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Fgf16 is required for specification of GABAergic neurons and oligodendrocytes in the zebrafish forebrain.

Miyake A, Chitose T, Kamei E, Murakami A, Nakayama Y, Konishi M, Itoh N - PLoS ONE (2014)

Bottom Line: The knockdown of fgf16 decreased cell proliferation in the forebrain and midbrain. fgf16 was also essential for development of the ventral telencephalon and diencephalon, whereas fgf16 was not required for dorsoventral patterning in the midbrain. fgf16 was additionally required for the specification and differentiation of γ-aminobutyric acid (GABA)ergic interneurons and oligodendrocytes, but not for those of glutamatergic neurons in the forebrain.The fgf16 morphant phenotype was similar to that of the fgf19 morphant and embryos blocked Hh signaling.The results of the present study indicate that Fgf16 signaling, which is regulated by the downstream pathways of Hh-Fgf19 in the forebrain, is involved in forebrain development.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetic Biochemistry, Kyoto University Graduate School of Pharmaceutical Sciences, Sakyo, Kyoto, Japan.

ABSTRACT
Fibroblast growth factor (Fgf) signaling plays crucial roles in various developmental processes including those in the brain. We examined the role of Fgf16 in the formation of the zebrafish brain. The knockdown of fgf16 decreased cell proliferation in the forebrain and midbrain. fgf16 was also essential for development of the ventral telencephalon and diencephalon, whereas fgf16 was not required for dorsoventral patterning in the midbrain. fgf16 was additionally required for the specification and differentiation of γ-aminobutyric acid (GABA)ergic interneurons and oligodendrocytes, but not for those of glutamatergic neurons in the forebrain. Cross talk between Fgf and Hedgehog (Hh) signaling was critical for the specification of GABAergic interneurons and oligodendrocytes. The expression of fgf16 in the forebrain was down-regulated by the inhibition of Hh and Fgf19 signaling, but not by that of Fgf3/Fgf8 signaling. The fgf16 morphant phenotype was similar to that of the fgf19 morphant and embryos blocked Hh signaling. The results of the present study indicate that Fgf16 signaling, which is regulated by the downstream pathways of Hh-Fgf19 in the forebrain, is involved in forebrain development.

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Effects of fgf16 on the development of glutamatergic neurons, GABAergic interneurons, and oligodendrocyte progenitor cells.(A–D) The expression of ngn1 (A, B) and isl1 (C, D) in wild-type embryos (A, C) and fgf16 morphants (B, D) at 24 hpf. Lateral views with anterior to the left and dorsal to the top. (E–J) The expression of gad1 (E, F), olig2 (G, H), and slc17a6a (I, J) in wild-type embryos (E, G, I) and fgf16 morphants (F, H, J) at 28 hpf. Lateral views with anterior to the left and dorsal to the top.
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pone-0110836-g006: Effects of fgf16 on the development of glutamatergic neurons, GABAergic interneurons, and oligodendrocyte progenitor cells.(A–D) The expression of ngn1 (A, B) and isl1 (C, D) in wild-type embryos (A, C) and fgf16 morphants (B, D) at 24 hpf. Lateral views with anterior to the left and dorsal to the top. (E–J) The expression of gad1 (E, F), olig2 (G, H), and slc17a6a (I, J) in wild-type embryos (E, G, I) and fgf16 morphants (F, H, J) at 28 hpf. Lateral views with anterior to the left and dorsal to the top.

Mentions: In addition to patterning in the brain, Fgfs are involved in the development of neuronal subpopulations [8], [66], [67]. To determine whether an injection of fgf16 MO affected neuronal differentiation in the forebrain, the expression of the basic helix-loop helix (bHLH) proneural gene, ngn1, was analyzed in fgf16 morphants at 24 hpf. The expression of ngn1 was unaffected in the dorsal telencephalon of fgf16 morphants, whereas it was reduced in the diencephalon (n = 11/11) (Fig. 6A, B). We then examined whether the injection of fgf16 MO affected the expression of isl1, a neuronal marker gene, in the forebrain. In the forebrain, isl1 is expressed by ventral neurons in the telencephalon and diencephalon, and by neurons in the epiphysis at 24 hpf. The expression of isl1 was reduced in the ventral telencephalon, anterior ventral thalamus, and epiphysis of fgf16 morphants (n = 15/20) (Fig. 6C, D). These results indicated that neuronal differentiation in the ventral region in both the telencephalon and diencephalon was suppressed in fgf16 morphants.


Fgf16 is required for specification of GABAergic neurons and oligodendrocytes in the zebrafish forebrain.

Miyake A, Chitose T, Kamei E, Murakami A, Nakayama Y, Konishi M, Itoh N - PLoS ONE (2014)

Effects of fgf16 on the development of glutamatergic neurons, GABAergic interneurons, and oligodendrocyte progenitor cells.(A–D) The expression of ngn1 (A, B) and isl1 (C, D) in wild-type embryos (A, C) and fgf16 morphants (B, D) at 24 hpf. Lateral views with anterior to the left and dorsal to the top. (E–J) The expression of gad1 (E, F), olig2 (G, H), and slc17a6a (I, J) in wild-type embryos (E, G, I) and fgf16 morphants (F, H, J) at 28 hpf. Lateral views with anterior to the left and dorsal to the top.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4214708&req=5

pone-0110836-g006: Effects of fgf16 on the development of glutamatergic neurons, GABAergic interneurons, and oligodendrocyte progenitor cells.(A–D) The expression of ngn1 (A, B) and isl1 (C, D) in wild-type embryos (A, C) and fgf16 morphants (B, D) at 24 hpf. Lateral views with anterior to the left and dorsal to the top. (E–J) The expression of gad1 (E, F), olig2 (G, H), and slc17a6a (I, J) in wild-type embryos (E, G, I) and fgf16 morphants (F, H, J) at 28 hpf. Lateral views with anterior to the left and dorsal to the top.
Mentions: In addition to patterning in the brain, Fgfs are involved in the development of neuronal subpopulations [8], [66], [67]. To determine whether an injection of fgf16 MO affected neuronal differentiation in the forebrain, the expression of the basic helix-loop helix (bHLH) proneural gene, ngn1, was analyzed in fgf16 morphants at 24 hpf. The expression of ngn1 was unaffected in the dorsal telencephalon of fgf16 morphants, whereas it was reduced in the diencephalon (n = 11/11) (Fig. 6A, B). We then examined whether the injection of fgf16 MO affected the expression of isl1, a neuronal marker gene, in the forebrain. In the forebrain, isl1 is expressed by ventral neurons in the telencephalon and diencephalon, and by neurons in the epiphysis at 24 hpf. The expression of isl1 was reduced in the ventral telencephalon, anterior ventral thalamus, and epiphysis of fgf16 morphants (n = 15/20) (Fig. 6C, D). These results indicated that neuronal differentiation in the ventral region in both the telencephalon and diencephalon was suppressed in fgf16 morphants.

Bottom Line: The knockdown of fgf16 decreased cell proliferation in the forebrain and midbrain. fgf16 was also essential for development of the ventral telencephalon and diencephalon, whereas fgf16 was not required for dorsoventral patterning in the midbrain. fgf16 was additionally required for the specification and differentiation of γ-aminobutyric acid (GABA)ergic interneurons and oligodendrocytes, but not for those of glutamatergic neurons in the forebrain.The fgf16 morphant phenotype was similar to that of the fgf19 morphant and embryos blocked Hh signaling.The results of the present study indicate that Fgf16 signaling, which is regulated by the downstream pathways of Hh-Fgf19 in the forebrain, is involved in forebrain development.

View Article: PubMed Central - PubMed

Affiliation: Department of Genetic Biochemistry, Kyoto University Graduate School of Pharmaceutical Sciences, Sakyo, Kyoto, Japan.

ABSTRACT
Fibroblast growth factor (Fgf) signaling plays crucial roles in various developmental processes including those in the brain. We examined the role of Fgf16 in the formation of the zebrafish brain. The knockdown of fgf16 decreased cell proliferation in the forebrain and midbrain. fgf16 was also essential for development of the ventral telencephalon and diencephalon, whereas fgf16 was not required for dorsoventral patterning in the midbrain. fgf16 was additionally required for the specification and differentiation of γ-aminobutyric acid (GABA)ergic interneurons and oligodendrocytes, but not for those of glutamatergic neurons in the forebrain. Cross talk between Fgf and Hedgehog (Hh) signaling was critical for the specification of GABAergic interneurons and oligodendrocytes. The expression of fgf16 in the forebrain was down-regulated by the inhibition of Hh and Fgf19 signaling, but not by that of Fgf3/Fgf8 signaling. The fgf16 morphant phenotype was similar to that of the fgf19 morphant and embryos blocked Hh signaling. The results of the present study indicate that Fgf16 signaling, which is regulated by the downstream pathways of Hh-Fgf19 in the forebrain, is involved in forebrain development.

Show MeSH
Related in: MedlinePlus