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 anci...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-09-01
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| Series: | Frontiers in Neuroanatomy |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fnana.2019.00083/full |
| _version_ | 1819066706827411456 |
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| author | Daniel Sobrido-Cameán Luis Alfonso Yáñez-Guerra Francesco Lamanna Candela Conde-Fernández Henrik Kaessmann Maurice R. Elphick Ramón Anadón María Celina Rodicio Antón Barreiro-Iglesias |
| author_facet | Daniel Sobrido-Cameán Luis Alfonso Yáñez-Guerra Francesco Lamanna Candela Conde-Fernández Henrik Kaessmann Maurice R. Elphick Ramón Anadón María Celina Rodicio Antón Barreiro-Iglesias |
| author_sort | Daniel Sobrido-Cameán |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-12-21T16:06:38Z |
| format | Article |
| id | doaj.art-b9030a5d44f5430cacb998508e798080 |
| institution | Directory Open Access Journal |
| issn | 1662-5129 |
| language | English |
| last_indexed | 2024-12-21T16:06:38Z |
| publishDate | 2019-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroanatomy |
| spelling | doaj.art-b9030a5d44f5430cacb998508e7980802022-12-21T18:57:53ZengFrontiers Media S.A.Frontiers in Neuroanatomy1662-51292019-09-011310.3389/fnana.2019.00083488011Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinusDaniel Sobrido-Cameán0Luis Alfonso Yáñez-Guerra1Francesco Lamanna2Candela Conde-Fernández3Henrik Kaessmann4Maurice R. Elphick5Ramón Anadón6María Celina Rodicio7Antón Barreiro-Iglesias8Department of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, SpainSchool of Biological and Chemical Sciences, Queen Mary University of London, London, United KingdomCenter for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, Heidelberg, GermanyDepartment of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, SpainCenter for Molecular Biology of Heidelberg University (ZMBH), DKFZ-ZMBH Alliance, Heidelberg, GermanySchool of Biological and Chemical Sciences, Queen Mary University of London, London, United KingdomDepartment of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, SpainDepartment of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, SpainDepartment of Functional Biology, CIBUS, Faculty of Biology, Universidade de Santiago de Compostela, Santiago de Compostela, SpainGalanin 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.https://www.frontiersin.org/article/10.3389/fnana.2019.00083/fulllampreygalanintelencephalonhypothalamusstriatumneuropeptides |
| spellingShingle | Daniel Sobrido-Cameán Luis Alfonso Yáñez-Guerra Francesco Lamanna Candela Conde-Fernández Henrik Kaessmann Maurice R. Elphick Ramón Anadón María Celina Rodicio Antón Barreiro-Iglesias Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus Frontiers in Neuroanatomy lamprey galanin telencephalon hypothalamus striatum neuropeptides |
| title | Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus |
| title_full | Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus |
| title_fullStr | Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus |
| title_full_unstemmed | Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus |
| title_short | Galanin in an Agnathan: Precursor Identification and Localisation of Expression in the Brain of the Sea Lamprey Petromyzon marinus |
| title_sort | galanin in an agnathan precursor identification and localisation of expression in the brain of the sea lamprey petromyzon marinus |
| topic | lamprey galanin telencephalon hypothalamus striatum neuropeptides |
| url | https://www.frontiersin.org/article/10.3389/fnana.2019.00083/full |
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