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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Format: | Article |
Language: | English |
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eLife Sciences Publications Ltd
2019-10-01
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Series: | eLife |
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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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institution | Directory Open Access Journal |
issn | 2050-084X |
language | English |
last_indexed | 2024-12-10T03:50:28Z |
publishDate | 2019-10-01 |
publisher | eLife Sciences Publications Ltd |
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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 |
work_keys_str_mv | AT minhqnguyen stereotypedtranscriptomictransformationofsomatosensoryneuronsinresponsetoinjury AT claireelepichon stereotypedtranscriptomictransformationofsomatosensoryneuronsinresponsetoinjury AT nicholasryba stereotypedtranscriptomictransformationofsomatosensoryneuronsinresponsetoinjury |