Evidence map›Paper›PMID 38081433›Full record

ReviewBrain, behavior, and immunity2024

Interleukin-10 signaling in somatosensory neurons controls CCL2 release and inflammatory response.

Sabrina de Souza, Jesús Rosario Claudio, Jaewon Sim, Kufreobong E Inyang, Andrew Dagenais, Karli Monahan, Beenhwa Lee, Hariharan Ramakrishnan, Visha Parmar, Matan Geron and 3 more

Open access · greenAbstract readReview
In one paragraph

Review in Brain, behavior, and immunity, 2024. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 23 papers.

0numbers the graph read from it
0cells of the map it votes in
23citing papers in PubMed
3.9field-weighted citation impact, top 5% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

23 citing papers in PubMed, 32 citations in OpenAlex.

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  20. Cytokines reprogram airway sensory neurons in asthma.bioRxiv : the preprint server for biology · 2024
    Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

13 authors at 2 institutions in 1 country.

Sabrina de SouzaDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Jesús Rosario ClaudioDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Jaewon SimDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Kufreobong E InyangDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Andrew DagenaisDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Karli MonahanDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Beenhwa LeeDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Hariharan RamakrishnanDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Visha ParmarDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Matan GeronDepartment of Cell Biology and Physiology, Department of Pharmacology, UNC Neuroscience Center, University of North Carolina, Chapel Hill, NC, USA.
Grégory ScherrerDepartment of Cell Biology and Physiology, Department of Pharmacology, UNC Neuroscience Center, University of North Carolina, Chapel Hill, NC, USA; New York Stem Cell Foundation - Robertson Investigator, University of North Carolina, Chapel Hill, NC, USA.
Joseph K FolgerDepartment of Physiology, Michigan State University, East Lansing, MI, USA.
Geoffroy LaumetDepartment of Physiology, Michigan State University, East Lansing, MI, USA; Department of Physiology, Michigan State University, Interdisciplinary Science and Technology Building, 766 Service Rd, East Lansing, MI 48826, USA. Electronic address: laumetge@msu.edu.
Michigan State University · USUniversity of North Carolina at Chapel Hill · US

Funding

Bridge to the PhD in NeuroscienceR25NS090989 · NINDS · MICHIGAN STATE UNIVERSITY · PI IRVING E VEGA · 2015 to 2026
$4.0M
Neuroimmune interactions regulating the balance between remission and relapse of painR01NS121259 · NINDS · MICHIGAN STATE UNIVERSITY · PI LAUMET, GEOFFROY O · 2021 to 2025
$2.0M
Identification of cells and signaling mechanisms underlying opioid analgesia and side effectsR01DA044481 · NIDA · UNIV OF NORTH CAROLINA CHAPEL HILL · PI SCHERRER, GREGORY · 2017 to 2021
$1.8M
NIDA NIH HHS R01 DA044481NINDS NIH HHS R01 NS121259NINDS NIH HHS R25 NS090989
6 · The paper itself

Abstract

Appropriate regulation of the inflammatory response is essential for survival. Interleukin-10 (IL-10), a well-known anti-inflammatory cytokine, plays a major role in controlling inflammation. In addition to immune cells, we previously demonstrated that the IL-10 receptor (IL-10R1) is expressed in dorsal root ganglion sensory neurons. There is emerging evidence that these sensory neurons contribute to immunoregulation, and we hypothesized that IL-10 signaling in dorsal root ganglion (DRG) neurons facilitates the regulation of the inflammatory response. We showed that mice that lack IL-10R1 specifically on advillin-positive neurons have exaggerated blood nitric oxide levels, spinal microglia activation, and cytokine upregulation in the spinal cord, liver, and gut compared to wild-type (WT) counterparts in response to systemic lipopolysaccharide (LPS) injection. Lack of IL-10R1 in DRG and trigeminal ganglion (TG) neurons also increased circulating and DRG levels of proinflammatory C-C motif chemokine ligand 2 (CCL2). Interestingly, analysis of published scRNA-seq data revealed that Ccl2 and Il10ra are expressed by similar types of DRG neurons; nonpeptidergic P2X purinoceptor (P2X3R + ) neurons. In primary cultures of DRG neurons, we demonstrated that IL-10R1 inhibits the production of CCL2, but not that of the neuropeptides substance P and calcitonin-gene related peptide (CGRP). Furthermore, our data indicate that ablation of Transient receptor potential vanilloid (TRPV)1 + neurons does not impact the regulation of CCL2 production by IL-10. In conclusion, we showed that IL-10 binds to its receptor on sensory neurons to downregulate CCL2 and contribute to immunoregulation by reducing the attraction of immune cells by DRG neuron-derived CCL2. This is the first evidence that anti-inflammatory cytokines limit inflammation through direct binding to receptors on sensory neurons. Our data also add to the growing literature that sensory neurons have immunomodulatory functions.

Indexed as

InflammationInterleukin-10AnimalsAnti-Inflammatory AgentsGanglia, SpinalLigandsMiceSensory Receptor CellsAnti-Inflammatory AgentsInterleukin-10LigandsCCL2CytokineDRG sensory neuronsInflammationInterleukin-10 (IL-10)LPSNeuro-immune

Identifiers

PMID38081433
PMCPMC10843623
OpenAlexW4389509833

What OpenQuestion holds

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LicenceTDM
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.