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

Santos-Durán, Gabriel N.; Menuet, Arnaud; Lagadec, Ronan; Mayeur, Hélène; Ferreiro-Galve, Susana; Mazan, Sylvie; Rodríguez‐Moldes, Isabel; Candal, Eva

doi:10.3389/fnana.2015.00037

Cited by 22 publications

(103 citation statements)

References 47 publications

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“…The basal expression of these and other genes lead to the identification of tuberal/retrotuberal (Tu/RTu), perimamillary/periretromamillary (PM/PRM) and mamillary/retromamillary (MM/RM) domains, apparently homologous to those described in murine models. Besides, a molecular hypothalamo-telencephalic border (HTB) and a hypothalamo-diencephalic border (HDB), matching with those described in the model, were identified in the shark, together with an IHB defined, as in mouse (Puelles et al, 2012), based on the course of ascending tracts to the telencephalon (see Santos-Durán et al, 2015). …”

Section: Introductionmentioning

confidence: 90%

“…We applied ISH for ScOtp (Santos-Durán et al, 2015), ScDlx2 (Quintana-Urzainqui et al, 2012, 2015; Compagnucci et al, 2013; Debiais-Thibaud et al, 2013; Santos-Durán et al, 2015), ScDlx5 (Compagnucci et al, 2013; Debiais-Thibaud et al, 2013; Santos-Durán et al, 2015), ScLhx9 (Pose-Méndez et al, 2015; Quintana-Urzainqui et al, 2015), ScLhx5, ScNkx2 (Quintana-Urzainqui et al, 2012, 2015; Santos-Durán et al, 2015), ScNkx2.8, ScTbr1 (Quintana-Urzainqui et al, 2015; Santos-Durán et al, 2015), and ScNeurog2 genes. These probes were selected from a collection of S. canicula embryonic cDNA library (mixed stages S9–S22), constructed in pSPORT1, and submitted to high throughput EST sequencing.…”

Section: Methodsmentioning

confidence: 99%

“…The relationships among these domains and hypothalamic nuclei have been pointed out: the TPa/PPa domain gives rise to magnocellular and parvocellular neurosecretory populations of the supraopto-paraventricular complex; the TSPa/PSPa domain will form mainly the suprachiasmatic nucleus, the anterior hypothalamic nucleus, and the subparaventricular zone, while the basal hypothalamus gives rise to classical tuberal and mamillary derivatives (Morales-Delgado et al, 2011; Puelles et al, 2012; Herget et al, 2014; Herget and Ryu, 2015). Finally, additional histogenic domains are recognized in the acroterminal territory, the rostral-most portion of the neural tube (see Puelles et al, 2012; Ferrán et al, 2015; Puelles and Rubenstein, 2015; Santos-Durán et al, 2015). This median region is responsible of the development of structures such as the lamina terminalis or the optic chiasm in the alar hypothalamus.…”

Section: Introductionmentioning

confidence: 99%

“…Recently, we have carried out a preliminary study of the molecular histogenetic organization of the hypothalamus of an elasmobranch representative, the catshark Scyliorhinus canicula , and we analyzed this organization under the updated prosomeric framework (see Santos-Durán et al, 2015). Such analysis revealed a strikingly high degree in the conservation of hypothalamic histogenetic compartments between chondrichthyan and murine models.…”

Section: Introductionmentioning

confidence: 99%

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

Santos-Durán¹,

Ferreiro-Galve²,

Menuet³

et al. 2016

Front. Neuroanat.

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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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Section: Introductionmentioning

confidence: 90%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Santos-Durán¹,

Ferreiro-Galve²,

Menuet³

et al. 2016

Front. Neuroanat.

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“…In situ hybridization was applied on sections for the genes ScTbr1 [Quintana-Urzainqui et al, 2015;Santos-Durán et al, 2015], ScEn2 [Pose-Méndez et al, 2016a, b], ScLhx9 [QuintanaUrzainqui et al, 2015;Pose-Méndez et al, 2016a], and ScLhx5. These probes were selected from a collection of S. canicula embryonic cDNA library (mixed stages, S9 to S22) submitted to highthroughput EST sequencing (coordinated by S. Mazan).…”

Section: In Situ Hybridizationmentioning

confidence: 99%

A Developmental Study of the Cerebellar Nucleus in the Catshark, a Basal Gnathostome

et al. 2017

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The output of the cerebellar cortex is mainly released via cerebellar nuclei which vary in number and complexity among gnathostomes, extant vertebrates with a cerebellum. Cartilaginous fishes, a basal gnathostome lineage, show a conspicuous, well-organized cerebellar nucleus, unlike ray-finned fishes. To gain insight into the evolution and development of the cerebellar nucleus, we analyzed in the shark Scyliorhinus canicula (a chondrichthyan model species) the developmental expression of several genes coding for transcription factors (ScLhx5,ScLhx9,ScTbr1, and ScEn2) and the distribution of the protein calbindin, since all appear to be involved in cerebellar nuclei patterning in other gnathostomes. Three regions (subventricular, medial or central, and lateral or superficial) became recognizable in the cerebellar nucleus of this shark during development. Present genoarchitectonic and neurochemical data in embryos provide insight into the origin of the cerebellar nucleus in chondrichthyans and support a tripartite mediolateral organization of the cerebellar nucleus, as previously described in adult sharks. Furthermore, the expression pattern of ScLhx5,ScLhx9, and ScTbr1 in this shark, together with that of markers of proliferation, migration, and early differentiation of neurons, is compatible with the hypothesis that, as in mammals, different subsets of cerebellar nucleus neurons are originated from progenitors of 2 different sources: the ventricular zone of the cerebellar plate and the rhombic lip. We also present suggestive evidence that Lhx9 expression is involved in cerebellar nuclei patterning early on in gnathostome evolution, rather than representing an evolutionary innovation of the dentate nucleus in mammals, as previously hypothesized.

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Analysis of Islet‐1, Nkx2.1, Pax6, and Orthopedia in the forebrain of the sturgeon Acipenser ruthenus identifies conserved prosomeric characteristics

López

Jiménez

Morona

et al. 2021

J of Comparative Neurology

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The distribution patterns of a set of conserved brain developmental regulatory transcription factors were analyzed in the forebrain of the basal actinopterygian fish Acipenser ruthenus, consistent with the prosomeric model. In the telencephalon, the pallium was characterized by ventricular expression of Pax6. In the subpallium, the combined expression of Nkx2.1/Islet-1 (Isl1) allowed to propose ventral and dorsal areas, as the septo-pallidal (Nkx2.1/Isl1+) and striatal derivatives (Isl1+), respectively, and a dorsal portion of the striatal derivatives, ventricularly rich in Pax6 and devoid of Isl1 expression. Dispersed Orthopedia (Otp) cells were found in the supracommissural and posterior nuclei of the ventral telencephalon, related to the medial portion of the amygdaloid complex. The preoptic area was identified by the Nkx2.1/Isl1 expression. In the alar hypothalamus, an Otp-expressing territory, lacking Nkx2.1/Isl1, was identified as the paraventricular domain. The adjacent subparaventricular domain (Spa) was subdivided in a rostral territory expressing Nkx2.1 and an Isl1+ caudal one. In the basal hypothalamus, the tuberal region was defined by the Nkx2.1/Isl1 expression and a rostral Otp-expressing domain was identified. Moreover, the Otp/Nkx2.1 combination showed an additional zone lacking Isl1, tentatively identified as the mamillary area. In the diencephalon, both Pax6 and Isl1 defined the prethalamic domain, and within the basal prosomere 3, scattered Pax6-and Isl1-expressing cells were observed in the posterior tubercle. Finally, a small group of Pax6 cells was observed in the pretectal area.These results improve the understanding of the forebrain evolution and demonstrate that its basic bauplan is present very early in the vertebrate lineage.

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

Cited by 22 publications

References 47 publications

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

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

A Developmental Study of the Cerebellar Nucleus in the Catshark, a Basal Gnathostome

Analysis of Islet‐1, Nkx2.1, Pax6, and Orthopedia in the forebrain of the sturgeon Acipenser ruthenus identifies conserved prosomeric characteristics

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