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Selected Cyclic Citrullinated Peptides Derived From Selected cyclic citrullinated peptides derived from the sequence of mutated and citrullinated vimentin (MCV) are targeted by different antibodies subclasses in patients with rheumatoid arthritis in Russian patients O. Derganova1,2, L. Martinez-Gamboa1, K. Egerer1,3, H. Bang4, G. Fredenhagen4, D. Roggenbuck5,6, I. Esaulenko2, G.R. Burmester1, T. Chernykh2, E. Feist1 1Department of Rheumatology and Clinical Immunology, Charite-Universitätsmedizin, Berlin, Germany; 2Voronezh N.N. Burdenko State Medical Academy, Voronezh, Russia; 3Labor Berlin GmbH, Berlin, Germany; 4Orgentec Diagnostika GmbH, Mainz, Germany; 5Medipan GmbH, Dahlewitz/Berlin, Germany; 6Faculty of Science, Lausitz University of Applied Sciences, Senftenberg, Germany. Abstract Objective Antibodies against citrullinated antigens (ACPA) represent one rheumatoid arthritis (RA) classification criteria. Recently, mutated and citrullinated vimentin (MCV), containing approx. 45 potentially citrullinated sites, was characterised as another modified autoantigenic RA target. Therefore, we wanted to screen, select and validate predominant MCV autoantigenic epitopes (called here MCE) as possible new diagnostic targets. Methods MCV-derived peptides with citrullinated sites were screened in healthy controls and patients. Based on this, twelve selected MCE were used for validation of ACPA isotypes (IgA/IgG/IgM) with ELISA in early RA (ERA, <12 months) and established RA (>12 months) Russian patients. Sensitivity of MCE reactivity was compared to commercially available ELISAs for anti-CCP IgG, anti-MCV IgG, and anti-RF IgA/IgM/IgG. Results Anti-MCE IgG/IgA//IgM antibodies were observed in 64.1%, 23.1%, and 15.4% ERA, and 63.9%, 26.7%, and 13.1% established RA patients, respectively. Anti-MCV IgG was present in 64.1% ERA and 55.0% RA patients. Furthermore, anti-CCP IgG and RF IgG/IgA/IgM were detectable in up to 76.9%, 71.8%, 71.8%, and 38.5% ERA, and 80.1%, 72.3%, 67.5%, and 43.0% RA patients. Anti-CCP IgG single positivity was observed in 7.7% ERA and 6.3% RA patients. Only one RA patient was anti-MCE single positive. Conclusion MCV autoantigenic epitopes were emulated by cyclic citrullinated MCV-derived peptides and recognised by all autoantibody-Ig subclasses in RA. Tested MCE were recognized more frequently by IgG as the original MCV antigen. High antibody prevalence against CCP epitopes suggests a strong CCP-linkage to RA pathogenesis in the investigated Russian cohort. Key words rheumatoid arthritis, citrullinated peptides, ACPA, modified vimentin Clinical and Experimental Rheumatology 2014; 32: 622-629. Selected MCV-derived epitopes in RA / O. Derganova et al. Olga Derganova, MD, PhD* Introduction far the CCPs have been the most specific Lorena Martinez-Gamboa* In rheumatoid arthritis (RA), as a autoantigenic structures available for the Karl Egerer, PhD chronic autoimmune disease with ero- serological diagnosis of RA (14, 15). Holger Bang, PhD sive arthritis and systemic involvement, In the past years, additional proteins Gert Fredenhagen, Dirk Roggenbuck, MD, Prof. certain post-translational protein modi- (e.g. fibrinogen, vimentin and alpha- Igor Esaulenko, MD, PhD fications can lead to the formation of au- enolase) have been identified as modi- Gerd Rüdiger Burmester, MD, Prof. toantigens (1). The so far best described fied autoantigens in the pathophysiol- Tatiana Chernykh, MD, PhD modifications include citrullination and ogy of RA. Nowadays these different Eugen Feist, MD mutation of targeted proteins such as humoral autoimmune responses, in- *These authors contributed equally vimentin, fibrinogen, collagen type cluding abs to CCP, are summarised to this study. 2, and alpha-enolase (2-6). Recently, as ACPA. These abs provide superior Please address correspondence proteins with homocitrullin residues (a specificity compared to RF, and also and reprint requests to: carbamylated lysine residue) have also contribute to the prediction of course Eugen Feist, MD, been described as autoantigens in pa- and outcome of disease (16). The sen- Charité Universitätsmedizin Berlin, Department of Rheumatology tients with RA (7). In this context, rab- sitivity of ACPA in the diagnosis of RA and Clinical Rheumatology, bits immunised with homocitrullinated is 70-80%, with a very high specificity Chariteplatz 1, albumin generated antibodies strongly of more than 90% (15). Importantly, the 10117 Berlin, Germany. cross react with commercial cyclic cit- sensitivity of anti-CCP IgG for patients E-mail: [email protected] rullinated peptide (CCP) but weakly with early RA (ERA) is also high, with Received on July 5, 2013; accepted in with mutated citrullinated vimentin approximately 60% (17, 18). revised form on January 22, 2014. (MCV). It has been shown that protein Recently, MCV was isolated from © Copyright CLINICAL AND citrullination could be influenced by synovial fluid of patients with RA and EXPERIMENTAL RHEUMATOLOGY 2014. environmental factors such as smoking characterised as a new promising au- and that it is closely linked to a genetic toantigen (6). Anti-MCV abs as well as background of the shared epitope (8). few other ACPAs, including abs to third Thus, multiple coincidental and cross- generation CCP, are now used for diag- linked factors are involved in the patho- nostic purposes in the clinic (19). In this genesis of RA leading to the specific study, we have identified and selected autoimmune response observed. antigenic epitopes of MCV (MCE) to Early diagnosis of RA is essential but generate cyclic peptides thereof. These often hindered by a slow onset of unspe- selected antigens were used for char- cific symptoms such as fatigue, loss of acterisation of autoantibody immuno- appetite, weakness, morning stiffness, globulin (Ig) subclass reactivities in arthralgias, and mono- or oligoarthritis, comparison to standard anti-MCV, anti- which can be also seen in many other CCP, and RF assays in RA patients. diseases. Therefore, to improve early diagnosis of RA, new classification cri- Methods teria have recently been developed (9, Patients and controls 10). Considering the relative weight of For standardisation and validation the different available diagnostic pa- of the self-developed ELISA test for rameters, specific laboratory markers, evaluation of reactivity against selected namely seropositivity for rheumatoid MCV peptides, samples from healthy factor (RF) and/or anti-citrullinated controls (n=437, mean age 38 years ± protein antibodies (ACPA), strongly standard deviation (SD) = 13.5 years) contribute to the early identification of were tested. Furthermore, samples from patients with RA (11). individuals with different diseases (e.g. Competing interests: For detection of citrullin-specific anti- rheumatoid arthritis, n=147; arthral- H. Bang and G. Fredenhagen are bodies (abs), anti-CCP assays with dif- gia, n=10; Sjögren’s syndrome, n=10; employees of Orgentec Diagnostika ferent performances are used as a stand- systemic lupus erythematosus (SLE), GmbH, Mainz, Germany; ard worldwide (12). In this context, n=23; polymyalgia, n=1; psoriasis ar- D. Roggenbuck is employee of Medipan the employed citrullinated peptides are thritis, n=28; reactive arthritis, n=5; GmbH, Dahlewitz/Berlin, Germany; artificial and arranged in a cyclic struc- spondylarthritis, n=4; spondylitis anky- the other co-authors have declared no ture. Furthermore, the sequence of CCP losans (Morbus Bechterew), n=1) were competing interests. This work was not supported by any used for the first generation test is de- collected and included for analysis as external financial sources. rived from filaggrine, and it has not been disease controls. In order to examine Test kits were kindly provided by shown that this antigen is expressed in if anti-MCE are detected in infectious Orgentec and Medipan. the synovial tissue (13). Nevertheless, so diseases, additional individuals with 623 Selected MCV-derived epitopes in RA / O. Derganova et al. hepatitis C virus infection (anti-HCV Table I. Clinical characteristics of Russian patients with RA. positive, n=31) were tested by ELISA Clinical characteristics ERA Established RA for anti-MCE (Orgentec) and anti-CCP (n=39) n=191) (Medipan). For further validation and evaluation of autoantibody reactivity Activity of disease (DAS 28 ESR) remission (DAS28<2.6) 0 1 (0.5%) against cyclic epitopes of MCV, we in- low (2.6<DAS28<3.2) 5 (12.8%) 22 (11.5%) vestigated serum samples from a cohort moderate (3.2<DAS28≤5.1) 32 (82.1%) 140 (73.3%) of Russian patients with RA (n=230, high (DAS28>5.1) 2 (5.1%) 28 (14.7%) mean age ± SD= 52.06±12.07 years, X-ray / Steinbroker‘s stage female:male=4:1) fulfilling the 2010 re- Stage I 8 (20.5%) 20 (10.5%) Stage II 28 (71%) 110 (57.9%) vised criteria of the American College of Stage III 2 (5.1%) 51 (26.7%) Rheumatology (ACR) and the European Stage IV 0 10 (5.2%) League Against Rheumatism (EULAR) RA Functional class (9, 10). Patients were classified accord- Class I 5 (12.8%) 12 (6.3%) ing to the duration of disease as ERA Class II 34 (87.2%) 127 (66.5%) Class III 0 49 (25.7%) (<12 months; n=39, mean age ± SD= Class IV 0 3 (1.6%) 47.33±12.22 years, female:male=3:1) or established RA (>12 months; n=191 Summary of clinical characteristics of Russian patients with early RA (ERA) and established RA ac- cording to DAS28 ESR, radiographic stage by Steinbroker’s method, and functional class by ACR mean age ± SD=53.03±11.84 years, revised criteria for classification of functional status in RA. Given are absolute patients’ numbers and female:male=5:1). Clinical characterisa- percentages (in brackets) from each group. (From one ERA patient, there were no data available regard- tion of patients was performed with a dis- ing x-ray status classification) ease activity score using 28 joint counts (DAS28 ESR), radiographic stage ac- (Orgentec Diagnostika GmbH, Mainz, with 1 μg/ml streptavidin (Perbio Sci- cording to Steinbrocker, and functional Germany). Measurement of RF IgM ence) in phosphate-buffered saline class according to the ACR revised cri- was confirmed by using a second ELISA (PBS, pH=7.6).
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