Molecular Markers of Adult Neurogenesis in the Telencephalon and Tectum of Rainbow Trout, Oncorhynchus mykiss

Abstract

In the brain of teleost fish, radial glial cells are the major type of astroglial cells. To answer the question as to how radial glia structures adapt to the continuous growth of the brain, which is characteristic of salmonids, it is necessary to study various types of cells (neuronal precursors, astroglial cells, and cells in a state of neuronal differentiation) in the major integrative centers of the salmon brain (telencephalon and tectum opticum), using rainbow trout, Oncorhynchus mykiss, as a model. A study of the distribution of several molecular markers in the telencephalon and tectum with the identification of neural stem/progenitor cells, neuroblasts, and radial glia was carried out on juvenile (three-year-old) O. mykiss. The presence of all of these cell types provides specific conditions for the adult neurogenesis processes in the trout telencephalon and tectum. The distribution of glutamine synthetase, a molecular marker of neural stem cells, in the trout telencephalon revealed a large population of radial glia (RG) corresponding to adult-type neural stem cells (NSCs). RG dominated the pallial region of the telencephalon, while, in the subpallial region, RG was found in the lateral and ventral zones. In the optic tectum, RG fibers were widespread and localized both in the marginal layer and in the periventricular gray layer. Doublecortin (DC) immunolabeling revealed a large population of neuroblasts formed in the postembryonic period, which is indicative of intense adult neurogenesis in the trout brain. The pallial and subpallial regions of the telencephalon contained numerous DC+ cells and their clusters. In the tectum, DC+ cells were found not only in the stratum griseum periventriculare (SGP) and longitudinal torus (TL) containing proliferating cells, but also in the layers containing differentiated neurons: the central gray layer, the periventricular gray and white layers, and the superficial white layer. A study of the localization patterns of vimentin and nestin in the trout telencephalon and tectum showed the presence of neuroepithelial neural stem cells (eNSCs) and ependymoglial cells in the periventricular matrix zones of the brain. The presence of vimentin and nestin in the functionally heterogeneous cell types of adult trout indicates new functional properties of these proteins and their heterogeneous involvement in intracellular motility and adult neurogenesis. Investigation into the later stages of neuronal development in various regions of the fish brain can substantially elucidate the major mechanisms of adult neurogenesis, but it can also contribute to understanding the patterns of formation of certain brain regions and the involvement of RG in the construction of the definite brain structure.

Constitutive Neurogenesis and Neuronal Plasticity in the Adult Cerebellum and Brainstem of Rainbow Trout, Oncorhynchus mykiss

“…In the trout cerebellum, a relatively low level of vimentin (Vim) immunopositivity was revealed ( Figure 7 A), which is consistent with the data for optic tectum [ 3 ]. A few dense, intensely labeled Vim+ clusters of undifferentiated and elongated cells were found in the DMZ ( Figure 7 A, black inset, Table 4 ).…”

“…Under normal conditions, this mechanism prevents the neurotoxic accumulation of glutamate in neural tissue, protecting neurons from cell death. In fish, GS often labels radial glial cells [ 3 ] but can also be detected in glia-like cells [ 9 ]. In the A. leptorhynchus cerebellum, the amount of GS increases after injury [ 38 ], while the synthesis of this enzyme in the mammalian CNS decreases after injury [ 37 ].…”

“…the telencephalon and tectum of trout and chum salmon O. keta [3,8]. Monoclonal antibodies against vimentin were previously used in our laboratory to detect NSPCs in the mesencephalic tegmentum of juvenile chum salmon, O. keta, [8] and cerebellum of juvenile masu salmon, O. masou [13].…”

“…The study of the neuronal development stages in different parts of the fish brain not only elucidates the basic mechanisms of adult neurogenesis but also contributes to understanding the formation patterns in certain brain regions and the involvement of adult neural stem/progenitor cells (aNSPCs) in the construction of the definitive brain structure [ 1 , 2 ]. Previously, the distribution of aNSPCs, formed during the homeostatic neurogenesis in the telencephalon and tectum of the brain, was studied in 3-year-old rainbow trout, Oncorhynchus mykiss , in order to address the question concerning the mode of adaptation of the radial glia (RG) structures and the population of neuroepithelial (NE) cells to the continuous brain growth characteristic of salmon [ 3 ].…”

“…In contrast to mammalian models, we consider the rainbow trout brain as a preferred vertebrate model to extend our understanding of the cellular and molecular programs required for successful CNS growth and regeneration. A distinctive feature of the salmon brain is fetalization, or the presence of signs of the embryonic brain structure in juvenile Oncorhynchus keta [ 8 ], Oncorhynchus masou [ 9 ], and adult Oncorhynchus mykiss individuals [ 3 ]. In this regard, the study of the expression of glutamine synthetase (GS), vimentin (Vim), and nestin (Nes), which are molecular markers of aNSPCs in zebrafish [ 11 , 12 , 24 , 28 ] and Apteronotus leptorhynchus [ 35 ], contributes to extending our knowledge of the nature of aNSPCs in less studied fish models and, therefore, is important for the comparative study of neurogenesis in general.…”