Role of TRP Channels in Shaping the Gut Microbiome

Transient receptor potential (TRP) channel family proteins are sensors for pain, which sense a variety of thermal and noxious chemicals. Sensory neurons innervating the gut abundantly express TRPA1 and TRPV1 channels and are in close proximity of gut microbes. Emerging evidence indicates a bi-direct...

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Main Authors: Ravinder Nagpal, Santosh Kumar Mishra, Gagan Deep, Hariom Yadav
Format: Article
Language:English
Published: MDPI AG 2020-09-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/9/9/753
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author Ravinder Nagpal
Santosh Kumar Mishra
Gagan Deep
Hariom Yadav
author_facet Ravinder Nagpal
Santosh Kumar Mishra
Gagan Deep
Hariom Yadav
author_sort Ravinder Nagpal
collection DOAJ
description Transient receptor potential (TRP) channel family proteins are sensors for pain, which sense a variety of thermal and noxious chemicals. Sensory neurons innervating the gut abundantly express TRPA1 and TRPV1 channels and are in close proximity of gut microbes. Emerging evidence indicates a bi-directional gut–brain cross-talk in several entero-neuronal pathologies; however, the direct evidence of TRP channels interacting with gut microbial populations is lacking. Herein, we examine whether and how the knockout (KO) of TRPA1 and TRPV1 channels individually or combined TRPA1/V1 double-knockout (dKO) impacts the gut microbiome in mice. We detect distinct microbiome clusters among the three KO mouse models versus wild-type (WT) mice. All three TRP-KO models have reduced microbial diversity, harbor higher abundance of Bacteroidetes, and a reduced proportion of <i>Firmicutes</i>. Specifically distinct arrays in the KO models are determined mainly by <i>S24-7</i>, <i>Bacteroidaceae</i>, <i>Clostridiales</i>, <i>Prevotellaceae, Helicobacteriaceae, Rikenellaceae,</i> and <i>Ruminococcaceae</i>. A1KO mice have lower <i>Prevotella, Desulfovibrio, Bacteroides</i>, <i>Helicobacter</i> and higher <i>Rikenellaceae</i> and <i>Tenericutes</i>; V1KO mice demonstrate higher <i>Ruminococcaceae, Lachnospiraceae, Ruminococcus, Desulfovibrio</i> and <i>Mucispirillum</i>; and A1V1dKO mice exhibit higher <i>Bacteroidetes, Bacteroides</i> and <i>S24-7</i> and lower <i>Firmicutes, Ruminococcaceae, Oscillospira, Lactobacillus</i> and <i>Sutterella</i> abundance. Furthermore, the abundance of taxa involved in biosynthesis of lipids and primary and secondary bile acids is higher while that of fatty acid biosynthesis-associated taxa is lower in all KO groups. To our knowledge, this is the first study demonstrating distinct gut microbiome signatures in TRPA1, V1 and dKO models and should facilitate prospective studies exploring novel diagnostic/ therapeutic modalities regarding the pathophysiology of TRP channel proteins.
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spelling doaj.art-8363f3259a0a47d7bc0975df9b5d7e142023-11-20T13:52:10ZengMDPI AGPathogens2076-08172020-09-019975310.3390/pathogens9090753Role of TRP Channels in Shaping the Gut MicrobiomeRavinder Nagpal0Santosh Kumar Mishra1Gagan Deep2Hariom Yadav3Department of Internal Medicine-Molecular Medicine, Wake Forest School of Medicine, Winston-Salem, NC 27101, USADepartment of Molecular Biomedical Sciences, NC State Veterinary Medicine, Raleigh, NC 27606, USADepartment of Cancer Biology, Wake Forest School of Medicine, Winston-Salem, NC 27157, USADepartment of Internal Medicine-Molecular Medicine, Wake Forest School of Medicine, Winston-Salem, NC 27101, USATransient receptor potential (TRP) channel family proteins are sensors for pain, which sense a variety of thermal and noxious chemicals. Sensory neurons innervating the gut abundantly express TRPA1 and TRPV1 channels and are in close proximity of gut microbes. Emerging evidence indicates a bi-directional gut–brain cross-talk in several entero-neuronal pathologies; however, the direct evidence of TRP channels interacting with gut microbial populations is lacking. Herein, we examine whether and how the knockout (KO) of TRPA1 and TRPV1 channels individually or combined TRPA1/V1 double-knockout (dKO) impacts the gut microbiome in mice. We detect distinct microbiome clusters among the three KO mouse models versus wild-type (WT) mice. All three TRP-KO models have reduced microbial diversity, harbor higher abundance of Bacteroidetes, and a reduced proportion of <i>Firmicutes</i>. Specifically distinct arrays in the KO models are determined mainly by <i>S24-7</i>, <i>Bacteroidaceae</i>, <i>Clostridiales</i>, <i>Prevotellaceae, Helicobacteriaceae, Rikenellaceae,</i> and <i>Ruminococcaceae</i>. A1KO mice have lower <i>Prevotella, Desulfovibrio, Bacteroides</i>, <i>Helicobacter</i> and higher <i>Rikenellaceae</i> and <i>Tenericutes</i>; V1KO mice demonstrate higher <i>Ruminococcaceae, Lachnospiraceae, Ruminococcus, Desulfovibrio</i> and <i>Mucispirillum</i>; and A1V1dKO mice exhibit higher <i>Bacteroidetes, Bacteroides</i> and <i>S24-7</i> and lower <i>Firmicutes, Ruminococcaceae, Oscillospira, Lactobacillus</i> and <i>Sutterella</i> abundance. Furthermore, the abundance of taxa involved in biosynthesis of lipids and primary and secondary bile acids is higher while that of fatty acid biosynthesis-associated taxa is lower in all KO groups. To our knowledge, this is the first study demonstrating distinct gut microbiome signatures in TRPA1, V1 and dKO models and should facilitate prospective studies exploring novel diagnostic/ therapeutic modalities regarding the pathophysiology of TRP channel proteins.https://www.mdpi.com/2076-0817/9/9/753intestinal microfloramicrobiotapaintransient receptor potentialTRP channelsTRPA1
spellingShingle Ravinder Nagpal
Santosh Kumar Mishra
Gagan Deep
Hariom Yadav
Role of TRP Channels in Shaping the Gut Microbiome
Pathogens
intestinal microflora
microbiota
pain
transient receptor potential
TRP channels
TRPA1
title Role of TRP Channels in Shaping the Gut Microbiome
title_full Role of TRP Channels in Shaping the Gut Microbiome
title_fullStr Role of TRP Channels in Shaping the Gut Microbiome
title_full_unstemmed Role of TRP Channels in Shaping the Gut Microbiome
title_short Role of TRP Channels in Shaping the Gut Microbiome
title_sort role of trp channels in shaping the gut microbiome
topic intestinal microflora
microbiota
pain
transient receptor potential
TRP channels
TRPA1
url https://www.mdpi.com/2076-0817/9/9/753
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