SENSITIVITY AND SPECIFICITY OF ANTI-Jo-1 ANTIBODIES IN AUTOIMMUNE DISEASES WITH MYOSITIS

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1 292 ARTHRITIS & RHEUMATISM Vol. 39, No. 2, February 1996, pp , American College of Rheumatology SENSITIVITY AND SPECIFICITY OF ANTI-Jo-1 ANTIBODIES IN AUTOIMMUNE DISEASES WITH MYOSITIS DOLORES VAZQUEZ-ABAD and OMI F. ROTHFIELD Objective. To determine the sensitivity and specificity of anti-jo-1 in systemic sclerosis (SSc) patients with and without myositis. Methods. Immunoblots on HeLa nuclei were used to screen sera from 554 consecutive connective tissue disease patients. Those who had kd bands, all patients with polymyositis/derrnatomyositis (PM/DM), and a random selection of SSc, Raynaud s disease, systemic lupus erythematosus, and rheumatoid arthritis patients were also studied by anti-jo-1 enzyme-linked immunosorbent assay and by immunoblots on rabbit pooled aminoacyl-transfer R synthetase. Results. Anti-Jo-1 was present only in 8 of the 4 PM/DM patients. Conclusion. Anti-Jo-1 is specific for PM/DM. Anti-Jo- 1 antibodies are found in polymyositis/ dermatomyositis (PM/DM) patients, especially in those with lung involvement (1). Anti-Jo-1 is directed at histidyl-transfer R (tr) synthetase (Jo-1 autoantigen), which is a dimer of 5-kd subunits found in the cytoplasm (1,2). Anti-Jo-1 may be detected by double immunodiffusion, immunoblotting, and enzyme-linked immunosorbent assay (ELISA) (3) using an antigen containing Jo-1 and standard positive and negative control sera. The presence of anti-jo-1 in systemic sclerosis (SSc) patients has not been examined in large-scale studies. SSc patients frequently present with lung involvement, and, in some cases, with myositis. Therefore, in the present study, we decided to screen our large series of consecutive SSc patients for the Dr. Rothfield s work was supported by NIH grants AR and AR Dolores VAzquez-Abad, MD, Naomi F. Rothfield, MD: University of Connecticut School of Medicine, Farmington. Address reprint requests to Dolores Vhzquez-Abad, MD, Division of Rheumatic Diseases, University of Connecticut School of Medicine, 263 Farmington Ave, Farmington, CT Submitted for publication July 25, 1995; accepted in revised form September 29, presence of anti-jo-1 and compare them with other connective tissue disease patients with and without myositis. Our results show that anti-jo-1 is present in 2.% of PM/DM patients (8 of 4), and is absent from SSc patients sera, including those with PM/DM overlap and those with elevated creatine phosphokinase (CPK) levels and muscle pain, but who do not fulfill criteria for PM/DM, with or without interstitial lung fibrosis. PATIENTS AND METHODS Patients and controls. All patients and controls were seen in the Rheumatology Clinics at the University of Connecticut School of Medicine, Farmington. A total of 429 patients with SSc or Raynaud s disease with or without overlap syndromes (excluding patients with PM/DM overlap), 31 patients with rheumatoid arthritis (RA), 54 patients with systemic lupus erythematosus (SLE) who did not have Raynaud s disease or SSc, and 4 patients with PMIDM (21 PM and 19 DM), including 6 DM and 4 PM patients with Raynaud s overlap and 6 PM and 4 DM patients with SSc overlap, were studied (Table 1). All patients met the American College of Rheumatology criteria for classification (4-6), and the polymyositis group met the criteria of Bohan and Peter (7). Sera were collected from all patients and kept at -7 C. An anti-jo-1 positive control from the Centers for Disease Control and Prevention (CDC anti-jo-i) was used for all experiments. A pool of normal human serum devoid of autoantibodies (NHS) was used as a negative control (8). HeLa immunoblots. All sera were immunoblotted on HeLa cell nuclei, as previously described (8,9). Rabbit tr synthetase-enriched supernatant immunoblots (RSI). Rabbit kidney cells (LCC-RKI) were kindly provided by Drs. Deutschter and Filonenko. The LCC-RK1 were grown, harvested, washed with PBS and suspended in 2 mm HEPES-KOH buffer (ph 7.4) containing 1 mm dithiothreitol,.2 mm EDTA, 1 mm MgCI,,.4 mm phenylmethylsulfonyl fluoride, 5 mg/ml leupeptin, and 5 mg/ml cu,-macroglobulin. After 1 minutes of incubation at 4 C, lysis was achieved by 1 strokes of a Dounce homogenizer. The homogenate was supplemented with 5% volume/ volume of the same buffer containing 21% glycerol and

2 ANTI-Jo- 1 IN MY OSITIS PATIENTS 293 Table 1. Characteristics of the patients and sera studied* Myositis only Pulmonary fibrosis Myositislpulmonary kd + HeLa ELISA and RSI Diagnosis (n) (n = 5) only (n = 113) fibrosis (n = 49) blots (n = 554)t (n = 161)t SScICREST (213) RD (216) RA (31) SLE (54) PMIDM (4) Pnmary (16) Overlap with RD (1) SScICREST (1) Other CTD (4) I /54 8/4 4/16 2/ /4 4/16 2/ * ELISA = enzyme-linked immunosorbent assay; RSI = rabbit transfer R synthetase-enriched supernatant immunoblot; SSc = systemic sclerosis; CREST = calcinosis, Raynaud s phenomenon, esophageal dysmotility, sclerodactyly, telangiectasias; RD = Raynaud s disease; RA = rheumatoid arthritis; SLE = systemic lupus erythematosus: PMIDM = polymyositisldermatomyositis; CTD = connective tissue disease. t Values are the number positiveltotal number tested..495m potassium acetate, and centrifuged at 1,OOOg for 15 minutes. The supernatant (RS) was withdrawn and stored at - 2 C. RS, which are enriched for aminoacyl-tr synthetases, were used for sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) separation and for immunoblots, as previously published (1). Briefly, RS were separated on 1% SDS-PAGE under reducing conditions, and transferred to nitrocellulose paper (BioRad, Hercules, CA). After 1 hour at room temperature in PBS containing 4% bovine serum albumin, the strips were incubated with the different sera at a 1 : 1,OOO dilution in the same buffer. After 1 hour of incubation, the strips were thoroughly washed and incubated with rabbit anti-human 7, a, p, K, and A chains coupled to horseradish peroxidase (HRP; Dakopatts, Copenhagen, Denmark) for 1 hour and after thorough washes, they were developed with the ECL system (Amersham, Arlington Heights, IL), or with the KPI system (Kirkegaard & Perry, Gaithersburg, MD). Besides the human sera, a mouse monoclonal anti-rabbit arginyl-tr transferase (kindly provided by Drs. Filonenko and Deutscher) was used in the RSI blots to verify the quality of the RS blots. This strip was incubated with goat anti-mouse IgG coupled to HRP (Dakopatts) before development. All 4 sera from PM/DM patients, random samples of sera from the other groups of patients (65 of 213 SScl CREST, 25 of 216 Raynaud s disease, 2 of 31 RA, and 29 of 54 SLE patients) that includes all sera with a band at kd on HeLa immunoblots were further tested by RSI (Table 1). Tested sera included 13 of 25 SSc/CREST patients and 1 of 1 RA patient with myositis without pulmonary fibrosis, 18 of 32 SSc/CREST patients and 1 of 1 RA patient with myositis and pulmonary fibrosis, and 15 of 113 SSc/CREST patients with pulmonary fibrosis without myositis. Not all sera were so tested because of the limited supply of the purified antigen. Anti-Jo-1 ELISA. An ELISA kit with affinity-purified Jo-1 from calf thymus (Diamedix, Miami, FL) was used to screen the same sera that was tested on RSI (see above). Statistical analysis. Fisher s exact test was used to compare the prevalence of anti-jo-1 in the different groups of patients. Odds ratios were calculated to determine the relative risk of interstitial lung fibrosis in the presence or absence of anti-jo-1 in the PM/DM patients. Bayes theorem was used to calculate the sensitivity and specificity of the anti-jo-1 result by ELISA and RSI. RESULTS The CDC anti-jo-1 serum showed a distinct 5-kd band when tested by immunoblotting on extracts of HeLa cell chromosomes separated on SDS-PAGE (+ in Figure 1A). The CDC anti-jo-1 serum reacted with only a single band at 5 kd on the RSI blot (+ in Figure lb), and was positive by ELISA. The NHS was negative when tested for the presence of anti-jo-1 by all 3 methods (- in Figures 1A and B; ELISA results not shown). Fifty-five sera found to react with a band in the range of kd and 16 random sera with no bands between 45 and 55 kd were further tested for the presence of anti-jo-1 by ELISA and RSI blots. Eight of the 4 PM/DM patients had a 5-kd band on HeLa blots, and were positive for anti-jo-1 using ELISA and RSI blots (Table 1). Figure 1A shows the HeLa blots from 4 of these 8 anti-jo-1 positive patients with the distinct 5-kd band. Figure 1B shows the results of the RSI blots using a mouse monoclonal antibody to anti-rabbit arginyl-tr transferase that reacts with 6-kd, 66-kd, and 12-kd bands, and 4 of the 8 anti- Jo-1 positive sera reacting with the 5-kd band. All other sera, whether or not they reacted with a kd band, were negative for anti-jo-1 by ELISA and RSI blots. The results of the ELISA and RSI blots correlated completely. All 8 anti-jo-1 positive sera by ELISA and RSI, had a 5-kd band by HeLa chromo-

3 294 VAZQUEZ-ABAD AND ROTHFIELD A B (-) (+) MoAb H 66 5 Figure 1. Immunoblots of normal human serum negative control (-), Centers for Disease Control and Prevention anti-jo-i positive control (+), 4 anti-jo-1 positive patients (lanes M), and a mouse monoclonal anti-rabbit arginyl-transfer R transferase (MoAb), using A, extracts of HeLa nuclei and B, extracts of rabbit kidney cell supernatants. Numbers to the left are molecular weight markers (in kd); arrows show the Jo-1 band; H = histones. some blots; thus, there were no false-negative results by HeLa blots. Three of the 8 anti-jo-1 positive patients had primary PM, 1 had primary DM, 2 had Raynaud s disease and DM, 1 fulfilled criteria for RA and DM, and 1 fulfilled criteria for RA and PM. Using the Bayes theorem, the specificity and sensitivity of anti- Jo-1 for PM/DM are 1% and 2%, respectively. Six of the 8 anti-jo-1 positive patients had interstitial lung disease, compared with 1 of the 32 anti-jo-1 negative PM/DM patients (odds ratio 6.6, confidence interval between.88 and 47.37; P <.4). DISCUSSION Anti-Jo-1 is the most frequent autoantibody in PM/DM and is specific for this disease, identifying a clinical subset of patients different from those with other PM/DM-related autoantibodies (1-3). Among these other antibodies, a low percentage of patients shares an antibody with 4% of SSc patients, i.e., the PM/Scl autoantibodies that detect an 8-kd and a 1-kd band on HeLa cell nuclear blots (2). On the other hand, in SSc the 3 most frequently seen autoantibodies are anticentromere, anti-topoisomerase I, and anti-r polymerase 1 and I11 autoantibodies (1 1). These autoantibodies are specific for the SSc spectrum of diseases and identify different clinical subsets (2,ll). None of these clinical subsets is characterized by the presence of rnyositis with or without the interstitial lung fibrosis frequently found in SSc patients. In this study, we have shown that none of the 213 SSc patients had anti-jo-1. Among the 213 SSc patients studied, 57 had elevated CPK levels and muscle pain, but did not fulfill criteria for PM/DM. Their electromyograms and muscle biopsy samples were negative or were deemed unnecessary (and were not considered overlap syndrome). Of these 57 SSc patients with rnyositis, 32 had interstitial lung fibrosis. Among the 4 PM/DM patients, 1 also fulfilled criteria for SSc (PM/DM overlap with SSc), and were all negative anti-jo-l. Hence, the absence of anti-jo-1 antibodies in SSc patients is not explained by selection bias and exclusion of patients with rnyositis and/or interstitial lung fibrosis in that disease group. To confirm that these negative results were not due to a detection error in our technique, we screened our population of PM/DM patients and found 8 of 4 patients (2%) with PMDM to be positive for anti- Jo-1. This prevalence is similar to that previously reported (1). Furthermore, the association between interstitial lung disease in PMDM and anti-jo-1 positivity was similar to that previously published (1,2). Two previous studies described investigations of large series of sera from SSc patients by immunoprecipitation (12,13). In the figures published with those studies, a few sera can be seen to precipitate a

4 ANTI-Jo-1 IN MYOSITIS PATIENTS 295 protein at approximately 5 kd. Anti-Jo-1 was not specifically investigated in either study (12,13). In the report by Bernstein et al, a survey of autoantibodies in 1,11 I sera was carried out (14). Anti-Jo- I was found in 9 of 36 patients with myositis and in 1 of 161 patients with SSc by counterimmunoelectrophoresis; however, no definitions or criteria for the diagnosis of SSc or myositis were provided. An evaluation of an ELISA using purified Jo-1 included 21 SSc sera along with a large series of DM/PM patients and patients with other connective tissue diseases (15). Some of the sera were gifts to the investigators from 2 other institutions. None of the 21 SSc sera had anti-jo-1. Of the 19 patients with PM/DM overlap, 3 had anti-jo-1 (2 overlap with SSc, 1 with RA). We did not find any anti-jo-1 positive sera among 1 patients with PM/DM and SSc overlap. Perhaps the difference between our findings and those of Biswas et al results from studying only 1 patients with PM/DM and SSc overlap in our series. However, the exact number of patients with PM/DM and SSc overlap in their study was not stated (15). On the other hand, the discrepancy may be due to differences in criteria used for the diagnosis of PM/DM and SSc overlap. There is a retrospective collaborative study in which chart reviews of patients whose sera were positive for anti-jo-1 in 2 hospital laboratories over an 8-year period were conducted (16). Sera testing positive by counterimmunoelectrophoresis were further tested for anti-jo-1 by immunoprecipitation and enzyme inhibition assays. Sixteen of the 19 anti-jo-1 positive patients met criteria for myositis. An unusual finding was that of the 19 anti-jo-1 positive patients, 17 had Raynaud s phenomenon, 15 sclerodactyly, 6 dysphagia, 6 telangiectasias, and 4 had soft tissue calcification. Thus, there was a high prevalence of anti-jo-1 in patients with the CREST features in that retrospective study. We did not find anti-jo-1 in any of our CREST patients. The criteria used to diagnose SSc were not stated, and the clinical manifestations were obtained from a chart review. There is the possibility that the clinical manifestations cannot be compared within the patient groups in that study, nor between that patient group and ours. Another explanation for these remarkably contrasting results may be that the study populations, and thus, the humoral responses, are different. This is possible, since antinuclear antibodies are associated with dissimilar clinical manifestations in SSc patients of different ethnic backgrounds (17). In myositis patients from different ethnic back- grounds, the prevalence of anti-jo-1 is different (Uthman I et al: unpublished data). From the present study, we conclude that anti- Jo-1 antibodies are disease-specific autoantibodies similar to anti-topoisomerase I in SSc (11). SSc and PMDM have highly specific and exclusive autoantibodies, suggesting that in both diseases, the patients humoral responses undergo similar selection and proliferation processes that determine the presence of anti-jo-i only in PMDM and of anti-topoisomerase I only in SSc. These results support the concept of a selected and restricted B cell dysregulation associated with the establishment of PM/DM and SSc (18). ACKNOWLEDGMENTS We appreciate the helpful discussions and technical suggestions of Murray Deutscher, MD and Valery Filonenko, PhD, and the excellent technical support of Lesley S. Daniels and Sean M. Cusick. I REFERENCES Medsger TA, Oddis CV: Inflammatory muscle disease: clinical features. In, Rheumatology. Edited by JH Klippel, PA Dieppe. London, Mosby-Year Book Europe Limited, 1994 Targoff I: Autoantibodies in polymyositis. Rheum Dis Clin North Am 18:455432, 1992 Yoshida S, Akizuki M, Mimori T, Yamagata H, lnada S, Homma M: The precipitating antibody to an acidic nuclear protein antigen, the Jo-I, in connective tissue diseases: a marker for polymyositis with interstitial pulmonary fibrosis. Arthritis Rheum 26:64-611, 1984 Arnett FC. Edworthy SM, Bloch DA, McShane DJ, Fries JF, Cooper NS, Healey LA, Kaplan SR, Liang MH, Luthra HS, Medsger TA Jr, Mitchell DM, Neustadt DH, Pinals RS, Schaller JG, Sharp JT, Wilder RL, Hunder GG: The American Rheumatism Association 1987 revised criteria for the classification of rheumatoid arthritis. Arthritis Rheum 31: , 1988 Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Tala1 N, Winchester RJ: The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 25: , 1982 Subcommittee for Scleroderma Criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee: preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum , 198 Bohan A, Peter JB, Bowman RL, Pearson CM: A computerassisted analysis of 153 patients with polymyositis and dermatomyositis. Medicine (Baltimore) 56: , 1977 VBzquez-Abad D, Wallace S, Seneca1 J-L, Joyal F, Roussin A, Earnshaw WC, Rothfield N: Anticentromere autoantibodies: evaluation of an ELISA using recombinant fusion protein CENP-B as antigen. Arthritis Rheum 37: , 1994 Weiner ES, Earnshaw WC, Seneca1 J-L, Bordwell B, Johnson P, Rothfield NF: Clinical associations of anticentromere antibodies and antibodies to topoisomerase 1: a study of 355 patients. Arthritis Rheum 31: , 1988 VBzquez-Abad D, Pascual V, Zanetti M, Rothfield NF: Analysis

5 296 VAZQUEZ-ABAD AND ROTHFIELD of human antitopoisomerase4 idiotypes. J Clin Invest 92: , VAzquez-Abad D, Rothfield NF: Autoantibodies in systemic sclerosis. Rev Immunol 12: , Kipnis RJ, Craft J, Hardin JA: The analysis of antinuclear and antinucleolar autoantibodies of scleroderma by radioimmunoprecipitation assays. Arthritis Rheum 33: , Okano Y, Steen VD, Medsger TA: Autoantibody reactive with R polymerase 111 in systemic sclerosis. Ann Intern Med 119:15-113, Bernstein RM, Bunn CC, Hughes GRV, Francoeur AM, Mathews MB: Cellular protein and R antigens in autoimmune disease. Mol Biol Med 2:15-12, Biswas T, Miller FW, Takagaki Y, Plotz PH: An enzyme-lynked immunosorbent assay for the detection and quantification of anti-jo-1 antibody in human serum. J Immunol Methods 98: , Marguene C, Bunn CC, Beynon HLC, Bernstein RM, Hughes GRB, So AK, Walport MJ: Polymyositis, pulmonary fibrosis and autoantibodies to aminoacyl-tr synthetase enzymes. Q J Med 77: , Kuwana M, Okano Y, Kaburaki J, Tojo T, Medsger TA Jr: Racial differences in the distribution of systemic sclerosisrelated serum antinuclear antibodies. Arthritis Rheum , Vgzquez-Abad D, Russell CA, Cusick SM, Earnshaw WC, Rothfield NF: Longitudinal analysis of anticentromere and antitopoisomerase I isotypes. Clin lmmunol Immunopathol 74: , 1995

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