Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease

Abstract Introduction Castleman disease (CD) represents a spectrum of heterogeneous lymphoproliferative disorders sharing peculiar histopathological features, clinically subdivided into unicentric CD (UCD) and multicentric CD (MCD) and presenting with variable inflammatory symptoms. Interleukin (IL)...

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Main Authors: Marco Lucioni, Gaia Morello, Caterina Cristinelli, Sara Fraticelli, Giuseppe Neri, Erica Travaglino, Marco Minetto, Francesca Antoci, Paolo Libretti, Marcello Gambacorta, Luca Arcaini, Claudio Tripodo, Marco Paulli
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Language:English
Published: Wiley 2024-12-01
Series:eJHaem
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Online Access:https://doi.org/10.1002/jha2.1034
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author Marco Lucioni
Gaia Morello
Caterina Cristinelli
Sara Fraticelli
Giuseppe Neri
Erica Travaglino
Marco Minetto
Francesca Antoci
Paolo Libretti
Marcello Gambacorta
Luca Arcaini
Claudio Tripodo
Marco Paulli
author_facet Marco Lucioni
Gaia Morello
Caterina Cristinelli
Sara Fraticelli
Giuseppe Neri
Erica Travaglino
Marco Minetto
Francesca Antoci
Paolo Libretti
Marcello Gambacorta
Luca Arcaini
Claudio Tripodo
Marco Paulli
author_sort Marco Lucioni
collection DOAJ
description Abstract Introduction Castleman disease (CD) represents a spectrum of heterogeneous lymphoproliferative disorders sharing peculiar histopathological features, clinically subdivided into unicentric CD (UCD) and multicentric CD (MCD) and presenting with variable inflammatory symptoms. Interleukin (IL)‐6 and other cytokines play a major role in mediating CD inflammatory manifestations. Although the local microenvironment seems to be among the major sources of hypercytokinemia, the precise cellular origin of IL‐6 production in CD is still debated. Methods A series of five nodal CD of different subtypes (one UCD, two idiopathic MCDs [iMCDs], one HIV‐negative human herpesvirus 8 (HHV8)‐associated MCD, and one HIV‐positive HHV8‐associated MCD) and a non‐CD reactive control were tested using RNAscope analysis and a dual in situ hybridization (ISH)/immunohistochemistry technique, in order to quantify IL‐6 expression and its spatial distribution. Quantitative analyses of in situ mRNA were performed on digitalized slides using the HISTOQUANT software (3DHISTECH) and differences between cases were evaluated by the Kruskal‐Wallis test. Results RNA‐ISH documented increased IL‐6 expression in all CD lymph nodes, independently from clinical and pathological subtypes, however, the highest levels were found in HHV8+ cases and statistically significant differences in IL‐6 expression were found only between HHV8+ MCD and control case. Dual RNA‐ISH for IL6 coupled with immunohistochemistry analysis showed that IL‐6 was overexpressed in CD31‐positive endothelial cells in 5/5 CD tested cases but not in the control case. Conclusion Our findings suggest that nodal IL‐6 expression seems to be significantly upregulated in HHV8+ MCD, but a trend toward increased nodal IL‐6 expression was noticed also in UCD and iMCD‐not otherwise specified. CD31+ endothelial cells probably represent one of the major sources of IL‐6 production in the nodal microenvironment.
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spelling doaj-art-9df71f47d78f44859b6f62ab80a193a42025-08-20T02:49:17ZengWileyeJHaem2688-61462024-12-01561182118910.1002/jha2.1034Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman diseaseMarco Lucioni0Gaia Morello1Caterina Cristinelli2Sara Fraticelli3Giuseppe Neri4Erica Travaglino5Marco Minetto6Francesca Antoci7Paolo Libretti8Marcello Gambacorta9Luca Arcaini10Claudio Tripodo11Marco Paulli12Department of Molecular Medicine University of Pavia Pavia ItalyDepartment of Sciences for Health Promotion and Mother‐Child Care “G.D'Alessandro” Tumor Immunology Unit University of Palermo Palermo ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyPathology Unit, Fondazione IRCCS Policlinico “San Matteo” Pavia ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyPathology Unit, Fondazione IRCCS Policlinico “San Matteo” Pavia ItalySynLab Italia Srl Castenedolo ItalyIRCCS SynLab SDN Naples ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyDepartment of Sciences for Health Promotion and Mother‐Child Care “G.D'Alessandro” Tumor Immunology Unit University of Palermo Palermo ItalyDepartment of Molecular Medicine University of Pavia Pavia ItalyAbstract Introduction Castleman disease (CD) represents a spectrum of heterogeneous lymphoproliferative disorders sharing peculiar histopathological features, clinically subdivided into unicentric CD (UCD) and multicentric CD (MCD) and presenting with variable inflammatory symptoms. Interleukin (IL)‐6 and other cytokines play a major role in mediating CD inflammatory manifestations. Although the local microenvironment seems to be among the major sources of hypercytokinemia, the precise cellular origin of IL‐6 production in CD is still debated. Methods A series of five nodal CD of different subtypes (one UCD, two idiopathic MCDs [iMCDs], one HIV‐negative human herpesvirus 8 (HHV8)‐associated MCD, and one HIV‐positive HHV8‐associated MCD) and a non‐CD reactive control were tested using RNAscope analysis and a dual in situ hybridization (ISH)/immunohistochemistry technique, in order to quantify IL‐6 expression and its spatial distribution. Quantitative analyses of in situ mRNA were performed on digitalized slides using the HISTOQUANT software (3DHISTECH) and differences between cases were evaluated by the Kruskal‐Wallis test. Results RNA‐ISH documented increased IL‐6 expression in all CD lymph nodes, independently from clinical and pathological subtypes, however, the highest levels were found in HHV8+ cases and statistically significant differences in IL‐6 expression were found only between HHV8+ MCD and control case. Dual RNA‐ISH for IL6 coupled with immunohistochemistry analysis showed that IL‐6 was overexpressed in CD31‐positive endothelial cells in 5/5 CD tested cases but not in the control case. Conclusion Our findings suggest that nodal IL‐6 expression seems to be significantly upregulated in HHV8+ MCD, but a trend toward increased nodal IL‐6 expression was noticed also in UCD and iMCD‐not otherwise specified. CD31+ endothelial cells probably represent one of the major sources of IL‐6 production in the nodal microenvironment.https://doi.org/10.1002/jha2.1034HHV8IL‐6 transcriptsmulticentric Castleman diseaseRNA‐ISHunicentric Castleman disease
spellingShingle Marco Lucioni
Gaia Morello
Caterina Cristinelli
Sara Fraticelli
Giuseppe Neri
Erica Travaglino
Marco Minetto
Francesca Antoci
Paolo Libretti
Marcello Gambacorta
Luca Arcaini
Claudio Tripodo
Marco Paulli
Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
eJHaem
HHV8
IL‐6 transcripts
multicentric Castleman disease
RNA‐ISH
unicentric Castleman disease
title Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
title_full Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
title_fullStr Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
title_full_unstemmed Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
title_short Interleukin‐6 transcripts up‐regulation in lymph nodes from unicentric and multicentric Castleman disease
title_sort interleukin 6 transcripts up regulation in lymph nodes from unicentric and multicentric castleman disease
topic HHV8
IL‐6 transcripts
multicentric Castleman disease
RNA‐ISH
unicentric Castleman disease
url https://doi.org/10.1002/jha2.1034
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