Expression of Satb2 in adult brain of key non-mammalian vertebrates: insights from evolution

Abstract

Satb2 is a transcription factor with functional and regulatory mechanisms, and post-translational modifications highly conserved in mammals. However, although its distribution has been analyzed in the mouse brain, there are few data in other non-mammal models. Therefore, in the present study we have analyzed the immunolocalization of Satb2 in the brain of adult specimens of different models at key evolutionary points of vertebrate diversification, including representative species of sarcopterygians and actinopterygians. In addition, we used other neuronal markers of highly conserved populations in the vertebrate brain, such as catecholaminergic, serotonergic and Otp populations, involved in the specificity of certain brain areas. The neuroanatomical pattern of Satb2, interpreted according to the current prosomeric model, serves to identify brain regions and compare them among the studied species, and with previous reported data, mainly for amniotes. We identified that Satb2 expressions have similar topologies in the subpallium of models studied, whereas striking differences were found in the pallium between sarcopterygian and actinopterygian vertebrates. Only the turtle showed expression in the dorsal derivatives of the pallium, specifically in the dorsal cortex, only scattered in Xenopus, whereas the lateral derivatives of the pallium expressed Satb2 in sarcopterygians, but not in actinopterygians. In the medial amygdala, or homologous structures, all models expressed Satb2, but only tetrapods also co-expressed Otp, probably originating from the paraventricular hypothalamic region, since only in those models a minor population of Satb2/Otp cells was also detected. In the caudal telencephalon, all models showed significant expression in the preoptic area, including the acroterminal domain of this region, where Satb2-expressing cells were dopaminergic. In the alar hypothalamus, all models showed Satb2 in the subparaventricular area, whereas in the basal hypothalamus only sarcopterygians showed a significant population in the tuberal hypothalamus, doubly labeled with Otp only in lungfish. The diencephalon of sarcopterygians showed Satb2 labeling in the prethalamus, and only turtles and lungfish showed expression in the thalamus. At midbrain levels, the optic tectum housed scattered Satb2 cells exclusively in turtles, while the expression along the rostrocaudal reticular formation and parabrachial nucleus was a conserved feature of sarcopterygians. The neuroanatomical pattern of Satb2 revealed important differences between sarcopterygians and actinopterygians, and these divergences may be related to the distinct functional involvement of Satb2 in the acquisition of various neural phenotypes and in the establishment of connectivity of these cells.