Original Article
Paraneoplastic Pemphigus — An Autoimmune Mucocutaneous Disease Associated with Neoplasia
N Engl J Med 1990; 323:1729-1735December 20, 1990
- Abstract
- Abstract
Background and Methods.
We describe five patients with underlying neoplasms in whom painful mucosal ulcerations and polymorphous skin lesions developed, usually with progression to blistering eruptions on the trunk and extremities. Histologic examination showed vacuolization of epidermal basal cells, keratinocyte necrosis, and acantholysis. Immunofluorescence testing revealed atypical pemphigus-like autoantibodies in perilesional epithelium and serum from all five patients. We studied the antigenic specificities of the autoantibodies by indirect immunofluorescence and immunoprecipitation, using extracts of 14C-labeled human keratinocytes. IgG purified from the serum of one patient was passively transferred to four neonatal mice to test for pathogenicity.
Results.
Immunofluorescence testing showed that the autoantibodies bound to the surface of tissues containing desmosomes, including complex and simple epithelia, and myocardium. An identical and unique complex of four polypeptides with molecular weights of 250, 230, 210, and 190 was immunoprecipitated by all serum samples. The 250-kd polypeptide comigrated with desmoplakin I (a protein found in the desmosomes of all epithelia), and the 230-kd antigen comigrated with the antigen of bullous pemphigoid. Cutaneous blisters, a positive Nikolsky's sign, and epidermal and esophageal acantholysis developed in all mice into which the autoantibody was injected. Electron microscopy showed epidermal acantholysis similar to lesions of experimentally induced pemphigus vulgaris.
Conclusions.
These five patients with cancer had a novel acantholytic mucocutaneous disease characterized by autoantibodies that were pathogenic after passive transfer. The autoantibodies from these patients reacted with an antigen complex composed of desmoplakin I and the 230-kd antigen of bullous pemphigoid and two as yet unidentified epithelial antigens. We suggest the term "paraneoplastic pemphigus" for this disease. (N Engl J Med 1990; 323:1729–35.)
Article Activity
- Article
THE term "pemphigus" refers to mucocutaneous diseases that are characterized by intraepithelial blisters, caused by a loss of normal cell-cell adhesion (acantholysis1), and are associated with autoantibodies against cell-surface proteins of stratified squamous epithelia.2 , 3 There are two clinically and immunologically distinct forms of pemphigus.4 5 6 In pemphigus vulgaris, autoantibodies are directed against a 130-kd antigen that forms a complex with a protein of desmosomal and adherens junctions, called plakoglobin.7 In pemphigus foliaceus, the autoantibodies are specific for a 160-kd antigen, called desmoglein I, that forms a similar complex with plakoglobin.7
Atypical cases of ulcerative and blistering mucocutaneous disease associated with pemphigus-like autoantibodies have been reported sporadically.8 9 10 11 12 In retrospect, patients with high titers of autoantibody apparently all had underlying neoplasms, most frequently lymphoma. We have now seen five such patients with strikingly similar clinical, histologic, and immunologic features. We believe that these patients have a paraneoplastic autoimmune disease, which we refer to as paraneoplastic pemphigus.
Case Report (Index Case)
In early 1987 a 62-year-old man (Patient 1, Table 1Table 1
Clinical and Laboratory Findings in Five Patients with Paraneoplastic Pemphigus.) was given a diagnosis of malignant follicular large-cell lymphoma. The tumor initially responded to therapy with cyclophosphamide, doxorubicin (Adriamycin), vincristine, bleomycin, and intravenous and intrathecal methotrexate. In January 1988 a pruritic urticarial skin eruption developed; it was assumed to be an allergic reaction to diltiazem, but it did not resolve after discontinuation of the drug. In May 1988 the lymphoma recurred and was treated with chlorambucil and prednisone, but both the lymphadenopathy and the skin eruption responded only partially. A skin biopsy showed focal acantholysis, with granular complement deposition at the epidermal basement-membrane zone and weak deposition of IgG within the intercellular substance of the epidermis. Indirect immunofluorescence testing of the patient's serum on sections of monkey esophagus3 showed the presence of pemphigus-like antibodies at a titer of 1:80. Treatment with azathioprine (100 mg per day) and prednisone (60 mg per day) was started, but the skin eruption worsened. Numerous confluent vesicles and erosions of the conjunctivas, oropharynx, and esophagus developed, accompanied by severe dysphagia, malaise, myalgia, and fatigue and numerous erosions on the trunk and extremities. Skin biopsies at that time showed necrosis of the epidermis that was consistent with severe erythema multiforme or toxic epidermal necrolysis, and the serum contained pemphigus-like antibodies at a titer of 1:160. Staphylococcal sepsis developed, and the patient was admitted to a burn-care unit with a presumed diagnosis of toxic epidermal necrolysis.On examination the patient was febrile and debilitated, with confluent crusted and denuded areas of skin, predominantly on the upper trunk. The lips, palate, and conjunctivas were covered with bleeding erosions. There was bilateral enlargement of cervical, supraclavicular, axillary, and inguinal nodes. Serum protein electrophoresis showed decreased albumin concentrations with no abnormal gamma globulin peaks. Computerized axial tomographic scanning showed enlargement of retroperitoneal, mediastinal, axillary, and supraclavicular nodes and infiltration of the spleen by tumor. Bone marrow biopsy showed tumor invasion. Blood, sputum, and skin cultures all grew Staphylococcus aureus.
The prednisone and azathioprine were discontinued, and imipenem was administered. On the 11th hospital day, new pruritic vesiculobullous lesions developed on the trunk and extremities and new oral and conjunctival erosions appeared. Biopsy of a skin lesion revealed an acantholytic intraepidermal blister consistent with pemphigus vulgaris. The epithelium adjacent to the blister showed vacuolar-interface change and necrosis of individual keratinocytes. Circulating pemphigus-like antibodies were present at a titer of 1:2560. The prednisone was restarted (40 mg per day), and the skin lesions slowly resolved, although mucosal lesions persisted. After discharge, notable findings included the presence of a pseudomembranous conjunctivitis, severe mucosal erosions throughout the oropharynx and nasopharynx, and healed erosions of the trunk and extremities.
The lymphoma was considered to be incurable, and the mucosal erosions improved only slightly during treatment with prednisone (60 mg per day). The patient was discharged home, where he had recurrent episodes of pneumonia and died in December 1988. Permission for an autopsy was not obtained.
Methods
Histologic and Electron-Microscopical Techniques
Histologic specimens were obtained from all five patients whom we studied. Specimens from mice into which the human autoantibody had been injected were obtained immediately after the animals had been decapitated, and were fixed in either 10 percent buffered formaldehyde for histologic examination or 2.5 percent glutaraldehyde for electron microscopy. The specimens obtained for electron microscopy were postfixed with osmium tetroxide, stained en bloc with uranyl acetate, and embedded in British Araldite.
Sources of Serum Samples and Immunofluorescence Techniques
Serum was obtained from the five patients at the time of evaluation. Control samples were obtained from 10 patients with pemphigus vulgaris, 10 with pemphigus foliaceus, 2 with coexistent pemphigus foliaceus and neoplasia (squamous-cell carcinoma in 1 patient and thymoma in the other), 10 with bullous pemphigoid, 12 with cicatricial pemphigoid, 2 with epidermolysis bullosa acquisita, 6 with linear IgA dermatitis, 10 with systemic lupus erythematosus with cutaneous involvement, and 6 healthy subjects.
Fresh tissues were embedded in OCT medium (Tissue-Tek, Miles Laboratories, Elkhart, Ind.) and snap-frozen in liquid nitrogen. The tissues obtained at autopsy that were studied included skin, buccal mucosa, and small intestine. Mice were killed by cervical dislocation, and the following tissues were examined: skin, esophagus, trachea, myocardium, skeletal muscle, small and large bowel, urinary bladder, and lung. Sections were frozen and later incubated with dilutions of serum from the five patients and the control subjects, followed by the addition of fluorescein-labeled antihuman IgG (Cappel Worthington, West Chester, Pa.).
In tests for polyclonality of the patients' autoantibodies, frozen sections of mouse skin were used. Dilutions of the patients' serum were applied as a source of the primary antibody. Murine monoclonal antibodies with established specificities for human IgG subclasses 1 through 413 as well as monoclonal antibodies against human immunoglobulin kappa and lambda light chains (Cappel) were used as a secondary antibody, followed by the addition of fluorescein-labeled antimurine IgG (Cappel). Slides were examined with a fluorescence microscope (Olympus, Tokyo).
Immunoprecipitation
Immunoprecipitation was performed according to the technique of Stanley et al.14 Human keratinocytes were incubated with l4C-labeled amino acids (NEN Research, Boston) in keratinocyte growth medium (KGM, Clonetics, San Diego, Calif). Primary cultures of murine keratinocytes were established15 and incubated with 35S-labeled methionine (Translabel, ICN Pharmaceuticals, Irvine, Calif.) in methionine-deficient Dulbecco's minimal essential medium with 13 percent fetal-calf serum (Gibco, Grand Island, N.Y.). Cultures were extracted in a nonionic detergent (0.5 percent NP-40, Calbiochem, La Jolla, Calif.) in TRIS-buffered saline at 4°C in the presence of 2 mM phenylmethylsulfonylflurone (Sigma, St. Louis) and centrifuged at 100,000×g for one hour; the supernatant was dialyzed against 0.3 percent NP-40 in TRIS-buffered saline. Labeled extracts were sequentially incubated with serum from the patients or controls and protein A—bearing staphylococci (Pansorbin, Calbiochem). Individual immunoprecipitates were analyzed by sodium dodecyl sulfate–polyacrylamide-gel electrophoresis in which a 5 percent slab gel was used, and the separated proteins were visualized by autoradiography.16
Identical techniques were employed to perform immunoprecipitation with a murine monoclonal antibody specific for desmoplakin I (clone DP 1&2–2.15, Boehringer–Mannheim, Indianapolis), except that staphylococcal protein G—Agarose (ImmuBind, Genex, Gaithersburg, Md.) was used in place of Pansorbin.
Immunoglobulin Preparation
Ammonium sulfate (Sigma) was added to serum from the patient described in the case report, to a final concentration of 24.3 g per deciliter. The resulting precipitate was resuspended and dialyzed against phosphate-buffered saline (pH 7.2) and then concentrated by pressure ultrafiltration in a stirred cell (Amicon, Bedford, Mass.) to a final protein concentration of 100 mg per milliliter. The final immunoglobulin-enriched solution was filter sterilized (Millex [pore size, 0.25 μm], Millipore, Bedford, Mass.) before it was injected into the mice. Control immunoglobulin fractions were prepared from pooled normal human serum in the same way.
Passive Transfer of Immunoglobulin
The pathogenicity of the human autoantibodies from the patient in the index case was tested by parenteral passive transfer of the antibodies into neonatal mice.17 In brief, eight BALB/c mice were obtained when 24 to 48 hours of age (body weight, 1.5 to 2.0 g). Four animals were given intraperitoneal injections of the enriched immunoglobulin solution (10 mg of total protein per gram of body weight) from the index patient. Four animals were given identical injections of the control immunoglobulin preparations. Approximately 18 hours after injection the mice were killed, and their skin was obtained for histologic and ultrastructural studies.
Results
Clinical and Histologic Findings
The clinical summaries of the five patients we identified are shown in Table 1. All five had persistent, painful erosions of the oropharynx and vermilion borders of the lips that were resistant to conventional therapy, and most also had severe pseudomembranous conjunctivitis (Fig. 1Figure 1
Mucosal and Cutaneous Lesions of Five Patients with Mucocutaneous Disease and Neoplasms (Paraneoplastic Pemphigus).). When cutaneous lesions developed, they were pruritic and characteristically polymorphous. Confluent erythema in the V area of the upper chest and back was common, and in most cases the affected skin also eroded, causing extensive denudation. Erythematous papules of the trunk and extremities evolved, forming target lesions with central blister formation and most frequently resembling erythema multiforme (Fig. 1) or toxic epidermal necrolysis in the most advanced stages. An instructive example was observed in Patient 5, whom we treated for pemphigus vulgaris. After three months during which his response to standard treatment was incomplete, an eruption indistinguishable from erythema multiforme major suddenly developed, with painful ulcerations of oral, nasal, and conjunctival mucosa, target lesions on the extremities, and confluent erythema on the upper trunk. The coincident occurrence of lesions characteristic of both pemphigus and erythema multiforme prompted us to suspect that the patient had paraneoplastic pemphigus. This suspicion was confirmed by the detection of an occult retroperitoneal sarcoma and a confirmatory immunoprecipitation assay. Apparently, such polymorphous lesions are characteristic of this disorder.Histologic studies of skin and mucosal specimens showed considerable variability, reflecting polymorphism of the clinical lesions. Three features predominated: suprabasilar intraepithelial acantholysis, necrosis of individual keratinocytes, and vacuolar-interface change (Fig. 2Figure 2
Histologic Specimen from Patient 1 (Hematoxylin and Eosin, ×80).). In four of the five patients, acantholytic lesions similar to those observed in patients with pemphigus vulgaris were present at some point; in the remaining patient, only papulosquamous lesions with vacuolar-interface change and oral ulcerations had been observed before the underlying neoplasm was detected (a thymoma, subsequently completely excised). It is noteworthy that only this patient (Patient 4) had a benign clinical course and an apparent remission. The other four patients had progressive mucocutaneous lesions that proved refractory to corticosteroids in high doses, plasmapheresis, and immunosuppressive therapy. In Patient 5, cutaneous blistering stopped after the bulk of the sarcoma was resected, but mucosal ulcerations and serum autoantibodies persisted.Immunofluorescence Testing
Immunofluorescence testing of perilesional tissue showed deposition of IgG in the intercellular spaces of the affected skin and mucosal epithelial cells, in a pattern similar to that seen in pemphigus, but the deposition was often faint and focal. Several biopsies also revealed high background cytoplasmic staining in the epidermis that made detection of the autoantibodies difficult (Fig. 3Figure 3
Results of Direct Immunofluorescence Testing of Three Skin Specimens from Patient 5 (×400).). A distinctive finding was the combined presence of granular—linear complement deposition along the basement-membrane zone as well as in the epithelial intercellular spaces.Indirect immunofluorescence examination of monkey esophagus and human and mouse skin showed binding of autoantibodies to the intercellular spaces that was identical to the binding seen in serum from patients with pemphigus vulgaris or foliaceus; however, unlike the autoantibody binding in pemphigus, the binding in these cases also involved other epithelial substrates (Fig. 4Figure 4
Results of Indirect Immunofluorescence Testing of Serum from Patients with Paraneoplastic Pemphigus (Left-Hand Panels, ×200) and Patients with Pemphigus Vulgaris (Right-Hand Panels, ×200).). The autoantibodies of the five patients bound consistently and strongly to the epithelium of urinary bladder, respiratory epithelium, small-bowel epithelium, and colon epithelium, and with variable intensity to intercalated disks of myocardium, skeletal muscle, and thyroid epithelium. Among these tissues, the strongest and most consistent binding was observed in urinary-bladder epithelium. Tissue from nonstratified squamous epithelia and myocardium, incubated with control serum samples from patients with pemphigus vulgaris and patients with pemphigus foliaceus, showed no autoantibody binding.The autoantibodies in the serum of all five patients were found to be polyclonal. IgG subclasses and light chains were distributed, in descending order, as follows: IgGl, IgG2, IgG4, IgG3; and lambda, kappa.
Immunoprecipitation
The serum of all five patients immunoprecipitated an identical complex of four polypeptides from human keratinocyte extracts, with estimated molecular weights of 250, 230, 210, and 190 (Fig. 5Figure 5
Immunoprecipitation of Antigen Bands from Metabolically Labeled Human Keratinocytes by Serum from Patients with Paraneoplastic Pemphigus (Patients 1 through 4).). The intensity of the four antigen bands immunoprecipitated by the serum varied, but the bands at 210 and 190 kd were most consistently visualized. A diffuse band was also visualized at 170 kd; however, this band was not present in all metabolically labeled extracts and was not consistently detected. These findings made us suspect that this band might represent a degradation product of one of the higher-molecular-weight antigens. A similar complex was immunoprecipitated in extracts from metabolically labeled murine keratinocytes (data not shown). This complex of antigens was not immunoprecipitated by any of the control serum samples.The monoclonal antibody specific for desmoplakin I precipitated a band at 250 kd that precisely comigrated in the polyacrylamide gels with the band for the highest-molecular-weight antigen, also about 250 kd (Fig. 5), suggesting that the high-molecular-weight antigen recognized by the serum might be desmoplakin I. Similarly, immunoprecipitation with serum from a patient with bullous pemphigoid identified the pemphigoid antigen at 230 kd, with relative migration identical to that of the 230-kd antigen recognized by serum from four of the five patients with underlying neoplasms (Fig. 5).
The complex detected by these serum samples was readily apparent on autoradiography after only three to five days of exposure. In contrast, the antigen complex immunoprecipitated by serum from patients with pemphigus vulgaris required approximately two weeks of development to be visualized. Exposure of gels for prolonged periods did not reveal any apparent pemphigus vulgaris antigen or pemphigus foliaceus antigen in the immunoprecipitates of the five patients with cancer (data not shown).
Passive Transfer of Antibody
All four mice given immunoglobulin solutions prepared from the serum of the index patient had extensive cutaneous blistering with a positive Nikolsky's sign1 within 18 hours of injection. Histologic examination of the animals' skin demonstrated the formation of intraepidermal acantholytic blisters with retention of adhesion of basal cells to the dermis. Acantholytic cells were also found in the superficial layers of the esophageal mucosa. No obvious epithelial defects were detected in other organs of the mice, such as the gastrointestinal tract or pulmonary or urinary-bladder epithelium.
Ultrastructural examination of the skin of the mice showed loss of cell—cell adhesion but normal basal-cell-dermal-cell attachment. The epidermal cells also showed some cytopathic changes, with mitochondrial swelling and cytoplasmic vacuolization.
Discussion
Paraneoplastic pemphigus is clinically distinct from pemphigus vulgaris and pemphigus foliaceus. Painful, persistent, and treatment-resistant erosions of the oral mucosa, vermilion borders of the lips, and conjunctivas were common to all cases. The initial skin lesions were polymorphous, often presenting as a pruritic papulosquamous eruption with subsequent blistering. The occurrence of blisters of the palms and soles suggested a diagnosis of erythema multiforme in three of our five patients, raising the interesting possibility that previously reported cases of erythema multiforme associated with underlying tumors may have in fact been unrecognized cases of paraneoplastic pemphigus. The clinical polymorphism is reflected by histologic variability.8 , 9 The combination of acantholysis with interface dermatitis or with keratinocyte necrosis within a single biopsy specimen seems characteristic of paraneoplastic pemphigus.
The autoantibodies of paraneoplastic pemphigus differ from those of pemphigus vulgaris and pemphigus foliaceus in their antigenic specificity, as demon-strated by immunofluorescence testing and by immunoprecipitation. The antibodies in our five patients had broad tissue specificity, reacting with all epithelia, and immunoprecipitated a characteristic complex of four high-molecular-weight antigens. The broad specificity may be due to binding of the autoantibodies to desmoplakin I, a protein that is common to the cytoplasmic plaque of desmosomes in all epithelia and that has regions of marked homology with the 230-kd antigen of bullous pemphigoid.18 , 19 At present, we employ indirect immunofluorescence testing of rodent bladder as a convenient and cost-effective method of screening for this syndrome, since bladder epithelium has numerous desmosomes,20 but the antigens of pemphigus vulgaris and pemphigus foliaceus are not expressed in this tissue.
The passive transfer of an immunoglobulin solution from Patient 1 to mice produced cell—cell detachment in the epidermis and esophagus of the animals, providing evidence that serum from such patients contains autoantibodies that are pathogenic in paraneoplastic pemphigus and are not merely an epiphenomenon. A critical feature of this disorder is the specificity of the autoantibodies, which we have only partly determined. Other paraneoplastic autoimmune diseases have been better defined, and in these one can find biologic precedents for the kind of phenomena that we have described in paraneoplastic pemphigus. Paraneoplastic diseases include Eaton—Lambert (myasthenic) syndrome, sensory neuropathies,21 cerebellar dysfunction,22 and loss of visual acuity.23 , 24 These neurologic disorders are associated with autoantibodies that cross-react with both the patients' tumors and the target neuronal tissue.25 In paraneoplastic cerebellar degeneration, autoantibodies bind to antigens found in both the tumor and Purkinje cells. These autoantibodies recognize a tandem repeat-peptide consensus sequence consisting of the hexapeptide Phe—Leu—Glu—Asp—Val—Asp. These autoantibodies have broad cross-reactivity, for this hexapeptide is also present in some unrelated serum proteins, such as alpha1,-trypsin inhibitor and alpha2-macroglobulin.26 We are currently attempting to determine the epitope specificity of the autoantibodies of paraneoplastic pemphigus within antigens extracted from both patients' tumors and normal epithelia.
In summary, we suggest the following five criteria to define paraneoplastic pemphigus: painful mucosal erosions and a polymorphous skin eruption, with papular lesions progressing to blisters and erosive lesions affecting the trunk, extremities, and palms and soles, in the context of an occult or confirmed neoplasm; cutaneous histologic changes — intraepidermal acantholysis, keratinocyte necrosis, and vacuolar-interface dermatitis; deposition of IgG and complement in the epidermal intercellular spaces, as well as granular-linear complement deposition along the epidermal basement-membrane zone, on direct immunofluorescence testing; serum autoantibodies that bind the cell surface of skin and mucosae in a pattern typical of pemphigus, but in addition bind to simple, columnar, and transitional epithelia; and a complex of four proteins (250, 230, 210, and 190 kd) immunoprecipitated from keratinocytes by these autoantibodies. The 250-kd antigen apparently comigrates with desmoplakin I, and the 230-kd antigen comigrates with the 230-kd antigen of bullous pemphigoid. The 210-kd and 190-kd antigens are the most consistently and heavily labeled, but their identities have not yet been established.
We conclude that the five patients with neoplasms and polymorphous mucocutaneous lesions have a single autoimmune condition mediated by a unique and characteristic autoantibody response. Defining the events that result in this autoimmune disease should provide further insights into the relation between tumor surveillance and autoimmunity.
Supported in part by grants (RO1-AR-32490 and KO4-AR-01686 [to Dr. Anhalt]) from the National Institutes of Health.
Presented in part to the American Society for Clinical Investigation, Washington, D.C., May 1990.
We are indebted to Drs. R. Sontheimer, P.D. Cruz, and L. Matsuoka for assembling clinical material for this report.
Source Information
From the Departments of Dermatology (G.J.A., S.C.K., H.I., H.R., D.M., L.A.-A., R.S.L.) and Ophthalmology (D.A.J.), Johns Hopkins University School of Medicine, Baltimore; the Dermatology Branch, National Cancer Institute, Bethesda, Md. (J.R.S., N.J.K.); and Ohio State University, Columbus (M.K.). Address reprint requests to Dr. Anhalt at the Department of Dermatology, Johns Hopkins University, 600 N. Wolfe St., Baltimore, MD 21205.
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