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The transient receptor potential vanilloid-1 is localized at excitatory synapses in the mouse dentate gyrus

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Abstract

The transient receptor potential vanilloid type 1 (TRPV1) is a non-selective cation channel that plays an important role in pain perception and modulates neurotransmitter release and synaptic plasticity in the brain. TRPV1 function must lay on its anatomical distribution in the peripheral and central nervous system regions involved in the physiological roles of the channel. However, the anatomical localization of TRPV1 is well established in the periphery, but in the brain it is a matter of debate. While some studies support the presence of TRPV1 in several brain regions, recent evidences suggest a restricted distribution of the channel in the central nervous system. To investigate to what extent central TRPV1 function stands on a precise brain distribution of the channel, we examined the mouse hippocampal dentate molecular layer (ML) where TRPV1 mediates long-term synaptic plasticity. Using pre-embedding immunocytochemistry for high resolution electron microscopy, we show that TRPV1 immunoparticles are highly concentrated in postsynaptic dendritic spines to asymmetric perforant path synapses in the outer 2/3 of the ML. However, TRPV1 is poorly expressed at the excitatory hilar mossy cell synapses in the inner 1/3 of this layer. Importantly, the TRPV1 pattern distribution disappeared in the ML of TRPV1-knockout mice. Taken together, these findings support the notion of the presence of TRPV1 in a brain region where the channel has been shown to have a functional role, such as the perforant path synapses in the hippocampal dentate ML.

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Abbreviations

2-AG:

2-Arachidonoylglycerol

ABC:

Avidin–biotin peroxidase complex

BSA:

Bovine serum albumin

DGL-α:

Diacylglycerol lipase-α

LTD:

Long-term depression

mGluR:

Metabotropic glutamate receptor

ML:

Molecular layer

NAPE-PLD:

N-Acyl phosphatidylethanolamine phospholipase D

RT:

Room temperature

PB:

Phosphate buffer

PBS:

Phosphate buffered saline

TBS:

Tris–HCl buffered saline

TRPV1:

Transient receptor potential vanilloid type 1

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Acknowledgments

Funding for P. Grandes’ laboratory is provided by Ministerio de Economía y Competitividad (BFU2012-33334); The Basque Country Government Grant IT764-13, and by Red de Trastornos Adictivos, RETICS, Instituto de Salud Carlos III, Grant Number: RD07/0001/2001, RD12/0028/0004. L. Reguero was supported by a Postdoctoral Specialization Contract from the University of the Basque Country UPV/EHU. Supported by grants to EFE by: Plan Andaluz de Investigación (BIO127, Junta de Andalucía); Plan Nacional sobre drogas (ref. 2009I039) and Spanish Ministerio de Sanidad (RETICS, Red de Trastornos Adictivos, RD06/001/002; Instituto Carlos III, co-financing with FEDER, European Fund for Regional Development). The authors thank Mara Guerra and Silvia Castellano  (University of Seville) for animal care and genotyping.

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Authors and Affiliations

  1. Department of Neurosciences, Faculty of Medicine and Dentistry, University of the Basque Country UPV/EHU, 48940, Leioa, Spain

    Nagore Puente, Leire Reguero, Izaskun Elezgarai, Miren-Josune Canduela, Juan Mendizabal-Zubiaga, Almudena Ramos-Uriarte & Pedro Grandes

  2. Department of Medical Physiology and Biophysics, Faculty of Medicine, Universidad de Sevilla, Seville, Spain

    Emilio Fernández-Espejo

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  1. Nagore Puente
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  2. Leire Reguero
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  8. Pedro Grandes
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Correspondence to Pedro Grandes.

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Puente, N., Reguero, L., Elezgarai, I. et al. The transient receptor potential vanilloid-1 is localized at excitatory synapses in the mouse dentate gyrus. Brain Struct Funct 220, 1187–1194 (2015). https://doi.org/10.1007/s00429-014-0711-2

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  • DOI: https://doi.org/10.1007/s00429-014-0711-2

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