IL-33 potentiates histaminergic itch

[Display omitted] Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while rece...

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Published in	Journal of allergy and clinical immunology Vol. 153; no. 3; pp. 852 - 859.e3
Main Authors	Trier, Anna M., Ver Heul, Aaron M., Fredman, Avery, Le, Victoria, Wang, Zhen, Auyeung, Kelsey, Meixiong, James, Lovato, Paola, Holtzman, Michael J., Wang, Fang, Dong, Xinzhong, Ji, Andrew L., Kim, Brian S.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 01.03.2024
Subjects	Animals Chronic spontaneous urticaria histamine Histamine - metabolism Histamine Antagonists Humans IL-13 IL-33 Interleukin-13 - genetics Interleukin-13 - metabolism Interleukin-33 - metabolism itch mast cell Mice Mice, Knockout neuroimmunology Pruritus - pathology Quality of Life Skin - pathology itch LM histamine ImmGen CSU mast cell OSM Chronic spontaneous urticaria IL-13 C48/80 IL-33 neuroimmunology His scRNA-Seq OVA IL-33R WT
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Abstract	[Display omitted] Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while receiving maximal doses. Mechanisms that drive resistance to antihistamines are poorly defined. Signaling of the alarmin cytokine IL-33 in sensory neurons is postulated to drive chronic itch by inducing neuronal sensitization to pruritogens. Thus, we sought to determine if IL-33 can augment histamine-induced (histaminergic) itch. Itch behavior was assessed in response to histamine after IL-33 or saline administration. Various stimuli and conditional and global knockout mice were utilized to dissect cellular mechanisms. Multiple existing transcriptomic data sets were evaluated, including single-cell RNA sequencing of human and mouse skin, microarrays of isolated mouse mast cells at steady state and after stimulation with IL-33, and microarrays of skin biopsy samples from subjects with CSU and healthy controls. IL-33 amplifies histaminergic itch independent of IL-33 signaling in sensory neurons. Mast cells are the top expressors of the IL-33 receptor in both human and mouse skin. When stimulated by IL-33, mouse mast cells significantly increase IL-13 levels. Enhancement of histaminergic itch by IL-33 relies on a mast cell– and IL-13–dependent mechanism. IL-33 receptor expression is increased in lesional skin of subjects with CSU compared to healthy controls. Our findings suggest that IL-33 signaling may be a key driver of histaminergic itch in mast cell–associated pruritic conditions such as CSU.
AbstractList	[Display omitted] Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while receiving maximal doses. Mechanisms that drive resistance to antihistamines are poorly defined. Signaling of the alarmin cytokine IL-33 in sensory neurons is postulated to drive chronic itch by inducing neuronal sensitization to pruritogens. Thus, we sought to determine if IL-33 can augment histamine-induced (histaminergic) itch. Itch behavior was assessed in response to histamine after IL-33 or saline administration. Various stimuli and conditional and global knockout mice were utilized to dissect cellular mechanisms. Multiple existing transcriptomic data sets were evaluated, including single-cell RNA sequencing of human and mouse skin, microarrays of isolated mouse mast cells at steady state and after stimulation with IL-33, and microarrays of skin biopsy samples from subjects with CSU and healthy controls. IL-33 amplifies histaminergic itch independent of IL-33 signaling in sensory neurons. Mast cells are the top expressors of the IL-33 receptor in both human and mouse skin. When stimulated by IL-33, mouse mast cells significantly increase IL-13 levels. Enhancement of histaminergic itch by IL-33 relies on a mast cell– and IL-13–dependent mechanism. IL-33 receptor expression is increased in lesional skin of subjects with CSU compared to healthy controls. Our findings suggest that IL-33 signaling may be a key driver of histaminergic itch in mast cell–associated pruritic conditions such as CSU. Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while receiving maximal doses. Mechanisms that drive resistance to antihistamines are poorly defined. Signaling of the alarmin cytokine IL-33 in sensory neurons is postulated to drive chronic itch by inducing neuronal sensitization to pruritogens. Thus, we sought to determine if IL-33 can augment histamine-induced (histaminergic) itch. Itch behavior was assessed in response to histamine after IL-33 or saline administration. Various stimuli and conditional and global knockout mice were utilized to dissect cellular mechanisms. Multiple existing transcriptomic data sets were evaluated, including single-cell RNA sequencing of human and mouse skin, microarrays of isolated mouse mast cells at steady state and after stimulation with IL-33, and microarrays of skin biopsy samples from subjects with CSU and healthy controls. IL-33 amplifies histaminergic itch independent of IL-33 signaling in sensory neurons. Mast cells are the top expressors of the IL-33 receptor in both human and mouse skin. When stimulated by IL-33, mouse mast cells significantly increase IL-13 levels. Enhancement of histaminergic itch by IL-33 relies on a mast cell- and IL-13-dependent mechanism. IL-33 receptor expression is increased in lesional skin of subjects with CSU compared to healthy controls. Our findings suggest that IL-33 signaling may be a key driver of histaminergic itch in mast cell-associated pruritic conditions such as CSU. Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while receiving maximal doses. Mechanisms that drive resistance to antihistamines are poorly defined.BACKGROUNDItch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the first-line treatment for itch, in conditions like chronic spontaneous urticaria (CSU), many patients remain symptomatic while receiving maximal doses. Mechanisms that drive resistance to antihistamines are poorly defined.Signaling of the alarmin cytokine IL-33 in sensory neurons is postulated to drive chronic itch by inducing neuronal sensitization to pruritogens. Thus, we sought to determine if IL-33 can augment histamine-induced (histaminergic) itch.OBJECTIVESSignaling of the alarmin cytokine IL-33 in sensory neurons is postulated to drive chronic itch by inducing neuronal sensitization to pruritogens. Thus, we sought to determine if IL-33 can augment histamine-induced (histaminergic) itch.Itch behavior was assessed in response to histamine after IL-33 or saline administration. Various stimuli and conditional and global knockout mice were utilized to dissect cellular mechanisms. Multiple existing transcriptomic data sets were evaluated, including single-cell RNA sequencing of human and mouse skin, microarrays of isolated mouse mast cells at steady state and after stimulation with IL-33, and microarrays of skin biopsy samples from subjects with CSU and healthy controls.METHODSItch behavior was assessed in response to histamine after IL-33 or saline administration. Various stimuli and conditional and global knockout mice were utilized to dissect cellular mechanisms. Multiple existing transcriptomic data sets were evaluated, including single-cell RNA sequencing of human and mouse skin, microarrays of isolated mouse mast cells at steady state and after stimulation with IL-33, and microarrays of skin biopsy samples from subjects with CSU and healthy controls.IL-33 amplifies histaminergic itch independent of IL-33 signaling in sensory neurons. Mast cells are the top expressors of the IL-33 receptor in both human and mouse skin. When stimulated by IL-33, mouse mast cells significantly increase IL-13 levels. Enhancement of histaminergic itch by IL-33 relies on a mast cell- and IL-13-dependent mechanism. IL-33 receptor expression is increased in lesional skin of subjects with CSU compared to healthy controls.RESULTSIL-33 amplifies histaminergic itch independent of IL-33 signaling in sensory neurons. Mast cells are the top expressors of the IL-33 receptor in both human and mouse skin. When stimulated by IL-33, mouse mast cells significantly increase IL-13 levels. Enhancement of histaminergic itch by IL-33 relies on a mast cell- and IL-13-dependent mechanism. IL-33 receptor expression is increased in lesional skin of subjects with CSU compared to healthy controls.Our findings suggest that IL-33 signaling may be a key driver of histaminergic itch in mast cell-associated pruritic conditions such as CSU.CONCLUSIONSOur findings suggest that IL-33 signaling may be a key driver of histaminergic itch in mast cell-associated pruritic conditions such as CSU. IL-33 stimulates a mast cell- and IL-13-dependent axis to exacerbate of histaminergic itch. These findings provide insight into mast cell-associated itch conditions such as chronic spontaneous urticaria.
Author	Ver Heul, Aaron M. Fredman, Avery Lovato, Paola Wang, Zhen Dong, Xinzhong Wang, Fang Trier, Anna M. Kim, Brian S. Le, Victoria Holtzman, Michael J. Auyeung, Kelsey Ji, Andrew L. Meixiong, James
AuthorAffiliation	6 The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21209, USA 7 LEO Pharma A/S, Industriparken 55, Ballerup, Denmark 15 Allen Discovery Center for Neuroimmune Interactions, New York, NY 10029, USA 3 Division of Allergy and Immunology, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA 8 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA 10 Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21209, USA 13 Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA 2 Division of Dermatology, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA 1 Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA 5 Mark
AuthorAffiliation_xml	– name: 5 Mark Lebwohl Center for Neuroinflammation & Sensation, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 3 Division of Allergy and Immunology, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 12 Tisch Cancer Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029 – name: 15 Allen Discovery Center for Neuroimmune Interactions, New York, NY 10029, USA – name: 6 The Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21209, USA – name: 8 Division of Pulmonary and Critical Care Medicine, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 10 Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21209, USA – name: 4 Kimberly and Eric J. Waldman Department of Dermatology, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 11 Black Family Stem Cell Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 14 Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – name: 1 Center for the Study of Itch and Sensory Disorders, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 7 LEO Pharma A/S, Industriparken 55, Ballerup, Denmark – name: 2 Division of Dermatology, Department of Medicine, Washington University School of Medicine, St. Louis, MO 63110, USA – name: 9 Department of Dermatology, The First Affiliated Hospital, Sun Yat-sen University, Guangzhou 510080, Guangdong, China – name: 13 Marc and Jennifer Lipschultz Precision Immunology Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Keywords	itch LM histamine ImmGen CSU mast cell OSM Chronic spontaneous urticaria IL-13 C48/80 IL-33 neuroimmunology His scRNA-Seq OVA IL-33R WT
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Snippet	[Display omitted] Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are... Itch is a common symptom that can greatly diminish quality of life. Histamine is a potent endogenous pruritogen, and while antihistamines are often the... IL-33 stimulates a mast cell- and IL-13-dependent axis to exacerbate of histaminergic itch. These findings provide insight into mast cell-associated itch...
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SubjectTerms	Animals Chronic spontaneous urticaria histamine Histamine - metabolism Histamine Antagonists Humans IL-13 IL-33 Interleukin-13 - genetics Interleukin-13 - metabolism Interleukin-33 - metabolism itch mast cell Mice Mice, Knockout neuroimmunology Pruritus - pathology Quality of Life Skin - pathology
Title	IL-33 potentiates histaminergic itch
URI	https://www.clinicalkey.com/#!/content/1-s2.0-S0091674923014653 https://dx.doi.org/10.1016/j.jaci.2023.08.038 https://www.ncbi.nlm.nih.gov/pubmed/37984799 https://www.proquest.com/docview/2892271021 https://pubmed.ncbi.nlm.nih.gov/PMC10939899
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