MRGPRX2 Is the Codeine Receptor of Human Skin Mast Cells: Desensitization through β-Arrestin and Lack of Correlation with the FcεRI Pathway
Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including opioids, to elicit pseudoallergic reactions, but whether it represents the main opiate receptor of skin mast cells remains unknown. By combining...
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| Published in | Journal of investigative dermatology Vol. 141; no. 5; pp. 1286 - 1296.e4 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
01.05.2021
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| Online Access | Get full text |
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| Abstract | Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including opioids, to elicit pseudoallergic reactions, but whether it represents the main opiate receptor of skin mast cells remains unknown. By combining a number of approaches, including the silencing of MRGPRX2, we now report that MRGPRX2 is indeed the dominant codeine receptor of dermal mast cells. Activation by codeine displayed profound subject variability and correlated with secretion elicited by compound 48/80 or substance P but not by FcεRI aggregation. Degranulation by codeine was attenuated by stem cell factor, whereas the opposite was found for FcεRI. Compound 48/80 or codeine alone was able to achieve maximum MRGPRX2 activation. MRGPRX2 was rapidly internalized on codeine binding in a β-arrestin-1‒dependent manner. Codeine-triggered β-arrestin activation was also established by the Tango assay. Prestimulation with MRGPRX2 agonists (but not C3a or FcεRI aggregation) resulted in refractoriness to further stimulation by the same or another MRGPRX2 ligand (cross desensitization). This was duplicated in a cell line (RBL-MRGPRX2). Collectively, codeine degranulates skin mast cells through MRGPRX2, at which it acts as a balanced ligand. It has yet to be determined whether codeine-induced refractoriness could be exploited to desensitize MRGPRX2 to prevent severe pseudoallergic reactions. |
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| AbstractList | Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including opioids, to elicit pseudoallergic reactions, but whether it represents the main opiate receptor of skin mast cells remains unknown. By combining a number of approaches, including the silencing of MRGPRX2, we now report that MRGPRX2 is indeed the dominant codeine receptor of dermal mast cells. Activation by codeine displayed profound subject variability and correlated with secretion elicited by compound 48/80 or substance P but not by FcεRI aggregation. Degranulation by codeine was attenuated by stem cell factor, whereas the opposite was found for FcεRI. Compound 48/80 or codeine alone was able to achieve maximum MRGPRX2 activation. MRGPRX2 was rapidly internalized on codeine binding in a β-arrestin-1‒dependent manner. Codeine-triggered β-arrestin activation was also established by the Tango assay. Prestimulation with MRGPRX2 agonists (but not C3a or FcεRI aggregation) resulted in refractoriness to further stimulation by the same or another MRGPRX2 ligand (cross desensitization). This was duplicated in a cell line (RBL-MRGPRX2). Collectively, codeine degranulates skin mast cells through MRGPRX2, at which it acts as a balanced ligand. It has yet to be determined whether codeine-induced refractoriness could be exploited to desensitize MRGPRX2 to prevent severe pseudoallergic reactions. Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including opioids, to elicit pseudoallergic reactions, but whether it represents the main opiate receptor of skin mast cells remains unknown. By combining a number of approaches, including the silencing of MRGPRX2, we now report that MRGPRX2 is indeed the dominant codeine receptor of dermal mast cells. Activation by codeine displayed profound subject variability and correlated with secretion elicited by compound 48/80 or substance P but not by FcεRI aggregation. Degranulation by codeine was attenuated by stem cell factor, whereas the opposite was found for FcεRI. Compound 48/80 or codeine alone was able to achieve maximum MRGPRX2 activation. MRGPRX2 was rapidly internalized on codeine binding in a β-arrestin-1‒dependent manner. Codeine-triggered β-arrestin activation was also established by the Tango assay. Prestimulation with MRGPRX2 agonists (but not C3a or FcεRI aggregation) resulted in refractoriness to further stimulation by the same or another MRGPRX2 ligand (cross desensitization). This was duplicated in a cell line (RBL-MRGPRX2). Collectively, codeine degranulates skin mast cells through MRGPRX2, at which it acts as a balanced ligand. It has yet to be determined whether codeine-induced refractoriness could be exploited to desensitize MRGPRX2 to prevent severe pseudoallergic reactions.Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including opioids, to elicit pseudoallergic reactions, but whether it represents the main opiate receptor of skin mast cells remains unknown. By combining a number of approaches, including the silencing of MRGPRX2, we now report that MRGPRX2 is indeed the dominant codeine receptor of dermal mast cells. Activation by codeine displayed profound subject variability and correlated with secretion elicited by compound 48/80 or substance P but not by FcεRI aggregation. Degranulation by codeine was attenuated by stem cell factor, whereas the opposite was found for FcεRI. Compound 48/80 or codeine alone was able to achieve maximum MRGPRX2 activation. MRGPRX2 was rapidly internalized on codeine binding in a β-arrestin-1‒dependent manner. Codeine-triggered β-arrestin activation was also established by the Tango assay. Prestimulation with MRGPRX2 agonists (but not C3a or FcεRI aggregation) resulted in refractoriness to further stimulation by the same or another MRGPRX2 ligand (cross desensitization). This was duplicated in a cell line (RBL-MRGPRX2). Collectively, codeine degranulates skin mast cells through MRGPRX2, at which it acts as a balanced ligand. It has yet to be determined whether codeine-induced refractoriness could be exploited to desensitize MRGPRX2 to prevent severe pseudoallergic reactions. |
| Author | Guhl, Sven Artuc, Metin Zuberbier, Torsten Babina, Magda Roy, Saptarshi Wang, Zhao Franke, Kristin Ali, Hydar |
| AuthorAffiliation | 1 Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universitätzu Berlin, and Berlin Institute of Health, Berlin, Germany 3 These authors contributed equally as senior authors 2 Department of Basic and Translational Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA |
| AuthorAffiliation_xml | – name: 1 Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universitätzu Berlin, and Berlin Institute of Health, Berlin, Germany – name: 2 Department of Basic and Translational Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA – name: 3 These authors contributed equally as senior authors |
| Author_xml | – sequence: 1 givenname: Magda orcidid: 0000-0002-4500-7615 surname: Babina fullname: Babina, Magda email: magda.babina@charite.de organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany – sequence: 2 givenname: Zhao orcidid: 0000-0002-2679-5695 surname: Wang fullname: Wang, Zhao organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany – sequence: 3 givenname: Saptarshi orcidid: 0000-0002-4649-0741 surname: Roy fullname: Roy, Saptarshi organization: Department of Basic and Translational Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA – sequence: 4 givenname: Sven orcidid: 0000-0002-7969-1654 surname: Guhl fullname: Guhl, Sven organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany – sequence: 5 givenname: Kristin orcidid: 0000-0002-7402-4211 surname: Franke fullname: Franke, Kristin organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany – sequence: 6 givenname: Metin orcidid: 0000-0001-8851-5196 surname: Artuc fullname: Artuc, Metin organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany – sequence: 7 givenname: Hydar orcidid: 0000-0001-9190-1960 surname: Ali fullname: Ali, Hydar organization: Department of Basic and Translational Sciences, School of Dental Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA – sequence: 8 givenname: Torsten orcidid: 0000-0002-1466-8875 surname: Zuberbier fullname: Zuberbier, Torsten organization: Department of Dermatology and Allergy, Allergy Center Charité, Charité–Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33058860$$D View this record in MEDLINE/PubMed |
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| Snippet | Codeine stimulates skin mast cells and is therefore used in skin tests and as an inducer of experimental itch. MRGPRX2 responds to various drugs, including... |
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| SubjectTerms | beta-Arrestins - physiology Cell Degranulation - drug effects Cells, Cultured Codeine - pharmacology Humans Mast Cells - drug effects Mast Cells - physiology Nerve Tissue Proteins - physiology Receptors, G-Protein-Coupled - physiology Receptors, IgE - physiology Receptors, Neuropeptide - physiology Receptors, Opioid - physiology Signal Transduction - physiology Skin - drug effects |
| Title | MRGPRX2 Is the Codeine Receptor of Human Skin Mast Cells: Desensitization through β-Arrestin and Lack of Correlation with the FcεRI Pathway |
| URI | https://dx.doi.org/10.1016/j.jid.2020.09.017 https://www.ncbi.nlm.nih.gov/pubmed/33058860 https://www.proquest.com/docview/2451853126 https://pubmed.ncbi.nlm.nih.gov/PMC8041898 |
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