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Prosomeric organization of the hypothalamus in an elasmobranch, the catshark Scyliorhinus canicula.

Santos-Durán GN, Menuet A, Lagadec R, Mayeur H, Ferreiro-Galve S, Mazan S, Rodríguez-Moldes I, Candal E - Front Neuroanat (2015)

Bottom Line: Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain.Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates.These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Centro de Investigaciones Biológicas, Department of Cell Biology and Ecology, University of Santiago de Compostela Santiago de Compostela, Spain.

ABSTRACT
The hypothalamus has been a central topic in neuroanatomy because of its important physiological functions, but its mature organization remains elusive. Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain. Here we studied the molecular organization of the hypothalamus and neighboring telencephalic domains in a cartilaginous fish, the catshark, Scyliorhinus canicula, focusing on ScFoxg1a, ScShh, ScNkx2.1, ScDlx2/5, ScOtp, and ScTbr1 expression profiles and on the identification α-acetylated-tubulin-immunoreactive (ir), TH-ir, 5-HT-ir, and GFAP-ir structures by means of immunohistochemistry. Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates. These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

No MeSH data available.


Phylogenetic analysis of the Scyliorhinus canicula genes analyzed in this study. Phylogenetic trees for the Foxg1, Hedgehog, Nkx2.1/Nkx2.4, Otp and Tbr1/Tbx21/Eomes families are shown in (A–E) respectively. The number of substitutions per site is indicated at the bottom of each tree, on the left. S. canicula genes are displayed in red. Abbreviations used: Hs, Homo sapiens (human); Gg, Gallus gallus (chick); Ac, Anolis carolinensis (anole lizard); Xt, Xenopus tropicalis (African clawed frog); Lc, Latimeria chalumnae (coelacanth); Lo, Lepisosteus oculatus (spotted gar); Ol, Oryzias latipes (medaka); Dr, Danio rerio (zebrafish); Cm, Callorhinchus milii (elephant shark); Sc, Scyliorhinus canicula (catshark or lesser spotted dogfish); Bf, Branchiostoma floridae (amphioxus).
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Figure 1: Phylogenetic analysis of the Scyliorhinus canicula genes analyzed in this study. Phylogenetic trees for the Foxg1, Hedgehog, Nkx2.1/Nkx2.4, Otp and Tbr1/Tbx21/Eomes families are shown in (A–E) respectively. The number of substitutions per site is indicated at the bottom of each tree, on the left. S. canicula genes are displayed in red. Abbreviations used: Hs, Homo sapiens (human); Gg, Gallus gallus (chick); Ac, Anolis carolinensis (anole lizard); Xt, Xenopus tropicalis (African clawed frog); Lc, Latimeria chalumnae (coelacanth); Lo, Lepisosteus oculatus (spotted gar); Ol, Oryzias latipes (medaka); Dr, Danio rerio (zebrafish); Cm, Callorhinchus milii (elephant shark); Sc, Scyliorhinus canicula (catshark or lesser spotted dogfish); Bf, Branchiostoma floridae (amphioxus).

Mentions: Exhaustive phylogenetic characterizations of the catshark Dlx gene repertoire have been previously published (Debiais-Thibaud et al., 2013), confirming the identity of ScDlx2 and ScDlx5. In order to unambiguously identify the catshark orthologues of Foxg1, Shh, Nkx2.1, Otp, and Tbr1, we conducted systematic phylogenetic analyses of the corresponding vertebrate gene families, including all the vertebrate classes derived from duplications of a single ancestral chordate orthologue (Figure 1). In each case, phylogenies were constructed from alignments containing deduced amino acid sequences of all paralogous sequences retrieved from catshark transcriptomic databases and from a representative sampling of actinopterygians and sarcopterygians. The trees were rooted using a Branchiostoma floridae sequence, except in the case of Otp which could not be found in the amphioxus Ensembl database. In the case of Foxg1, three strongly supported classes (posterior probability or PP > 90%), each containing a catshark and several osteichthyan sequences, were retrieved, highlighting for the first time the presence of three gnathostome Foxg1 classes (Figure 1A). These classes were termed Foxg1a, Foxg1b, and Foxg1c, respectively. One coelacanth and several actinopterygian sequences, but no amphibian or amniote sequence, were found in the Foxg1b and Foxg1c classes, suggesting a loss of their representatives in tetrapods. We focused the expression analysis on ScFoxg1a, the catshark orthologue of the only Foxg1 gene retained in all major gnathostome lineages including tetrapods. The tree topology obtained for the Hedgehog family confirmed the presence of the three gnathostome classes, corresponding to the Indian Hedgehog, Desert Hedgehog and Sonic Hedgehog classes already reported in osteichthyans, and confirmed ScShh as the representative of the latter (Figure 1B). Concerning the Nkx2.1/Nkx2.4 family, a single catshark gene could be identified and it was unambiguously assigned to the Nkx2.1 class based on the strongly supported grouping of its deduced amino acid sequence with teleost, chick, and human Nkx2.1 sequences (PP = 97%; Figure 1C). This gene is therefore referred to as ScNkx2.1 hereafter. A single catshark Otp related sequence, termed ScOtp, could be found and as expected, it clustered with the elephant shark sequence annotated as Otp in the reconstruction shown in Figure 1D. Finally, the Tbr1, Tbx21, and Eomes classes were retrieved with high statistical support (PP = 83, 100, and 99%, respectively) within the Tbr1/Tbx21/Eomes family. Each class contained a single catshark sequence at the expected position, allowing an unambiguous identification of the ScTbr1 gene analyzed in this study (Figure 1E).


Prosomeric organization of the hypothalamus in an elasmobranch, the catshark Scyliorhinus canicula.

Santos-Durán GN, Menuet A, Lagadec R, Mayeur H, Ferreiro-Galve S, Mazan S, Rodríguez-Moldes I, Candal E - Front Neuroanat (2015)

Phylogenetic analysis of the Scyliorhinus canicula genes analyzed in this study. Phylogenetic trees for the Foxg1, Hedgehog, Nkx2.1/Nkx2.4, Otp and Tbr1/Tbx21/Eomes families are shown in (A–E) respectively. The number of substitutions per site is indicated at the bottom of each tree, on the left. S. canicula genes are displayed in red. Abbreviations used: Hs, Homo sapiens (human); Gg, Gallus gallus (chick); Ac, Anolis carolinensis (anole lizard); Xt, Xenopus tropicalis (African clawed frog); Lc, Latimeria chalumnae (coelacanth); Lo, Lepisosteus oculatus (spotted gar); Ol, Oryzias latipes (medaka); Dr, Danio rerio (zebrafish); Cm, Callorhinchus milii (elephant shark); Sc, Scyliorhinus canicula (catshark or lesser spotted dogfish); Bf, Branchiostoma floridae (amphioxus).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4389657&req=5

Figure 1: Phylogenetic analysis of the Scyliorhinus canicula genes analyzed in this study. Phylogenetic trees for the Foxg1, Hedgehog, Nkx2.1/Nkx2.4, Otp and Tbr1/Tbx21/Eomes families are shown in (A–E) respectively. The number of substitutions per site is indicated at the bottom of each tree, on the left. S. canicula genes are displayed in red. Abbreviations used: Hs, Homo sapiens (human); Gg, Gallus gallus (chick); Ac, Anolis carolinensis (anole lizard); Xt, Xenopus tropicalis (African clawed frog); Lc, Latimeria chalumnae (coelacanth); Lo, Lepisosteus oculatus (spotted gar); Ol, Oryzias latipes (medaka); Dr, Danio rerio (zebrafish); Cm, Callorhinchus milii (elephant shark); Sc, Scyliorhinus canicula (catshark or lesser spotted dogfish); Bf, Branchiostoma floridae (amphioxus).
Mentions: Exhaustive phylogenetic characterizations of the catshark Dlx gene repertoire have been previously published (Debiais-Thibaud et al., 2013), confirming the identity of ScDlx2 and ScDlx5. In order to unambiguously identify the catshark orthologues of Foxg1, Shh, Nkx2.1, Otp, and Tbr1, we conducted systematic phylogenetic analyses of the corresponding vertebrate gene families, including all the vertebrate classes derived from duplications of a single ancestral chordate orthologue (Figure 1). In each case, phylogenies were constructed from alignments containing deduced amino acid sequences of all paralogous sequences retrieved from catshark transcriptomic databases and from a representative sampling of actinopterygians and sarcopterygians. The trees were rooted using a Branchiostoma floridae sequence, except in the case of Otp which could not be found in the amphioxus Ensembl database. In the case of Foxg1, three strongly supported classes (posterior probability or PP > 90%), each containing a catshark and several osteichthyan sequences, were retrieved, highlighting for the first time the presence of three gnathostome Foxg1 classes (Figure 1A). These classes were termed Foxg1a, Foxg1b, and Foxg1c, respectively. One coelacanth and several actinopterygian sequences, but no amphibian or amniote sequence, were found in the Foxg1b and Foxg1c classes, suggesting a loss of their representatives in tetrapods. We focused the expression analysis on ScFoxg1a, the catshark orthologue of the only Foxg1 gene retained in all major gnathostome lineages including tetrapods. The tree topology obtained for the Hedgehog family confirmed the presence of the three gnathostome classes, corresponding to the Indian Hedgehog, Desert Hedgehog and Sonic Hedgehog classes already reported in osteichthyans, and confirmed ScShh as the representative of the latter (Figure 1B). Concerning the Nkx2.1/Nkx2.4 family, a single catshark gene could be identified and it was unambiguously assigned to the Nkx2.1 class based on the strongly supported grouping of its deduced amino acid sequence with teleost, chick, and human Nkx2.1 sequences (PP = 97%; Figure 1C). This gene is therefore referred to as ScNkx2.1 hereafter. A single catshark Otp related sequence, termed ScOtp, could be found and as expected, it clustered with the elephant shark sequence annotated as Otp in the reconstruction shown in Figure 1D. Finally, the Tbr1, Tbx21, and Eomes classes were retrieved with high statistical support (PP = 83, 100, and 99%, respectively) within the Tbr1/Tbx21/Eomes family. Each class contained a single catshark sequence at the expected position, allowing an unambiguous identification of the ScTbr1 gene analyzed in this study (Figure 1E).

Bottom Line: Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain.Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates.These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

View Article: PubMed Central - PubMed

Affiliation: Centro de Investigaciones Biológicas, Department of Cell Biology and Ecology, University of Santiago de Compostela Santiago de Compostela, Spain.

ABSTRACT
The hypothalamus has been a central topic in neuroanatomy because of its important physiological functions, but its mature organization remains elusive. Deciphering its embryonic and adult organization is crucial in an evolutionary approach of the organization of the vertebrate forebrain. Here we studied the molecular organization of the hypothalamus and neighboring telencephalic domains in a cartilaginous fish, the catshark, Scyliorhinus canicula, focusing on ScFoxg1a, ScShh, ScNkx2.1, ScDlx2/5, ScOtp, and ScTbr1 expression profiles and on the identification α-acetylated-tubulin-immunoreactive (ir), TH-ir, 5-HT-ir, and GFAP-ir structures by means of immunohistochemistry. Analysis of the results within the updated prosomeric model framework support the existence of alar and basal histogenetic compartments in the hypothalamus similar to those described in the mouse, suggesting the ancestrality of these subdivisions in jawed vertebrates. These data provide new insights into hypothalamic organization in cartilaginous fishes and highlight the generality of key features of the prosomeric model in jawed vertebrates.

No MeSH data available.