Persistence of Autoreactive IgA-Secreting B Cells Despite Multiple Immunosuppressive Medications Including Rituximab
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1 Research Case Report/Case Series Persistence of Autoreactive IgA-Secreting B Cells Despite Multiple Immunosuppressive Medications Including Rituximab Yong He, MD; Michiko Shimoda, PhD; Yoko Ono, MD; Itzel Bustos Villalobos, MD, PhD; Anupam Mitra, MD; Thomas Konia, MD; Sergei A. Grando, MD; John J. Zone, MD; Emanual Maverakis, MD IMPORTANCE Immunobullous diseases mediated by IgA are often difficult to manage, but to date no mechanism has been proposed. Rituximab is an anti-cd2 monoclonal antibody that has demonstrated good efficacy in the treatment of refractory mucous membrane pemphigoid. However, not all cases of mucous membrane pemphigoid respond to rituximab. Herein we present a case of treatment-refractory mucous membrane pemphigoid and propose a mechanism to explain the lack of response to therapy. OBSERVATIONS Before treatment, direct immunofluorescent examination of a biopsy sample from the patient s perilesional skin demonstrated linear deposition of IgG and IgA along the dermoepidermal junction. After a multidrug immunosuppressive regimen that included rituximab, results of a second biopsy demonstrated only IgA along the dermoepidermal junction. This finding correlated well with flow cytometry data from the same patient that demonstrated a persistent population of IgA-secreting plasmablasts/plasma cells, despite depletion of CD2 + cells. In addition, results of immunohistochemical analysis of the perilesional skin remained positive for CD19 and CD138 immune cells (plasmablast/plasma cell markers). CONCLUSIONS AND RELEVANCE These findings suggest that current available immunosuppressive medications, including rituximab, cannot eliminate IgA-secreting plasmablasts/plasma cells, which are likely central to the pathophysiology of IgA-mediated immunobullous diseases. Future studies are needed to develop alternative therapeutic strategies that target autoreactive IgA-secreting plasmablasts/plasma cells. JAMA Dermatol. 21;11(6): doi:1.11/jamadermatol.21.9 Published online April 22, 21. Author Affiliations: Department of Dermatology, University of California, Davis, School of Medicine, Sacramento (He, Shimoda, Ono, Villalobos, Mitra, Maverakis); Department of Pathology, University of California, Davis, School of Medicine, Sacramento (Konia); Department of Dermatology, University of California, Irvine, School of Medicine (Grando); Department of Dermatology, University of Utah School of Medicine, Salt Lake City (Zone). Corresponding Author: Emanual Maverakis, MD, Department of Dermatology, University of California, Davis, School of Medicine, 331 C St, Ste 14, Sacramento, CA 9816 (emaverakis@ucdavis.edu). Mucous membrane pemphigoid (MMP), also known as cicatricial pemphigoid, constitutes a heterogeneous group of autoimmune blistering diseases that result from autoantibodies directed against epidermal basement membrane proteins. 1-4 Although presentations vary, patients can have involvement of their conjunctiva, sometimes experiencing a progressive disease course resulting in vision loss. Rituximab is a chimeric murine-human anti-cd2 monoclonal antibody that has demonstrated good efficacy in the treatment of severe refractory immunobullous diseases, including difficult-to-treat cases of MMP that involve the conjunctiva, trachea, and oropharynx. -9 The mechanism of action of rituximab is not entirely clear, but the drug depletes CD2-expressing cells, which constitute the majority of B cells. In most cases, this depletion results in a decrease in the circulating levels of autoreactive antibodies and a resolution of the autoimmune disease state. However, not all patients respond to rituximab. Herein we present a case of refractory MMP and propose that the preferential depletion of autoreactive IgGbut not IgA-secreting plasmablasts/plasma cells was responsible for the patient s treatment-resistant disease course. Report of a Case An older man presented to the Department of Dermatology, University of California, Davis, with generalized cutaneous bullae and oral erosions. A skin biopsy specimen underwent direct immunofluorescence and revealed a strong continuous linear basement membrane zone deposition of IgG, IgA, and C3 (Mayo Clinic, Rochester, Minnesota). In addition, BP18- and BP23-specific IgG were detected by enzyme-linked immunosorbent assay (titer, 1:11 for both; ARUP Laboratories, Salt Lake City, Utah). The patient subsequently developed bilateral conjunctival bullae and was treated with prednisone (8 646 JAMA Dermatology June 21 Volume 11, Number 6 (Reprinted) jamadermatology.com Copyright 21 American Medical Association. All rights reserved. Downloaded From: on 11/18/217
2 -Resistant IgA Immunobullous Diseases Case Report/Case Series Research Figure 1. Persistent Autoreactive IgA Despite Aggressive Immunosuppressive Therapy A course CD 19 + Differential Count, % 2 Mycophenolate mofetil Prednisone, dapsone, niacinamide Mycophenolic acid Azathioprine Rituximab Cyclophosphamide IVIG CD19 + cells Days B Ocular scarring C Direct immunofluorescence IgA pos IgG neg D Immunohistochemical analysis CD19 + CD19 + CD138 + CD138 + A, Timeline of treatment course and CD19 + cell depletion after rituximab treatment. After rituximab administration (represented by downward-facing antibody symbols), CD19 cells (diamonds) were rapidly depleted and remained persistently depleted without additional courses of rituximab. Each upward-facing antibody symbol represents days of intravenous immunoglobulin (IVIG) administration (4 mg/kg per day). Cyclophosphamide (solid black circles with attached lines) was administered as an intravenous pulse of 1 mg/kg. Diamond markers represent points when CD19 markers were checked, corresponding to the effectiveness of rituximab B cell depletion. B, Clinical photograph of the left eye demonstrating the ocular sequelae of persistent mucous membrane pemphigoid, including conjunctival hyperemia, corneal erosions, and lower lid symblepharon. C, Direct immunofluorescence demonstrating linear deposition of IgA along the dermoepidermal junction; IgG was undetectable (arrowhead). Direct immunofluorescence was performed by the Dermatopathology Service of University of California, Davis, School of Medicine. D, Immunohistochemical analysis demonstrates presence of CD19 + (original magnification 2 [left] and 4 [right]) and CD138 + (original magnification 2 [left] and 4 [right]) plasmablasts and plasma cells in the dermis. mg/d), dapsone (1 mg twice daily), mycophenolate mofetil hydrochloride (1 mg twice daily), and niacinamide ( mg 3 times daily), resulting in minimal improvement. Rituximab (37 mg/m 2 of body surface area once weekly for 4 weeks), intravenous immunoglobulin (4 mg/kg daily for days), and intravenous pulsed cyclophosphamide (1 mg/kg once monthly for months) were sequentially added to his treatment regimen, again resulting in minimal improvement (Figure 1A). Results of peripheral blood CD19 + counts persisted at less than 1%, confirming rituximab activity. Disease progression continued and eventually resulted in worsening oral ulcerations, odynophagia, and significant ocular scarring (Figure 1B). The jamadermatology.com (Reprinted) JAMA Dermatology June 21 Volume 11, Number Copyright 21 American Medical Association. All rights reserved. Downloaded From: on 11/18/217
3 Research Case Report/Case Series -Resistant IgA Immunobullous Diseases Figure 2. Persistence of IgA-Secreting Plasmablasts/Plasma Cells After Aggressive Immunosuppressive Therapy A B-cell population 8 CD CD CD19 Differential Count, % P < CD CD CD CD CD CD Plasmablasts/Plasma Cells, % 1 1 P <.8 B IgA-expressing CD3 - CD14 - CD2 - CD19 + CD IgA-Secreting Cells, % IgA IgA C IgA-expressing CD3 - CD14 - CD2 + CD19 + CD IgA IgA IgA-Secreting Cells, % A, Left, Levels of CD3 CD14 CD19 + cells are depleted after rituximab treatment (.1% vs 7.3% in healthy control sample; P =.2). Middle, CD2 CD27 + plasmablasts/plasma cells (red outline) represent a large proportion of the residual CD19 + cells after treatment (17.7% vs.7% in healthy control; P =.8). Right, Bar graphs illustrate changes in cell levels. indicates peripheral blood mononuclear cell. B, Levels of IgA-secreting cells (arrowhead) are increased in the CD2 CD19 + CD27 + population (originating from the red outline in part A) after treatment. C, Levels of IgA-secreting cells are increased within the CD2 + CD19 + CD27 + population (originating from the blue outline in part A) after treatment. 648 JAMA Dermatology June 21 Volume 11, Number 6 (Reprinted) jamadermatology.com Copyright 21 American Medical Association. All rights reserved. Downloaded From: on 11/18/217
4 -Resistant IgA Immunobullous Diseases Case Report/Case Series Research patient developed macular edema, and prednisone eye drops were added to his treatment regimen. His therapy was also switched from mycophenolate mofetil to azathioprine sodium, and he received several additional cycles of intravenous immunoglobulin, again with minimal improvement. After the patient did not respond to rituximab, intravenous immunoglobulin, and cyclophosphamide, a second biopsy specimen was obtained for direct immunofluorescence. The results demonstrated deposition of linear IgA, sparse granular C3, but no IgG along the dermoepidermal junction (Figure 1C). Results of a second enzyme-linked immunosorbent assay confirmed resolution of autoreactive BP18- and BP23-specific IgG (ARUP Laboratories). Given that the results of direct immunofluorescence studies demonstrated persistent deposition of autoreactive IgA, despite aggressive immunosuppressive therapy, peripheral blood was drawn for a detailed characterization of the treatmentresistant B cells. The medical ethics committee of the University of California, Davis, School of Medicine approved all aspects of this study according to the Declaration of Helsinki principles. Peripheral blood mononuclear cells were analyzed for expression of CD19, CD2, and CD27. In contrast to blood samples from healthy individuals, circulating CD2 CD19 + CD27 + cells representative of the plamablasts/plasma cell population (red outline) occupied a large proportion of the B-cell pool in the treated patient (17.7% vs.7%) (Figure 2A). Further analysis revealed that IgA-expressing cells were greatly expanded within the CD2 CD19 + CD27 + plasmablast/plasmacellpopulationaftertreatment, conservativelymeasuredat33.7%(figure2b). Anincreased population of CD2 + CD19 + CD27 + IgA-expressing memory B cells (blue outline) was also detected (2.9%) after treatment (Figure 2C). Thus, in our patient, IgA-expressing plasmablasts/ plasma cells were strongly resistant to aggressive immunosuppressive therapy that included B-cell depletion with rituximab. To gain further insight into the origin of the autoreactive IgA antibodies, the posttreatment perilesional skin biopsy specimen was reevaluated using immunohistochemical analysis for CD19 and CD138, which demonstrated the presence of CD19 + and CD138 + plasmablasts/plasma cells (Figure 1D). These immune cells are presumed to contribute to the pathogenic autoreactive IgA antibodies that were detected by direct immunofluorescence (Figure 1C). Furthermore, indirect immunofluorescence performed on a normal skin specimen with posttreatment serum using the salt split technique demonstrated IgA reactivity to the epidermal side of the split at a titer of 1:16 (ARUP Laboratories). No IgG was detectable via indirect immunofluorescence. Discussion Meietal 1 recently reported that rituximab fails to deplete selfreplenishing IgA B cells of mucosal origin, although their study lacked patients with IgA-mediated autoimmunity. We speculate that the treatment-resistant peripherally circulating IgAexpressing plasmablasts/plasma cells in our patient are also derived from a self-sufficient population of tissue-resident B cells that are thought to be inherently resistant to anti-cd2 therapy. 1,11 Our patient s MMP did not respond to several additional immunosuppressive medications in addition to rituximab. We therefore hypothesize that his autoreactive IgAsecreting cells are very slowly regenerating or are a long-lived population. Otherwise, they should have been susceptible to the nitrogen mustard alkylating agent, cyclophosphamide, which is especially toxic to proliferating cells. Also noteworthy was the depletion of B cells longer than 1 days after rituximab administration in our patient. This duration has been reported rarely in published studies. 12 The patient is now being treated with combination therapy consisting of prednisone, 2 mg/d, leflunomide, 2 mg/d, and dapsone, 1 mg twice daily. Conclusions To our knowledge, this report is the first to show that autoreactive IgA-secreting B cells are resistant to multiple immunosuppressive medications, including rituximab. Our study, although limited to a single case, may explain why MMP resulting from autoreactive IgA and IgG manifests more severe disease when compared with MMP mediated by IgG alone. 2 Future studies are needed to develop therapeutic strategies to target autoreactive rituximab-resistant IgA-expressing plasmablasts/ plasma cells. ARTICLE INFORMATION Accepted for Publication: January 1, 21. Published Online: April 22, 21. doi:1.11/jamadermatol Author Contributions: Drs He and Maverakis had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: He, Ono, Grando, Zone, Maverakis. Acquisition, analysis, or interpretation of data: He, Shimoda, Ono, Villalobos, Mitra, Konia, Grando, Maverakis. Drafting of the manuscript: He, Shimoda, Ono, Mitra, Grando, Maverakis. Critical revision of the manuscript for important intellectual content: He, Shimoda, Villalobos, Konia, Grando, Zone, Maverakis. Statistical analysis: Ono, Grando, Maverakis. Obtained funding: Grando, Maverakis. Administrative, technical, or material support: Shimoda, Villalobos, Mitra, Maverakis. Study supervision: Grando, Zone. Conflict of Interest Disclosures: None reported. Funding/Support: This study was supported by career awards from the Howard Hughes Medical Institute and the Burroughs Wellcome Fund (Dr Maverakis) and by New Innovator Award 1DP2 OD872 from the National Institutes of Health. Role of the Funder/Sponsor: The funding sources had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. REFERENCES 1. Schmidt E, Skrobek C, Kromminga A, et al. Cicatricial pemphigoid: IgA and IgG autoantibodies target epitopes on both intra- and extracellular domains of bullous pemphigoid antigen 18. Br J Dermatol. 21;14(): Schmidt E, Zillikens D. Pemphigoid diseases. Lancet. 213;381(9863): Kourosh AS, Yancey KB. Pathogenesis of mucous membrane pemphigoid. Dermatol Clin. 211;29(3): , x. 4. Chan LS, Ahmed AR, Anhalt GJ, et al. The first international consensus on mucous membrane pemphigoid: definition, diagnostic criteria, jamadermatology.com (Reprinted) JAMA Dermatology June 21 Volume 11, Number Copyright 21 American Medical Association. All rights reserved. Downloaded From: on 11/18/217
5 Research Case Report/Case Series -Resistant IgA Immunobullous Diseases pathogenic factors, medical treatment, and prognostic indicators. Arch Dermatol. 22;138(3): Foster CS, Chang PY, Ahmed AR. Combination of rituximab and intravenous immunoglobulin for recalcitrant ocular cicatricial pemphigoid: a preliminary report. Ophthalmology. 21;117(): Le Roux-Villet C, Prost-Squarcioni C, Alexandre M, et al. Rituximab for patients with refractory mucous membrane pemphigoid. Arch Dermatol. 211;147(7): Li Y, Foshee JB, Sontheimer RD. Sustained clinical response to rituximab in a case of life-threatening overlap subepidermal autoimmune blistering disease. J Am Acad Dermatol. 211;64 (4): Ross AH, Jaycock P, Cook SD, Dick AD, Tole DM. The use of rituximab in refractory mucous membrane pemphigoid with severe ocular involvement. Br J Ophthalmol. 29;93(4): , Schumann T, Schmidt E, Booken N, Goerdt S, Goebeler M. Successful treatment of mucous membrane pemphigoid with the anti CD-2 antibody rituximab. Acta Derm Venereol. 29;89 (1): Mei HE, Frölich D, Giesecke C, et al. Steady-state generation of mucosal IgA + plasmablasts is not abrogated by B-cell depletion therapy with rituximab. Blood. 21;116(24): Raderer M, Jäger G, Brugger S, et al. Rituximab for treatment of advanced extranodal marginal zone B cell lymphoma of the mucosa-associated lymphoid tissue lymphoma. Oncology. 23;6(4): Lu TY-T, Jónsdóttir T, van Vollenhoven RF, Isenberg DA. Prolonged B-cell depletion following rituximab therapy in systemic lupus erythematosus: a report of two cases [published correction appears in Ann Rheum Dis. 29;68():764]. Ann Rheum Dis. 28;67(1): NOTABLE NOTES Archeological Sites and Dermatologic Medications More Similar Than One May Think Kara M. Trapp, BA; Scott A. Norton, MD, MPH We noticed that names of medications often resemble names of ancient archeological sites. This may be a coincidence with no significance (a sphinx without a secret), but let s see how well you can tell one from the other. Here s your challenge: match the names of dermatologic medications and of Egyptian, Greek, and Mayan archeological sites with their appropriate descriptions (Figure). Author Affiliations: Georgetown University School of Medicine, Washington, DC (Trapp); Children s National Medical Center, Washington, DC (Norton). Corresponding Author: Kara M. Trapp, BA, 39 Reservoir Rd NW, Washington, DC 27 (kmt72@georgetown.edu). Medications and Ancient Archeological Sites Quiz A 1. Oxyrhynchus A. Mayan archeological site in Yucatán, Mexico 2. Oxybutynin B. Humanized antibody used for the treatment of chronic idiopathic urticaria and moderate to severe persistent allergic asthma 3. Oxcutzcab C. Medication used for the treatment of generalized hyperhidrosis 4. Omalizumab D. Egyptian archeological site located in Upper Egypt. Obelisk E. Medication used for the treatment of acute bacterial skin infections 6. Oritavancin F. Egyptian archeological site in Aswan, Egypt Quiz B 1. Epidaurus A. Medication used for the treatment of facial hirsutism 2. Everolimus B. Egyptian archeological site and island located in the Nile River 3. Epirus C. Medication used for the prevention of graft-vs-host disease 4. Etanercept D. Greek archeological site that was the home of Asclepius, the god of healing. Elephantine E. Medication used for the treatment of psoriatic arthritis and plaque psoriasis 6. Eflornithine F. Region of Greece that is rich in archeological sites Quiz C 1. Ingenol A. Medication used for the treatment of Raynaud phenomenon 2. Izamal B. Medication used for the treatment of melanoma 3. Ixtonton C. Mayan archeological site in Yucatán, Mexico 4. Isoxsuprine D. Mayan archeological site in the Petén Department of Guatemala. Izapa E. Medication used for the treatment of actinic keratosis 6. Ipilimumab F. Mayan archeological site in Chiapas, Mexico Quiz C Answers: 1E, 2C, 3D, 4A, F, 6B Quiz B Answers: 1D, 2C, 3F, 4E, B, 6A Quiz A Answers: 1D, 2C, 3A, 4B, F, 6E 6 JAMA Dermatology June 21 Volume 11, Number 6 (Reprinted) jamadermatology.com Copyright 21 American Medical Association. All rights reserved. Downloaded From: on 11/18/217
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