Pattern of calbindin‐D28k and calretinin immunoreactivity in the brain ofXenopus laevisduring embryonic and larval development

Morona, Ruth; González, Agustı́n

doi:10.1002/cne.23163

Cited by 13 publications

(25 citation statements)

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“…The identification of the pallial territories, mainly at early developmental stages, was achieved by the use of specific pallial versus subpallial markers. It should be noted that in Xenopus the embryonic development ends at stage 45 (4 dpf) when the animal starts feeding, and it is followed by a long larval period generally subdivided into three set of stages (see Bandín et al, 2013, 2015; Morona and González, 2013): (1) premetamorphosis (stages 46–52), which comprises the initial set of stages in which the larvae merely grow in size and early buds of the hind limbs start to be visible on the lateral side of the body; (2) prometamorphosis (stages 53–58), the period through which the hind limbs progressively develop; and (3) metamorphic climax (stages 59–65), period in which the tail of the tadpole is reabsorbed and leads to the tailless, four-legged froglet. In the brain of the recently metamorphosed juvenile (stages 65-66) all main anatomical characteristics as in the adult brain are already recognizable.…”

Section: Resultsmentioning

confidence: 99%

“…In contrast, the Lhx2 expressing cells located away from the vz, which were very abundant at these larval stages, were never found to express Sox2 (empty arrowheads in Figure 9N ). Sox2 expression analyzed in combination with calretinin (marker of a mature interneuron population in the Xenopus pallium; Morona and González, 2008, 2013) demonstrated lack of colocalization ( Figures 9R,R ′). Finally the analysis at larval stages of BLBP expression in RGc demonstrated the ventricular position of these cells ( Figures 9O,P ).…”

Section: Resultsmentioning

confidence: 99%

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Pattern of Neurogenesis and Identification of Neuronal Progenitor Subtypes during Pallial Development in Xenopus laevis

Moreno

González

2017

Front. Neuroanat.

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The complexity of the pallium during evolution has increased dramatically in many different respects. The highest level of complexity is found in mammals, where most of the pallium (cortex) shows a layered organization and neurons are generated during development following an inside-out order, a sequence not observed in other amniotes (birds and reptiles). Species-differences may be related to major neurogenetic events, from the neural progenitors that divide and produce all pallial cells. In mammals, two main types of precursors have been described, primary precursor cells in the ventricular zone (vz; also called radial glial cells or apical progenitors) and secondary precursor cells (called basal or intermediate progenitors) separated from the ventricle surface. Previous studies suggested that pallial neurogenetic cells, and especially the intermediate progenitors, evolved independently in mammalian and sauropsid lineages. In the present study, we examined pallial neurogenesis in the amphibian Xenopus laevis, a representative species of the only group of tetrapods that are anamniotes. The pattern of pallial proliferation during embryonic and larval development was studied, together with a multiple immunohistochemical analysis of putative progenitor cells. We found that there are two phases of progenitor divisions in the developing pallium that, following the radial unit concept from the ventricle to the mantle, finally result in an outside-in order of mature neurons, what seems to be the primitive condition of vertebrates. Gene expressions of key transcription factors that characterize radial glial cells in the vz were demonstrated in Xenopus. In addition, although mitotic cells were corroborated outside the vz, the expression pattern of markers for intermediate progenitors differed from mammals.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Pattern of Neurogenesis and Identification of Neuronal Progenitor Subtypes during Pallial Development in Xenopus laevis

Moreno

González

2017

Front. Neuroanat.

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“…For a ready interpretation of the developing brain in Xenopus, we used essentially the same nomenclature as in previous developmental studies López et al, , 2006Domínguez et al, 2013Domínguez et al, , 2014Morona and González, 2013], including the terminology of the prosomeric model for the forebrain Rubenstein, 2003, 2015]. in the alar part of the hypothalamus ( fig.…”

Section: Evaluation and Presentation Of The Resultsmentioning

confidence: 99%

Spatiotemporal Development of the Orexinergic (Hypocretinergic) System in the Central Nervous System of Xenopus laevis

López¹,

Morales²,

González³

2016

Brain Behav Evol

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The present immunohistochemical study represents a detailed spatiotemporal analysis of the localization of orexin-immunoreactive (OX-ir) cells and fibers throughout development in the brain of the anuran amphibian Xenopus laevis, a model frequently used in developmental studies. Anurans undergo remarkable physiological changes during the early life stages, and very little is known about the ontogeny and the localization of the centers that control functions such as appetite and feed ingestion in the developing brain. We examined the onset of the orexinergic system, demonstrated to be involved in appetite regulation, using antibodies against mammalian orexin-A and orexin-B peptides. Simultaneous detection of orexins with other territorial markers was used to assess the precise location of the orexinergic cells in the hypothalamus, analyzed within a segmental paradigm. Double staining of orexins and tyrosine hydroxylase served to evaluate possible interactions with the catecholaminergic systems. At early embryonic stages, the first OX-ir cells were detected in the hypothalamus and, soon after, long descending projections were observed through the brainstem to the spinal cord. As brain development proceeded, the double-staining techniques demonstrated that this OX-ir cell group was located in the suprachiasmatic nucleus within the alar hypothalamus. Throughout larval development, the number of OX-ir cells increased notably and a widespread fiber network that innervated the main areas of the forebrain and brainstem was progressively formed, including innervation in the posterior tubercle and mesencephalon, the locus coeruleus, and the nucleus of the solitary tract where catecholaminergic cells are present. In addition, orexinergic cells were detected in the preoptic area and the tuberal hypothalamus only at late prometamorphic stages. The final distribution pattern, largely similar to that of the adult, was achieved through metamorphic climax. The early expression of orexins in Xenopus suggests important roles in brain development in the embryonic period before feeding, and the progression of the temporal and spatial complexity of the orexinergic system might be correlated to the maturation of appetite control regulation, among other functions.

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“…Their relative localization was framed attending to the neuromeric organization of the brain. We used the same nomenclature as in our previous studies (Morona and González, 2008, 2009, 2013; Domínguez et al, 2011, 2013a,b; Morona et al, 2011). Single and double-labeled sections were analyzed with an Olympus BX51 microscope equipped for fluorescence with appropriate filter combinations, and selected sections were photographed using a digital camera Olympus DP72.…”

Section: Methodsmentioning

confidence: 99%

“…The immunohistochemical techniques employed in the present study allow high-resolution analysis of expressing cells (Hitchcock et al, 1996; Wullimann and Rink, 2001; González and Northcutt, 2009; Domínguez et al, 2011, 2013a,b; Ferreiro-Galve et al, 2012; Joven et al, 2013a,b). To identify accurately the cell groups expressing Pax7, we used combined immunohistofluorescence to simultaneously reveal several neuronal markers, which served to highlight the boundaries and landmarks of numerous brain regions, as previously reported (González et al, 1994, 2002; Tuinhof et al, 1994; Barale et al, 1996; López and González, 2002; Morona and González, 2008, 2009, 2013; Domínguez et al, 2013a,b). These markers included the γ-amino butyric acid (GABA), calretinin (CR), nitric oxide synthase (NOS), tyrosine hydroxylase (TH), and the transcription factors Nkx2.1 and Otp.…”

Section: Introductionmentioning

confidence: 99%

Regional expression of Pax7 in the brain of Xenopus laevis during embryonic and larval development

Bandín¹,

Morona²,

Moreno³

et al. 2013

Front. Neuroanat.

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Pax7 is a member of the highly conserved Pax gene family that is expressed in restricted zones of the central nervous system (CNS) during development, being involved in early brain regionalization and the maintenance of the regional identity. Using sensitive immunohistochemical techniques we have analyzed the spatiotemporal pattern of Pax7 expression in the brain of the anuran amphibian Xenopus laevis, during development. Pax7 expression was first detected in early embryos in the basal plate of prosomere 3, roof and alar plates of prosomere 1 and mesencephalon, and the alar plate of rhombomere 1. As development proceeded, Pax7 cells were observed in the hypothalamus close to the catecholaminergic population of the mammillary region. In the diencephalon, Pax7 was intensely expressed in a portion of the basal plate of prosomere 3, in the roof plate and in scattered cells of the thalamus in prosomere 2, throughout the roof of prosomere 1, and in the commissural and juxtacommissural domains of the pretectum. In the mesencephalon, Pax7 cells were localized in the optic tectum and, to a lesser extent, in the torus semicircularis. The rostral portion of the alar part of rhombomere 1, including the ventricular layer of the cerebellum, expressed Pax7 and, gradually, some of these dorsal cells were observed to populate ventrally the interpeduncular nucleus and the isthmus (rhombomere 0). Additionally, Pax7 positive cells were found in the ventricular zone of the ventral part of the alar plate along the rhombencephalon and the spinal cord. The findings show that the strongly conserved features of Pax7 expression through development shared by amniote vertebrates are also present in the anamniote amphibians as a common characteristic of the brain organization of tetrapods.

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Pattern of calbindin‐D28k and calretinin immunoreactivity in the brain ofXenopus laevisduring embryonic and larval development

Cited by 13 publications

References 238 publications

Pattern of Neurogenesis and Identification of Neuronal Progenitor Subtypes during Pallial Development in Xenopus laevis

Pattern of Neurogenesis and Identification of Neuronal Progenitor Subtypes during Pallial Development in Xenopus laevis

Spatiotemporal Development of the Orexinergic (Hypocretinergic) System in the Central Nervous System of <b><i>Xenopus laevis</i></b>

Regional expression of Pax7 in the brain of Xenopus laevis during embryonic and larval development

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