A vesicular glutamate transporter in lampreys: cDNA cloning and early expression in the nervous system

Villar-Cerviño, Verona; Rocancourt, Claire; Menuet, Arnaud; Silva, Corinne Da; Wincker, Patrick; Anadón, Ramón; Mazan, Sylvie; Rodicio, Marı́a Celina

doi:10.1016/j.jchemneu.2010.03.009

Cited by 10 publications

(13 citation statements)

References 41 publications

(47 reference statements)

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“…In all sea lamprey brain nuclei containing Gαt‐S‐ir neurons, ISH with probes to vesicular glutamate transporter and immunohistochemistry against glutamate have revealed an abundance of glutamatergic neurons (Villar‐Cerviño et al, ). Glutamatergic transmission has been reported for intrinsically photoreceptive retinal ganglion cells (Engelund, Fahrenkrug, Harrison, & Hannibal, ) and glutamate appears to be the neurotransmitter used by the sea lamprey retinal and pineal photoreceptors that express opsin and Gαt‐S immunoreactivities (Villar‐Cerviño et al, ; present results). Together, these findings suggest that putative deep brain photoreceptors may be glutamatergic in the sea lamprey, but this needs to be assessed by further studies.…”

Section: Discussionsupporting

confidence: 67%

“…This nomenclature is different from that used by García‐Fernández et al (), who followed a columnar model of the lamprey forebrain (Schober, ). For brainstem regions, the nomenclature of Villar‐Cerviño, et al () was adopted. For spinal cord‐projecting brain nuclei, we used the nomenclature of Davis and McClellan () and Barreiro‐Iglesias et al ().…”

Section: Methodsmentioning

confidence: 99%

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Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

Barreiro‐Iglesias

Fernández-López

Sobrido‐Cameán

et al. 2017

J of Comparative Neurology

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We employed an anti-transducin antibody (Gαt-S), in combination with other markers, to characterize the Gαt-S-immunoreactive (ir) system in the CNS of the sea lamprey, Petromyzon marinus. Gαt-S immunoreactivity was observed in some neuronal populations and numerous fibers distributed throughout the brain. Double Gαt-S- and opsin-ir neurons (putative photoreceptors) are distributed in the hypothalamus (postoptic commissure nucleus, dorsal and ventral hypothalamus) and caudal diencephalon, confirming results of García-Fernández et al. (Cell and Tissue Research, 288, 267-278, 1997). Singly Gαt-S-ir cells were observed in the midbrain and hindbrain, increasing the known populations. Our results reveal for the first time in vertebrates the extensive innervation of many brain regions and the spinal cord by Gαt-S-ir fibers. The Gαt-S innervation of the habenula is very selective, fibers densely innervating the lamprey homologue of the mammalian medial nucleus (Stephenson-Jones et al., Proceedings of the National Academy of Sciences of the United States of America, 109, E164-E173, 2012), but not the lateral nucleus homologue. The lamprey neurohypophysis was not innervated by Gαt-S-ir fibers. We also analyzed by double immunofluorescence the relation of this system with other systems. A dopaminergic marker (TH), serotonin (5-HT) or GABA do not co-localize with Gαt-S-ir neurons although codistribution of fibers was observed. Codistribution of Gαt-S-ir fibers and isolectin-labeled extrabulbar primary olfactory fibers was observed in the striatum and hypothalamus. Neurobiotin retrograde transport from the spinal cord combined with immunofluorescence revealed spinal-projecting Gαt-S-ir reticular neurons in the caudal hindbrain. Present results in an ancient vertebrate reveal for the first time a collection of brain targets of Gαt-S-ir neurons, suggesting they might mediate non-visual modulation by light in many systems.

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Section: Discussionsupporting

confidence: 67%

Section: Methodsmentioning

confidence: 99%

Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

Barreiro‐Iglesias

Fernández-López

Sobrido‐Cameán

et al. 2017

J of Comparative Neurology

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“…The probes used correspond to two sequence fragments (of 584 and 3,483 bp) of a lamprey VGLUT recently cloned in Sylvie Mazan’s laboratory from a lamprey EST database, as reported elsewhere [39]. Plasmid DNA was purified from the selected clones, and the corresponding inserted fragments were excised as control.…”

Section: Methodsmentioning

confidence: 99%

“…To the best of our knowledge, there has been no report in non-mammalian adult vertebrates of the expression of VGLUTs in the spinal cord, or comprehensive studies of spinal glutamatergic populations using glutamate immunohistochemistry. The recent cloning of a cDNA coding for a lamprey vesicular glutamate transporter (VGLUT) [39] affords an alternative tool to assess the glutamatergic character of lamprey neurons, as reported in the brain [40], [41].…”

Section: Introductionmentioning

confidence: 99%

The Glutamatergic Neurons in the Spinal Cord of the Sea Lamprey: An In Situ Hybridization and Immunohistochemical Study

et al. 2012

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Glutamate is the main excitatory neurotransmitter involved in spinal cord circuits in vertebrates, but in most groups the distribution of glutamatergic spinal neurons is still unknown. Lampreys have been extensively used as a model to investigate the neuronal circuits underlying locomotion. Glutamatergic circuits have been characterized on the basis of the excitatory responses elicited in postsynaptic neurons. However, the presence of glutamatergic neurochemical markers in spinal neurons has not been investigated. In this study, we report for the first time the expression of a vesicular glutamate transporter (VGLUT) in the spinal cord of the sea lamprey. We also study the distribution of glutamate in perikarya and fibers. The largest glutamatergic neurons found were the dorsal cells and caudal giant cells. Two additional VGLUT-positive gray matter populations, one dorsomedial consisting of small cells and another one lateral consisting of small and large cells were observed. Some cerebrospinal fluid-contacting cells also expressed VGLUT. In the white matter, some edge cells and some cells associated with giant axons (Müller and Mauthner axons) and the dorsolateral funiculus expressed VGLUT. Large lateral cells and the cells associated with reticulospinal axons are in a key position to receive descending inputs involved in the control of locomotion. We also compared the distribution of glutamate immunoreactivity with that of γ-aminobutyric acid (GABA) and glycine. Colocalization of glutamate and GABA or glycine was observed in some small spinal cells. These results confirm the glutamatergic nature of various neuronal populations, and reveal new small-celled glutamatergic populations, predicting that some glutamatergic neurons would exert complex actions on postsynaptic neurons.

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“…Activation of NMDA receptors can induce fictive locomotion in some types of neuron in the lamprey spinal cord (Brodin and Grillner, ). As regards glutamate, a sea lamprey VGLUT gene has recently been cloned (Villar‐Cerviño et al, ) and its extended mRNA distribution revealed by in situ hybridization in the brain and spinal cord of the sea lamprey. VGLUT distribution is similar to that of glutamate‐containing neurons revealed by glutamate immunohistochemistry (Villar‐Cerviño et al, ; Fernández‐López et al, ).…”

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confidence: 99%

Aspartate‐containing neurons of the brainstem and rostral spinal cord of the sea lamprey Petromyzon marinus: Distribution and comparison with γ‐aminobutyric acid

Villar-Cerviño

Fernández-López

Rodicio

et al. 2014

J of Comparative Neurology

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The amino acid L-aspartate (ASP) is one of the most abundant excitatory neurotransmitters in the mammalian brain, but its distribution in other vertebrates has not yet been well characterized. We investigated the distribution of ASP in the brainstem and rostral spinal cord of the adult sea lamprey by using ASP immunohistochemistry. Our results indicate that ASP is accumulated in specific neurons, but not in glia (tanycytes). ASP-immunoreactive neuronal populations were rather similar as the glutamatergic populations reported in the adult sea lamprey (Villar-Cerviño et al. [2013] J Comp Neurol 521:522-557), although some important differences were noted. Characteristically, the largest reticular neurons of the lamprey brainstem (Müller cells) showed ASP immunoreactivity in perikarya and processes, in contrast to the absence or faint glutamate immunoreactivity reported in these perikarya. We also compared the distribution of ASP and γ-aminobutyric acid (GABA) in brainstem neurons by using double immunofluorescence methods. In regions such as the midbrain tectum, dorsal isthmus, and motor nuclei, ASP and GABA immunoreactivity was mostly located in different neurons, whereas in other nuclei (torus semicircularis, octavolateralis area, parvocellular reticular formation), many of the ASP-immunonegative neurons displayed colocalization with GABA. These results, together with those of our previous studies of colocalization of glutamate and GABA, suggest that some lamprey neurons may co-release both excitatory and inhibitory neurotransmitters. Further investigation is needed to elucidate the pathways of uptake and release of ASP by ASP-immunoreactive neurons. Our results indicate that ASP is a neurotransmitter in the central nervous system representative of agnathans, the earliest vertebrate group.

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A vesicular glutamate transporter in lampreys: cDNA cloning and early expression in the nervous system

Cited by 10 publications

References 41 publications

Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

Organization of alpha‐transducin immunoreactive system in the brain and retina of larval and young adult Sea Lamprey (Petromyzon marinus), and their relationship with other neural systems

The Glutamatergic Neurons in the Spinal Cord of the Sea Lamprey: An In Situ Hybridization and Immunohistochemical Study

Aspartate‐containing neurons of the brainstem and rostral spinal cord of the sea lamprey Petromyzon marinus: Distribution and comparison with γ‐aminobutyric acid

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