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1 Cytokine 56 (211) Contents lists available at SciVerse ScienceDirect Cytokine journal homepage: www. elsevier. com/ locate/ is sn/ Macrophage Colony Stimulating Factor and Monocyte Chemoattractant Protein 2 are elevated in intrinsic tics Rana Dajani a,, Esraa Al-Haj Ali a, Basem Dajani b a Department of Biology and Biotechnology, Hashemite University, Zarqa, Jordan b Jordan Allergy Institute, Amman, Jordan a r t i c l e i n f o a b s t r a c t Article history: Received 28 February 211 Received in revised form 9 July 211 Accepted 3 August 211 Available online 25 September 211 Keywords: Chemokines Cytokines Intrinsic Macrophage Colony Stimulating Factor Monocyte Chemoattractant Protein Background: Intrinsic, etiology unknown, occurs later in life, mostly in females. It is associated with nasal polyps and massive eosinopillic infiltration of the respiratory mucous membrane, aspirin intolerance and steroid dependence. The aim of the study was to determine the cytokine and chemokine profile in sera of intrinsic tics and control subjects. Methods: Blood was taken from 1 intrinsic tic female and 12 control female subjects. Expression profile of 42 different cytokines and chemokines were measured using a microarray composed of antibodies against the cytokines and chemokines. Complete blood count and C-reactive protein were measured, to assess the state of inflammation in both groups. Results: We have identified Macrophage Colony Stimulating Factor, a proinflammatory cytokine and Monocyte Chemoattractant Protein 2, a CC chemokine as having significantly higher expression levels in intrinsic tic subjects compared to controls ( ± SEM Signal intensity) versus ( ± 28.9 SEM Signal intensity), p=.36 and (397.7 ± SEM Signal intensity) versus ( ± SEM Signal intensity), p=.36, respectively. There were no significant differences in the other cytokines and chemokines measured nor were there any differences in the inflammatory measurements between the two groups except for eosinophil counts, the hall mark of intrinsic. Conclusion: Macrophage Colony Stimulating Factor and Monocyte Chemoattractant Protein are elevated in sera of intrinsic tics compared to normal controls. These cytokines may have a critical role in the inflammatory pathology of intrinsic. Ó 211 Elsevier Ltd. All rights reserved. 1. Introduction Asthma is a complex; inflammatory disease of the lungs characterized by reversible airway obstruction, chronic airway inflammation, and airway hyperresponsiveness [1,2]. Asthma is one of the most common chronic diseases in the world, around million people in the world have, and there may be an additional 1 million persons with by 225 [3]. Asthma is commonly divided into two types: extrinsic which is more common and is IgE mediated and intrinsic [4]. Intrinsic usually occurs in older individuals with preponderance in females. They have onset symptoms in later life and have no history of IgE dependent hypersensitivity [5,6]. Intrinsic is associated with nasal polyps and massive eosinopillic infiltration of the Abbreviations: BMI, Body mass index; CBC, Complete blood count; CRP,C-reactive protein; EGF, Epidermal growth factor; ENA-78, Epithelial neutrophil activating protein; FGF, Fibroblast growth factor; GCSF, Granulocyte Colony Stimulating Factor; GM-CSF, Granulocyte-macrophage Colony Stimulating Factor; GRO, Growth regulated oncogene; GRO-a, Growth regulated peptide a; HASMC, Human airway smooth-muscle cells; I-39, Inflammatory chemokine-39; IFN-c, Interferon gamma; IgA, Immunoglobulin A; IgE, Immunoglobulin E; IgG, Immunoglobulin G; IL-1, Interleukin1; IL-2, Interleukin 2; IL-3, Interleukin 3; IL-4, Interleukin 4; IL-5, Interleukin 5; IL-6, Interleukin 6; IL-7, Interleukin 7; IL-8, Interleukin 8; IL-9, Interleukin 9; IL-1, Interleukin 1; IL-11, Interleukin 11; IL-12, Interleukin 12; IL-12p4, Interleukin 8; IL-13, Interleukin 13; IL-15, Interleukin 15; IL-16, Interleukin 16; IL-17, Interleukin 17; IL-18, Interleukin 18; IP-1, Interferon-gamma-induced protein; LAK, Lymphokine activated killer; MCH, Mean corpuscular hemoglobin; MCHC, Mean corpuscular hemoglobin concentration; MCP-1, Monocyte Chemoattractant Protein-1; MCP-2, Monocyte Chemoattractant Protein-2; MCP-3, Monocyte Chemoattractant Protein-3; MCSF, Macrophage Colony Stimulating Factor; MCV, Mean corpuscular volume; MDC, Macrophage derived chemokines; MIG, Monokines induced by gamma interferon; MIP, Macrophage inhibitory protein; NK cell, Natural Killer cell; PAE, Platelet activating factor; PDGF, Platelet derived growth factor; RANTES, Regulated on activation normal T cell expressed and secreted; RBC, Red blood cell; SDF-1, Stromal cell-derived factor1; SCF, Sertoli cell factor; TARC, Thymus and activation regulated chemokines; TH1, T helper1; TH2, T helper2; TGF-b, Transforming growth factor beta; TNF-a, Tumor necrosis factor alpha; VCAM-1, Vascular cell adhesion molecule-1; VEGF, Vascular endothelial growth factor; WBC, White blood cell. Corresponding author. Address: Department of Biology and biotechnology, Hashemite University, P.O. Box 15459, Zarqa Jordan 13133, Jordan. Tel.: ; fax: addresses: rdajani@hu.edu.jo (R. Dajani), noor.dajani@hotmail.com (B. Dajani) /$ - see front matter Ó 211 Elsevier Ltd. All rights reserved. doi:1.116/j.cyto
2 642 R. Dajani et al. / Cytokine 56 (211) respiratory mucous membrane [7]. Patients have negative skin prick test for all aeroallergens, serum levels of immunoglobulin E are within the normal range [8,9], aspirin intolerance and steroid dependency are common [6]. Thus, the intrinsic form of appears to have unique inflammatory mechanisms that differ from those playing a role in the extrinsic form. There is paucity of research dealing with inflammatory mechanisms unique to intrinsic. The reason may be because there is no animal model for intrinsic [1]. The pathogenesis of intrinsic is presently thought to be caused by unknown reasons [7]. The inflammatory mechanism in intrinsic, the role and function of macrophages and chemokines that mobilize and recruit eosinophils have not been thoroughly investigated [5]. The aim of the study was to determine the cytokine and chemokine profile in sera of intrinsic tics and control subjects. 2. Methods and materials 2.1. Human subject description and sample collection This study was approved by the Hashemite University IRB committee (3/26). The Hashemite IRB committee follows the Helsinki recommendations. Intrinsic tic women and control women were invited by telephone call to give a blood sample. Informed consent was obtained for participation in the study. All samples of the study group and the controls were taken between 1 and 12 AM in the same lab and by the same technician. The study was carried out from August 28 to June 29. The tic patients and controls were referred by the Jordan Allergy Institute in Amman, Jordan. Both groups were identical in being: (1). Non diabetic to avoid complication from other inflammatory diseases (2). Females since it has been shown that intrinsic occurs in women later in life (3). Between 2 and 4 years of age (4). Not pregnant (5). Off of any oral medication for two weeks prior to taking of sample (6). Non smokers. In addition to the above, the study group were tics suffering from airway obstruction, wheezing and cough, with 15% reversibility of pulmonary function tests and having negative skin test to 5 common inhalant allergen (Stallergenes S.A., France) by skin prick test supplementary Table 1. All patients take inhaled corticosteroids and beta agonists to control their disease. It is important to note that medications administered were similar in all patients. Ethical consideration prevented us from stopping the medication prior to taking of the sample. The presence of nasal polyps and history of aspirin intolerance were identified in the study group. The body mass index (BMI) was assessed for both groups. Sample collection: 12 ml of peripheral blood samples were taken from intrinsic tic and control women in a clinical laboratory. Complete blood count (CBC) and C-reactive protein (CRP) were measured in the clinical lab according to standard procedure. 7 ml of blood were put in a plain tube and centrifuged at 5 rpm for 5 min after that 5 ml of serum was obtained, transferred to 5 eppendorf tubes each one contained 1 ml of serum and stored at 2 C Cytokine determination The cytokines from 22 samples were measured using RayBio Ò Human Cytokine Antibody Array III (Ray Biotech, Norcross, GA) according to the manufacturer s instructions. The cytokine antibody array is based on the sandwich enzyme-linked immunosorbent assay (ELISA) method for detecting proteins. This array allows for semiquantitative analysis. Actual concentrations are not determined. The array can detect 42 cytokines; the cytokines that will be quantified are listed below: ENA-78, GCSF, GM-CSF, GRO, GRO-a, I-39, IL-1a, IL-1B, IL-2, IL- 3, IL-4, IL-5, IL-6, IL-7, IL-8, IL-1, IL-12p4p7, IL-13, IL-15, IFN-g, MCP-1, MCP-2, MCP-3, MCSF, MDC, MIG, MIP-1d, RANTES, SCF, SDF-1, TARC, TGF-B1, TNFa, TNFB, EGF, IGF-1, Angiogenin, Oncostatin M, Thromboietin, VEGF, PDGF BB, Leptin. The intensities of signals were quantified by densitometer (PTW-Densix, Germany) and positive controls were used to normalize the results from different arrays according to the formula: normalized signal intensity of particular spot = signal intensity of particular spot x (postive1/ positive signal intensity sample in particular spot). positive1: The positive control of first sample. Detection limits for each mediator is in supplementary Table Statistical analysis Clinical data were entered using Excel software running with windows XP23. Densitometric data were entered and normalized with Array Analysis Tools 3 software provided by manufacturer RayBio Ò Human Cytokine Antibody Array III (Ray Biotech, Norcross, GA). Data were analyzed using SPSS software version 12. Differences between the means of the intrinsic tic group and control group were tested using Independent t-test. The differences were considered statistically significant at p <.5. Data are stated as means ± mean of standard error (SEM). 3. Theory The etiology of intrinsic is unknown. We theorize that intrinsic involves a unique inflammatory mechanism that may be reflected in a unique cytokine and chemokine profile. We propose to look at the cytokine and chemokine profile in sera of intrinsic tics for changes in levels of expression compared to controls. 4. Results A total of 1 intrinsic tic women and a total of 12 control women were included in this study. Sixty percent of patients had nasal polyps, and 5% of patients were aspirin intolerant. BMI was not significantly different between control and intrinsic tic groups (p >.5). All clinical features are summarized for the two groups in Table CBC and CRP measurement CBC and CRP measurements for the intrinsic tic group and the control group are summarized in Table 2. The data indicate that hemoglobin, Hematocrit, MCV, MCH, MCHC measurements were not significantly different between control and intrinsic tic groups (p >.5). In addition the data demonstrate that red blood cell counts and platelet counts displayed no significant differences between the two groups (p >.5). Measurement of white blood cell count and differential count specify that the number of eosinophils in the intrinsic tic group is significantly higher than that in the control group (415 ± 14 vs. 17 ± 26, p =.2). In contrast there were no significant differences in white blood cells, neutrophils, monocytes, lymphocytes between both groups (p >.5). CRP measurements were negative for both groups (<6 mg/l) Table Cytokines determination In an effort to screen and identify cytokines and chemokines that may be associated with intrinsic, we used a microarray composed of antibodies against 42 different cytokines and
3 R. Dajani et al. / Cytokine 56 (211) chemokines. We measured cytokines and chemokines expressed by each group using serum separated from blood samples of intrinsic tic and control groups as described in the Methods section. The signal intensity for each cytokine and chemokine was quantified by densitometry (Fig. 1) Determination of lymphokines Expression levels of lymphokines are presented in (Fig. 2). Data in this figure demonstrates that there are no significant differences in the expression levels of IL-2, IL-3, IL-4, IL-5, IL-7, IL-13 and IL-15 lymphokines between both groups (p >.5), but their expression levels were greater in the intrinsic tic group. Exact p values are in Table Determination of proinflammatory cytokines The data in (Fig. 3) confirmed that the expression level of MCSF proinflammatory cytokine was significantly higher in the intrinsic tic group ( ± signal intensity) compared to the control group ( ± 28.9 signal intensity), (p =.36). While the expression levels of IL-1a, IL-1b, TNF-a, TNF-b, SCF, GCSF, GM-CSF showed no significant differences between intrinsic tic and control groups (P >.5). Exact p values are in Table Determination of growth factors Table 1 Clinical features of intrinsic tic and control groups. Group Age BMI = w/h2 Nasal polyps Intrinsic No No Intrinsic Yes No Intrinsic 4 24 Yes No Intrinsic Yes Yes Intrinsic Yes Yes Intrinsic No No Intrinsic No No Intrinsic Yes Yes Intrinsic Yes Yes Intrinsic No Yes Mean + SEM = 32.3 ± ± No No No No No No No No No No No No No No No No No No No No No No No No Mean + SEM = 23.2 ± ± 1.3 Aspirin intolerance Values are expressed as mean ± SEM, tic group n = 1 and control group n = 12. The data in (Fig. 4) show that expression levels of growth factors, EGF, IGF-1, VGEF, PDGF-BB and TGF-beta1 were not significantly different between intrinsic tic and control groups (p >.5). Exact p values are in Table Determination of inhibitory cytokines The data in (Fig. 5) indicate that expression levels of inhibitory cytokines IL-1, IL-12p4, TNF-gamma were not significantly different between intrinsic tic and control groups (p >.5). Exact p values are in Table Determination of CXC chemokines Expression levels of CXC chemokines are presented in (Fig. 6). Expression levels of IL-8, MIG, SDF-1, GRO, GRO-alpha and ENA- 78 display no significant differences in expression levels between intrinsic tic and control groups (p >.5). Exact p values are in Table Determination of CC chemokines The data in (Fig. 7) revealed that CC chemokine, MCP-2 had a significant higher expression level in intrinsic tic (397.7 ± signal intensity) than control ( ± signal intensity), (p =.36). In contrast MCP-1, MCP-3, I-39, MAD, MIP delta, RANTES and TARC had no significant differences in their expression levels between intrinsic tic and control groups (p >.5). Expression levels of angiogenin, oncostatin M, thrombopoietin, leptin were not significantly different between intrinsic tic and control groups (p >.5) (Fig. 8). Exact p values are in Table Discussion Nasal polyps, aspirin intolerance and eosinopillic infiltration of the respiratory mucous membranes are frequently seen in patients with intrinsic in addition to the hallmarks of the disease; reversible airway obstruction and airway hyperresponsivness. The etiology of intrinsic is not known. Progress in the study of intrinsic has been limited and new insights into the etiology of this apparent phenotype of are few. Unfortunately, little pathophysiological data are available that clearly delineate non-atopic [11]. Many theories have been suggested. Persistent respiratory infections may play a central role in the development of intrinsic [12]. Other theories proposed are dependent on epidemiological studies which indicate that adultonset may be initiated by stress (anxiety and depression), obesity and menopause, the Multi-Hit Endocrine Model of Adult- Onset Asthma [13]. The BMI measured in our intrinsic tic patients did not support the obesity part of this model Table 1. There are conflicting studies concerning the association between menstrual cycle and [14]. It would be interesting to study the effect of the menstrual cycle on the cytokine profile of intrinsic tic patients. Superantigens may also be important in intrinsic as airway epithelial cells may be colonized by Staphylococci and other superantigen-producing microbes [15]. An alternative view is that an abnormality in the airway smooth muscle cell, which is capable of producing inflammatory, immunological and growth factors as well as molecules, which facilitate interaction with inflammatory cells, is the primary event. Evidence is rapidly accumulating that the smooth muscle is abnormal, in that it proliferates faster, produces more chemokines and cytokines as well as a different profile of extracellular matrix proteins than its non-tic counterpart. Candidates such as eotaxin and IP-1 have been implicated [16].
4 644 R. Dajani et al. / Cytokine 56 (211) Table 2 CBC and CRP measurement of intrinsic tic and control groups. CBC Measurement Mean ± SEM p value (n = 12) Intrinsic (n = 1) Hemoglobin (g/dl) 13.5 ± ± Hematocrit (%) 41 ±.3 4 ±.3.4 RBC (ll 1 ) ± ± WBC (ll 1 ) 7775 ± ± MCV (fl) ± ± MCH (pg/cell) ± ± MCHC (ghb/dl) ± ± Platelets (ll 1 ) 2895 ± ± Neutrophils (ll 1 ) 4661 ± ± Monocytes (ll 1 ) 412 ± 4 45 ± 42.5 Lymphocytes (ll 1 ) 2763 ± ± Eosinophils (ll 1 ) 17 ± ± 14.2 CRP (mg/l) Negative (<6) Negative (<6) Values are expressed as mean ± SEM. Fig. 1. A, Panel representing the pattern of cytokine and chemokine expression for intrinsic tic patients, B, Panel representing the pattern of cytokine and chemokine expression for control individuals, C, The map of RayBio Ò Human Cytokine Antibody Array III. In our results we found elevated levels of two cytokines, MCP-2 and MCSF in intrinsic tics compared to normal controls. While there were no significant differences in the serum levels of all the other cytokines measured compared to controls. In spite of the small sample size, the size of the sample was statistically considered in assessing the significance of the results. M-CSF is responsible for the survival, proliferation, differentiation and activation of macrophages at various stages of their development. It is produced by endothelial cells, fibroblasts, and mononuclear phagocytes. Activation of monocytes/macrophages by MCSF is likely to be an important part of the immune and inflammatory response. Prior studies demonstrated that M-CSF produced by human-joint tissue cells (chondrocytes, synovial fibroblasts) in vitro in response to the inflammatory cytokines, IL-1 and TNF-a may play a key role in chronic inflammatory autoimmune diseases, such as rheumatoid arthritis check reference if cell from patients [17]. Thus increased levels of MCSF in the intrinsic tic sera may indicate a similar inflammatory pathway in the pathogenesis of these patients. MCP-2 is a chemoattractant for eosinophils and basophil. Also MCP-2 induces T cell migration. MCP-2 activates basophils and causes histamine and leukotriene secretion independently of IgE. Prior studies have demonstrated that MCP-1 is detectable in a variety of inflammatory diseases but so far little is known about the
5 R. Dajani et al. / Cytokine 56 (211) IL-2 IL-3 IL-4 IL-5 IL-7 IL-13 IL-15 Intrinsic Fig. 2. Expression levels of lymphokines in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p >.5) Intrinsic IL-1α IL-1β L-6 TNF-α TNF-β SCF MCSF GCSF GM-CSF Fig. 3. Expression levels of proinflammatory cytokines in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p <.5). * Table 3 Cytokine levels in intrinsic tics and control groups. Cytokines Mean ± SEM (signal intensity) t-test (p) Intrinsic ENA ± ± GCSF ± ± GM-CSF ± ± GRO ± ± GRO-a ± ± I ± ± IL-1a ± ± IL-1B 257 ± ± IL ± ± IL ± ± IL ± ± IL ± ± IL ± ± IL ± ± IL ± ± IL ± ± IL-12p ± ± IL ± ± IL ± ± TNF-gamma ± ± MCP ± ± MCP ± ± MCP ± ± MCSF ± ± MDC ± ± MIG ± ± MIP-1delta ± ± RANTES ± ± SCF ± ± SDF ± ± TARC ± ± TGF-beta ± ± TNF-a ± ± TNF-b ± ± EGF ± ± IGF ± ± Angiogenin ± ± Oncostatin M ± ± TPO ± ± VEGF ± ± PDGF-BB ± ± Leptin ± ± Values are expressed as mean ± SEM, tic group n = 1 and control group n = 12. role of MCP-2 in the pathology of inflammatory diseases. In addition MCP-2 levels were significantly high in synovial fluids of EGF IGF-1 VGEF PDGF-BB TGF- β1 Intrinsic Fig. 4. Expression levels of growth factors in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p >.5) IL-1 IL-12-P4 TNF-γ Intrinsic Fig. 5. Expression levels of inhibitory cytokines in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p >.5). rheumatoid arthritic patients [18]. These increased levels of MCP-2 in the intrinsic tic sera suggest that they may play a role in macrophage, eosinophil and basophil recruitment and activation as well as contribute to the inflammatory pathology of
6 646 R. Dajani et al. / Cytokine 56 (211) IL-8 MIG SDF-1 ENA-78 GRO GRO-α Intrinsic Fig. 6. Expression levels of CXC chemokines in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p >.5). The above findings may suggest a common mechanism that links intrinsic with some autoimmune diseases such as rheumatoid arthritis. Recently, in chronic idiopathic urticaria, a significant number of patients have been shown to have IgG auto antibodies [19]. Lacking a definitive animal model for intrinsic, observations in IgE-deficient mice showed that bronchial inflammation is undiminished and it is possible that these mice produce an IgG response. As a result, mast cells sensitized by IgG antibodies might have a role in IgE-deficient mice inflammation, by secreting mediators and cytokines. The fact that eosinophil associated inflammation occurs in this model bears witness [2]. All in all evidence cited above of increased MCSF and MCP2 in intrinsic tics compared to their normal counterparts in this study may open a new venue in the clarification of the etiology and pathophysiology of intrinsic. Both link to an autoimmune disease through MCSF stimulated mechanisms and MCP2 recruitment of eosinophils. 6. Conclusions * Intrinsic In conclusion, MCSF and MCP-2 were elevated in sera of intrinsic tic patients compared to normal controls. These findings provide a promising future direction for research regarding intrinsic including the possible identification of local expression of MCSF and MCP-2 in lungs airways and the role of basophils and monocytes in the inflammatory response as well as correlation with severity of the disease. Conflict of interest All authors declare that they do not have any conflict of interest. 1 I-39 MCP-1 MCP-2 MCP-3 MDC MIP-1δ RANTES TARC Fig. 7. Expression levels of CC chemokines in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p <.5) Angiogenin Oncostatin M Thrombopoitin Leptin Intrinsic Fig. 8. Expression levels of angiogenin, Oncostatin M, Thrombopoitin and Leptin in control and intrinsic tic groups. (Values are expressed as mean ± SEM, p >.5). intrinsic. These results may push us to theorize that intrinsic has features common to some autoimmune diseases. We realize that such a statement is an extrapolation yet since there is paucity of research in this area we hope that this will stimulate further research. Acknowledgements This research was funded by the Hashemite University. The Hashemite University played no role in study design, in the collection, analysis and interpretation of data, in the writing of the report and in the decision to submit the paper for publication. Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:1.116/j.cyto References [1] Wills-Karp M. Immunologic basis of antigen-induced airway hyperresponsiveness. Annu Rev Immunol 1999;17: [2] Cohn L, Elias JA, Chupp GL. Asthma: mechanisms of disease persistence and progression. Annu Rev Immunol 24;22: [3] Masoli M, Fabian D, Holt S, Beasley R. The global burden of : executive summary of the GINA Dissemination Committee report. Allergy 24;59: [4] Craig SAR, Bowen L. A multi-hit endocrine model of intrinsic adult-onest. Ageing Res Rev 28;7: [5] Humbert MM, Ying G, Corrigan S, Robinson CL, Durham SR. Extrinsic(atopic) and intrinsic(non-atopic):more similarities than differences. Immunol Today 1999;2: [6] Humbert M. Does intrinsic exist? Rev Mal Respir 2;17: [7] Rochat T. [Is intrinsic or non-atopic a particular disease?]. Rev Med Suisse 25;1: [8] Backer VU, Wendeboe CS. Distribution of serum IgE in children and adolescent aged 7to16 years in Copenhagen in relation to factors of importance. Allergy 1992;47: [9] Dirksen A. Clinical vs paraclinical data in allergy. Dan Med Bull 1982;29: [1] Boyce JA, Austen KF. No audible wheezing: nuggets and conundrums from mouse models. J Exp Med 25;21: [11] King MJ, Hanania NA. Asthma in the elderly: current knowledge and future directions. Curr Opin Pulm Med 21;16:55 9.
7 R. Dajani et al. / Cytokine 56 (211) [12] Dahlberg PE, Busse WW. Is intrinsic synonymous with infection? Clin Exp Allergy 29;39: [13] Atwood CS, Bowen RL. A multi-hit endocrine model of intrinsic adult-onset. Ageing Res Rev 28;7: [14] van den Berge M, Heijink HI, van Oosterhout AJ, Postma DS. The role of female sex hormones in the development and severity of allergic and non-allergic. Clin Exp Allergy 29;39: [15] Barnes P. Intrinsic : not so different from allergic but driven by superantigens? Clin Exp Allergy. 29;39: [16] Black JL, Roth M. Intrinsic : is it intrinsic to the smooth muscle? Clin Exp Allergy 29;39: [17] Schett G. Review: immune cells and mediators of inflammatory arthritis. Autoimmunity 28;41: [18] Pierer M, Rethage J, Seibl R, Lauener R, Brentano F, Wagner U, et al. Chemokine secretion of rheumatoid arthritis synovial fibroblasts stimulated by Toll-like receptor 2 ligands. J Immunol 24;172: [19] Kaplan AP, Greaves M. Pathogenesis of chronic urticaria. Clin Exp Allergy 29;39: [2] Kwon B, Lee HA, Chol GS, Ye YM, Nahm DH, Park HS. Increased IgG antibodyinduced cytotoxicity against airway epithelial cells in patients with nonallergic. J Clin Immunol 29;29:
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