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The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends

View Article: PubMed Central - PubMed

ABSTRACT

The hypothalamus is an important physiologic center of the vertebrate brain involved in the elaboration of individual and species survival responses. To better understand the ancestral organization of the alar hypothalamus we revisit previous data on ScOtp, ScDlx2/5, ScTbr1, ScNkx2.1 expression and Pax6 immunoreactivity jointly with new data on ScNeurog2, ScLhx9, ScLhx5, and ScNkx2.8 expression, in addition to immunoreactivity to serotonin (5-HT) and doublecortin (DCX) in the catshark Scyliorhinus canicula, a key species for this purpose since cartilaginous fishes are basal representatives of gnathostomes (jawed vertebrates). Our study revealed a complex genoarchitecture for the chondrichthyan alar hypothalamus. We identified terminal (rostral) and peduncular (caudal) subdivisions in the prosomeric paraventricular and subparaventricular areas (TPa/PPa and TSPa/PSPa, respectively) evidenced by the expression pattern of developmental genes like ScLhx5 (TPa) and immunoreactivity against Pax6 (PSPa) and 5-HT (PPa and PSPa). Dorso-ventral subdivisions were only evidenced in the SPa (SPaD, SPaV; respectively) by means of Pax6 and ScNkx2.8 (respectively). Interestingly, ScNkx2.8 expression overlaps over the alar-basal boundary, as Nkx2.2 does in other vertebrates. Our results reveal evidences for the existence of different groups of tangentially migrated cells expressing ScOtp, Pax6, and ScDlx2. The genoarchitectonic comparative analysis suggests alternative interpretations of the rostral-most alar plate in prosomeric terms and reveals a conserved molecular background for the vertebrate alar hypothalamus likely acquired before/during the agnathan-gnathostome transition, on which Otp, Pax6, Lhx5, and Neurog2 are expressed in the Pa while Dlx and Nkx2.2/Nkx2.8 are expressed in the SPa.

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Regionalization of the alar hypothalamus and neighbor territories in embryos of S. canicula at stages 29–30 based on the expression of ScNkx2.1(A–C,D″) and ScNkx2.8(D,E) on sagittal (A) and transverse (B,E) sections. Some sections were labeled (D′) or double labeled for immunohistochemistry against Shh (B–D′). (C′) Detail of the squared regions in Figure (C). It results from the overlapping of two parallel sections hybridized with ScDlx2/5andScNkx2.1 probes, respectively. Color for ScDlx2/5 and ScNkx2.1 was digitally converted to brown and purple to ease comparison. (A–C)ScNkx2.1 expression at indicated stages. (D,E)ScNkx2.8 expression at indicated stages. Note that Shh immunoreactivity does not reach the ABB (D′,D″). For other labels, see legend Figure 1. For abbreviations, see list.
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Figure 4: Regionalization of the alar hypothalamus and neighbor territories in embryos of S. canicula at stages 29–30 based on the expression of ScNkx2.1(A–C,D″) and ScNkx2.8(D,E) on sagittal (A) and transverse (B,E) sections. Some sections were labeled (D′) or double labeled for immunohistochemistry against Shh (B–D′). (C′) Detail of the squared regions in Figure (C). It results from the overlapping of two parallel sections hybridized with ScDlx2/5andScNkx2.1 probes, respectively. Color for ScDlx2/5 and ScNkx2.1 was digitally converted to brown and purple to ease comparison. (A–C)ScNkx2.1 expression at indicated stages. (D,E)ScNkx2.8 expression at indicated stages. Note that Shh immunoreactivity does not reach the ABB (D′,D″). For other labels, see legend Figure 1. For abbreviations, see list.

Mentions: At stage 29, ScNkx2.1 is expressed ventral to the optic stalk through the basal hypothalamus except in the RM compartment (not shown), forming a sharp limit with the ABB (see continuous red line in Figures 4A–C; see also Santos-Durán et al., 2015). Furthermore, ScNkx2.1 and Shh immunoreactivity co-distribute in the Tu region (Figures 4B,C), though Shh immunoreactivity does not match the dorsal border of ScNkx2.1 expression. Notably, the dorsal border of ScNkx2.1 appears to abut the ventral border of ScDlx2/5 in the TSPa/PSPa area (Figure 4C′). Dorsal to the alar hypothalamus, ScNkx2.1 expression and Shh immunoreactivity also co-distribute in the preoptic subpallium (data not shown; see Quintana-Urzainqui et al., 2012, 2015). Both genes abut the dorsal limit of the alar hypothalamus (Figures 4A,B).


The Shark Alar Hypothalamus: Molecular Characterization of Prosomeric Subdivisions and Evolutionary Trends
Regionalization of the alar hypothalamus and neighbor territories in embryos of S. canicula at stages 29–30 based on the expression of ScNkx2.1(A–C,D″) and ScNkx2.8(D,E) on sagittal (A) and transverse (B,E) sections. Some sections were labeled (D′) or double labeled for immunohistochemistry against Shh (B–D′). (C′) Detail of the squared regions in Figure (C). It results from the overlapping of two parallel sections hybridized with ScDlx2/5andScNkx2.1 probes, respectively. Color for ScDlx2/5 and ScNkx2.1 was digitally converted to brown and purple to ease comparison. (A–C)ScNkx2.1 expression at indicated stages. (D,E)ScNkx2.8 expression at indicated stages. Note that Shh immunoreactivity does not reach the ABB (D′,D″). For other labels, see legend Figure 1. For abbreviations, see list.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
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Figure 4: Regionalization of the alar hypothalamus and neighbor territories in embryos of S. canicula at stages 29–30 based on the expression of ScNkx2.1(A–C,D″) and ScNkx2.8(D,E) on sagittal (A) and transverse (B,E) sections. Some sections were labeled (D′) or double labeled for immunohistochemistry against Shh (B–D′). (C′) Detail of the squared regions in Figure (C). It results from the overlapping of two parallel sections hybridized with ScDlx2/5andScNkx2.1 probes, respectively. Color for ScDlx2/5 and ScNkx2.1 was digitally converted to brown and purple to ease comparison. (A–C)ScNkx2.1 expression at indicated stages. (D,E)ScNkx2.8 expression at indicated stages. Note that Shh immunoreactivity does not reach the ABB (D′,D″). For other labels, see legend Figure 1. For abbreviations, see list.
Mentions: At stage 29, ScNkx2.1 is expressed ventral to the optic stalk through the basal hypothalamus except in the RM compartment (not shown), forming a sharp limit with the ABB (see continuous red line in Figures 4A–C; see also Santos-Durán et al., 2015). Furthermore, ScNkx2.1 and Shh immunoreactivity co-distribute in the Tu region (Figures 4B,C), though Shh immunoreactivity does not match the dorsal border of ScNkx2.1 expression. Notably, the dorsal border of ScNkx2.1 appears to abut the ventral border of ScDlx2/5 in the TSPa/PSPa area (Figure 4C′). Dorsal to the alar hypothalamus, ScNkx2.1 expression and Shh immunoreactivity also co-distribute in the preoptic subpallium (data not shown; see Quintana-Urzainqui et al., 2012, 2015). Both genes abut the dorsal limit of the alar hypothalamus (Figures 4A,B).

View Article: PubMed Central - PubMed

ABSTRACT

The hypothalamus is an important physiologic center of the vertebrate brain involved in the elaboration of individual and species survival responses. To better understand the ancestral organization of the alar hypothalamus we revisit previous data on ScOtp, ScDlx2/5, ScTbr1, ScNkx2.1 expression and Pax6 immunoreactivity jointly with new data on ScNeurog2, ScLhx9, ScLhx5, and ScNkx2.8 expression, in addition to immunoreactivity to serotonin (5-HT) and doublecortin (DCX) in the catshark Scyliorhinus canicula, a key species for this purpose since cartilaginous fishes are basal representatives of gnathostomes (jawed vertebrates). Our study revealed a complex genoarchitecture for the chondrichthyan alar hypothalamus. We identified terminal (rostral) and peduncular (caudal) subdivisions in the prosomeric paraventricular and subparaventricular areas (TPa/PPa and TSPa/PSPa, respectively) evidenced by the expression pattern of developmental genes like ScLhx5 (TPa) and immunoreactivity against Pax6 (PSPa) and 5-HT (PPa and PSPa). Dorso-ventral subdivisions were only evidenced in the SPa (SPaD, SPaV; respectively) by means of Pax6 and ScNkx2.8 (respectively). Interestingly, ScNkx2.8 expression overlaps over the alar-basal boundary, as Nkx2.2 does in other vertebrates. Our results reveal evidences for the existence of different groups of tangentially migrated cells expressing ScOtp, Pax6, and ScDlx2. The genoarchitectonic comparative analysis suggests alternative interpretations of the rostral-most alar plate in prosomeric terms and reveals a conserved molecular background for the vertebrate alar hypothalamus likely acquired before/during the agnathan-gnathostome transition, on which Otp, Pax6, Lhx5, and Neurog2 are expressed in the Pa while Dlx and Nkx2.2/Nkx2.8 are expressed in the SPa.

No MeSH data available.


Related in: MedlinePlus