Stereotyped transcriptomic transformation of somatosensory neurons in response to injury

In mice, spared nerve injury replicates symptoms of human neuropathic pain and induces upregulation of many genes in somatosensory neurons. Here we used single cell transcriptomics to probe the effects of partial infraorbital transection of the trigeminal nerve at the cellular level. Uninjured neuro...

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Main Authors: Minh Q Nguyen, Claire E Le Pichon, Nicholas Ryba
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2019-10-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/49679
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author Minh Q Nguyen
Claire E Le Pichon
Nicholas Ryba
author_facet Minh Q Nguyen
Claire E Le Pichon
Nicholas Ryba
author_sort Minh Q Nguyen
collection DOAJ
description In mice, spared nerve injury replicates symptoms of human neuropathic pain and induces upregulation of many genes in somatosensory neurons. Here we used single cell transcriptomics to probe the effects of partial infraorbital transection of the trigeminal nerve at the cellular level. Uninjured neurons were unaffected by transection of major nerve branches, segregating into many different classes. In marked contrast, axotomy rapidly transformed damaged neurons into just two new and closely-related classes where almost all original identity was lost. Remarkably, sensory neurons also adopted this transcriptomic state following various minor peripheral injuries. By genetically marking injured neurons, we showed that the injury-induced transformation was reversible, with damaged cells slowly reacquiring normal gene expression profiles. Thus, our data expose transcriptomic plasticity, previously thought of as a driver of chronic pain, as a programed response to many types of injury and a potential mechanism for regulating sensation during wound healing.
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spelling doaj.art-aad1cb7d2fd04798ae250bb390cd5b742022-12-22T02:03:16ZengeLife Sciences Publications LtdeLife2050-084X2019-10-01810.7554/eLife.49679Stereotyped transcriptomic transformation of somatosensory neurons in response to injuryMinh Q Nguyen0Claire E Le Pichon1https://orcid.org/0000-0002-9274-3615Nicholas Ryba2https://orcid.org/0000-0002-2060-8393National Institute of Dental and Craniofacial Research, Bethesda, United StatesNational Institute of Child Health and Human Development, Bethesda, United StatesNational Institute of Dental and Craniofacial Research, Bethesda, United StatesIn mice, spared nerve injury replicates symptoms of human neuropathic pain and induces upregulation of many genes in somatosensory neurons. Here we used single cell transcriptomics to probe the effects of partial infraorbital transection of the trigeminal nerve at the cellular level. Uninjured neurons were unaffected by transection of major nerve branches, segregating into many different classes. In marked contrast, axotomy rapidly transformed damaged neurons into just two new and closely-related classes where almost all original identity was lost. Remarkably, sensory neurons also adopted this transcriptomic state following various minor peripheral injuries. By genetically marking injured neurons, we showed that the injury-induced transformation was reversible, with damaged cells slowly reacquiring normal gene expression profiles. Thus, our data expose transcriptomic plasticity, previously thought of as a driver of chronic pain, as a programed response to many types of injury and a potential mechanism for regulating sensation during wound healing.https://elifesciences.org/articles/49679transcriptomic analysisspared nerve injurysomatosensationtrigeminal neuronstranscriptomic plasticityperipheral injury
spellingShingle Minh Q Nguyen
Claire E Le Pichon
Nicholas Ryba
Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
eLife
transcriptomic analysis
spared nerve injury
somatosensation
trigeminal neurons
transcriptomic plasticity
peripheral injury
title Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
title_full Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
title_fullStr Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
title_full_unstemmed Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
title_short Stereotyped transcriptomic transformation of somatosensory neurons in response to injury
title_sort stereotyped transcriptomic transformation of somatosensory neurons in response to injury
topic transcriptomic analysis
spared nerve injury
somatosensation
trigeminal neurons
transcriptomic plasticity
peripheral injury
url https://elifesciences.org/articles/49679
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AT claireelepichon stereotypedtranscriptomictransformationofsomatosensoryneuronsinresponsetoinjury
AT nicholasryba stereotypedtranscriptomictransformationofsomatosensoryneuronsinresponsetoinjury