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Galanin in an Agnathan: precursor identification and localisation of expression in the brain of the Sea Lamprey Petromyzon marinus

Galanin in an Agnathan: precursor identification and localisation of expression in the brain of the Sea Lamprey Petromyzon marinus
Galanin in an Agnathan: precursor identification and localisation of expression in the brain of the Sea Lamprey Petromyzon marinus

Galanin is a neuropeptide that is widely expressed in the mammalian brain, where it regulates many physiological processes, including feeding and nociception. Galanin has been characterized extensively in jawed vertebrates (gnathostomes), but little is known about the galanin system in the most ancient extant vertebrate class, the jawless vertebrates or agnathans. Here, we identified and cloned a cDNA encoding the sea lamprey (Petromyzon marinus) galanin precursor (PmGalP). Sequence analysis revealed that PmGalP gives rise to two neuropeptides that are similar to gnathostome galanins and galanin message-associated peptides. Using mRNA in situ hybridization, the distribution of PmGalP-expressing neurons was mapped in the brain of larval and adult sea lampreys. This revealed PmGalP-expressing neurons in the septum, preoptic region, striatum, hypothalamus, prethalamus, and displaced cells in lateral areas of the telencephalon and diencephalon. In adults, the laterally migrated PmGalP-expressing neurons are observed in an area that extends from the ventral pallium to the lateral hypothalamus and prethalamus. The striatal and laterally migrated PmGalP-expressing cells of the telencephalon were not observed in larvae. Comparison with studies on jawed vertebrates reveals that the presence of septal and hypothalamic galanin-expressing neuronal populations is highly conserved in vertebrates. However, compared to mammals, there is a more restricted pattern of expression of the galanin transcript in the brain of lampreys. This work provides important new information on the early evolution of the galanin system in vertebrates and provides a genetic and neuroanatomical basis for functional analyses of the galanin system in lampreys.

galanin, hypothalamus, lamprey, neuropeptides, striatum, telencephalon
Sobrido-Cameán, Daniel
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Yáñez-Guerra, Luis Alfonso
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Lamanna, Francesco
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Conde-Fernández, Candela
c1f5d7af-4e44-45bd-a661-9b430c944b8e
Kaessmann, Henrik
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Elphick, Maurice R.
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Anadón, Ramón
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Rodicio, María Celina
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Barreiro-Iglesias, Antón
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Sobrido-Cameán, Daniel
d7af31f2-90e7-456a-bbb1-e4ecb6e88295
Yáñez-Guerra, Luis Alfonso
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Lamanna, Francesco
ac0062db-7184-4143-93bd-44ae36b6f817
Conde-Fernández, Candela
c1f5d7af-4e44-45bd-a661-9b430c944b8e
Kaessmann, Henrik
3f3c8e38-0612-4ce7-8821-ffa763ad1391
Elphick, Maurice R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Anadón, Ramón
8772c611-9ecc-4b3b-a82f-2db1518caeab
Rodicio, María Celina
82e8ca7c-dbb3-43b8-a53c-78441814ca33
Barreiro-Iglesias, Antón
f0aec648-e32f-4d53-82fd-4cd2de087525

Sobrido-Cameán, Daniel, Yáñez-Guerra, Luis Alfonso, Lamanna, Francesco, Conde-Fernández, Candela, Kaessmann, Henrik, Elphick, Maurice R., Anadón, Ramón, Rodicio, María Celina and Barreiro-Iglesias, Antón (2019) Galanin in an Agnathan: precursor identification and localisation of expression in the brain of the Sea Lamprey Petromyzon marinus. Frontiers in Neuroanatomy, 13, [83]. (doi:10.3389/fnana.2019.00083).

Record type: Article

Abstract

Galanin is a neuropeptide that is widely expressed in the mammalian brain, where it regulates many physiological processes, including feeding and nociception. Galanin has been characterized extensively in jawed vertebrates (gnathostomes), but little is known about the galanin system in the most ancient extant vertebrate class, the jawless vertebrates or agnathans. Here, we identified and cloned a cDNA encoding the sea lamprey (Petromyzon marinus) galanin precursor (PmGalP). Sequence analysis revealed that PmGalP gives rise to two neuropeptides that are similar to gnathostome galanins and galanin message-associated peptides. Using mRNA in situ hybridization, the distribution of PmGalP-expressing neurons was mapped in the brain of larval and adult sea lampreys. This revealed PmGalP-expressing neurons in the septum, preoptic region, striatum, hypothalamus, prethalamus, and displaced cells in lateral areas of the telencephalon and diencephalon. In adults, the laterally migrated PmGalP-expressing neurons are observed in an area that extends from the ventral pallium to the lateral hypothalamus and prethalamus. The striatal and laterally migrated PmGalP-expressing cells of the telencephalon were not observed in larvae. Comparison with studies on jawed vertebrates reveals that the presence of septal and hypothalamic galanin-expressing neuronal populations is highly conserved in vertebrates. However, compared to mammals, there is a more restricted pattern of expression of the galanin transcript in the brain of lampreys. This work provides important new information on the early evolution of the galanin system in vertebrates and provides a genetic and neuroanatomical basis for functional analyses of the galanin system in lampreys.

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More information

Published date: 13 September 2019
Additional Information: Funding Information: The authors thank the staff of Ximonde Biological Station for providing the lampreys used in this study. Funding. Grant sponsors: Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund 2007–2013 (Grant number: BFU-2017-87079-P). LY-G was supported by a Ph.D. studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612), and Queen Mary University of London. Publisher Copyright: © Copyright © 2019 Sobrido-Cameán, Yáñez-Guerra, Lamanna, Conde-Fernández, Kaessmann, Elphick, Anadón, Rodicio and Barreiro-Iglesias.
Keywords: galanin, hypothalamus, lamprey, neuropeptides, striatum, telencephalon

Identifiers

Local EPrints ID: 483962
URI: http://eprints.soton.ac.uk/id/eprint/483962
PURE UUID: b3ba7db7-a750-4cc7-89fa-877c2423dea2
ORCID for Luis Alfonso Yáñez-Guerra: ORCID iD orcid.org/0000-0002-2523-1310

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Date deposited: 07 Nov 2023 18:54
Last modified: 18 Mar 2024 04:15

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Contributors

Author: Daniel Sobrido-Cameán
Author: Luis Alfonso Yáñez-Guerra ORCID iD
Author: Francesco Lamanna
Author: Candela Conde-Fernández
Author: Henrik Kaessmann
Author: Maurice R. Elphick
Author: Ramón Anadón
Author: María Celina Rodicio
Author: Antón Barreiro-Iglesias

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