB is extended in Ebf2−/− mice compared to w-t controls, conversely it is diminished in the septum of Ebf2−/− mice compared to w-t controls (K–N). Arrow shows that fewer cells migrate out the CH towards the dorsal PPL of Ebf2−/− mice compared to w-t controls, whereas arrowhead points to cells in the lateral PPL, possibly deriving from the PSPB (A–N). Ebf1 was unchanged (O–P′). Wnt3a domain in the CH is expanded in mutants compared to w-t controls (S, T). p73 cells in the mutant septum are not dispersed along the medial axis as in w-t control (T compared to S, arrows). More p73cells are found in the mutant CH, ChP and TE (T′ compared to S′). CH: cortical hem, ChP: choroid plexus; PPL: preplate, PSPB: pallial subpallial boundary, Sp: septum, St: striatum, TE: thalamic eminences. Scale bars: 100 μm.
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f0030: The distribution of CR cell subpopulations is affected in Ebf2−/− mice. At E12.5, Reelin and Dbx1 expressions are diminished in the septum and augmented in the CH and PSPB of Ebf2−/− mice, respectively (A–H). Cxcr4 expression was diminished in CH and in the dorsal pallium of Ebf2−/− mice compared to w-t littermates (I, J). Ebf3 in the CH and PSPB is extended in Ebf2−/− mice compared to w-t controls, conversely it is diminished in the septum of Ebf2−/− mice compared to w-t controls (K–N). Arrow shows that fewer cells migrate out the CH towards the dorsal PPL of Ebf2−/− mice compared to w-t controls, whereas arrowhead points to cells in the lateral PPL, possibly deriving from the PSPB (A–N). Ebf1 was unchanged (O–P′). Wnt3a domain in the CH is expanded in mutants compared to w-t controls (S, T). p73 cells in the mutant septum are not dispersed along the medial axis as in w-t control (T compared to S, arrows). More p73cells are found in the mutant CH, ChP and TE (T′ compared to S′). CH: cortical hem, ChP: choroid plexus; PPL: preplate, PSPB: pallial subpallial boundary, Sp: septum, St: striatum, TE: thalamic eminences. Scale bars: 100 μm.

Mentions: The expression of Reelin was found diminished in the septum of Ebf2−/− mice compared to wt controls (Fig. 6A compared to B). Interestingly, a stronger signal for Reelin was detected in the CH of Ebf2−/− mice compared to w-t controls (Fig. 6C compared to D). Furthermore, it was expressed less in the dorsal PPL and more strongly in the lateral PPL of Ebf2−/− mice (Fig. 6D) compared to w-t controls (Fig. 6C), indicating that CR cells are trapped in the CH. Dbx1, a homeodomain transcription factor, specifies two CR cell subpopulations originating from the septum and PSPB (Bielle et al., 2005; Griveau et al., 2010). Its expression was found in the expected territories in Ebf2−/− mice. However, Dbx1 signal in the septum of Ebf2−/− was reduced, whereas it was augmented in the PSPB compared to w-t controls (Fig. 6E compared to F, septum; G compared H, PSPB). Ebf3 was expressed in the PPL (Fig. 6M) but, its expression was less in the dorsal PPL and more in the lateral PPL of Ebf2−/− mice (Fig. 6N) compared to w-t controls. This phenotype together with the upregulation of Ebf3 in the CH (Fig. 6M compared to N) resembled Reelin changes observed in Ebf2−/− mice. Furthermore, similar to Dbx1, Ebf3 expression was found diminished in the septum and increased in the PSPB in Ebf2−/− mice compared to w-t controls (Fig. 6K compared to L). On the other hand, the expression of Ebf1 in the CH was unchanged in Ebf2−/− mice compared to w-t controls (Fig. 6O′ compared to P′). Ebf1 was not expressed in the septum of Ebf2−/− animals as in w-t controls (Fig. 6O compared to P). Wnt3a, a secreted signalling molecule specifically expressed in the CH, was found in the expected territories of Ebf2−/− mice, but expanded ventrally compared to wt controls (Fig. 6Q compared to R).


Early B-cell factors 2 and 3 (EBF2/3) regulate early migration of Cajal-Retzius cells from the cortical hem.

Chiara F, Badaloni A, Croci L, Yeh ML, Cariboni A, Hoerder-Suabedissen A, Consalez GG, Eickholt B, Shimogori T, Parnavelas JG, Rakić S - Dev. Biol. (2012)

The distribution of CR cell subpopulations is affected in Ebf2−/− mice. At E12.5, Reelin and Dbx1 expressions are diminished in the septum and augmented in the CH and PSPB of Ebf2−/− mice, respectively (A–H). Cxcr4 expression was diminished in CH and in the dorsal pallium of Ebf2−/− mice compared to w-t littermates (I, J). Ebf3 in the CH and PSPB is extended in Ebf2−/− mice compared to w-t controls, conversely it is diminished in the septum of Ebf2−/− mice compared to w-t controls (K–N). Arrow shows that fewer cells migrate out the CH towards the dorsal PPL of Ebf2−/− mice compared to w-t controls, whereas arrowhead points to cells in the lateral PPL, possibly deriving from the PSPB (A–N). Ebf1 was unchanged (O–P′). Wnt3a domain in the CH is expanded in mutants compared to w-t controls (S, T). p73 cells in the mutant septum are not dispersed along the medial axis as in w-t control (T compared to S, arrows). More p73cells are found in the mutant CH, ChP and TE (T′ compared to S′). CH: cortical hem, ChP: choroid plexus; PPL: preplate, PSPB: pallial subpallial boundary, Sp: septum, St: striatum, TE: thalamic eminences. Scale bars: 100 μm.
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f0030: The distribution of CR cell subpopulations is affected in Ebf2−/− mice. At E12.5, Reelin and Dbx1 expressions are diminished in the septum and augmented in the CH and PSPB of Ebf2−/− mice, respectively (A–H). Cxcr4 expression was diminished in CH and in the dorsal pallium of Ebf2−/− mice compared to w-t littermates (I, J). Ebf3 in the CH and PSPB is extended in Ebf2−/− mice compared to w-t controls, conversely it is diminished in the septum of Ebf2−/− mice compared to w-t controls (K–N). Arrow shows that fewer cells migrate out the CH towards the dorsal PPL of Ebf2−/− mice compared to w-t controls, whereas arrowhead points to cells in the lateral PPL, possibly deriving from the PSPB (A–N). Ebf1 was unchanged (O–P′). Wnt3a domain in the CH is expanded in mutants compared to w-t controls (S, T). p73 cells in the mutant septum are not dispersed along the medial axis as in w-t control (T compared to S, arrows). More p73cells are found in the mutant CH, ChP and TE (T′ compared to S′). CH: cortical hem, ChP: choroid plexus; PPL: preplate, PSPB: pallial subpallial boundary, Sp: septum, St: striatum, TE: thalamic eminences. Scale bars: 100 μm.
Mentions: The expression of Reelin was found diminished in the septum of Ebf2−/− mice compared to wt controls (Fig. 6A compared to B). Interestingly, a stronger signal for Reelin was detected in the CH of Ebf2−/− mice compared to w-t controls (Fig. 6C compared to D). Furthermore, it was expressed less in the dorsal PPL and more strongly in the lateral PPL of Ebf2−/− mice (Fig. 6D) compared to w-t controls (Fig. 6C), indicating that CR cells are trapped in the CH. Dbx1, a homeodomain transcription factor, specifies two CR cell subpopulations originating from the septum and PSPB (Bielle et al., 2005; Griveau et al., 2010). Its expression was found in the expected territories in Ebf2−/− mice. However, Dbx1 signal in the septum of Ebf2−/− was reduced, whereas it was augmented in the PSPB compared to w-t controls (Fig. 6E compared to F, septum; G compared H, PSPB). Ebf3 was expressed in the PPL (Fig. 6M) but, its expression was less in the dorsal PPL and more in the lateral PPL of Ebf2−/− mice (Fig. 6N) compared to w-t controls. This phenotype together with the upregulation of Ebf3 in the CH (Fig. 6M compared to N) resembled Reelin changes observed in Ebf2−/− mice. Furthermore, similar to Dbx1, Ebf3 expression was found diminished in the septum and increased in the PSPB in Ebf2−/− mice compared to w-t controls (Fig. 6K compared to L). On the other hand, the expression of Ebf1 in the CH was unchanged in Ebf2−/− mice compared to w-t controls (Fig. 6O′ compared to P′). Ebf1 was not expressed in the septum of Ebf2−/− animals as in w-t controls (Fig. 6O compared to P). Wnt3a, a secreted signalling molecule specifically expressed in the CH, was found in the expected territories of Ebf2−/− mice, but expanded ventrally compared to wt controls (Fig. 6Q compared to R).

Bottom Line: Here, we show that Ebf transcription factors are expressed in forebrain signalling centres-the septum, cortical hem and the pallial-subpallial boundary-known to generate CR cells.Accordingly, using in vitro preparations, we demonstrated that both Ebf2 and Ebf3, singly or together, control the migration of CR cells arising in the cortical hem.These findings provide evidence that Ebfs directly regulate CR cell development.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, University College London, UK.

Show MeSH
Related in: MedlinePlus