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VASCULITIS 2011 Pag Both Th2 and Th17 responses are involved in the pathogenesis of Churg-Strauss syndrome B. Jakiela, M. Sanak, W. Szczeklik, B. Sokolowska, H. Plutecka, L. Mastalerz, J. Musial, A. Szczeklik Department of Medicine, ABSTRACT Introduction Jagiellonian University Medical College, Objectives. Churg-Strauss syndrome Churg-Strauss syndrome (CSS) is char- Krakow, Poland. (CSS) is a rare systemic vasculitis as- acterised by asthma, necrotising vascu- Bogdan Jakiela, MD, PhD sociated with eosinophilia and granu- litis, peripheral blood and tissue eosi- Marek Sanak, MD, PhD loma formation. The contribution of nophilia, and granuloma formation (1- Wojciech Szczeklik, MD, PhD in-dividual T-helper cell lineages in 3). Histological lesions typical for CSS Barbara Sokolowska, MD, PhD Hanna Plutecka, PhD pathogenesis of CSS is unknown. We constitute of small-vessel vasculitis with Lucyna Mastalerz, MD, PhD hypothesised that in CSS an imbalance adjacent eosinophil rich infiltrates (4). Jacek Musial, MD, PhD of major effector T-cell subpopulations The mechanism of tissue eosinophil ac- Andrzej Szczeklik, MD, PhD takes place, and is further influenced cumulation has not been fully explained, This study was supported by grants from by the mode of treatment. though it is likely a consequence of T- The Ministry of Science and High Methods. We investigated the immu- helper (Th)2 mediated release of IL-5 Education as well as by The Foundation nophenotype, cytokine production and and eosinophil specific chemokines (5, for Development of Polish Pharmacy and transcriptome profile in peripheral 6). Nonetheless, it does not fully explain Medicine. blood lymphocytes (PBL) from 19 pa- the mechanisms leading to vasculitis or Reprints are not available from the authors. tients with stable CSS (10 were treated autoimmunisation. Please address correspondence to: with glucocorticoids alone (CSS/GC), 9 The classical view of Th2 and Th1 adap- Andrzej Szczeklik, MD, PhD, with steroids and other immunosuppres- tive immune responses has been recent- Department of Medicine, Jagiellonian University Medical College, sive drugs (CSS/IS)), and 13 healthy ly challenged by the discovery of Th17 ul. Skawinska 8, controls. Furthermore, serum IL-5 and cells, which differentiate from naïve T 31-066 Krakow, Poland. CCR4-active chemokines (CCL17, cells upon stimulation with mediators E-mail: [email protected] CCL22) were measured in six patients of innate immunity, and produce large Received on June 25, 2010; accepted in with active disease and upon remission. amounts of potent proinflammatory cy- revised form on September 13, 2010. Results. All CSS patients had decreased tokines IL-17A, IL-17F and IL-22 (7, 8). Clin Exp Rheumatol 2011; 29 (Suppl. 64): percentage of FoxP3+ regulatory T This picture is even more complicated, S23-S34. cells. In the CSS/GC group we found an as the function of effector T-helper cells, © Copyright CLINICAL AND increase in the Th17/Treg ratio and up- apart from their reciprocal interactions, EXPERIMENTAL RHEUMATOLOGY 2011. regulation of both Th2 and Th17 mark- is also controlled by regulatory T-lym- ers as evidenced by (1) over expression phocytes (Treg), secreting anti-inflam- Key words: Churg-Strauss syndrome, of Th2-related genes (GATA3, STAT6) matory TGF-β and IL-10 (9). T helper cells, Th2 cells, Th17 cells, in PBL, (2) elevated concentrations It has been established that sustained CCR4-active chemokines, of serum IL-5 and CCL17, and (3) a activation of effector T-cell responses, immunosuppressive treatment concomitant increase in the number of while meeting defective suppressory Th17 cells, and secretion of IL-17A by mechanisms, can drive the onset of al- stimulated PBL. The level of CCR4-ac- lergy, autoimmunity or other chronic tive chemokines was increased in active- inflammatory diseases. Similar dys- CSS, and correlated with blood eosino- regulation could be responsible for the philia. The combined treatment with development of CSS (1, 3). Indeed, a steroids and other immunosuppressive recently published study described the drugs was associated with a significant imbalance between Th17 lymphocytes decrease in both Th2-related chemo- and regulatory T cells during active kines and the number of Th17 cells. phase of the disease (10). The contribu- Conclusion. Our results indicate that tion of Th17 cells to the eosinophilic both Th2 and Th17 lineages are in- inflammation is still not well under- volved in the pathogenesis of CSS, stood. Furthermore, not all CSS pa- while CCR4-active chemokines con- tients express high levels of IL-5 (11). tribute to eosinophilia in the active dis- Additionally, a proportion of CSS pa- ease. These phenomena are down regu- tients experience disease flares despite Competing interests: none declared. lated by immunosuppressive therapy. steroid treatment, and little is known S-23 Th2 and Th 17 cells in Churg-Strauss syndrome / B. Jakiela et al. whether Th17 cells or other mediators and intracellulary stained with FITC- (0.7μg/mL) for 5 or 48 hours. Culture could drive eosinophilia in these cas- anti-FoxP3 (eBiosciences, San Diego, supernatants were frozen for cytokine es. Therefore, in the current study, we CA). Samples were washed with PBS measurements. Total RNA was isolated aimed to analyse functional subsets of or Perm/Wash buffer (BD Biosciences) from pelleted cells with Total RNA Iso- CD4+ lymphocytes, expression of T- and analysed by flow cytometry (Coul- lation Kit (A&A Biotechnology, Gdy- helper cell genes, and the profile of se- ter EPICS XL, Beckman Coulter, Full- nia, Poland) and reverse transcribed creted cytokines in patients with CSS. erton, CA). Data were presented as the (HC Reverse Transcription KIT, Ap- We also evaluated the impact of immu- percentage of the marker-specific frac- plied Biosystems, Foster City, CA). nosuppressive therapy by comparing tion of lymphocytes in comparison to Relative expression of mRNA was patients treated only with steroids with the relevant isotype controls. Treg cells quantified with real time-PCR using those receiving additional immunosup- were recognised as CD4+ cells express- target specific primers (TIB Molbiol, pressive agents. ing CD25high and FoxP3+ protein. Poznan, Poland; see Supplementary Table S1) and SYBR-Green I (Amres- Methods Stimulation of peripheral co, Solon, OH), using iCycler System Patients and study design blood lymphocytes and detection (BioRad, Hercules, CA). Data were Nineteen patients with confirmed di- of intracellular cytokines normalised to the mean CT (threshold agnosis of CSS (fulfilling at least 4 Frozen PBL were thawed, washed in cycle) value of GAPDH and ACTB, criteria of the American College of RPMI-1640 (10% ABS) and pre-cul- and relative quantities (RQ) of indi- Rheumatology (2)) were studied. The tured for 2 hours (2x 106 cells per well) vidual transcripts were estimated using severity of the disease was evaluated before assessment of viability (>98% as 2-∆∆CT method (13). In volcano graphs, using the Birmingham Vasculitis Activ- verified by flow cytometry) and addi- log2 RQ values (fold change, biological ity Score (BVAS) (12). Eleven sex- and tion of stimuli. PBL were then left un- significance) are plotted against –log10 age-matched healthy non-atopic volun- treated (baseline control) or incubated p-values (statistical significance) esti- teers served as controls. The study was for 5 hours with PMA (final 50ng/mL; mated using the t-test. approved by the ethics committee of the Sigma-Aldrich) and ionomycin (0.7μg/ Jagiellonian University. Informed con- mL; Sigma-Aldrich) in the presence of Measurement of cytokine concentrations sent was obtained from all participants. brefeldin-A (10μg/mL; Sigma-Aldrich). in sera and culture supernatants Cells were washed in PBS and labelled Serum samples and culture superna- Isolation of peripheral with PerCP-CD4 (all antibodies from tants were stored at -80o C. Levels of blood lymphocytes BD Biosciences, if not otherwise stated). IL-5, IL-17A, C-C motif chemokine Peripheral blood mononuclear cells Samples were fixed and permeabilised 17 (CCL17) and C-C motif chemokine (PBMC) were isolated from EDTA- with Cytofix/Cytoperm Kit (BD Bio- 22 (CCL22) were measured by ELISA anticoagulated blood by Histopaque sciences) and double-stained for 30min (Quantikine Human ELISA Kits, R&D 1.077 (Sigma-Aldrich, St. Louis, MO) with appropriate monoclonal antibod- Systems, Minneapolis, MN) according gradient centrifugation. PBMC were ies: FITC-IFN-γ, PE-IL-4, PE-IL-17A to the manufacturer instruction. resuspended in RPMI-1640 (Sigma- (eBiosciences), and PE-IL-5. Samples Aldrich) with 5% human AB serum were washed in Perm/Wash buffer and Statistical analysis (ABS, Lonza, Basel, Switzerland) and analysed by flow cytometry. Specificity The statistical analysis was performed incubated for 30 min at 37o C in a plas- of cytokine staining was confirmed with using GraphPad Prism 4.0 (GraphPad tic flask in order to deplete monocytes. relevant isotype controls. Cytokine ex- Software, Inc., San Diego, CA). All Non-adherent PBL (peripheral blood pressing CD4+ cells were classified as data were presented as medians and lymphocytes) were cryopreserved for Th1 (producing only IFN-γ), Th2 (pro- IQR (interquartile range). The between- further experiments up to one month. ducing only IL-4), IL-4+ (all cells pro- group comparison was determined us- ducing IL-4), Th17 (producing IL-17A, ing the Mann-Whitney U- or the Fried- Lymphocyte immunophenotyping but not IFN-γ), Th1/17 (producing both man test. Differences between three PBL were washed in phosphate buff- IL-17A and IFN-γ), and IL-5+ (all cells groups were analysed with the ANOVA ered saline (PBS) and triple stained for producing IL-5). Representative dot or the Kruskal-Wallis test. Spearman’s 30 minutes with labelled monoclonal plots and gating strategy used in iden- rank sum test was used to analyse cor- antibodies (all from BD Biosciences) tification of individual phenotypes are relation coefficients. For convenience, to identify subpopulations of periph- presented in Figure 1. in correlation statistics real-time PCR eral blood lymphocytes: CD45, CD3, data were transformed according to CD4, CD8, CD45RA, CD45RO.
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