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 in | Frontiers in immunology Vol. 11; p. 588322 |
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Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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26.11.2020
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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. |
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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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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. Attribution: http://creativecommons.org/licenses/by This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 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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References | Schnitzler (B1) 1972 Krause (B6) 2017; 139 Zhou (B15) 2010; 13 Novick (B29) 2013; 25 Noster (B23) 2016; 138 Galon (B19) 2000; 12 Pizzirani (B14) 2009; 48 Gusdorf (B9) 2017; 19 Kluger (B20) 2009; 72 Feriotti (B28) 2017; 8 Simon (B2) 2013; 68 Néel (B11) 2014; 13 Jéru (B17) 2010; 62 de Koning (B7) 2014; 4 Wilson (B27) 2007; 8 de Koning (B3) 2007; 37 Lasigliè (B26) 2011; 6 Pascual (B24) 2005; 201 Esensten (B25) 2009; 5 Kyle (B5) 2003; 102 Jéru (B18) 2011; 63 Lipsker (B8) 2010; 5 Launay (B13) 2013; 8 Migliorini (B21) 2009; 20 Ryan (B12) 2008; 121 Zhou (B10) 2015; 67 Claus (B22) 2019; 39 Ibrahim (B16) 2014; 69 Claes (B4) 2008; 158 |
References_xml | – volume: 5 start-page: 38 year: 2010 ident: B8 article-title: The Schnitzler syndrome publication-title: Orphanet J Rare Dis doi: 10.1186/1750-1172-5-38 contributor: fullname: Lipsker – volume: 8 year: 2017 ident: B28 article-title: NOD-Like Receptor P3 Inflammasome Controls Protective Th1/Th17 Immunity against Pulmonary Paracoccidioidomycosis publication-title: Front Immunol doi: 10.3389/fimmu.2017.00786 contributor: fullname: Feriotti – volume: 13 year: 2014 ident: B11 article-title: Long-term effectiveness and safety of interleukin-1 receptor antagonist (anakinra) in Schnitzler’s syndrome: a French multicenter study publication-title: Autoimmun Rev doi: 10.1016/j.autrev.2014.08.031 contributor: fullname: Néel – volume: 5 year: 2009 ident: B25 article-title: Regulatory T cells as therapeutic targets in rheumatoid arthritis publication-title: Nat Rev Rheumatol doi: 10.1038/nrrheum.2009.183 contributor: fullname: Esensten – volume: 67 year: 2015 ident: B10 article-title: Cryopyrin-associated Periodic Syndrome Caused by a Myeloid-Restricted Somatic NLRP3 Mutation publication-title: Arthritis Rheumatol Hoboken NJ doi: 10.1002/art.39190 contributor: fullname: Zhou – volume: 4 start-page: 41 year: 2014 ident: B7 article-title: Schnitzler’s syndrome: lessons from 281 cases publication-title: Clin Transl Allergy doi: 10.1186/2045-7022-4-41 contributor: fullname: de Koning – year: 1972 ident: B1 article-title: Lésions urticariennes chroniques permanentes (érythème pétaloïde?) Case cliniques n.46 B publication-title: J Dermatol Angers contributor: fullname: Schnitzler – volume: 13 year: 2010 ident: B15 article-title: Conceptual and methodological issues relevant to cytokine and inflammatory marker measurements in clinical research publication-title: Curr Opin Clin Nutr Metab Care doi: 10.1097/MCO.0b013e32833cf3bc contributor: fullname: Zhou – volume: 102 year: 2003 ident: B5 article-title: Long-term follow-up of IgM monoclonal gammopathy of undetermined significance publication-title: Blood doi: 10.1182/blood-2003-03-0801 contributor: fullname: Kyle – volume: 139 year: 2017 ident: B6 article-title: Efficacy and safety of canakinumab in Schnitzler syndrome: A multicenter randomized placebo-controlled study publication-title: J Allergy Clin Immunol doi: 10.1016/j.jaci.2016.07.041 contributor: fullname: Krause – volume: 63 year: 2011 ident: B18 article-title: Role of interleukin-1β in NLRP12-associated autoinflammatory disorders and resistance to anti-interleukin-1 therapy publication-title: Arthritis Rheum doi: 10.1002/art.30378 contributor: fullname: Jéru – volume: 201 year: 2005 ident: B24 article-title: Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade publication-title: J Exp Med doi: 10.1084/jem.20050473 contributor: fullname: Pascual – volume: 158 year: 2008 ident: B4 article-title: Another devastating complication of the Schnitzler syndrome: AA amyloidosis publication-title: Br J Dermatol doi: 10.1111/j.1365-2133.2007.08251.x contributor: fullname: Claes – volume: 138 start-page: 1161 year: 2016 ident: B23 article-title: Dysregulation of proinflammatory versus anti-inflammatory human TH17 cell functionalities in the autoinflammatory Schnitzler syndrome publication-title: J Allergy Clin Immunol doi: 10.1016/j.jaci.2015.12.1338 contributor: fullname: Noster – volume: 69 year: 2014 ident: B16 article-title: Ex vivo PBMC cytokine profile in familial Mediterranean fever patients: Involvement of IL-1β, IL-1α and Th17-associated cytokines and decrease of Th1 and Th2 cytokines publication-title: Cytokine doi: 10.1016/j.cyto.2014.06.012 contributor: fullname: Ibrahim – volume: 19 start-page: 46 year: 2017 ident: B9 article-title: Schnitzler Syndrome: a Review publication-title: Curr Rheumatol Rep doi: 10.1007/s11926-017-0673-5 contributor: fullname: Gusdorf – volume: 72 year: 2009 ident: B20 article-title: Tocilizumab as a potential treatment in Schnitzler syndrome publication-title: Med Hypotheses doi: 10.1016/j.mehy.2008.12.002 contributor: fullname: Kluger – volume: 37 year: 2007 ident: B3 article-title: Schnitzler Syndrome Study Group. Schnitzler syndrome: beyond the case reports: review and follow-up of 94 patients with an emphasis on prognosis and treatment publication-title: Semin Arthritis Rheum doi: 10.1016/j.semarthrit.2007.04.001 contributor: fullname: de Koning – volume: 62 year: 2010 ident: B17 article-title: Functional consequences of a germline mutation in the leucine-rich repeat domain of NLRP3 identified in an atypical autoinflammatory disorder publication-title: Arthritis Rheum doi: 10.1002/art.27326 contributor: fullname: Jéru – volume: 6 start-page: e20014 year: 2011 ident: B26 article-title: Role of IL-1 Beta in the Development of Human TH17 Cells: Lesson from NLPR3 Mutated Patients publication-title: PloS One doi: 10.1371/journal.pone.0020014 contributor: fullname: Lasigliè – volume: 25 year: 2013 ident: B29 article-title: Interleukin-18, more than a Th1 cytokine publication-title: Semin Immunol doi: 10.1016/j.smim.2013.10.014 contributor: fullname: Novick – volume: 39 year: 2019 ident: B22 article-title: Variable Responses to Tocilizumab in Four Patients with Schnitzler Syndrome publication-title: J Clin Immunol doi: 10.1007/s10875-019-00644-1 contributor: fullname: Claus – volume: 12 year: 2000 ident: B19 article-title: TNFRSF1A mutations and autoinflammatory syndromes publication-title: Curr Opin Immunol doi: 10.1016/S0952-7915(00)00124-2 contributor: fullname: Galon – volume: 8 year: 2007 ident: B27 article-title: Development, cytokine profile and function of human interleukin 17-producing helper T cells publication-title: Nat Immunol doi: 10.1038/ni1497 contributor: fullname: Wilson – volume: 48 year: 2009 ident: B14 article-title: Dysfunctional inflammasome in Schnitzler’s syndrome publication-title: Rheumatol Oxf Engl doi: 10.1093/rheumatology/kep222 contributor: fullname: Pizzirani – volume: 8 start-page: e59327 year: 2013 ident: B13 article-title: Effect of in vitro and in vivo anakinra on cytokines production in Schnitzler syndrome publication-title: PloS One doi: 10.1371/journal.pone.0059327 contributor: fullname: Launay – volume: 20 year: 2009 ident: B21 article-title: Free circulating interleukin-18 is increased in Schnitzler syndrome: a new autoinflammatory disease publication-title: Eur Cytokine Netw doi: 10.1684/ecn.2009.0164 contributor: fullname: Migliorini – volume: 68 year: 2013 ident: B2 article-title: Schnitzler’s syndrome: diagnosis, treatment, and follow-up publication-title: Allergy doi: 10.1111/all.12129 contributor: fullname: Simon – volume: 121 year: 2008 ident: B12 article-title: IL-1 blockade in Schnitzler syndrome: ex vivo findings correlate with clinical remission publication-title: J Allergy Clin Immunol doi: 10.1016/j.jaci.2007.09.021 contributor: fullname: Ryan |
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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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