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Spatial landscape of malignant pleural and peritoneal mesothelioma tumor immune microenvironment

Xiaojun Ma, David Lembersky, Elena S Kim, Tullia C Bruno, Joseph R. Testa, View ORCID ProfileHatice U Osmanbeyoglu
doi: https://doi.org/10.1101/2023.09.06.556559
Xiaojun Ma
1UPMC Hillman Cancer Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
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David Lembersky
1UPMC Hillman Cancer Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
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Elena S Kim
1UPMC Hillman Cancer Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
4Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
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Tullia C Bruno
1UPMC Hillman Cancer Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
2Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
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Joseph R. Testa
3Cancer Prevention and Control Program, Fox Chase Cancer Center, Philadelphia, PA, USA
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Hatice U Osmanbeyoglu
1UPMC Hillman Cancer Center, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
4Department of Biomedical Informatics, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
5Department of Bioengineering, University of Pittsburgh School of Engineering, Pittsburgh, USA
6Department of Biostatistics, University of Pittsburgh School of Public Health, Pittsburgh, PA, USA
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  • ORCID record for Hatice U Osmanbeyoglu
  • For correspondence: osmanbeyogluhu@pitt.edu
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Abstract

Immunotherapies have shown modest clinical benefit thus far for malignant mesothelioma (MM). A deeper understanding of immune cell spatial distribution within the tumor immune microenvironment (TIME) is needed to identify interactions between tumor and different immune cell types that might impact the effectiveness of potential immunotherapies. We performed multiplex immunofluorescence (mIF) using tissue microarrays (TMAs, n=3) of samples from patients with malignant peritoneal (n=25) and pleural (n=88) mesothelioma (MPeM and MPM, respectively) to elucidate the spatial distributions of major immune cell populations and their association with LAG3, BAP1, NF2, and MTAP expression, the latter as a proxy for CDKN2A/B. We also analyzed the relationship between the spatial distribution of major immune cell types with MM patient prognosis and clinical features. The distribution of immune cells within the TIME is similar between MPM and MPeM. However, there is a higher level of interaction between immune cells and tumor cells in MPM than MPeM. Within MPM tumors, there is increased amount of interaction between tumor cells and CD8+ T cells in BAP1-low than in BAP1-high expressing tumors. The cell-cell interactions identified in this investigation have potential implications for the immune response against MM tumors and could be a factor in the different behaviors of MPM and MPeM. Our findings provide a valuable resource for the MM cancer research community and exemplifies the utility of spatial resolution within single-cell analyses.

Our mesothelioma spatial atlas mIF dataset is available at https://mesotheliomaspatialatlas.streamlit.app/.

Competing Interest Statement

JRT has provided legal consultation regarding the role of genetic alterations in MM. The remaining authors declare no conflict of interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted September 07, 2023.
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Spatial landscape of malignant pleural and peritoneal mesothelioma tumor immune microenvironment
Xiaojun Ma, David Lembersky, Elena S Kim, Tullia C Bruno, Joseph R. Testa, Hatice U Osmanbeyoglu
bioRxiv 2023.09.06.556559; doi: https://doi.org/10.1101/2023.09.06.556559
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Spatial landscape of malignant pleural and peritoneal mesothelioma tumor immune microenvironment
Xiaojun Ma, David Lembersky, Elena S Kim, Tullia C Bruno, Joseph R. Testa, Hatice U Osmanbeyoglu
bioRxiv 2023.09.06.556559; doi: https://doi.org/10.1101/2023.09.06.556559

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