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Immunity to the microbiota promotes sensory neuron regeneration

Enamorado, Michel ; Kulalert, Warakorn ; Han, Seong-Ji ; Rao, Indira ; Delaleu, Jérémie ; Link, Verena M ; Yong, Daniel ; Smelkinson, Margery ; Gil, Louis and Nakajima, Saeko , et al. (2023) In Cell 186(3). p.17-620
Abstract

Tissue immunity and responses to injury depend on the coordinated action and communication among physiological systems. Here, we show that, upon injury, adaptive responses to the microbiota directly promote sensory neuron regeneration. At homeostasis, tissue-resident commensal-specific T cells colocalize with sensory nerve fibers within the dermis, express a transcriptional program associated with neuronal interaction and repair, and promote axon growth and local nerve regeneration following injury. Mechanistically, our data reveal that the cytokine interleukin-17A (IL-17A) released by commensal-specific Th17 cells upon injury directly signals to sensory neurons via IL-17 receptor A, the transcription of which is specifically... (More)

Tissue immunity and responses to injury depend on the coordinated action and communication among physiological systems. Here, we show that, upon injury, adaptive responses to the microbiota directly promote sensory neuron regeneration. At homeostasis, tissue-resident commensal-specific T cells colocalize with sensory nerve fibers within the dermis, express a transcriptional program associated with neuronal interaction and repair, and promote axon growth and local nerve regeneration following injury. Mechanistically, our data reveal that the cytokine interleukin-17A (IL-17A) released by commensal-specific Th17 cells upon injury directly signals to sensory neurons via IL-17 receptor A, the transcription of which is specifically upregulated in injured neurons. Collectively, our work reveals that in the context of tissue damage, preemptive immunity to the microbiota can rapidly bridge biological systems by directly promoting neuronal repair, while also identifying IL-17A as a major determinant of this fundamental process.

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publishing date
type
Contribution to journal
publication status
published
subject
keywords
Axons, Interleukin-17, Microbiota, Nerve Regeneration/physiology, Sensory Receptor Cells, Animals, Mice, Th17 Cells/cytology
in
Cell
volume
186
issue
3
pages
17 - 620
publisher
Cell Press
external identifiers
  • scopus:85147105808
  • pmid:36640762
ISSN
1097-4172
DOI
10.1016/j.cell.2022.12.037
language
English
LU publication?
no
additional info
Published by Elsevier Inc.
id
68e658b4-eb7a-400d-965a-5b80726c6a34
date added to LUP
2025-12-20 13:27:17
date last changed
2025-12-22 14:58:29
@article{68e658b4-eb7a-400d-965a-5b80726c6a34,
  abstract     = {{<p>Tissue immunity and responses to injury depend on the coordinated action and communication among physiological systems. Here, we show that, upon injury, adaptive responses to the microbiota directly promote sensory neuron regeneration. At homeostasis, tissue-resident commensal-specific T cells colocalize with sensory nerve fibers within the dermis, express a transcriptional program associated with neuronal interaction and repair, and promote axon growth and local nerve regeneration following injury. Mechanistically, our data reveal that the cytokine interleukin-17A (IL-17A) released by commensal-specific Th17 cells upon injury directly signals to sensory neurons via IL-17 receptor A, the transcription of which is specifically upregulated in injured neurons. Collectively, our work reveals that in the context of tissue damage, preemptive immunity to the microbiota can rapidly bridge biological systems by directly promoting neuronal repair, while also identifying IL-17A as a major determinant of this fundamental process.</p>}},
  author       = {{Enamorado, Michel and Kulalert, Warakorn and Han, Seong-Ji and Rao, Indira and Delaleu, Jérémie and Link, Verena M and Yong, Daniel and Smelkinson, Margery and Gil, Louis and Nakajima, Saeko and Linehan, Jonathan L and Bouladoux, Nicolas and Wlaschin, Josette and Kabat, Juraj and Kamenyeva, Olena and Deng, Liwen and Gribonika, Inta and Chesler, Alexander T and Chiu, Isaac M and Le Pichon, Claire E and Belkaid, Yasmine}},
  issn         = {{1097-4172}},
  keywords     = {{Axons; Interleukin-17; Microbiota; Nerve Regeneration/physiology; Sensory Receptor Cells; Animals; Mice; Th17 Cells/cytology}},
  language     = {{eng}},
  month        = {{02}},
  number       = {{3}},
  pages        = {{17--620}},
  publisher    = {{Cell Press}},
  series       = {{Cell}},
  title        = {{Immunity to the microbiota promotes sensory neuron regeneration}},
  url          = {{http://dx.doi.org/10.1016/j.cell.2022.12.037}},
  doi          = {{10.1016/j.cell.2022.12.037}},
  volume       = {{186}},
  year         = {{2023}},
}