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Macrophages transfer mitochondria to sensory neurons to resolve inflammatory pain

Ramin Raoof, View ORCID ProfileMichiel van der Vlist, Hanneke L.D.M. Willemen, Judith Prado, Sabine Versteeg, Martijn Vos, Roeland Lockhorst, R. Jeroen Pasterkamp, William Khoury-Hanold, View ORCID ProfileLinde Meyaard, View ORCID ProfileNiels Eijkelkamp
doi: https://doi.org/10.1101/2020.02.12.940445
Ramin Raoof
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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Michiel van der Vlist
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
2Oncode Institute, Utrecht, The Netherlands
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  • ORCID record for Michiel van der Vlist
Hanneke L.D.M. Willemen
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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Judith Prado
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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Sabine Versteeg
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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Martijn Vos
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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Roeland Lockhorst
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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R. Jeroen Pasterkamp
3Department of Translational Neuroscience, UMC Utrecht Brain Center, University Medical Center Utrecht, Utrecht University, Utrecht, The Netherlands
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William Khoury-Hanold
4Department of Immunobiology, Yale University School of Medicine, New Haven, CT 06510, USA
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Linde Meyaard
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
2Oncode Institute, Utrecht, The Netherlands
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  • ORCID record for Linde Meyaard
Niels Eijkelkamp
1Center for Translational Immunology, University Medical Center Utrecht, Utrecht University, Utrecht, the Netherlands
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  • ORCID record for Niels Eijkelkamp
  • For correspondence: n.eijkelkamp@umcutrecht.nl
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Abstract

The current paradigm states that inflammatory pain passively resolves following the cessation of the inflammatory insult. Yet, in a substantial proportion of patients with inflammatory diseases, such as rheumatoid arthritis and inflammatory bowel disease, spontaneous or treatment-induced resolution of inflammation is not sufficient to resolve pain, resulting in chronic pain1–5. Mechanistic insight as how inflammatory pain is resolved is lacking. Here we show that macrophages actively control resolution of inflammatory pain remotely from the site of inflammation by transferring mitochondria to sensory neurons. During resolution of inflammatory pain in mice, M2-like macrophages infiltrate the dorsal root ganglia that contain the somata of sensory neurons, concurrent with the recovery of oxidative phosphorylation in sensory neurons. To resolve pain, macrophages transfer mitochondria to sensory neurons. This transfer requires expression of CD200 Receptor (CD200R) on macrophages and the non-canonical CD200R-ligand iSec1 on sensory neurons. Our data reveal a novel mechanism for active resolution of inflammatory pain and suggests a new direction for treatment of chronic pain.

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Posted February 13, 2020.
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Macrophages transfer mitochondria to sensory neurons to resolve inflammatory pain
Ramin Raoof, Michiel van der Vlist, Hanneke L.D.M. Willemen, Judith Prado, Sabine Versteeg, Martijn Vos, Roeland Lockhorst, R. Jeroen Pasterkamp, William Khoury-Hanold, Linde Meyaard, Niels Eijkelkamp
bioRxiv 2020.02.12.940445; doi: https://doi.org/10.1101/2020.02.12.940445
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Macrophages transfer mitochondria to sensory neurons to resolve inflammatory pain
Ramin Raoof, Michiel van der Vlist, Hanneke L.D.M. Willemen, Judith Prado, Sabine Versteeg, Martijn Vos, Roeland Lockhorst, R. Jeroen Pasterkamp, William Khoury-Hanold, Linde Meyaard, Niels Eijkelkamp
bioRxiv 2020.02.12.940445; doi: https://doi.org/10.1101/2020.02.12.940445

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