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Microenvironment and Immunology

Neogenesis of Lymphoid Structures and Antibody Responses Occur in Human Melanoma Metastases

Arcadi Cipponi, Marjorie Mercier, Teofila Seremet, Jean-François Baurain, Ivan Théate, Joost van den Oord, Marguerite Stas, Thierry Boon, Pierre G. Coulie and Nicolas van Baren
Arcadi Cipponi
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Marjorie Mercier
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Teofila Seremet
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Jean-François Baurain
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Ivan Théate
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Joost van den Oord
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Marguerite Stas
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Thierry Boon
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Pierre G. Coulie
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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Nicolas van Baren
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
Authors' Affiliations: 1de Duve Institute, Université catholique de Louvain; 2Service d'Anatomie Pathologique, Cliniques Universitaires Saint-Luc; 3Ludwig Institute for Cancer Research Ltd, Brussels Branch, 4WELBIO, de Duve Institute, Université catholique de Louvain, Brussels; 5Medical Oncology Department, Centre du Cancer des Cliniques Universitaires Saint-Luc, Université catholique de Louvain, Bruxelles; 6Laboratory for Translational Cell & Tissue Research, Department of Imaging and Pathology, and 7Department of Surgical Oncology, University Hospitals, Katholieke Universiteit Leuven, Leuven, Belgium
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DOI: 10.1158/0008-5472.CAN-12-1377 Published August 2012
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Abstract

Lymphoid neogenesis, or the development of lymphoid structures in nonlymphoid organs, is frequently observed in chronically inflamed tissues, during the course of autoimmune, infectious, and chronic graft rejection diseases, in which a sustained lymphocyte activation occurs in the presence of persistent antigenic stimuli. The presence of such ectopic lymphoid structures has also been reported in primary lung, breast, and germline cancers, but not yet in melanoma. In this study, we observed ectopic lymphoid structures, defined as lymphoid follicles comprising clusters of B lymphocytes and follicular dendritic cells (DC), associated with high endothelial venules (HEV) and clusters of T cells and mature DCs, in 7 of 29 cutaneous metastases from melanoma patients. Some follicles contained germinal centers. In contrast to metastatic lesions, primary melanomas did not host follicles, but many contained HEVs, suggesting an incomplete lymphoid neogenesis. Analysis of the repertoire of rearranged immunoglobulin genes in the B cells of microdissected follicles revealed clonal amplification, somatic mutation and isotype switching, indicating a local antigen-driven B-cell response. Surprisingly, IgA responses were observed despite the nonmucosal location of the follicles. Taken together, our findings show the existence of lymphoid neogenesis in melanoma and suggest that the presence of functional ectopic lymphoid structures in direct contact with the tumor makes the local development of antimelanoma B- and T-cell responses possible. Cancer Res; 72(16); 3997–4007. ©2012 AACR.

Footnotes

  • Note: Supplementary data for this article are available at Cancer Research Online (http://cancerres.aacrjournals.org/).

  • Received April 10, 2012.
  • Revision received May 18, 2012.
  • Accepted May 19, 2012.
  • ©2012 American Association for Cancer Research.
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Cancer Research: 72 (16)
August 2012
Volume 72, Issue 16
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Neogenesis of Lymphoid Structures and Antibody Responses Occur in Human Melanoma Metastases
Arcadi Cipponi, Marjorie Mercier, Teofila Seremet, Jean-François Baurain, Ivan Théate, Joost van den Oord, Marguerite Stas, Thierry Boon, Pierre G. Coulie and Nicolas van Baren
Cancer Res August 15 2012 (72) (16) 3997-4007; DOI: 10.1158/0008-5472.CAN-12-1377

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Neogenesis of Lymphoid Structures and Antibody Responses Occur in Human Melanoma Metastases
Arcadi Cipponi, Marjorie Mercier, Teofila Seremet, Jean-François Baurain, Ivan Théate, Joost van den Oord, Marguerite Stas, Thierry Boon, Pierre G. Coulie and Nicolas van Baren
Cancer Res August 15 2012 (72) (16) 3997-4007; DOI: 10.1158/0008-5472.CAN-12-1377
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