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Single-cell spatial immune landscapes of primary and metastatic brain tumours

by Sorin, Mark , Rezanejad, Morteza , Siegel, Peter M. , Karimi, Elham , Fallah, Parvaneh , Petrecca, Kevin , Yu, Miranda W. , Zuo, Dongmei , Ramsay, LeeAnn , Watson, Ian R. , Maritan, Sarah M. , Park, Morag , Perus, Lucas J. M. , Chan, Jennifer A. , Kloosterman, Daan J. , Fiset, Benoit , Roldan Urgoiti, Gloria , Lam, Stephanie , Wei, Yuhong , Alsajjan, Roa , Brandsma, Dieta , Doré, Samuel , Dankner, Matthew , Akkari, Leila , Senger, Donna L. , Guiot, Marie-Christine , Walsh, Logan A. , Quail, Daniela F.

in 14 / 14/105 / 631/114/2400 / 631/250/580 / 631/67/1922 / 631/67/327 / Brain / Brain - immunology / Brain - pathology / Brain cancer / Brain Neoplasms - immunology / Brain Neoplasms - pathology / Brain Neoplasms - secondary / Brain tumors / Cancer / Cytometry / Cytotoxicity / Datasets as Topic / Dendritic cells / Glioblastoma / Glioblastoma - immunology / Glioblastoma - pathology / Glioma / Glioma - immunology / Glioma - pathology / Histopathology / Humanities and Social Sciences / Humans / Immunology / Lymphocytes / Macrophages / Macrophages - enzymology / Melanoma / Metastases / Metastasis / Microenvironments / multidisciplinary / Neoplasm Metastasis / Neuroimaging / Neutrophils / Patients / Peroxidase / Science / Science (multidisciplinary) / Single-Cell Analysis / Spatial discrimination / Spatial resolution / Survival / Tumor microenvironment / Tumor Microenvironment - immunology / Tumors

2023

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Single-cell spatial immune landscapes of primary and metastatic brain tumours

2023

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2023

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Journal Article

Single-cell spatial immune landscapes of primary and metastatic brain tumours

Sorin, Mark,

Rezanejad, Morteza,

Siegel, Peter M.,

Karimi, Elham,

Fallah, Parvaneh,

Petrecca, Kevin,

Yu, Miranda W.,

Zuo, Dongmei,

Ramsay, LeeAnn,

Watson, Ian R.,

Maritan, Sarah M.,

Park, Morag,

Perus, Lucas J. M.,

Chan, Jennifer A.,

Kloosterman, Daan J.,

Fiset, Benoit,

Roldan Urgoiti, Gloria,

Lam, Stephanie,

Wei, Yuhong,

Alsajjan, Roa,

Brandsma, Dieta,

Doré, Samuel,

Dankner, Matthew,

Akkari, Leila,

Senger, Donna L.,

Guiot, Marie-Christine,

Walsh, Logan A.,

Quail, Daniela F.

2023

Overview

Single-cell technologies have enabled the characterization of the tumour microenvironment at unprecedented depth and have revealed vast cellular diversity among tumour cells and their niche. Anti-tumour immunity relies on cell–cell relationships within the tumour microenvironment 1 , 2 , yet many single-cell studies lack spatial context and rely on dissociated tissues 3 . Here we applied imaging mass cytometry to characterize the immunological landscape of 139 high-grade glioma and 46 brain metastasis tumours from patients. Single-cell analysis of more than 1.1 million cells across 389 high-dimensional histopathology images enabled the spatial resolution of immune lineages and activation states, revealing differences in immune landscapes between primary tumours and brain metastases from diverse solid cancers. These analyses revealed cellular neighbourhoods associated with survival in patients with glioblastoma, which we leveraged to identify a unique population of myeloperoxidase (MPO)-positive macrophages associated with long-term survival. Our findings provide insight into the biology of primary and metastatic brain tumours, reinforcing the value of integrating spatial resolution to single-cell datasets to dissect the microenvironmental contexture of cancer. Imaging mass cytometry of human brain tumours provides spatial information that, combined with existing transcriptomic data, reveals the existence of a cellular neighbourhood containing a rare macrophage population associated with prolonged survival.

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Publisher

Nature Publishing Group UK,Nature Publishing Group

Subject

/ 14/105

/ Brain