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A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates

Cerebrospinal fluid contacting neurons (CSF-cNs) are a specific type of neurons located around the ventricles in the brain and the central canal in the spinal cord and have been demonstrated to be intrinsic sensory neurons in the central nervous system. One of the important channels responsible for...

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Autores principales: Liu, Xiaohe, Rich, Karen, Nasseri, Sohail M., Li, Guifa, Hjæresen, Simone, Finsen, Bente, Scherberger, Hansjörg, Svenningsen, Åsa, Zhang, Mengliang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10488076/
https://www.ncbi.nlm.nih.gov/pubmed/37686387
http://dx.doi.org/10.3390/ijms241713582
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author Liu, Xiaohe
Rich, Karen
Nasseri, Sohail M.
Li, Guifa
Hjæresen, Simone
Finsen, Bente
Scherberger, Hansjörg
Svenningsen, Åsa
Zhang, Mengliang
author_facet Liu, Xiaohe
Rich, Karen
Nasseri, Sohail M.
Li, Guifa
Hjæresen, Simone
Finsen, Bente
Scherberger, Hansjörg
Svenningsen, Åsa
Zhang, Mengliang
author_sort Liu, Xiaohe
collection PubMed
description Cerebrospinal fluid contacting neurons (CSF-cNs) are a specific type of neurons located around the ventricles in the brain and the central canal in the spinal cord and have been demonstrated to be intrinsic sensory neurons in the central nervous system. One of the important channels responsible for the sensory function is the polycystic kidney disease 2-like 1 (PKD2L1) channel. Most of the studies concerning the distribution and function of the PKD2L1-expressing CSF-cNs in the spinal cord have previously been performed in non-mammalian vertebrates. In the present study immunohistochemistry was performed to determine the distribution of PKD2L1-immunoreactive (IR) CSF-cNs in the spinal cords of four mammalian species: mouse, rat, cat, and macaque monkey. Here, we found that PKD2L1-expressing CSF-cNs were present at all levels of the spinal cord in these animal species. Although the distribution pattern was similar across these species, differences existed. Mice and rats presented a clear PKD2L1-IR cell body labeling, whereas in cats and macaques the PKD2L1-IR cell bodies were more weakly labeled. Ectopic PKD2L1-IR neurons away from the ependymal layer were observed in all the animal species although the abundance and the detailed locations varied. The apical dendritic protrusions with ciliated fibers were clearly seen in the lumen of the central canal in all the animal species, but the sizes of protrusion bulbs were different among the species. PKD2L1-IR cell bodies/dendrites were co-expressed with doublecortin, MAP2 (microtubule-associated protein 2), and aromatic L-amino acid decarboxylase, but not with NeuN (neuronal nuclear protein), indicating their immature properties and ability to synthesize monoamine transmitters. In addition, in situ hybridization performed in rats revealed PKD2L1 mRNA expression in the cells around the central canal. Our results indicate that the intrinsic sensory neurons are conserved across non-mammalian and mammalian vertebrates. The similar morphology of the dendritic bulbs with ciliated fibers (probably representing stereocilia and kinocilia) protruding into the central canal across different animal species supports the notion that PKD2L1 is a chemo- and mechanical sensory channel that responds to mechanical stimulations and maintains homeostasis of the spinal cord. However, the differences of PKD2L1 distribution and expression between the species suggest that PKD2L1-expressing neurons may receive and process sensory signals differently in different animal species.
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spelling pubmed-104880762023-09-09 A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates Liu, Xiaohe Rich, Karen Nasseri, Sohail M. Li, Guifa Hjæresen, Simone Finsen, Bente Scherberger, Hansjörg Svenningsen, Åsa Zhang, Mengliang Int J Mol Sci Article Cerebrospinal fluid contacting neurons (CSF-cNs) are a specific type of neurons located around the ventricles in the brain and the central canal in the spinal cord and have been demonstrated to be intrinsic sensory neurons in the central nervous system. One of the important channels responsible for the sensory function is the polycystic kidney disease 2-like 1 (PKD2L1) channel. Most of the studies concerning the distribution and function of the PKD2L1-expressing CSF-cNs in the spinal cord have previously been performed in non-mammalian vertebrates. In the present study immunohistochemistry was performed to determine the distribution of PKD2L1-immunoreactive (IR) CSF-cNs in the spinal cords of four mammalian species: mouse, rat, cat, and macaque monkey. Here, we found that PKD2L1-expressing CSF-cNs were present at all levels of the spinal cord in these animal species. Although the distribution pattern was similar across these species, differences existed. Mice and rats presented a clear PKD2L1-IR cell body labeling, whereas in cats and macaques the PKD2L1-IR cell bodies were more weakly labeled. Ectopic PKD2L1-IR neurons away from the ependymal layer were observed in all the animal species although the abundance and the detailed locations varied. The apical dendritic protrusions with ciliated fibers were clearly seen in the lumen of the central canal in all the animal species, but the sizes of protrusion bulbs were different among the species. PKD2L1-IR cell bodies/dendrites were co-expressed with doublecortin, MAP2 (microtubule-associated protein 2), and aromatic L-amino acid decarboxylase, but not with NeuN (neuronal nuclear protein), indicating their immature properties and ability to synthesize monoamine transmitters. In addition, in situ hybridization performed in rats revealed PKD2L1 mRNA expression in the cells around the central canal. Our results indicate that the intrinsic sensory neurons are conserved across non-mammalian and mammalian vertebrates. The similar morphology of the dendritic bulbs with ciliated fibers (probably representing stereocilia and kinocilia) protruding into the central canal across different animal species supports the notion that PKD2L1 is a chemo- and mechanical sensory channel that responds to mechanical stimulations and maintains homeostasis of the spinal cord. However, the differences of PKD2L1 distribution and expression between the species suggest that PKD2L1-expressing neurons may receive and process sensory signals differently in different animal species. MDPI 2023-09-01 /pmc/articles/PMC10488076/ /pubmed/37686387 http://dx.doi.org/10.3390/ijms241713582 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Liu, Xiaohe
Rich, Karen
Nasseri, Sohail M.
Li, Guifa
Hjæresen, Simone
Finsen, Bente
Scherberger, Hansjörg
Svenningsen, Åsa
Zhang, Mengliang
A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title_full A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title_fullStr A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title_full_unstemmed A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title_short A Comparison of PKD2L1-Expressing Cerebrospinal Fluid Contacting Neurons in Spinal Cords of Rodents, Carnivores, and Primates
title_sort comparison of pkd2l1-expressing cerebrospinal fluid contacting neurons in spinal cords of rodents, carnivores, and primates
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10488076/
https://www.ncbi.nlm.nih.gov/pubmed/37686387
http://dx.doi.org/10.3390/ijms241713582
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