Polyclonal lymphoid expansion drives paraneoplastic autoimmunity in neuroblastoma
Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding can...
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| Published in | Cell reports (Cambridge) Vol. 42; no. 8; p. 112879 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
29.08.2023
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2211-1247 2211-1247 |
| DOI | 10.1016/j.celrep.2023.112879 |
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| Abstract | Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB∗01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology.
[Display omitted]
•OMAS-associated neuroblastomas contain more B and T cells than control neuroblastomas•OMAS-associated neuroblastoma B and T cell repertoires are diverse, with small clones•Tertiary lymphoid structures are enriched in OMAS-associated neuroblastomas•Gene expression correlated to neurological symptom severity nominates autoantigens
Rosenberg et al. sought features of the systemic immune response underlying improved tumor outcomes and neurological dysfunction in patients with opsoclonus myoclonus ataxia syndrome (OMAS), an autoimmune disease caused by neuroblastoma. Diverse B and T cell lymphocytic infiltration organized in enriched tertiary lymphoid structures predominate in OMAS-associated tumors. |
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| AbstractList | Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB∗01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology. Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB*01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology. Rosenberg et al. sought features of the systemic immune response underlying improved tumor outcomes and neurological dysfunction in patients with opsoclonus myoclonus ataxia syndrome (OMAS), an autoimmune disease caused by neuroblastoma. Diverse B and T cell lymphocytic infiltration organized in enriched tertiary lymphoid structures predominate in OMAS-associated tumors. Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB∗01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology.Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB∗01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology. Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB 01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology. Neuroblastoma is a lethal childhood solid tumor of developing peripheral nerves. Two percent of children with neuroblastoma develop opsoclonus myoclonus ataxia syndrome (OMAS), a paraneoplastic disease characterized by cerebellar and brainstem-directed autoimmunity but typically with outstanding cancer-related outcomes. We compared tumor transcriptomes and tumor-infiltrating T and B cell repertoires from 38 OMAS subjects with neuroblastoma to 26 non-OMAS-associated neuroblastomas. We found greater B and T cell infiltration in OMAS-associated tumors compared to controls and showed that both were polyclonal expansions. Tertiary lymphoid structures (TLSs) were enriched in OMAS-associated tumors. We identified significant enrichment of the major histocompatibility complex (MHC) class II allele HLA-DOB∗01:01 in OMAS patients. OMAS severity scores were associated with the expression of several candidate autoimmune genes. We propose a model in which polyclonal auto-reactive B lymphocytes act as antigen-presenting cells and drive TLS formation, thereby supporting both sustained polyclonal T cell-mediated anti-tumor immunity and paraneoplastic OMAS neuropathology. [Display omitted] •OMAS-associated neuroblastomas contain more B and T cells than control neuroblastomas•OMAS-associated neuroblastoma B and T cell repertoires are diverse, with small clones•Tertiary lymphoid structures are enriched in OMAS-associated neuroblastomas•Gene expression correlated to neurological symptom severity nominates autoantigens Rosenberg et al. sought features of the systemic immune response underlying improved tumor outcomes and neurological dysfunction in patients with opsoclonus myoclonus ataxia syndrome (OMAS), an autoimmune disease caused by neuroblastoma. Diverse B and T cell lymphocytic infiltration organized in enriched tertiary lymphoid structures predominate in OMAS-associated tumors. |
| ArticleNumber | 112879 |
| Author | Irwin, Meredith S. Naranjo, Arlene Ulitsky, Igor Reshef, Dan de Alarcon, Pedro A. Greenstein, Erez Gibbs, David L. Yang, Lei Vaksman, Zalman Mikl, Martin Rosenberg, Miriam I. Matthay, Katherine K. Yaari, Gur Maris, John M. Friedman, Nir Peres, Ayelet Panzer, Jessica A. Buchkovich, Martin Santoni-Rugiu, Eric Salovin, Amy Weigman, Victor |
| AuthorAffiliation | 11 Division of Neurology, Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA 4 Bio-engineering, Faculty of Engineering, Bar Ilan University, Ramat Gan, Israel 1 Hebrew University of Jerusalem, Edmond Safra Campus, Givat Ram, Jerusalem 91904, Israel 6 Department of Pathology, Rigshospitalet, Copenhagen University Hospital and Department of Clinical Medicine, University of Copenhagen, 2100 Copenhagen, Denmark 13 Department of Biostatistics, University of Florida, Children’s Oncology Group Statistics & Data Center, Gainesville, FL, USA 3 Q2 Solutions, Durham, NC, USA 18 These authors contributed equally 8 Department of Human Biology, Faculty of Natural Sciences, University of Haifa, Mount Carmel, Haifa 31905, Israel 15 Department of Pediatrics, Hematology/Oncology, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA 10 Institute for Systems Biology, 401 Terry Avenue N, Seattle, WA 98109, USA 2 Department of Immunology, Weizmann Institute |
| AuthorAffiliation_xml | – name: 14 Department of Immunology & Regenerative Biology, Weizmann Institute of Science, Rehovot 7610001, Israel – name: 7 Pacific Northwest Research Institute, Seattle, WA 98122, USA – name: 2 Department of Immunology, Weizmann Institute of Science, Rehovot 7610001, Israel – name: 13 Department of Biostatistics, University of Florida, Children’s Oncology Group Statistics & Data Center, Gainesville, FL, USA – name: 8 Department of Human Biology, Faculty of Natural Sciences, University of Haifa, Mount Carmel, Haifa 31905, Israel – name: 9 New York Genome Center, New York, NY 10013, USA – name: 16 Department of Pediatrics, UCSF School of Medicine, San Francisco, CA 94143, USA – name: 11 Division of Neurology, Department of Pediatrics, Children’s Hospital of Philadelphia, Philadelphia, PA 19104, USA – name: 1 Hebrew University of Jerusalem, Edmond Safra Campus, Givat Ram, Jerusalem 91904, Israel – name: 10 Institute for Systems Biology, 401 Terry Avenue N, Seattle, WA 98109, USA – name: 12 Department of Pediatrics and Division of Hematology-Oncology, Hospital for Sick Children, University of Toronto, 555 University Avenue, Toronto, ON M5G1X8, Canada – name: 4 Bio-engineering, Faculty of Engineering, Bar Ilan University, Ramat Gan, Israel – name: 6 Department of Pathology, Rigshospitalet, Copenhagen University Hospital and Department of Clinical Medicine, University of Copenhagen, 2100 Copenhagen, Denmark – name: 3 Q2 Solutions, Durham, NC, USA – name: 19 Lead contact – name: 5 Bar Ilan Institute of Nanotechnologies and Advanced Materials, Bar Ilan University, Ramat Gan, Israel – name: 18 These authors contributed equally – name: 15 Department of Pediatrics, Hematology/Oncology, University of Illinois College of Medicine Peoria, Peoria, IL 61605, USA – name: 17 Department of Pediatrics and Division of Oncology, Children’s Hospital of Philadelphia and Perelman School of Medicine at the University of Pennsylvania, Philadelphia, PA 19104, USA |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37537844$$D View this record in MEDLINE/PubMed |
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| Keywords | CP: Immunology repertoires myoclonus ataxia autoimmunity CP: Cancer neuroblastoma immune profiling TCRB opsoclonus IgH paraneoplastic |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2023 The Authors. Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS M.I.R. designed the project with J.A.P. and led the project; performed tumor imaging, data analysis, and synthesis; and wrote the manuscript with contributions from all authors. E.G. led TCR analysis with contributions from D.R. and supervision by N.F. M.B. carried out bioinformatics analysis, including differential expression, SNP analysis, immune landscape signature, and HLA analyses, and implementation of immune subtype pipeline. L.Y. contributed network analyses, statistical analysis, and bioinformatics. Z.V. carried out transcriptome analysis. M.M. carried out machine learning experiments (XGBoost) and contributed statistical and bioinformatic analysis. A.P. led BCR analysis under the supervision of G.Y. E.S.-R. carried out the histopathological scoring and immunohistochemical phenotyping. A.S. contributed to immunohistochemical analyses. D.L.G. carried out additional immune subtype analysis and bioinformatics. I.U. contributed to bioinformatic analysis. A.N., M.S.I., K.K.M., and P.A.d.A. led the clinical trial from which samples for this study were obtained. V.W. supervised transcriptome analysis and HLA analysis and design and provided bioinformatics support. J.M.M. supervised the project. |
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| Title | Polyclonal lymphoid expansion drives paraneoplastic autoimmunity in neuroblastoma |
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