Mitral cell development in the olfactory bulb of sharks: evidences of a conserved pattern of glutamatergic neurogenesis

Abstract

In mammals, the development of the olfactory bulb (OB) relies in part on the expression of transcription factors involved in the specifications/differentiation of glutamatergic cells. In a previous study from our group, a high molecular similarity was reported between mammals and cartilaginous fishes regarding the neurogenic mechanisms underlying the development of glutamatergic cells in the telencephalon. However, information about the transcriptional program operating in the development of the glutamatergic system (mainly represented by mitral cells) in the OB is lacking in the catshark Scyliorhinus canicula , a cartilaginous fish. Using immunohistochemistry and in situ hybridization techniques, we have found that, previously to the appearance of the olfactory primordium (OP), proliferating cells expressing Pax6 with molecular hallmarks of progenitor radial glia were located in the ventrolateral pallial ventricular zone. Later in development, when the OP is recognizable, a stream of Pax6-positive cells were observed between the ventricular zone and the OP, where transcription factors involved in mitral cell development in mammals ( ScTbr2 , ScNeuroD, Tbr1) are expressed. Later in development, these transcription factors became expressed in a layered-like structure where ScVglut1 , a marker of mitral cells, is also present. Our data suggest that the transcriptional program related with the specification/differentiation of glutamatergic cells in the telencephalon has been conserved throughout the evolution of vertebrates. These results, in combination with previous studies concerning GABAergic neurogenesis in sharks, have evidenced that the OB of mammals and sharks shares similarities in the timing and molecular programs of development.

Morphological Diversity of Calretinin Interneurons Generated From Adult Mouse Olfactory Bulb Core Neural Stem Cells

“…We then asked whether adult OB neurogenesis could be regulated by transcription factor expression by injecting retroviral vectors expressing Tbr1, a transcription factor critical for the differentiation of mitral (glutamatergic) neurons in the OB ( Bulfone et al, 1995 ; Méndez-Gómez et al, 2011 ; Docampo-Seara et al, 2019 ). We overexpressed Tbr1 in the adult OB core NSCs to examine whether this might induce the formation of mitral neurons, and/or modify the pattern of interneuron migration and differentiation.…”

Localization and Characterization of Major Neurogenic Niches in the Brain of the Lesser-Spotted Dogfish Scyliorhinus canicula

“…In the spotted catshark, on the other hand, the lateral ventricle extends into the olfactory bulbs. During embryonic development, mitral cells are produced locally in the OB [ 39 ]; however, there is still the possibility that the pallial/subpallial neurogenic zones generate some neurons of the OB during adulthood.…”

“…Due to ease of collection and possibility of captive breeding, this species has become a model chondrichthyan. The patterns of embryonic neurogenesis in the spotted catshark Scyliorhinus canicula were described in a series of papers that analyzed embryonic neurogenesis in the telencephalon and the cerebellum, and adult neurogenesis was demonstrated in the adult telencephalon and retina with a clear, age-dependent decline, at least in the retina [ 38 , 39 , 40 , 41 , 42 , 43 , 44 , 45 ]. The analysis of the adult telencephalon, in particular, demonstrated the existence of a neurogenic niche lining the entire third ventricle and confirmed the presence of mitotically active RG cells, indicating that the organization of the telencephalic niche is similar to the SVZ of tetrapods.…”

Tbr1 Misexpression Alters Neuronal Development in the Cerebral Cortex

“…All these processes are tightly controlled during development by transcription factors (TFs) like T-box brain 1 (Tbr1 or TES-56), which is expressed strongly in the developing dorsal telencephalon (neocortex, hippocampus and olfactory bulb (OB)). Tbr1 is expressed by newborn neocortical neurons, specifically Cajal-Retzius cells, subplate cells and layer VI glutamatergic neurons, as well as the cells in the developing hippocampus and OB [10][11][12][13][14][15][16][17][18][19][20][21][22]. Moreover, Tbr1 has also been detected in dividing NPCs, giving rise to OB mitral neurons [23,24] Tbr1 is necessary for the differentiation of the preplate and layer VI neurons, for axon pathfinding and for the correct acquisition of the regional and laminar identity of projection neurons [12,[25][26][27][28][29].…”

“…All these processes are tightly controlled during development by transcription factors (TFs) like T-box brain 1 (Tbr1 or TES-56), which is expressed strongly in the developing dorsal telencephalon (neocortex, hippocampus and olfactory bulb (OB)). Tbr1 is expressed by newborn neocortical neurons, specifically Cajal-Retzius cells, subplate cells and layer VI glutamatergic neurons, as well as the cells in the developing hippocampus and OB [ 10 – 22 ]. Moreover, Tbr1 has also been detected in dividing NPCs, giving rise to OB mitral neurons [ 23 , 24 ]…”