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A Mast Cell–Specific Receptor Is Critical for Granuloma Induced by Intrathecal Morphine Infusion

Tao Zhang, Rui Liu, Delu Che, Priyanka Pundir, Nan Wang, Shengli Han, Jiao Cao, Yanni Lv, Haiyan Dong, Fang Fang, Jue Wang, Pengyu Ma, Tingting Zhao, Ting Lei, Xinzhong Dong and Langchong He
J Immunol September 4, 2019, ji1801423; DOI: https://doi.org/10.4049/jimmunol.1801423
Tao Zhang
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Rui Liu
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
†The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD 21205;
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Delu Che
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Priyanka Pundir
†The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD 21205;
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Nan Wang
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
†The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD 21205;
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Shengli Han
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Jiao Cao
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Yanni Lv
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Haiyan Dong
‡Department of Pharmacy, The First Affiliated Hospital of Xi’an Jiaotong University, Xi’an 710061, China;
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Fang Fang
§National Center for Magnetic Resonance in Wuhan, State Key Laboratory of Magnetic Resonance and Atomic and Molecular Physics, Wuhan Institute of Physics and Mathematics, Chinese Academy of Sciences, Wuhan 430071, China; and
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Jue Wang
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Pengyu Ma
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Tingting Zhao
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Ting Lei
¶School of Basic Medical Science, Xi’an Jiaotong University, Xi’an 710061, China
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Xinzhong Dong
†The Solomon H. Snyder Department of Neuroscience, School of Medicine, Johns Hopkins University, Baltimore, MD 21205;
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Langchong He
*School of Pharmacy, Xi’an Jiaotong University, Xi’an 710061, China;
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Key Points

  • A mouse model of granuloma induced by intrathecal morphine was established.

  • Mast cell–specific receptor MrgprB2 is essential for granuloma pathogenesis.

  • Activation of MrgprB2 in mast cells promote granuloma-related cell recruitment.

Abstract

Intrathecal morphine infusion is often applied to treat chronic pain related to cancer and other conditions. However, persistent pain can be caused by nerve compression because of granuloma formation. In this study, a mouse model of morphine-induced granuloma formation by intrathecal catheterization morphine infusion into the atlanto-occipital membrane of the foramen magnum was established in wild-type mice, MrgprB2 mutant (MrgprB2−/−) mice, and in mast cell–deficient W-sash c-kit mutant (KitW-sh/W-sh) mice. Heat-related pain after surgery was performed to investigate the antipain effect of morphine. H&E staining and immunofluorescence staining of the spinal cord were applied to analyze the mechanism of granuloma formation. Morphine-induced mast cell degranulation was assessed by measuring the Ca2+ influx and mediator release. Anaphylactoid reactions were measured after s.c. morphine infusion to the paws. Chemokine release by mast cells was determined by Human XL Cytokine Array. Experiments with wild-type, MrgprB2 mutant, and mast cell–deficient W-sash c-kit mutant mice demonstrated that morphine activated mast cells and inflammatory cell aggregation through MrgprB2 in intrathecal infusion sites. The chemokine production of human mast cells demonstrated that granuloma formation is correlated with chemokines release. In addition, morphine activated mouse primary mast cells and de novo chemokine synthesis via the MRGPRX2 in human LAD2 cells. We concluded that granuloma formation during intrathecal morphine infusion was associated with MrgprB2/X2. Reducing MRGPRX2 potentially blocks morphine-induced side effects, including granuloma formation.

Footnotes

  • This work was supported by the National Natural Science Foundation of China (Grants 81230079 and 81227802).

  • Received October 23, 2018.
  • Accepted August 1, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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A Mast Cell–Specific Receptor Is Critical for Granuloma Induced by Intrathecal Morphine Infusion
Tao Zhang, Rui Liu, Delu Che, Priyanka Pundir, Nan Wang, Shengli Han, Jiao Cao, Yanni Lv, Haiyan Dong, Fang Fang, Jue Wang, Pengyu Ma, Tingting Zhao, Ting Lei, Xinzhong Dong, Langchong He
The Journal of Immunology September 4, 2019, ji1801423; DOI: 10.4049/jimmunol.1801423

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A Mast Cell–Specific Receptor Is Critical for Granuloma Induced by Intrathecal Morphine Infusion
Tao Zhang, Rui Liu, Delu Che, Priyanka Pundir, Nan Wang, Shengli Han, Jiao Cao, Yanni Lv, Haiyan Dong, Fang Fang, Jue Wang, Pengyu Ma, Tingting Zhao, Ting Lei, Xinzhong Dong, Langchong He
The Journal of Immunology September 4, 2019, ji1801423; DOI: 10.4049/jimmunol.1801423
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