TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus

TRPV1 is an ion channel activated by heat and pungent agents including capsaicin, and has been extensively studied in nociception of sensory neurons. However, the location and function of TRPV1 in the hippocampus is debated. We found that TRPV1 is expressed in oriens-lacunosum-moleculare (OLM) inter...

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Autores principales: Hurtado-Zavala, Joaquin I., Ramachandran, Binu, Ahmed, Saheeb, Halder, Rashi, Bolleyer, Christiane, Awasthi, Ankit, Stahlberg, Markus A., Wagener, Robin J., Anderson, Kristin, Drenan, Ryan M., Lester, Henry A., Miwa, Julie M., Staiger, Jochen F., Fischer, Andre, Dean, Camin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2017
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Article
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5524938/
https://www.ncbi.nlm.nih.gov/pubmed/28722015
http://dx.doi.org/10.1038/ncomms15878
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author Hurtado-Zavala, Joaquin I.
Ramachandran, Binu
Ahmed, Saheeb
Halder, Rashi
Bolleyer, Christiane
Awasthi, Ankit
Stahlberg, Markus A.
Wagener, Robin J.
Anderson, Kristin
Drenan, Ryan M.
Lester, Henry A.
Miwa, Julie M.
Staiger, Jochen F.
Fischer, Andre
Dean, Camin
author_facet Hurtado-Zavala, Joaquin I.
Ramachandran, Binu
Ahmed, Saheeb
Halder, Rashi
Bolleyer, Christiane
Awasthi, Ankit
Stahlberg, Markus A.
Wagener, Robin J.
Anderson, Kristin
Drenan, Ryan M.
Lester, Henry A.
Miwa, Julie M.
Staiger, Jochen F.
Fischer, Andre
Dean, Camin
author_sort Hurtado-Zavala, Joaquin I.
collection PubMed
description TRPV1 is an ion channel activated by heat and pungent agents including capsaicin, and has been extensively studied in nociception of sensory neurons. However, the location and function of TRPV1 in the hippocampus is debated. We found that TRPV1 is expressed in oriens-lacunosum-moleculare (OLM) interneurons in the hippocampus, and promotes excitatory innervation. TRPV1 knockout mice have reduced glutamatergic innervation of OLM neurons. When activated by capsaicin, TRPV1 recruits more glutamatergic, but not GABAergic, terminals to OLM neurons in vitro. When TRPV1 is blocked, glutamatergic input to OLM neurons is dramatically reduced. Heterologous expression of TRPV1 also increases excitatory innervation. Moreover, TRPV1 knockouts have reduced Schaffer collateral LTP, which is rescued by activating OLM neurons with nicotine—via α2β2-containing nicotinic receptors—to bypass innervation defects. Our results reveal a synaptogenic function of TRPV1 in a specific interneuron population in the hippocampus, where it is important for gating hippocampal plasticity.
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spelling pubmed-55249382017-07-28 TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus Hurtado-Zavala, Joaquin I. Ramachandran, Binu Ahmed, Saheeb Halder, Rashi Bolleyer, Christiane Awasthi, Ankit Stahlberg, Markus A. Wagener, Robin J. Anderson, Kristin Drenan, Ryan M. Lester, Henry A. Miwa, Julie M. Staiger, Jochen F. Fischer, Andre Dean, Camin Nat Commun Article TRPV1 is an ion channel activated by heat and pungent agents including capsaicin, and has been extensively studied in nociception of sensory neurons. However, the location and function of TRPV1 in the hippocampus is debated. We found that TRPV1 is expressed in oriens-lacunosum-moleculare (OLM) interneurons in the hippocampus, and promotes excitatory innervation. TRPV1 knockout mice have reduced glutamatergic innervation of OLM neurons. When activated by capsaicin, TRPV1 recruits more glutamatergic, but not GABAergic, terminals to OLM neurons in vitro. When TRPV1 is blocked, glutamatergic input to OLM neurons is dramatically reduced. Heterologous expression of TRPV1 also increases excitatory innervation. Moreover, TRPV1 knockouts have reduced Schaffer collateral LTP, which is rescued by activating OLM neurons with nicotine—via α2β2-containing nicotinic receptors—to bypass innervation defects. Our results reveal a synaptogenic function of TRPV1 in a specific interneuron population in the hippocampus, where it is important for gating hippocampal plasticity. Nature Publishing Group 2017-07-19 /pmc/articles/PMC5524938/ /pubmed/28722015 http://dx.doi.org/10.1038/ncomms15878 Text en Copyright © 2017, The Author(s) http://creativecommons.org/licenses/by/4.0/ Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Hurtado-Zavala, Joaquin I.
Ramachandran, Binu
Ahmed, Saheeb
Halder, Rashi
Bolleyer, Christiane
Awasthi, Ankit
Stahlberg, Markus A.
Wagener, Robin J.
Anderson, Kristin
Drenan, Ryan M.
Lester, Henry A.
Miwa, Julie M.
Staiger, Jochen F.
Fischer, Andre
Dean, Camin
TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title_full TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title_fullStr TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title_full_unstemmed TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title_short TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus
title_sort trpv1 regulates excitatory innervation of olm neurons in the hippocampus
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5524938/
https://www.ncbi.nlm.nih.gov/pubmed/28722015
http://dx.doi.org/10.1038/ncomms15878
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