Original Article
Association between Lupus Psychosis and Antiribosomal P Protein Antibodies
N Engl J Med 1987; 317:265-271July 30, 1987DOI: 10.1056/NEJM198707303170503
- Abstract
- Abstract
In 18 of 20 patients with psychosis secondary to systemic lupus erythematosus (SLE), autoantibodies to ribosomal P proteins were detected by immunoblotting and measured with a new radioimmunoassay using a synthetic peptide as antigen.
The frequency of anti-P was not increased in patients with other central nervous system manifestations of SLE (3 of 20, by radioimmunoassay), in patients with transient behavioral abnormalities due to SLE (none of 8), in patients with psychosis who did not have SLE (none of 13), or in normal controls (none of 20). In four of five paired serum samples, anti-P-peptide antibody levels increased 5-fold to 30-fold during the active phase of lupus psychosis. Longitudinal studies of anti-P activity in two patients with psychosis revealed that anti-P levels increased before and during the active phases of psychosis but not during sepsis or other exacerbations of SLE, and that the elevations were selective for anti-P antibodies, as opposed to anti-DNA antibodies. Longitudinal studies of anti-P activity in two patients with anti-P but without psychosis showed less than threefold changes in anti-P levels despite exacerbations of disease.
We conclude that anti-P is associated with lupus psychosis and that synthetic peptide antigens may be useful for the detection and measurement of autoantibodies to intracellular proteins. (N Engl J Med 1987; 317:265–71.)
Article Activity
- Article
SYSTEMIC lupus erythematosus (SLE) is a multisystem autoimmune disease characterized by the presence of a variety of circulating autoantibodies.1 Anti-DNA antibodies are thought to cause tissue injury by forming antigen–antibody complexes in the circulation, with subsequent deposition in the kidneys and possibly other organs.2 , 3 The role of other autoantibodies in inducing clinical disease is less certain, although anti-Ro is associated with cutaneous manifestations and congenital heart block.4
Central nervous system manifestations of SLE occur in approximately half of all patients.5 6 7 Psychiatric features represent a common central nervous system manifestation and may be expressed as behavioral abnormalities resembling affective disorders or schizophrenia.5 6 7 Although numerous tests have been proposed to detect central nervous system manifestations of lupus, none have consistently had sufficient sensitivity and specificity to be used diagnostically.8 The diagnosis of central nervous system lupus in general and of lupus psychosis in particular is therefore based on clinical features, the duration of illness, a history of previous episodes, and exclusion of other factors temporally associated with the onset of psychosis.9
Autoantibodies have been proposed to be responsible for central nervous system disease in SLE.10 , 11 Bluestein and coworkers have noted an association between cerebral lupus and antibodies in the cerebrospinal fluid that are cytotoxic to a neuroblastoma cell line (SK-N-SH).12 Other investigators have provided additional evidence of immunologic activity, such as low levels of the complement component C4 and the presence of DNA-containing immune complexes in the cerebrospinal fluid.13 , 14 We have recently characterized the antiribosomal-protein antibodies that occur in approximately 12 percent of patients with SLE.15 , 16 These antibodies react with three large-subunit ribosomal phosphoproteins, called PO (38 kilodaltons[kd]), P1 (19 kd), and P2 (17 kd).15 We have localized the reactivity of all lupus anti-P serum tested to a single linear antigenic determinant contained within the carboxyl-terminal 22 amino acids of the P2 protein, and have synthesized this peptide by solid-phase methods.17 The same antigenic determinant is present on all three P proteins.17 In the present study, we report the presence of anti-P in 18 of 20 patients with lupus psychosis tested by a solid-phase radioimmunoassay to the synthetic P peptide antigen. We also demonstrate selective elevations of anti-P levels preceding the onset of psychotic episodes in two patients whom we studied serially.
Methods
Subjects
We studied the following groups: 20 normal healthy subjects, 20 patients with SLE and lupus psychosis, 14 patients with SLE and anti-P but without psychosis, 13 patients with acute or chronic episodes of psychosis (mania, depression, or schizophrenia) but without SLE, 13 patients with anti-Sm/RNP antibodies but without anti-P antibodies on Western blot analysis, 8 patients with SLE and transient behavioral disturbances thought to be due to a rapid increase or decrease in the dose of corticosteroids, and 20 patients with other central nervous system manifestations — 3 patients with aseptic meningitis, 10 with seizures, 3 with cranial-nerve palsies, 2 with stroke, 1 with coma, and 1 with recurrent migraine. A total of 32 patients with SLE and anti-P antibodies detectable on immunoblots have been identified. The majority of patients with anti-P antibodies but without psychosis, as well as patients with SLE and other central nervous system disorders, have been described in detail elsewhere.16 , 18 Six patients with SLE and anti-P antibodies were known to have psychosis,16 and 14 others with lupus psychosis were referred for autoantibody evaluation. Clinical information was obtained by retrospective chart review.
The following criteria were used to define lupus psychosis: a marked behavioral disturbance sufficient to warrant referral to a hospital and treatment with psychotropic drugs; a behavioral disturbance as the initial and dominant neurologic feature; a disturbance lasting two weeks or longer; the absence of other known causes of mental disorder, including drugs, infection, or metabolic derangements; and the absence of a localized neurologic lesion as determined by clinical examination or CT scanning.
Of the 20 patients with SLE19 who had psychosis, 8 had predominant affective psychosis (depression, mania, or both) and 12 had predominant schizophrenic features (paranoia, hallucinations, or catatonia). Eight of these patients had two or more psychotic episodes. Fifteen patients had clinical evidence of lupus activity in other organ systems at the onset of psychosis. In 15 patients, at least one episode of psychosis occurred when they were not taking corticosteroids or any other medication known to induce behavioral disorders. Five patients were taking steroids before the onset of an episode of psychosis. Three patients were taking stable doses of 30 mg or less of prednisone daily; a fourth patient had received several courses of steroids (60 mg daily) without neurologic effects and had been receiving a stable dose of 60 mg for one month before the onset of schizoid behavior. The fifth patient (Patient 2) is described in the Case Report below.
Detection of Autoantibodies and Total IgG
Serum samples from all patients were tested for autoantibodies to saline-soluble cellular antigens as described in detail elsewhere.20 , 21 In brief, counterimmunoelectrophoresis was performed according to the method of Kurata and Tan,22 with extracts of dog spleen and commercial rabbit thymus (Pel-Freez) used as antigen sources. Dog-spleen extracts and rat-liver ribosomes15 were used for Western blot analysis.23 In all cases, anti-P reactivity was confirmed by Western blot analysis using purified ribosomes as antigen, and the identities of Ro, La, Sm, and RNP were confirmed by immunoblotting after two-dimensional gel electrophoresis.21 Antibodies to double-stranded DNA were detected by indirect immunofluorescence on Crithidia luciliae,24 and quantitative radioimmunoassays were performed on DNA-coated microtiter plates according to the method of Koike et al.25 The blocking buffer contained 2 percent (wt/vol) bovine serum albumin and 1 percent (wt/vol) casein, rather than fetal-calf serum, to avoid any possible binding of rheumatoid factors. Total serum IgG was measured by radial immunodiffusion.26
Quantitative Radioimmunoassay of Anti-P-Peptide Antibodies
A synthetic peptide corresponding to the carboxyl-terminal 22 amino acids of the Artemia salina ribosomal P2 equivalent was synthesized by a solid-phase method.17 The purity of the peptide was confirmed by analytic high-pressure liquid chromatography, amino acid analysis, and microsequencing. The peptide was conjugated to bovine thyroglobulin or rabbit serum albumin with use of glutaraldehyde.27 Antibody reactivity with the synthetic peptide was measured by a solid-phase radioimmunoassay modified from a rheumatoid-factor assay.28 Plastic microtiter plates (Linbro) were coated with thyroglobulin or albumin-bound peptide at a concentration of 200 ng of peptide per well in phosphate-buffered saline (0.01 M phosphate, pH 7.4, containing 0.15 M saline). As a control, wells were coated with free bovine thyroglobulin or rabbit albumin at the same concentration used for the bound peptide. The plates were blocked with 1 percent (wt/vol) bovine albumin, and the wells were sequentially incubated with a 1:100 dilution of the test antibody in duplicate, followed by the addition of 100,000 cpm of a 125I-labeled goat antihuman IgG per well. The plates were incubated for five hours at room temperature. The results are expressed as mean counts per minute for binding in the peptide-coated wells, after correction for binding in the wells coated with thyroglobulin or rabbit albumin. To ensure consistency between assays, serial dilutions of known positive and negative serum samples were included in each study. Immunoassays were performed without knowledge of the clinical status of each subject.
Statistical analysis was performed by the chi-square test with Yates' correction.
Case Reports
Patient 1
A 22-year-old black woman presented in October 1983 with malar rash, palatal ulcers, lymphadenopathy, and diffuse arthralgia. On November 20, 1984, she was admitted to the hospital because of fever, rash, alopecia, arthralgia, palatal ulcers, and lymphadenopathy. She also had signs of paranoid ideation, disorientation, auditory hallucinations, and intermittent mutism. On November 29, she had a focal seizure. The cerebrospinal fluid, electroencephalogram, and CT scan were normal. The patient was treated with intravenous corticosteroids and phenytoin. Over the subsequent two weeks, she had frequent partial complex seizures. For three months, she remained unresponsive to verbal and painful stimuli; the doses of corticosteroids were gradually decreased, but there was no change in her mental status. Over the next two months, her mental status returned to normal. In October 1985, a malar rash, palatal ulcers, and arthritis developed. Her mental status was normal. In January 1986, bizarre behavior began, characterized by irritability, impulsiveness, and immaturity. The patient made several suicidal gestures and was hospitalized twice in March 1986 for psychiatric therapy.
Patient 2
A 17-year-old white girl presented with malar rash, fever, and nephritis in August 1983. Two weeks later, lethargy, suicidal ideation, and confusion developed. The cerebrospinal fluid protein level was 91 mg per deciliter (normal, 15 to 45), and an electroencephalogram revealed diffuse bilateral cortical slowing. A CT scan was normal. On September 22, focal seizures developed. The results of repeat lumbar puncture, electroencephalography, and CT scanning were unchanged. The patient's behavior became more bizarre, and visual hallucinations, withdrawal, and mutism developed. The psychosis gradually resolved, and by November 1983, there were no signs of disease activity. On July 30, 1985, malaise, fever, and myositis developed and were treated with prednisone. Two weeks later, mental dysfunction occurred, with disorientation, confusion, auditory hallucinations, and flight of ideas. In addition to corticosteroids, five courses of plasmapheresis were given. Psychotic features persisted for another 2 1/2 months, despite a gradual reduction in the dose of corticosteroids. The psychotic episode was judged to be due to lupus rather than to drugs because the manifestations were identical to those that had occurred during treatment with low doses of corticosteroids and because the psychosis lasted for three months and was not affected by a reduction in the dose of corticosteroids.
Patient 3
A 19-year-old black woman presented in October 1978 with fever, malar rash, migratory arthritis, and a grand mal seizure. After recurrent seizures, she lapsed into a coma, which persisted for two weeks. In July 1979, malar rash, vasculitic skin ulcers, arthritis, and lymphadenopathy recurred. Similar flare-ups of rash, arthritis, and lymphadenopathy occurred in November 1980, July 1981, November 1984, and January 1985.
Results
Features of Anti-P-Positive Patients with SLE
Since 18 of the 20 patients with SLE and psychosis were found to have anti-P antibodies (see below), clinical and serologic features were compared in 18 patients with these antibodies and psychosis and 14 patients with the antibodies but without psychosis (Table 1Table 1
Clinical and Serologic Features in 32 Patients with Lupus Who Were Positive for Anti-P.*). The groups with and without psychosis were similar in their ethnic origins, duration of disease, and frequency of various autoantibodies, although in the patients with psychosis, the lupus had a slightly later onset. No significant differences in the frequency of involvement of other organ systems were observed (data not shown). The results of Western blot testing using dog-spleen extract as an antigen source (containing Ro, La, Sm, RNP, P, and other protein antigens20 , 21) and serum from the first nine patients with psychosis and SLE are shown in Figure 1Figure 1
Immunoblot Reactivity of Serum from Nine Patients with Lupus Psychosis.. Anti-P reactivity was prominent in all nine patients, and binding to the Sm (B) antigen (25 to 26 kd) was also observed in six. The low frequency of binding to the Ro and RNP antigens (Table 1) is due to the low sensitivity of Western blotting for the detection of these antigens.20 , 21 , 29 30 31 The infrequency of anti-La antibodies (2 of 32 patients [6 percent]) in patients positive for anti-P cannot be explained by technical factors and has been noted previously.16 Overall, anti-P reactivity was detected by immunoblotting of serum from 18 of 20 patients (90 percent) with lupus psychosis. Of the 14 patients with lupus psychosis who were referred to us for determination of autoantibody specificities, 12 (86 percent) were found to have anti-P. When the latter frequency was compared with the 12 percent frequency of anti-P in 59 randomly selected patients with lupus,16 a significant difference was observed (chi-square = 28, P<0.001).Detection of Anti-P-Peptide Antibodies by Radioimmunoassay
Comparisons between binding in 32 patients who were positive for anti-P, 13 with SLE who were negative for anti-P but positive for Sm-RNP, and 20 normal subjects are shown in Figure 2Figure 2
Radioimmunoassay Detection of Anti-P Peptide with Use of a Synthetic Peptide as Antigen. and Table 2Table 2
Frequency of Anti-P Antibodies as Detected by Radioimmunoassay (RIA) and Western Blot Analysis.. All patients with anti-P detectable on Western blotting were positive (binding >3 SD above the mean values in the control group), whereas only 3 of the 13 patients positive for Sm-RNP had borderline elevations in binding activity. There was no overlap between the three groups of serum samples. These findings show that the radioimmunoassay is specific and at least as sensitive as Western blotting for the detection of anti-P. No patient was observed to have antibodies specific for bovine thyroglobulin or rabbit albumin.Since anti-P antibodies were demonstrated by both Western blotting and radioimmunoassay in the serum of 18 of 20 patients with SLE psychosis, the frequency of anti-P was determined in patients with SLE who had other central nervous system manifestations of lupus, as well as in patients without SLE who had psychosis. Anti-P peptide antibodies were detected in only 3 of 20 patients with other neurologic manifestations of lupus (Table 2). When this frequency was compared with the 86 percent frequency of anti-P in the 14 consecutive patients referred because of lupus psychosis, a significant difference was observed (chi-square = 14.0, P<0.001). Anti-P was not detected in any of the psychotic patients without SLE or in the eight patients with SLE and transient behavioral disturbances thought to be related to corticosteroids (Table 2 and Fig. 2).
Serial Studies of Anti-P-Peptide Antibodies and Relation to Psychosis
Paired serum samples (one taken during remission and one taken during the active phase of psychosis) were available from three patients. The titer of anti-P peptide was fivefold higher during active psychosis in two of these patients, whereas no change in anti-P activity was observed in the third patient. In two additional patients with psychosis, multiple serum samples had been stored between 1983 and 1986. All available samples were tested by radioimmunoassay, and the results are shown in Figure 3Figure 3
Serial Studies of Anti-P (Closed Circles) and Anti-DNA (Open Circles) Activities as Determined by Solid-Phase Radioimmunoassays.A and 3B. For comparison, the levels of anti-P peptide from a nonpsychotic patient with SLE and anti-P antibodies who had flare-ups of rash, arthritis, and adenopathy are shown in Figure 3C. The two patients with psychosis had 9-fold and 30-fold increases in anti-P levels shortly before the onset of psychosis. Patient 1 (Fig. 3A) had two episodes of psychosis and striking elevations in anti-P levels before and during both episodes. In contrast, no consistent changes in anti-DNA levels were observed, and the maximal increase in total IgG concentration was 1.6 times the base-line level (Table 3Table 3
Comparisons between the Total IgG Concentrations and Autoantibody Levels during the Active and Inactive Phases of Psychosis in Patients 1 and 2.*). As shown in Table 3, the maximal change in any other autoantibody detected in these two patients was a twofold increase in the anti-Ro titer in Patient 2. This patient had strong anti-Sm activity and weak anti-P activity during the inactive phase of psychosis (Fig. 4Figure 4
Immunoblot Reactivity of Serum Samples from Patient 2 during Remission (Lane a) and Psychosis (Lane b)., Lane a), but strong anti-P activity and weak anti-Sm activity during active psychosis (Fig. 4, Lane b). In the nonpsychotic patient with SLE, no significant changes in anti-P-peptide levels occurred over a six-year period despite flare-ups of clinical activity (Fig. 3C).In another patient without psychosis who was positive for anti-P, serum samples collected between 1980 and 1985 showed a maximal threefold difference in anti-P-peptide titer despite remissions and exacerbations of nephritis and thrombocytopenia (data not shown).
Discussion
The associations between anti-DNA antibodies, clinical activity, and renal disease could be established early in studies of SLE because DNA is relatively easy to purify in large amounts and to use in quantitative immunoassays.2 , 3 , 32 In contrast, the saline-soluble intracellular protein antigens in patients with SLE and related diseases1 have been extremely difficult to purify in sufficient quantities. The present study employed a synthetic peptide antigen to detect and measure autoantibodies to an intracellular protein antigen in patients with SLE. That this represents an important advance in the detection of such autoantibodies is indicated by the simplicity, sensitivity, and specificity of the assay. The radioimmunoassay is superior to Western blotting because it is quantitative and more economical in the use of serum, reagents, and labor. There was excellent agreement between the results obtained by radioimmunoassay and Western blotting, and the frequency of anti-P-peptide antibodies in the patients with SLE and nonpsychotic neurologic disease (15 percent) was similar to that detected previously in a randomly selected population of patients with SLE (12 percent).16 The borderline elevations in 3 of 13 serum samples positive for anti-Sm/RNP may have been due to hypergammaglobulinemia or the presence of anti-P antibodies in levels too low to be detectable by Western blotting.
In 90 percent (18 of 20) of patients with SLE psychosis, circulating anti-P antibodies were detectable by both Western blotting and radioimmunoassay. The association between anti-P and psychosis was enhanced by the 5-fold to 30-fold increases in levels of antibody to the synthetic P peptide in four of five patients with psychosis from whom paired samples were available. In the two patients with psychosis who were studied longitudinally, anti-P elevations appeared to be highly selective, since they did not occur during other exacerbations of SLE and were not accompanied by a similar increase in total IgG, anti-DNA, anti-Ro, or anti-Sm/RNP activity. Moreover, long-term serial studies in two patients without psychoses who were positive for anti-P showed little fluctuation in anti-P-peptide activity. Finally, we have demonstrated a selective enrichment of anti-P activity in the cerebrospinal fluid of one patient with anti-P antibodies and psychosis18 and have suggested that the positive cytoplasmic staining of neurons produced by serum from patients with cerebral lupus33 , 34 may, in some cases, have been due to unrecognized anti-P activity.
Although all the above findings support an association between anti-P activity and lupus psychosis, half the patients with anti-P did not have psychotic episodes. Several possibilities may explain these findings. First, the putative antibody that cross-reacts with neurons may be a subpopulation of anti-P or related antibodies. Western blotting and the synthetic peptide radioimmunoassay detect antibodies to the linear (sequential) determinant or determinants; however, considerable evidence of the existence of antibodies to conformation of the P proteins has also been obtained.17 The population of antibodies inducing cerebral disease may not even have anti-P specificity; instead, it may be linked to anti-P in much the same way that antibodies to Ro and La or antibodies to Sm and RNP are coexpressed in SLE.1 Finally, an anti-P antiidiotypic antibody population could induce disease by binding to membrane receptors, as has been shown with experimentally induced antibodies to the insulin35 and acetylcholine36 receptors. An important contributory factor is likely to be damage to the blood–brain barrier.10 , 11 Since most patients had evidence of lupus activity in other organ systems at the time of psychosis, vasculitis may have played a part, allowing autoantibodies to be transferred across the capillary endothelium. Whether such autoantibodies are directly cytotoxic, interfere with neurotransmitters, or penetrate neuronal cells37 , 38 remains to be determined. Regardless of the mechanisms involved, the absence of the other focal central nervous system manifestations suggests that the injury is relatively selective for cortical neurons. It is also likely that other autoantibodies10 and perhaps different mechanisms are responsible for behavioral disturbances in some patients with lupus. Since almost half the patients with anti-P antibodies did not have severe behavioral disturbances, a single measurement of anti-P is not diagnostic of lupus psychosis. Whether a fivefold or greater increase in anti-P levels will prove to be predictive of lupus psychosis must be determined by future prospective studies.
The high frequency of anti-Ro and the low frequency of anti-La in patients with anti-P have previously been noted16 and were confirmed in this study by immunoblotting. Since SLE is characterized by remissions and exacerbations, our demonstration of a selective increase in an antibody population in the two patients whom we studied longitudinally is also of interest. This finding suggests that different autoantibodies may be differentially stimulated or regulated in patients with SLE.
Supported in part by grants (AM-32845, AM-14627, and AM-32929) from the National Institutes of Health and by the Jacobs Foundation.
We are indebted to Drs. C. Christian, M. Lockshin, and S. Paget for helpful discussion, to Drs. J. Bussel, C. Christian, R. Furie, J. Hardin, M. Lockshin, J. Markenson, S. Paget, J. Licinio-Paixao, D. Ricciardi, M. Skinner, M. Rivelis, M. Sobel, R. Stern, and W. Stohl for providing patient information, and to W. Danho for peptide synthesis.
Source Information
From the Hospital for Special Surgery–Cornell University Medical Center, New York; the State University of New York at Stony Brook; and the Roche Institute of Molecular Biology, Roche Research Center, Nutley, N.J. Address reprint requests to Dr. Elkon at the Hospital for Special Surgery, 535 E. 70th St., New York, NY 10021.
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