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FoxK mediates TGF-beta signalling during midgut differentiation in flies.

Casas-Tinto S, Gomez-Velazquez M, Granadino B, Fernandez-Funez P - J. Cell Biol. (2008)

Bottom Line: Genet.This regulatory activity does not require direct labial activation by the TGF-beta effector Mad.Thus, we propose that the combined activity of the TGF-beta target genes FoxK and Dfos is critical for the direct activation of lab in the endoderm.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of Texas Medical Branch, Galveston, TX 77555, USA. scasas@cnio.es

ABSTRACT
Inductive signals across germ layers are important for the development of the endoderm in vertebrates and invertebrates (Tam, P.P., M. Kanai-Azuma, and Y. Kanai. 2003. Curr. Opin. Genet. Dev. 13:393-400; Nakagoshi, H. 2005. Dev. Growth Differ. 47:383-392). In flies, the visceral mesoderm secretes signaling molecules that diffuse into the underlying midgut endoderm, where conserved signaling cascades activate the Hox gene labial, which is important for the differentiation of copper cells (Bienz, M. 1997. Curr. Opin. Genet. Dev. 7:683-688). We present here a Drosophila melanogaster gene of the Fox family of transcription factors, FoxK, that mediates transforming growth factor beta (TGF-beta) signaling in the embryonic midgut endoderm. FoxK mutant embryos fail to generate midgut constrictions and lack Labial in the endoderm. Our observations suggest that TGF-beta signaling directly regulates FoxK through functional Smad/Mad-binding sites, whereas FoxK, in turn, regulates labial expression. We also describe a new cooperative activity of the transcription factors FoxK and Dfos/AP-1 that regulates labial expression in the midgut endoderm. This regulatory activity does not require direct labial activation by the TGF-beta effector Mad. Thus, we propose that the combined activity of the TGF-beta target genes FoxK and Dfos is critical for the direct activation of lab in the endoderm.

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Distribution of FoxK in Drosophila embryos. (A and B) Distinct temporal accumulation of the FoxK-L and FoxK-S transcripts by RT-PCR. FoxK-L is present in unfertilized embryos (UE), pupae (P), and head (H) and in thorax (T) and abdomen (Ab) from adult flies (A). FoxK-S accumulates in embryos (E) and salivary glands (SG) and gut from larvae (L). (C and D) In situ hybridization of wild-type embryos using digoxigenin-labeled FoxK-mRNA probes. In stage 16 embryos, the sense probe results in negative signal (C), whereas FoxK mRNA accumulates in the endoderm of parasegments (PS) 3 and 7 (D). (E and F) Single focal plane of whole-mount wild-type embryos stained with anti-FoxK antibody. (E) Stage 15 embryos revealed nuclear FoxK signal in the lining of the single vesicle of the midgut endoderm (arrow). (F) Stage 16 embryos accumulate FoxK in the lining of all four vesicles of the midgut endoderm and gastric constrictions (arrow). (G) Ventral view of an embryo showing FoxK (green) expression along the ventral nerve cord also labeled with anti-Elav (merged image). (H and I) Detail of G showing FoxK and Elav colocalization in the nuclei of ventral cord neurons (H, merge) or FoxK alone (I). All embryos are oriented with the anterior end to the left.
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fig3: Distribution of FoxK in Drosophila embryos. (A and B) Distinct temporal accumulation of the FoxK-L and FoxK-S transcripts by RT-PCR. FoxK-L is present in unfertilized embryos (UE), pupae (P), and head (H) and in thorax (T) and abdomen (Ab) from adult flies (A). FoxK-S accumulates in embryos (E) and salivary glands (SG) and gut from larvae (L). (C and D) In situ hybridization of wild-type embryos using digoxigenin-labeled FoxK-mRNA probes. In stage 16 embryos, the sense probe results in negative signal (C), whereas FoxK mRNA accumulates in the endoderm of parasegments (PS) 3 and 7 (D). (E and F) Single focal plane of whole-mount wild-type embryos stained with anti-FoxK antibody. (E) Stage 15 embryos revealed nuclear FoxK signal in the lining of the single vesicle of the midgut endoderm (arrow). (F) Stage 16 embryos accumulate FoxK in the lining of all four vesicles of the midgut endoderm and gastric constrictions (arrow). (G) Ventral view of an embryo showing FoxK (green) expression along the ventral nerve cord also labeled with anti-Elav (merged image). (H and I) Detail of G showing FoxK and Elav colocalization in the nuclei of ventral cord neurons (H, merge) or FoxK alone (I). All embryos are oriented with the anterior end to the left.

Mentions: Using oligonucleotide primers specific for different exons of the FoxK gene, we detected FoxK transcripts at all stages of Drosophila development (Fig. 3 A). Interestingly, we found a prominent temporal distribution of the FoxK-S and FoxK-L transcripts, whereas FoxK-S was predominantly expressed during the embryonic and larval stages, FoxK-L was mainly seen in pupae, adults, and unfertilized eggs. Moreover, FoxK transcripts were detected in all tissues analyzed: larval salivary glands and gut and adult head, thorax, and abdomen (Fig. 3 B).


FoxK mediates TGF-beta signalling during midgut differentiation in flies.

Casas-Tinto S, Gomez-Velazquez M, Granadino B, Fernandez-Funez P - J. Cell Biol. (2008)

Distribution of FoxK in Drosophila embryos. (A and B) Distinct temporal accumulation of the FoxK-L and FoxK-S transcripts by RT-PCR. FoxK-L is present in unfertilized embryos (UE), pupae (P), and head (H) and in thorax (T) and abdomen (Ab) from adult flies (A). FoxK-S accumulates in embryos (E) and salivary glands (SG) and gut from larvae (L). (C and D) In situ hybridization of wild-type embryos using digoxigenin-labeled FoxK-mRNA probes. In stage 16 embryos, the sense probe results in negative signal (C), whereas FoxK mRNA accumulates in the endoderm of parasegments (PS) 3 and 7 (D). (E and F) Single focal plane of whole-mount wild-type embryos stained with anti-FoxK antibody. (E) Stage 15 embryos revealed nuclear FoxK signal in the lining of the single vesicle of the midgut endoderm (arrow). (F) Stage 16 embryos accumulate FoxK in the lining of all four vesicles of the midgut endoderm and gastric constrictions (arrow). (G) Ventral view of an embryo showing FoxK (green) expression along the ventral nerve cord also labeled with anti-Elav (merged image). (H and I) Detail of G showing FoxK and Elav colocalization in the nuclei of ventral cord neurons (H, merge) or FoxK alone (I). All embryos are oriented with the anterior end to the left.
© Copyright Policy
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC2600746&req=5

fig3: Distribution of FoxK in Drosophila embryos. (A and B) Distinct temporal accumulation of the FoxK-L and FoxK-S transcripts by RT-PCR. FoxK-L is present in unfertilized embryos (UE), pupae (P), and head (H) and in thorax (T) and abdomen (Ab) from adult flies (A). FoxK-S accumulates in embryos (E) and salivary glands (SG) and gut from larvae (L). (C and D) In situ hybridization of wild-type embryos using digoxigenin-labeled FoxK-mRNA probes. In stage 16 embryos, the sense probe results in negative signal (C), whereas FoxK mRNA accumulates in the endoderm of parasegments (PS) 3 and 7 (D). (E and F) Single focal plane of whole-mount wild-type embryos stained with anti-FoxK antibody. (E) Stage 15 embryos revealed nuclear FoxK signal in the lining of the single vesicle of the midgut endoderm (arrow). (F) Stage 16 embryos accumulate FoxK in the lining of all four vesicles of the midgut endoderm and gastric constrictions (arrow). (G) Ventral view of an embryo showing FoxK (green) expression along the ventral nerve cord also labeled with anti-Elav (merged image). (H and I) Detail of G showing FoxK and Elav colocalization in the nuclei of ventral cord neurons (H, merge) or FoxK alone (I). All embryos are oriented with the anterior end to the left.
Mentions: Using oligonucleotide primers specific for different exons of the FoxK gene, we detected FoxK transcripts at all stages of Drosophila development (Fig. 3 A). Interestingly, we found a prominent temporal distribution of the FoxK-S and FoxK-L transcripts, whereas FoxK-S was predominantly expressed during the embryonic and larval stages, FoxK-L was mainly seen in pupae, adults, and unfertilized eggs. Moreover, FoxK transcripts were detected in all tissues analyzed: larval salivary glands and gut and adult head, thorax, and abdomen (Fig. 3 B).

Bottom Line: Genet.This regulatory activity does not require direct labial activation by the TGF-beta effector Mad.Thus, we propose that the combined activity of the TGF-beta target genes FoxK and Dfos is critical for the direct activation of lab in the endoderm.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, University of Texas Medical Branch, Galveston, TX 77555, USA. scasas@cnio.es

ABSTRACT
Inductive signals across germ layers are important for the development of the endoderm in vertebrates and invertebrates (Tam, P.P., M. Kanai-Azuma, and Y. Kanai. 2003. Curr. Opin. Genet. Dev. 13:393-400; Nakagoshi, H. 2005. Dev. Growth Differ. 47:383-392). In flies, the visceral mesoderm secretes signaling molecules that diffuse into the underlying midgut endoderm, where conserved signaling cascades activate the Hox gene labial, which is important for the differentiation of copper cells (Bienz, M. 1997. Curr. Opin. Genet. Dev. 7:683-688). We present here a Drosophila melanogaster gene of the Fox family of transcription factors, FoxK, that mediates transforming growth factor beta (TGF-beta) signaling in the embryonic midgut endoderm. FoxK mutant embryos fail to generate midgut constrictions and lack Labial in the endoderm. Our observations suggest that TGF-beta signaling directly regulates FoxK through functional Smad/Mad-binding sites, whereas FoxK, in turn, regulates labial expression. We also describe a new cooperative activity of the transcription factors FoxK and Dfos/AP-1 that regulates labial expression in the midgut endoderm. This regulatory activity does not require direct labial activation by the TGF-beta effector Mad. Thus, we propose that the combined activity of the TGF-beta target genes FoxK and Dfos is critical for the direct activation of lab in the endoderm.

Show MeSH
Related in: MedlinePlus