Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems
Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems
Cholecystokinin (CCK) is a neuropeptide that modulates processes such as digestion, satiety, and anxiety. CCK-type peptides have been characterized in jawed vertebrates and invertebrates, but little is known about CCK-type signalling in the most ancient group of vertebrates, the agnathans. Here, we have cloned and sequenced a cDNA encoding a sea lamprey (Petromyzon marinus L.) CCK-type precursor (PmCCK), which contains a CCK-type octapeptide sequence (PmCCK-8) that is highly similar to gnathostome CCKs. Using mRNA in situ hybridization, the distribution of PmCCK-expressing neurons was mapped in the CNS of P. marinus. This revealed PmCCK-expressing neurons in the hypothalamus, posterior tubercle, prethalamus, nucleus of the medial longitudinal fasciculus, midbrain tegmentum, isthmus, rhombencephalic reticular formation, and the putative nucleus of the solitary tract. Some PmCCK-expressing neuronal populations were only observed in adults, revealing important differences with larvae. We generated an antiserum to PmCCK-8 to enable immunohistochemical analysis of CCK expression, which revealed that GABA or glutamate, but not serotonin, tyrosine hydroxylase or neuropeptide Y, is co-expressed in some PmCCK-8-immunoreactive (ir) neurons. Importantly, this is the first demonstration of co-localization of GABA and CCK in neurons of a non-mammalian vertebrate. We also characterized extensive cholecystokinergic fibre systems of the CNS, including innervation of habenular subnuclei. A conspicuous PmCCK-8-ir tract ascending in the lateral rhombencephalon selectively innervates a glutamatergic population in the dorsal isthmic grey. Interestingly, this tract is reminiscent of the secondary gustatory/visceral tract of teleosts. In conclusion, this study provides important new information on the evolution of the cholecystokinergic system in vertebrates.
Brain, Cholecystokinin, GABA, Glutamate, Lamprey, Spinal cord
249-284
Sobrido-Cameán, D.
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Yáñez-Guerra, L. A.
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Robledo, D.
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López-Varela, E.
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Rodicio, M. C.
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Elphick, M. R.
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Anadón, R.
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Barreiro-Iglesias, Antón
f0aec648-e32f-4d53-82fd-4cd2de087525
1 January 2020
Sobrido-Cameán, D.
d7af31f2-90e7-456a-bbb1-e4ecb6e88295
Yáñez-Guerra, L. A.
cbca947b-bbf0-4b91-96b0-4a126e3b94b6
Robledo, D.
b0729dd6-bcf8-4748-b8cd-92f44a34dbca
López-Varela, E.
f4fc2ac6-72b9-4c02-a3e6-6cef7a89e350
Rodicio, M. C.
82e8ca7c-dbb3-43b8-a53c-78441814ca33
Elphick, M. R.
b4c8b4f9-bb5c-4a0a-bc9d-e941857d4800
Anadón, R.
8772c611-9ecc-4b3b-a82f-2db1518caeab
Barreiro-Iglesias, Antón
f0aec648-e32f-4d53-82fd-4cd2de087525
Sobrido-Cameán, D., Yáñez-Guerra, L. A., Robledo, D., López-Varela, E., Rodicio, M. C., Elphick, M. R., Anadón, R. and Barreiro-Iglesias, Antón
(2020)
Cholecystokinin in the central nervous system of the sea lamprey Petromyzon marinus: precursor identification and neuroanatomical relationships with other neuronal signalling systems.
Brain Structure and Function, 225 (1), .
(doi:10.1007/s00429-019-01999-2).
Abstract
Cholecystokinin (CCK) is a neuropeptide that modulates processes such as digestion, satiety, and anxiety. CCK-type peptides have been characterized in jawed vertebrates and invertebrates, but little is known about CCK-type signalling in the most ancient group of vertebrates, the agnathans. Here, we have cloned and sequenced a cDNA encoding a sea lamprey (Petromyzon marinus L.) CCK-type precursor (PmCCK), which contains a CCK-type octapeptide sequence (PmCCK-8) that is highly similar to gnathostome CCKs. Using mRNA in situ hybridization, the distribution of PmCCK-expressing neurons was mapped in the CNS of P. marinus. This revealed PmCCK-expressing neurons in the hypothalamus, posterior tubercle, prethalamus, nucleus of the medial longitudinal fasciculus, midbrain tegmentum, isthmus, rhombencephalic reticular formation, and the putative nucleus of the solitary tract. Some PmCCK-expressing neuronal populations were only observed in adults, revealing important differences with larvae. We generated an antiserum to PmCCK-8 to enable immunohistochemical analysis of CCK expression, which revealed that GABA or glutamate, but not serotonin, tyrosine hydroxylase or neuropeptide Y, is co-expressed in some PmCCK-8-immunoreactive (ir) neurons. Importantly, this is the first demonstration of co-localization of GABA and CCK in neurons of a non-mammalian vertebrate. We also characterized extensive cholecystokinergic fibre systems of the CNS, including innervation of habenular subnuclei. A conspicuous PmCCK-8-ir tract ascending in the lateral rhombencephalon selectively innervates a glutamatergic population in the dorsal isthmic grey. Interestingly, this tract is reminiscent of the secondary gustatory/visceral tract of teleosts. In conclusion, this study provides important new information on the evolution of the cholecystokinergic system in vertebrates.
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Published date: 1 January 2020
Additional Information:
Funding Information:
Grant sponsors: Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund 2007–2013 (Grant number: BFU-2017-87079-P). L.A.Y.G was supported by a PhD studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612) and Queen Mary University of London. D.R. is supported by Institute Strategic Funding Grants to The Roslin Institute (BBS/E/D/20002172, BBS/E/D/30002275 and BBS/E/D/10002070). The authors thank the staff of Ximonde Biological Station for providing the lampreys used in this study, and the Microscopy Service (University of Santiago de Compostela) and Dr. Mercedes Rivas Cascallar for confocal microscope facilities and help.
Funding Information:
Grant sponsors: Spanish Ministry of Economy and Competitiveness and the European Regional Development Fund 2007?2013 (Grant number: BFU-2017-87079-P). L.A.Y.G was supported by a PhD studentship awarded by the Mexican Council of Science and Technology (CONACyT studentship no. 418612) and Queen Mary University of London. D.R. is supported by Institute Strategic Funding Grants to The Roslin Institute (BBS/E/D/20002172, BBS/E/D/30002275 and BBS/E/D/10002070). The authors thank the staff of Ximonde Biological Station for providing the lampreys used in this study, and the Microscopy Service (University of Santiago de Compostela) and Dr. Mercedes Rivas Cascallar for confocal microscope facilities and help.
Publisher Copyright:
© 2019, Springer-Verlag GmbH Germany, part of Springer Nature.
Keywords:
Brain, Cholecystokinin, GABA, Glutamate, Lamprey, Spinal cord
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Local EPrints ID: 483963
URI: http://eprints.soton.ac.uk/id/eprint/483963
ISSN: 1863-2653
PURE UUID: 5bbdaa36-4045-4fbf-bcbd-74b45786ebe8
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Date deposited: 07 Nov 2023 18:55
Last modified: 18 Mar 2024 04:15
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Contributors
Author:
D. Sobrido-Cameán
Author:
L. A. Yáñez-Guerra
Author:
D. Robledo
Author:
E. López-Varela
Author:
M. C. Rodicio
Author:
M. R. Elphick
Author:
R. Anadón
Author:
Antón Barreiro-Iglesias
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