Full Anatomical Recovery of the Dopaminergic System after a Complete Spinal Cord Injury in Lampreys

Fernández-López, Blanca; Romaus-Sanjurjo, Daniel; Cornide‐Petronio, María Eugenia; Gómez-Fernández, Sonia; Barreiro‐Iglesias, Antón; Rodicio, Marı́a Celina

doi:10.1155/2015/350750

Cited by 18 publications

(15 citation statements)

References 40 publications

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“…We show that, in lampreys, the drastic initial decrease in the number of glutamate-ir cells and processes in response to a complete spinal cord lesion is followed by an almost complete recovery of the system; with the exception of the CSFc cells that are never recovered, even at 24 wpl. This is in contrast with the dopaminergic system, which undergoes full anatomical recovery following a complete injury at the same spinal cord level in lampreys34. However, the serotonergic system of lampreys also shows an incomplete recovery after SCI26.…”

Section: Discussionmentioning

confidence: 89%

“…However, neuronal overproduction after SCI in zebrafish is much larger, up to 5-fold the number of neurons in control animals29. By contrast, the number of dopaminergic neurons after SCI in lampreys increases progressively until reaching levels similar to those found in un-lesioned animals, but without an initial phase of overproduction of dopaminergic neurons34. This highlights the importance of studying the behaviour of neurons with different neurotransmitter phenotypes to decipher how they respond to the injury and their contribution to functional restoration after a lesion.…”

Section: Discussionmentioning

confidence: 96%

“…Complete transection of the spinal cord at the level of the 5 th gill was performed as previously described25272834. Sham-operated controls were processed in the same way but only performing the surgical incision of the dorsal body wall without injuring the spinal cord.…”

Section: Methodsmentioning

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: Discussionmentioning

confidence: 89%

Section: Discussionmentioning

confidence: 96%

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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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“…Positive in situ signal in sea lamprey brain sections had a granular appearance probably due to low expression of these mRNAs in each single cell of the sea lamprey. Previous studies looking at the expression of different neurotransmitter receptors in lampreys have shown that the in situ hybridization signals appeared as a dotted labeling in sections of the CNS: serotonin receptor 1A (Cornide-Petronio et al, 2013, 2014), dopamine receptor D2 (Robertson et al, 2012; Fernández-López et al, 2015), and dopamine receptor D4 (Pérez-Fernández et al, 2016); suggesting that low expression levels are a common feature of different metabotropic neurotransmitter receptors.…”

Section: Discussionmentioning

confidence: 98%

Cloning of the GABAB Receptor Subunits B1 and B2 and their Expression in the Central Nervous System of the Adult Sea Lamprey

et al. 2016

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In vertebrates, γ-aminobutyric acid (GABA) is the main inhibitory transmitter in the central nervous system (CNS) acting through ionotropic (GABAA) and metabotropic (GABAB) receptors. The GABAB receptor produces a slow inhibition since it activates second messenger systems through the binding and activation of guanine nucleotide-binding proteins [G-protein-coupled receptors (GPCRs)]. Lampreys are a key reference to understand molecular evolution in vertebrates. The importance of the GABAB receptor for the modulation of the circuits controlling locomotion and other behaviors has been shown in pharmacological/physiological studies in lampreys. However, there is no data about the sequence of the GABAB subunits or their expression in the CNS of lampreys. Our aim was to identify the sea lamprey GABAB1 and GABAB2 transcripts and study their expression in the CNS of adults. We cloned two partial sequences corresponding to the GABAB1 and GABAB2 cDNAs of the sea lamprey as confirmed by sequence analysis and comparison with known GABAB sequences of other vertebrates. In phylogenetic analyses, the sea lamprey GABAB sequences clustered together with GABABs sequences of vertebrates and emerged as an outgroup to all gnathostome sequences. We observed a broad and overlapping expression of both transcripts in the entire CNS. Expression was mainly observed in neuronal somas of the periventricular regions including the identified reticulospinal cells. No expression was observed in identifiable fibers. Comparison of our results with those reported in other vertebrates indicates that a broad and overlapping expression of the GABAB subunits in the CNS is a conserved character shared by agnathans and gnathostomes.

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“…Data sources: Amphioxus; GABAergic neuron, serotonergic neuron, dopaminergic neurons not found in spinal cord, no data on other types of neurons. Lamprey; glutamatergic, glutamate‐glycine, glutamate‐GABA neurons, dopamine‐GABA neurons, dopamine neurons, dopamine‐glutamate neurons, aspartate, aspartate‐GABA neurons, glycine, glycine‐GABA neurons, cholinergic neurons . Larval data instead of adult for serotoninergic and GABAergic neurons .…”

Section: Outgroups and Evolutionary Origins: Spinal Cords Cell Typesmentioning

confidence: 99%

Evolution of vertebrate spinal cord patterning

Leung

Shimeld

2019

Developmental Dynamics

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The vertebrate spinal cord is organized across three developmental axes, anterior‐posterior (AP), dorsal‐ventral (DV), and medial‐lateral (ML). Patterning of these axes is regulated by canonical intercellular signaling pathways: the AP axis by Wnt, fibroblast growth factor, and retinoic acid (RA), the DV axis by Hedgehog, Tgfβ, and Wnt, and the ML axis where proliferation is controlled by Notch. Developmental time plays an important role in which signal does what and when. Patterning across the three axes is not independent, but linked by interactions between signaling pathway components and their transcriptional targets. Combined this builds a sophisticated organ with many different types of cell in specific AP, DV, and ML positions. Two living lineages share phylum Chordata with vertebrates, amphioxus, and tunicates, while the jawless fish such as lampreys, survive as the most basally divergent vertebrate lineage. Genes and mechanisms shared between lampreys and other vertebrates tell us what predated vertebrates, while those also shared with other chordates tell us what evolved early in chordate evolution. Between these lie vertebrate innovations: genetic and developmental changes linked to evolution of new morphology. These include gene duplications, differences in how signals are received, and new regulatory connections between signaling pathways and their target genes.

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Full Anatomical Recovery of the Dopaminergic System after a Complete Spinal Cord Injury in Lampreys

Cited by 18 publications

References 40 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

Cloning of the GABAB Receptor Subunits B1 and B2 and their Expression in the Central Nervous System of the Adult Sea Lamprey

Evolution of vertebrate spinal cord patterning

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