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Featured ArticleResearch Articles, Cellular/Molecular

Deficiency of Inositol Monophosphatase Activity Decreases Phosphoinositide Lipids and Enhances TRPV1 Function In Vivo

Rebeca Caires, Briar Bell, Jungsoo Lee, Luis O. Romero, Valeria Vásquez and Julio F. Cordero-Morales
Journal of Neuroscience 20 January 2021, 41 (3) 408-423; DOI: https://doi.org/10.1523/JNEUROSCI.0803-20.2020
Rebeca Caires
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Briar Bell
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
2Integrated Biomedical Sciences Graduate Program, College of Graduate Health Sciences, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Jungsoo Lee
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Luis O. Romero
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
2Integrated Biomedical Sciences Graduate Program, College of Graduate Health Sciences, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Valeria Vásquez
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Julio F. Cordero-Morales
1Department of Physiology, College of Medicine, University of Tennessee Health Science Center, Memphis, Tennessee 38163
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Abstract

Membrane remodeling by inflammatory mediators influences the function of sensory ion channels. The capsaicin- and heat-activated transient receptor potential vanilloid 1 (TRPV1) channel contributes to neurogenic inflammation and pain hypersensitivity, in part because of its potentiation downstream of phospholipase C-coupled receptors that regulate phosphoinositide lipid content. Here, we determined the effect of phosphoinositide lipids on TRPV1 function by combining genetic dissection, diet supplementation, and behavioral, biochemical, and functional analyses in Caenorhabditis elegans. As capsaicin elicits heat and pain sensations in mammals, transgenic TRPV1 worms exhibit an aversive response to capsaicin. TRPV1 worms with low levels of phosphoinositide lipids display an enhanced response to capsaicin, whereas phosphoinositide lipid supplementation reduces TRPV1-mediated responses. A worm carrying a TRPV1 construct lacking the distal C-terminal domain features an enhanced response to capsaicin, independent of the phosphoinositide lipid content. Our results demonstrate that TRPV1 activity is enhanced when the phosphoinositide lipid content is reduced, and the C-terminal domain is key to determining agonist response in vivo.

  • Caenorhabditis elegans
  • in vivo calcium imaging
  • inositol monophosphatase
  • lipid regulation
  • phosphoinositides
  • TRPV1

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 41 (3)
Journal of Neuroscience
Vol. 41, Issue 3
20 Jan 2021
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Deficiency of Inositol Monophosphatase Activity Decreases Phosphoinositide Lipids and Enhances TRPV1 Function In Vivo
Rebeca Caires, Briar Bell, Jungsoo Lee, Luis O. Romero, Valeria Vásquez, Julio F. Cordero-Morales
Journal of Neuroscience 20 January 2021, 41 (3) 408-423; DOI: 10.1523/JNEUROSCI.0803-20.2020

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Deficiency of Inositol Monophosphatase Activity Decreases Phosphoinositide Lipids and Enhances TRPV1 Function In Vivo
Rebeca Caires, Briar Bell, Jungsoo Lee, Luis O. Romero, Valeria Vásquez, Julio F. Cordero-Morales
Journal of Neuroscience 20 January 2021, 41 (3) 408-423; DOI: 10.1523/JNEUROSCI.0803-20.2020
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Keywords

  • Caenorhabditis elegans
  • in vivo calcium imaging
  • inositol monophosphatase
  • lipid regulation
  • phosphoinositides
  • TRPV1

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