Exosomal cargo including microRNA regulates sensory neuron to macrophage communication after nerve trauma

Raffaele Simeoli, Karli Montague, Hefin R. Jones, Laura Castaldi, David Chambers, Jayne H. Kelleher, Valentina Vacca, Thomas Pitcher, John Grist, Hadil Al-Ahdal, Liang-Fong Wong, Mauro Perretti, Johnathan Lai, Peter Mouritzen, Paul Heppenstall and Marzia Malcangio ()
Additional contact information
Raffaele Simeoli: King’s College London
Karli Montague: King’s College London
Hefin R. Jones: Barts and The London School of Medicine, Queen Mary University of London
Laura Castaldi: EMBL Monterotondo
David Chambers: King’s College London
Jayne H. Kelleher: King’s College London
Valentina Vacca: King’s College London
Thomas Pitcher: King’s College London
John Grist: King’s College London
Hadil Al-Ahdal: Medical Science Building, University of Bristol
Liang-Fong Wong: Medical Science Building, University of Bristol
Mauro Perretti: Barts and The London School of Medicine, Queen Mary University of London
Johnathan Lai: Exiqon A/S
Peter Mouritzen: Exiqon A/S
Paul Heppenstall: EMBL Monterotondo
Marzia Malcangio: King’s College London

Nature Communications, 2017, vol. 8, issue 1, 1-17

Abstract: Abstract Following peripheral axon injury, dysregulation of non-coding microRNAs (miRs) occurs in dorsal root ganglia (DRG) sensory neurons. Here we show that DRG neuron cell bodies release extracellular vesicles, including exosomes containing miRs, upon activity. We demonstrate that miR-21-5p is released in the exosomal fraction of cultured DRG following capsaicin activation of TRPV1 receptors. Pure sensory neuron-derived exosomes released by capsaicin are readily phagocytosed by macrophages in which an increase in miR-21-5p expression promotes a pro-inflammatory phenotype. After nerve injury in mice, miR-21-5p is upregulated in DRG neurons and both intrathecal delivery of a miR-21-5p antagomir and conditional deletion of miR-21 in sensory neurons reduce neuropathic hypersensitivity as well as the extent of inflammatory macrophage recruitment in the DRG. We suggest that upregulation and release of miR-21 contribute to sensory neuron–macrophage communication after damage to the peripheral nerve.

Date: 2017
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DOI: 10.1038/s41467-017-01841-5

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