Neuronal release and successful astrocyte uptake of aminoacidergic neurotransmitters after spinal cord injury in lampreys

Fernández-López, Blanca; Valle-Maroto, Silvia María; Barreiro‐Iglesias, Antón; Rodicio, Marı́a Celina

doi:10.1002/glia.22678

Cited by 27 publications

(37 citation statements)

References 82 publications

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“…This is in agreement with our previous results in which we have reported a complete disappearance of glutamate immunoreactivity in region 2 of the spinal cord immediately after a SCI25. This is followed by a gradual increase until 4 to 10 wpl, when the number of glutamate-ir cells is slightly higher than that of control un-lesioned animals (between 1.2 to1.5 times higher).…”

Section: Discussionsupporting

confidence: 93%

“…In a recent study in lampreys, we found a complete disappearance of glutamate immunoreactivity immediately after a complete transection of the cord rostrally and caudally to the site of injury25, which was related to excessive glutamate release. Based on these previous results, the main aims of the present study were (1) to determine whether, in lampreys, axotomized glutamatergic neurons that lose glutamate immunoreactivity immediately after SCI are able to recover it later on, evaluating the possible contribution of cell death to this initial loss of glutamate immunoreactivity and (2) to study the long-term evolution of the glutamatergic system (cells and fibres) after a complete SCI in lampreys.…”

mentioning

confidence: 63%

“…In a previous study from our group we observed the complete loss of glutamate immunoreactivity in region 2 of the spinal cord immediately after a complete SCI25. Here, we used TUNEL labelling at 1 and 2 days post-lesion (dpl) to reveal a possible contribution of cell death to this initial loss of glutamate immunoreactivity (Fig.…”

Section: Resultsmentioning

confidence: 89%

“…The animals were processed at 1 and 2 weeks post-lesion (wpl) and region 2a was analysed. The time-points were chosen based on our previous study25, in which glutamate immunoreactivity in the spinal cord was recovered in the first 500 μm rostral and caudal from the site of injury at 1 wpl. Rostral to the site of injury, 45% of the glutamate-ir cells of the grey matter glutamatergic populations (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Excessive glutamate release in response to a lesion causes glutamate excitotoxicity, which can lead to neuronal and oligodendrocyte death212223, thus worsening the outcome of the lesion. While the short term changes in glutamate levels after SCI are well documented2124, even in lampreys25, as well as the changes of other neurotransmitter systems during regeneration in lampreys or zebrafish (for example, the serotonergic system)26272829; surprisingly, much less is known about the long term changes in the glutamatergic system.…”

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confidence: 99%

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Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Fernández-López

Barreiro‐Iglesias

Rodicio

2016

Sci Rep

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Lampreys recover locomotion following a spinal cord injury (SCI). Glutamate is necessary to initiate and control locomotion and recent data suggest a crucial role for intraspinal neurons in functional recovery following SCI. We aimed to determine whether, in lampreys, axotomized spinal glutamatergic neurons, which lose glutamate immunoreactivity immediately after SCI, recover it later on and to study the long-term evolution and anatomical recovery of the spinal glutamatergic system after SCI. We used glutamate immunoreactivity to study changes in the glutamatergic system, tract-tracing to label axotomized neurons and TUNEL labelling to study cell death. Transections of the cord were made at the level of the fifth gill. TUNEL experiments indicated that cell death is a minor contributor to the initial loss of glutamate immunoreactivity. At least some of the axotomized neurons lose glutamate immunoreactivity, survive and recover glutamate immunoreactivity 1 week post-lesion (wpl). We observed a progressive increase in the number of glutamatergic neurons/processes until an almost complete anatomical recovery at 10 wpl. Among all the glutamatergic populations, the population of cerebrospinal fluid-contacting cells is the only one that never recovers. Our results indicate that full recovery of the glutamatergic system is not necessary for the restoration of function in lampreys.

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Section: Discussionsupporting

confidence: 93%

mentioning

confidence: 63%

Section: Resultsmentioning

confidence: 89%

Section: Resultsmentioning

confidence: 99%

mentioning

confidence: 99%

See 3 more Smart Citations

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Fernández-López

Barreiro‐Iglesias

Rodicio

2016

Sci Rep

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Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

Bozzo

Lacalli

Obino

et al. 2021

Glia

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Glial cells play important roles in the development and homeostasis of metazoan nervous systems. However, while their involvement in the development and function in the central nervous system (CNS) of vertebrates is increasingly well understood, much less is known about invertebrate glia and the evolutionary history of glial cells more generally. An investigation into amphioxus glia is therefore timely, as this organism is the best living proxy for the last common ancestor of all chordates, and hence provides a window into the role of glial cell development and function at the transition of invertebrates and vertebrates. We report here our findings on amphioxus glia as characterized by molecular probes correlated with anatomical data at the transmission electron microscopy (TEM) level. The results show that amphioxus glial lineages express genes typical of vertebrate astroglia and radial glia, and that they segregate early in development, forming what appears to be a spatially separate cell proliferation zone positioned laterally, between the dorsal and ventral zones of neural cell proliferation. Our study provides strong evidence for the presence of vertebrate‐type glial cells in amphioxus, while highlighting the role played by segregated progenitor cell pools in CNS development. There are implications also for our understanding of glial cells in a broader evolutionary context, and insights into patterns of precursor cell deployment in the chordate nerve cord.

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GABAergic Mechanisms Can Redress the Tilted Balance between Excitation and Inhibition in Damaged Spinal Networks

et al. 2021

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Correct operation of neuronal networks depends on the interplay between synaptic excitation and inhibition processes leading to a dynamic state termed balanced network. In the spinal cord, balanced network activity is fundamental for the expression of locomotor patterns necessary for rhythmic activation of limb extensor and flexor muscles. After spinal cord lesion, paralysis ensues often followed by spasticity. These conditions imply that, below the damaged site, the state of balanced networks has been disrupted and that restoration might be attempted by modulating the excitability of sublesional spinal neurons. Because of the widespread expression of inhibitory GABAergic neurons in the spinal cord, their role in the early and late phases of spinal cord injury deserves full attention. Thus, an early surge in extracellular GABA might be involved in the onset of spinal shock while a relative deficit of GABAergic mechanisms may be a contributor to spasticity. We discuss the role of GABA A receptors at synaptic and extrasynaptic level to modulate network excitability and to offer a pharmacological target for symptom control. In particular, it is proposed that activation of GABA A receptors with synthetic GABA agonists may downregulate motoneuron hyperexcitability (due to enhanced persistent ionic currents) and, therefore, diminish spasticity. This approach might constitute a complementary strategy to regulate network excitability after injury so that reconstruction of damaged spinal networks with new materials or cell transplants might proceed more successfully.

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Neuronal release and successful astrocyte uptake of aminoacidergic neurotransmitters after spinal cord injury in lampreys

Cited by 27 publications

References 82 publications

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Anatomical recovery of the spinal glutamatergic system following a complete spinal cord injury in lampreys

Amphioxus neuroglia: Molecular characterization and evidence for early compartmentalization of the developing nerve cord

GABAergic Mechanisms Can Redress the Tilted Balance between Excitation and Inhibition in Damaged Spinal Networks

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