GFAP expression in the optic nerve and increased H₂S generation in the integration centers of the rainbow trout (Oncorhynchus mykiss) brain after unilateral eye injury

Abstract

Hydrogen sulfide (H 2 S) is considered as a protective factor against cardiovascular disorders. However, there are few reports on the effects of H 2 S in the central nervous system during stress or injury. Previous studies on goldfish have shown that astrocytic response occurs in the damaged and contralateral optic nerves. Glial fibrillary acidic protein (GFAP) concentration in the optic nerves of rainbow trout has not been measured previously. This study further characterized the astrocytic response in the optic nerve and the brain of a rainbow trout ( Oncorhynchus mykiss ) after unilateral eye injury and estimated the amount of H 2 S-producing enzyme cystathionine β-synthase (CBS) in the brain of the rainbow trout. Within 1 week after unilateral eye injury, a protein band corresponding to a molecular weight of 50 kDa was identified in the ipsi- and contralateral optic nerves of the rainbow trout. The concentration of GFAP in the injured optic nerve increased compared to the protein concentration on the contralateral side. The results of a quantitative analysis of GFAP + cell distribution in the contralateral optic nerve showed the largest number of GFAP + cells and fibers in the optic nerve head. In the damaged optic nerve, patterns of GFAP + cell migration and large GFAP + bipolar activated astrocytes were detected at 1 week after unilateral eye injury. The study of H 2 S-producing system after unilateral eye injury in the rainbow trout was conducted using enzyme-linked immunosorbent assay, western blot analysis, and immunohistochemistry of polyclonal antibodies against CBS in the integrative centers of the brain: telencephalon, optic tectum, and cerebellum. Enzyme-linked immunosorbent assay results showed a 1.7-fold increase in CBS expression in the rainbow trout brain at 1 week after unilateral eye injury compared with that in intact animals. In the ventricular and subventricular regions of the rainbow trout telencephalon, CBS + radial glia and neuroepithelial cells were identified. After unilateral eye injury, the number of CBS + neuroepithelial cells in the pallial and subpallial periventricular regions of the telencephalon increased. In the optic tectum, unilateral eye injury led to an increase in CBS expression in radial glial cells; simultaneously, the number of CBS + neuroepithelial cells decreased in intact animals. In the cerebellum of the rainbow trout, neuroglial interrelationships were revealed, where H 2 S was released, apparently, from astrocyte-like cells. The organization of H 2 S-producing cell complexes suggests that, the amount of glutamate produced in the rainbow trout cerebellum and its reuptake was controlled by astrocyte-like cells, reducing its excitotoxicity. In ...

Hydrogen Sulfide Modulates Adult and Reparative Neurogenesis in the Cerebellum of Juvenile Masu Salmon, Oncorhynchus masou

“…The activation of neurons in the cerebellum can lead to the release of glutamate, which, in turn, leads to an increase in intracellular calcium [ 45 , 47 ]. Thus, the wide distribution of type 2 cells in the cerebellum of juvenile O. masou is indicative of mediator–modulator intercellular interactions, which is consistent with previously obtained data on fish [ 12 , 84 ]. The high content of type 2 CBS+ cells also suggests intercellular neuron/glial/microglial interactions associated with the release of H 2 S from intensely labeled glia-like cells and/or microglia [ 86 , 87 ].…”

“…H 2 S is a diffusely spreading gaseous mediator that easily interacts with many signaling molecules, as well as modifies the structure of channel proteins and modulates neuroglia functions [ 47 ]. Thus, the high level of H 2 S production in the cerebellum of juvenile O. masou correlates with high neurogenic activity in the cerebellum and other parts of the brain, which is consistent with the results previously obtained for trout [ 12 ] and other fish species [ 84 ]. Studies on the PCNA localization in the cerebellum of O. masou showed that the patterns of constitutive proliferation were local, small in size, CNNs located in the area of the DMZ, as well as in the molecular layer of all neuroanatomical zones [ 68 ].…”

“…According to the data obtained on mammals, a high CBS concentration is necessary for the early maturation and growth of neuronal networks, which indicates the involvement of H 2 S in neuronal differentiation [ 85 ]. The results of studies on juvenile O. masou showed a larger number of cells and a higher level of CBS labeling intensity compared to older trout, O. mykiss [ 12 ]. This probably indicates more intense neurogenic processes in the cerebellum of juvenile O. masou .…”

“…Their ontogenesis is characterized by such phenomena as developmental delay and retention of signs of the embryonic organization of CNS which occur at the stage of active brain growth, where the morphogenesis processes are most clearly and fully expressed [ 11 ]. This feature of salmon CNS development, referred to as embrionalization, is confirmed by the presence of a large number of embryonic neuronal stem cells (NSCs) corresponding to cells of the neuroepithelial (NE) type, as well as radial glial (RG) cells corresponding to adult progenitors [ 12 , 13 , 14 , 15 ].…”

“…H 2 S plays an essential role in post-embryonic neurogenesis and in post-traumatic neuronal regeneration in adult animals by activating certain molecular pathways and cell–cell interactions [ 12 , 45 ]. H 2 S, like other gaseous transmitters, is spread by diffusion, which determines its involvement in the processes of intercellular signaling such as, in particular, the regulation of calcium fluxes in cell–cell interaction [ 46 ].…”