Immunohistochemical localization of orexins (hypocretins) in the brain of reptiles and its relation to monoaminergic systems

Domı́nguez, Laura; Morona, Ruth; Joven, Alberto; González, Agustı́n; López, Jesús M.

doi:10.1016/j.jchemneu.2009.07.007

Cited by 37 publications

(40 citation statements)

References 153 publications

(248 reference statements)

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“…The antisera anti-OX-A and anti-OX-B used in the present study, whose specificity has been previously confirmed [López et al, 2009a], were raised against a peptide mapping at the C-terminus of human OX-A or OX-B. This explains the common pattern of immunostaining obtained with both antibodies in the present and previous studies [Singletary et al, 2005[Singletary et al, , 2006López et al, 2009a, b;Domínguez et al, 2010b;Miranda et al, 2013;López et al, 2014], and therefore only orexin-immunoreactivity, in general, could be investigated with these antisera.…”

Section: Discussionsupporting

confidence: 76%

“…The antibodies against orexin-A and orexin-B used in the present study revealed patterns of immunoreactivity that were consistent among animals treated identically in each stage of development analyzed. No differences were observed in the pattern of immunoreactivity using anti-orexin-A or anti-orexin-B antisera, as has been reported in adult amphibians [López et al, 2009a] and other groups of vertebrates [López et al, 2009b[López et al, , 2014Domínguez et al, 2010b], and therefore we will refer in general to OX-ir structures. The ontogeny of Xenopus is divided into a relatively short embryonic phase and a long larval period, which starts with independent feeding and is generally subdivided into three sets of stages: (1) premetamorphic stages, (2) prometamorphic stages, and (3) metamorphic climax ( fig.…”

Section: Resultsmentioning

confidence: 67%

“…The close relationship between the orexinergic and catecholaminergic systems has been proposed in fishes [Kaslin et al, 2004;López et al, 2009b], adult amphibians [Suzuki et al, 2008;López et al, 2009a], reptiles [Domínguez et al, 2010b], and mammals, where reciprocal connections have been demonstrated between both systems. Thus, whereas the orexinergic neurons are directly inhibited by noradrenaline and dopamine [Yamanaka et al, 2003[Yamanaka et al, , 2006, orexins exert an excitatory effect via indirect presynaptic and direct postsynaptic mechanisms in noradrenergic and dopaminergic cells of the ventral tegmental area, the substantia nigra, the locus coeruleus, and the A1, A2, and A5 cell groups [Smith et al, 2002a;Baldo et al, 2003;Ciriello et al, 2003;Ferguson and Samson, 2003;Walling et al, 2004;Eriksson et al, 2010].…”

Section: Discussionmentioning

confidence: 96%

“…The present study provides the spatiotemporal sequence of the appearance of OX-ir cells and fibers through the brain development of X. laevis using antibodies against mammalian orexin-A and orexin B, which have been similarly used in previous studies in adult amphibian brains [López et al, 2009a], reptiles [Domínguez et al, 2010b], and some groups of fishes [López et al, 2009b;. The structure of orexins is highly preserved in all vertebrates, with only some variations in the amino acid sequence, with the C-terminal sequence being very conserved in the orexins of all of the vertebrate species analyzed [Sakurai et al, 1998;Shibahara et al, 1999;Kaslin et al, 2004;Panula, 2010;Wong et al, 2011;Yan et al, 2011].…”

Section: Discussionmentioning

confidence: 99%

“…In mammals, orexins are produced by a small population of neurons located in the lateral hypothalamus that profusely innervates all major subdivisions of the central nervous system Cutler et al, 1999;Nambu et al, 1999;McGranaghan and Piggins, 2001;Mintz et al, 2001;Novak and Albers, 2002;Sakurai, 2005;Nixon and Smale, 2007]. The highly phylogenetic conserved molecular structure of these neuropeptides [Shibahara et al, 1999;Wong et al, 2011] has allowed the immunohistochemical localization of orexinlike immunoreactive cells and fibers in the brain of nonmammalian vertebrates like birds [Ohkubo et al, 2002;Singletary et al, 2006;Miranda et al, 2013], reptiles [Domínguez et al, 2010b], amphibians [Shibahara et al, 1999;Galas et al, 2001;López et al, 2009a], and distinct fish groups like lungfishes [López et al, 2009b], teleosts [Kaslin et al, 2004;Huesa et al, 2005;Amiya et al, 2007;Panula, 2010;Matsuda et al, 2012;Pérez Sirkin et al, 2013], and cladistians [López et al, 2014]. All of these studies point to a conserved organization of the orexinergic system among vertebrates, with a general presence of orexin neurons in the hypothalamus (although the particular localization within this region can vary among vertebrate groups or even among species within the same group) and a pattern of extensive innervation on the main brain areas.…”

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confidence: 99%

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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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Section: Discussionsupporting

confidence: 76%

Section: Resultsmentioning

confidence: 67%

Section: Discussionmentioning

confidence: 96%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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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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Subdivisions of the turtle Pseudemys scripta subpallium based on the expression of regulatory genes and neuronal markers

Moreno

Morona

López

et al. 2010

J of Comparative Neurology

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The patterns of distribution of a set of conserved brain developmental regulatory transcription factors and neuronal markers were analyzed in the subpallium of the juvenile turtle, Pseudemys scripta. Immunohistochemical techniques were used with a combination of primary antibodies for the identification of the main boundaries and subdivisions in the basal telencephalon. In the basal ganglia, the combinatorial expression on Pax6, Nkx2.1, and GABA was a powerful tool for the identification of the nucleus accumbens, the dorsal portion of the striatum, and the pallidal regions. It was also possible to suggest migratory streams of neurons from the pallidum into the striatal regions. On the basis of GABA, Pax6, Tbr1, tyrosine hydroxylase, Darpp32, and Nkx2.1 combinatorial expression patterns, the boundaries of the septal subdivisions and their embryological origin were assessed. In particular, the bed nucleus of the stria terminalis was identified. Within the amygdaloid complex, the striatal central amygdala was characterized by Pax6 expression, whereas Orthopedia gene expression highlighted, at least, a subdivision of the medial amygdala. A newly identified preoptic commissural area and the boundaries of the preoptic area were assessed, mainly by the localization of Nkx2.1 expression. Finally, additional data were obtained by combining immunohistochemistry and tracing techniques on the interneuronal nature of the cholinerginergic, nitrergic, and Nkx2.1-positive striatal cells. Taken together, all the results of the present study allowed recognizing main features in the organization of the subpallium in reptiles that, in most cases, are shared with other amniotes and amphibians.

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Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers

Moreno

Domı́nguez

Morona

et al. 2011

J of Comparative Neurology

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The patterns of distribution of a set of conserved brain developmental regulatory transcription factors and neuronal markers were analyzed in the hypothalamus of the juvenile turtle, Pseudemys scripta. Combined immunohistochemical techniques were used for the identification of the main boundaries and subdivisions in the optic, paraventricular, tuberal, and mammillary hypothalamic regions. The combination of Tbr1 and Pax6 with Nkx2.1 allowed identification of the boundary between the telencephalic preoptic area, rich in Nkx2.1 expression, and the prethalamic eminence, rich in Tbr1 expression. In addition, at this level Nkx2.2 expression defined the boundary between the telencephalon and the hypothalamus. The dorsalmost hypothalamic domain was the supraoptoparaventricular region that was defined by the expression of Otp/Pax6 and the lack of Nkx2.1/Isl1. It is subdivided into rostral, rich in Otp and Nkx2.2, and caudal, only Otp-positive, portions. Ventrally, the suprachiasmatic area was identified by its catecholaminergic groups and the lack of Otp, and could be further divided into a rostral portion, rich in Nkx2.1 and Nkx2.2, and a caudal portion, rich in Isl1 and devoid of Nkx2.1 expression. The expressions of Nkx2.1 and Isl1 defined the tuberal hypothalamus, whereas only the rostral portion expressed Otp. Its caudal boundary was evident by the lack of Isl1 in the adjacent mammillary area, which expressed Nkx2.1 and Otp. All these results provide an important set of data on the interpretation of the hypothalamic organization in a reptile, and hence make a useful contribution to the understanding of hypothalamic evolution.

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Immunohistochemical localization of orexins (hypocretins) in the brain of reptiles and its relation to monoaminergic systems

Cited by 37 publications

References 153 publications

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

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

Subdivisions of the turtle Pseudemys scripta subpallium based on the expression of regulatory genes and neuronal markers

Subdivisions of the turtle Pseudemys scripta hypothalamus based on the expression of regulatory genes and neuronal markers

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