Cytokine Signature in Schnitzler Syndrome: Proinflammatory Cytokine Production Associated to Th Suppression

Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown. To deter...

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Published inFrontiers in immunology Vol. 11; p. 588322
Main Authors Masson Regnault, Marie, Frouin, Eric, Jéru, Isabelle, Delwail, Adriana, Charreau, Sandrine, Barbarot, Sébastien, Néel, Antoine, Masseau, Agathe, Puéchal, Xavier, Kyndt, Xavier, Gayet, Stephane, Lifermann, François, Asli, Bouchra, Balguerie, Xavier, Blanchard-Delaunay, Claire, Aubin, François, Rizzi, Rita, Rongioletti, Franco, Boyé, Thierry, Gusdorf, Laurence, Bessis, Didier, Morel, Franck, Hainaut, Ewa, Lipsker, Dan, Lecron, Jean-Claude
Format Journal Article
LanguageEnglish
Published Switzerland Frontiers 26.11.2020
Frontiers Media S.A
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Abstract Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown. To determine v cytokine profiles of Peripheral Blood Mononuclear Cells (PBMCs) from SchS patients prior to treatment and after initiation of anti-IL-1 therapy (anakinra). The sera cytokine profile was studied in parallel. We collected blood samples from thirty-six untreated or treated SchS. PBMCs were cultured with and without LPS or anti-CD3/CD28. Cytokine levels were evaluated in serum and cell culture supernatants using Luminex technology. Spontaneous TNFα, IL-6, IL-1β, IL-1α, and IL-1RA release by PBMCs of SchS patients were higher than in controls. LPS-stimulation further induced the secretion of these cytokines. In contrast, after T-cell stimulation, TNFα, IL-10, IFNγ, IL-17A, and IL-4 production decreased in SchS patients compared to healthy controls, but less in treated patients. Whereas IL-1β serum level was not detected in most sera, IL-6, IL-10, and TNFα serum levels were higher in patients with SchS and IFNγ and IL-4 levels were lower. Of note, IL-6 decreased after treatment in SchS ( = 0.04). Our data strengthen the hypothesis of myeloid inflammation in SchS, mediated in particular by IL-1β, TNFα, and IL-6, associated with overproduction of the inhibitors IL-1RA and IL-10. In contrast, we observed a loss of Th1, Th2, and Th17 cell functionalities that tends to be reversed by anakinra.
AbstractList BackgroundSchnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown.ObjectiveTo determine ex vivo cytokine profiles of Peripheral Blood Mononuclear Cells (PBMCs) from SchS patients prior to treatment and after initiation of anti-IL-1 therapy (anakinra). The sera cytokine profile was studied in parallel.MethodsWe collected blood samples from thirty-six untreated or treated SchS. PBMCs were cultured with and without LPS or anti-CD3/CD28. Cytokine levels were evaluated in serum and cell culture supernatants using Luminex technology.ResultsSpontaneous TNFα, IL-6, IL-1β, IL-1α, and IL-1RA release by PBMCs of SchS patients were higher than in controls. LPS-stimulation further induced the secretion of these cytokines. In contrast, after T-cell stimulation, TNFα, IL-10, IFNγ, IL-17A, and IL-4 production decreased in SchS patients compared to healthy controls, but less in treated patients. Whereas IL-1β serum level was not detected in most sera, IL-6, IL-10, and TNFα serum levels were higher in patients with SchS and IFNγ and IL-4 levels were lower. Of note, IL-6 decreased after treatment in SchS (p = 0.04).ConclusionOur data strengthen the hypothesis of myeloid inflammation in SchS, mediated in particular by IL-1β, TNFα, and IL-6, associated with overproduction of the inhibitors IL-1RA and IL-10. In contrast, we observed a loss of Th1, Th2, and Th17 cell functionalities that tends to be reversed by anakinra.
Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown. To determine v cytokine profiles of Peripheral Blood Mononuclear Cells (PBMCs) from SchS patients prior to treatment and after initiation of anti-IL-1 therapy (anakinra). The sera cytokine profile was studied in parallel. We collected blood samples from thirty-six untreated or treated SchS. PBMCs were cultured with and without LPS or anti-CD3/CD28. Cytokine levels were evaluated in serum and cell culture supernatants using Luminex technology. Spontaneous TNFα, IL-6, IL-1β, IL-1α, and IL-1RA release by PBMCs of SchS patients were higher than in controls. LPS-stimulation further induced the secretion of these cytokines. In contrast, after T-cell stimulation, TNFα, IL-10, IFNγ, IL-17A, and IL-4 production decreased in SchS patients compared to healthy controls, but less in treated patients. Whereas IL-1β serum level was not detected in most sera, IL-6, IL-10, and TNFα serum levels were higher in patients with SchS and IFNγ and IL-4 levels were lower. Of note, IL-6 decreased after treatment in SchS ( = 0.04). Our data strengthen the hypothesis of myeloid inflammation in SchS, mediated in particular by IL-1β, TNFα, and IL-6, associated with overproduction of the inhibitors IL-1RA and IL-10. In contrast, we observed a loss of Th1, Th2, and Th17 cell functionalities that tends to be reversed by anakinra.
Background Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown. Objective To determine ex v ivo cytokine profiles of Peripheral Blood Mononuclear Cells (PBMCs) from SchS patients prior to treatment and after initiation of anti-IL-1 therapy (anakinra). The sera cytokine profile was studied in parallel. Methods We collected blood samples from thirty-six untreated or treated SchS. PBMCs were cultured with and without LPS or anti-CD3/CD28. Cytokine levels were evaluated in serum and cell culture supernatants using Luminex technology. Results Spontaneous TNFα, IL-6, IL-1β, IL-1α, and IL-1RA release by PBMCs of SchS patients were higher than in controls. LPS-stimulation further induced the secretion of these cytokines. In contrast, after T-cell stimulation, TNFα, IL-10, IFNγ, IL-17A, and IL-4 production decreased in SchS patients compared to healthy controls, but less in treated patients. Whereas IL-1β serum level was not detected in most sera, IL-6, IL-10, and TNFα serum levels were higher in patients with SchS and IFNγ and IL-4 levels were lower. Of note, IL-6 decreased after treatment in SchS ( p = 0.04). Conclusion Our data strengthen the hypothesis of myeloid inflammation in SchS, mediated in particular by IL-1β, TNFα, and IL-6, associated with overproduction of the inhibitors IL-1RA and IL-10. In contrast, we observed a loss of Th1, Th2, and Th17 cell functionalities that tends to be reversed by anakinra.
BackgroundSchnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM gammopathy. Overactivation of the interleukin(IL)-1 system is reported, even though the exact pathophysiological pathways remain unknown. ObjectiveTo determine ex vivo cytokine profiles of Peripheral Blood Mononuclear Cells (PBMCs) from SchS patients prior to treatment and after initiation of anti-IL-1 therapy (anakinra). The sera cytokine profile was studied in parallel. MethodsWe collected blood samples from thirty-six untreated or treated SchS. PBMCs were cultured with and without LPS or anti-CD3/CD28. Cytokine levels were evaluated in serum and cell culture supernatants using Luminex technology. ResultsSpontaneous TNFα, IL-6, IL-1β, IL-1α, and IL-1RA release by PBMCs of SchS patients were higher than in controls. LPS-stimulation further induced the secretion of these cytokines. In contrast, after T-cell stimulation, TNFα, IL-10, IFNγ, IL-17A, and IL-4 production decreased in SchS patients compared to healthy controls, but less in treated patients. Whereas IL-1β serum level was not detected in most sera, IL-6, IL-10, and TNFα serum levels were higher in patients with SchS and IFNγ and IL-4 levels were lower. Of note, IL-6 decreased after treatment in SchS (p = 0.04). ConclusionOur data strengthen the hypothesis of myeloid inflammation in SchS, mediated in particular by IL-1β, TNFα, and IL-6, associated with overproduction of the inhibitors IL-1RA and IL-10. In contrast, we observed a loss of Th1, Th2, and Th17 cell functionalities that tends to be reversed by anakinra.
Author Gayet, Stephane
Lifermann, François
Hainaut, Ewa
Kyndt, Xavier
Jéru, Isabelle
Lecron, Jean-Claude
Morel, Franck
Rizzi, Rita
Delwail, Adriana
Frouin, Eric
Néel, Antoine
Boyé, Thierry
Puéchal, Xavier
Asli, Bouchra
Lipsker, Dan
Masseau, Agathe
Rongioletti, Franco
Charreau, Sandrine
Aubin, François
Gusdorf, Laurence
Masson Regnault, Marie
Barbarot, Sébastien
Bessis, Didier
Balguerie, Xavier
Blanchard-Delaunay, Claire
AuthorAffiliation 13 Centre Hospitalier Edouard Herriot-Lyon, Service de Médecine Interne , Lyon , France
14 Centre Hospitalier de Rouen, Service de Dermatologie , Rouen , France
22 Faculté de Médecine, Université de Strasbourg et Clinique Dermatologique, Hôpitaux Universitaires de Strasbourg , Strasbourg , France
16 Centre Hospitalier de Besançon, Service de Dermatologie , Besançon , France
18 Department of Medical Sciences and Public Health, Unit of Dermatology, University of Cagliari , Cagliari , Italy
5 ImageUP, Plate-forme d’Imagerie et Laboratoire Signalisation et Transport Ioniques Membranaires ERL CNRS 7003/EA 7349, Université de Poitiers , Poitiers , France
19 Service de Dermatologie, Hôpital d’instruction des Armées Sainte-Anne , Toulon , France
2 Laboratoire Inflammation, Tissus Epithéliaux et Cytokines (LITEC), EA4331, Université de Poitiers , Poitiers , France
6 Centre Hospitalo-universitaire de Nantes, Service de Dermatologie , Nantes , France
11 Service de Medecine Interne, Centre hospitalo-Univer
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  organization: CHU de Poitiers, Laboratoire Immunologie-Inflammation, Poitiers, France
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ContentType Journal Article
Copyright Copyright © 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron.
Attribution
Copyright © 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron
Copyright_xml – notice: Copyright © 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron.
– notice: Attribution
– notice: Copyright © 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron
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Keywords IL-1
PBMC (peripheral blood mononuclear cells)
inflammasome
cytokines
Schnitzler syndrome
IL-1 antagonist
ex vivo
Language English
License Copyright © 2020 Masson Regnault, Frouin, Jéru, Delwail, Charreau, Barbarot, Néel, Masseau, Puéchal, Kyndt, Gayet, Lifermann, Asli, Balguerie, Blanchard-Delaunay, Aubin, Rizzi, Rongioletti, Boyé, Gusdorf, Bessis, Morel, Hainaut, Lipsker and Lecron.
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PMCID: PMC7726442
Reviewed by: Karoline Krause, Charité–Universitätsmedizin Berlin, Germany; Yu-Jih Su, Kaohsiung Chang Gung Memorial Hospital, Taiwan
Edited by: Stefania Gallucci, Temple University, United States
Present address: Isabelle Jéru, Laboratoire Commun de Biologie et Génétique Moléculaires, AP-HP, Hôpital Saint-Antoine, Paris, France
These authors have contributed equally to this work and share first authorship
These authors have contributed equally to this work and share last authorship
This article was submitted to Autoimmune and Autoinflammatory Disorders, a section of the journal Frontiers in Immunology
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PublicationTitle Frontiers in immunology
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Snippet Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal IgM...
BackgroundSchnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal...
Background Schnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and...
BackgroundSchnitzler syndrome (SchS) is a rare autoinflammatory disease characterized by urticarial exanthema, bone and joint alterations, fever and monoclonal...
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SubjectTerms cytokines
IL-1
IL-1 antagonist
Immunology
inflammasome
Life Sciences
PBMC (peripheral blood mononuclear cells)
Schnitzler syndrome
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Title Cytokine Signature in Schnitzler Syndrome: Proinflammatory Cytokine Production Associated to Th Suppression
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