Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions
Neuropathic pain following peripheral nerve injury results from maladaptive changes in neurons and immune cells contribution to mechanisms underlying chronic pain. Specifically, in dorsal root ganglia (DRG), sensory neuron cell bodies release extracellular vesicles (EVs) which promote pro-inflammato...
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| Format: | Article |
| Language: | English |
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Elsevier
2025-01-01
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| Series: | Heliyon |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S2405844024172994 |
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| _version_ | 1841526185807314944 |
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| author | Francesca Picco Lynda Zeboudj Silvia Oggero Vincenzo Prato Thomas Burgoyne Nikita Gamper Marzia Malcangio |
| author_facet | Francesca Picco Lynda Zeboudj Silvia Oggero Vincenzo Prato Thomas Burgoyne Nikita Gamper Marzia Malcangio |
| author_sort | Francesca Picco |
| collection | DOAJ |
| description | Neuropathic pain following peripheral nerve injury results from maladaptive changes in neurons and immune cells contribution to mechanisms underlying chronic pain. Specifically, in dorsal root ganglia (DRG), sensory neuron cell bodies release extracellular vesicles (EVs) which promote pro-inflammatory macrophage accumulation that facilitates nociceptive signalling. Here, we show that macrophages shuttle EVs to neurons. Indeed, bone marrow-derived macrophages (BMDMs) release EVs containing microRNA-155 (miR-155) which are taken up by cultured sensory neurons. EV-mediated transfer of miR-155 suppresses phosphatase Ship1 expression and increases cytokine interleukin-6 (IL-6) contents. Intrathecal-injected BMDM-derived EVs accumulate in lumbar DRG and EVs containing miR-155 antagomir result in Ship1 upregulation, Il6 downregulation in neurons in concomitance to attenuation of neuropathic mechanical hypersensitivity. These data suggest that, under neuropathic conditions, pro-inflammatory macrophages shuttle EV-containing miR-155 to neurons and contribute to the expression of pronociceptive IL-6 in DRG. |
| format | Article |
| id | doaj-art-367480ee0e314a07afec702f6cfb5358 |
| institution | Kabale University |
| issn | 2405-8440 |
| language | English |
| publishDate | 2025-01-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Heliyon |
| spelling | doaj-art-367480ee0e314a07afec702f6cfb53582025-01-17T04:50:43ZengElsevierHeliyon2405-84402025-01-01111e41268Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditionsFrancesca Picco0Lynda Zeboudj1Silvia Oggero2Vincenzo Prato3Thomas Burgoyne4Nikita Gamper5Marzia Malcangio6Wolfson Sensory, Pain and Regeneration Centre, King’s College London, London, United KingdomWolfson Sensory, Pain and Regeneration Centre, King’s College London, London, United KingdomWolfson Sensory, Pain and Regeneration Centre, King’s College London, London, United KingdomFaculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, Leeds, United KingdomUCL Institute of Ophthalmology, University College London, London, EC1V 9EL, United Kingdom; Royal Brompton Hospital, Guy's and St Thomas' NHS Foundation Trust, London, United KingdomFaculty of Biological Sciences, School of Biomedical Sciences, University of Leeds, Leeds, United KingdomWolfson Sensory, Pain and Regeneration Centre, King’s College London, London, United Kingdom; Corresponding author.Neuropathic pain following peripheral nerve injury results from maladaptive changes in neurons and immune cells contribution to mechanisms underlying chronic pain. Specifically, in dorsal root ganglia (DRG), sensory neuron cell bodies release extracellular vesicles (EVs) which promote pro-inflammatory macrophage accumulation that facilitates nociceptive signalling. Here, we show that macrophages shuttle EVs to neurons. Indeed, bone marrow-derived macrophages (BMDMs) release EVs containing microRNA-155 (miR-155) which are taken up by cultured sensory neurons. EV-mediated transfer of miR-155 suppresses phosphatase Ship1 expression and increases cytokine interleukin-6 (IL-6) contents. Intrathecal-injected BMDM-derived EVs accumulate in lumbar DRG and EVs containing miR-155 antagomir result in Ship1 upregulation, Il6 downregulation in neurons in concomitance to attenuation of neuropathic mechanical hypersensitivity. These data suggest that, under neuropathic conditions, pro-inflammatory macrophages shuttle EV-containing miR-155 to neurons and contribute to the expression of pronociceptive IL-6 in DRG.http://www.sciencedirect.com/science/article/pii/S2405844024172994Neuropathic painDRG neuronsMacrophagesExtracellular vesiclesmicroRNAsCytokines |
| spellingShingle | Francesca Picco Lynda Zeboudj Silvia Oggero Vincenzo Prato Thomas Burgoyne Nikita Gamper Marzia Malcangio Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions Heliyon Neuropathic pain DRG neurons Macrophages Extracellular vesicles microRNAs Cytokines |
| title | Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| title_full | Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| title_fullStr | Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| title_full_unstemmed | Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| title_short | Macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| title_sort | macrophage to neuron communication via extracellular vesicles in neuropathic pain conditions |
| topic | Neuropathic pain DRG neurons Macrophages Extracellular vesicles microRNAs Cytokines |
| url | http://www.sciencedirect.com/science/article/pii/S2405844024172994 |
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