Journal Article
. 2018 Sep; 174(6):1373-1387.e19.
doi: 10.1016/j.cell.2018.08.039.

A Structured Tumor-Immune Microenvironment in Triple Negative Breast Cancer Revealed by Multiplexed Ion Beam Imaging

Leeat Keren 1 Marc Bosse 1 Diana Marquez 1 Roshan Angoshtari 1 Samir Jain 1 Sushama Varma 1 Soo-Ryum Yang 1 Allison Kurian 1 David Van Valen 2 Robert West 1 Sean C Bendall 3 Michael Angelo 4 
  • PMID: 30193111
  •     51 References
  •     129 citations


The immune system is critical in modulating cancer progression, but knowledge of immune composition, phenotype, and interactions with tumor is limited. We used multiplexed ion beam imaging by time-of-flight (MIBI-TOF) to simultaneously quantify in situ expression of 36 proteins covering identity, function, and immune regulation at sub-cellular resolution in 41 triple-negative breast cancer patients. Multi-step processing, including deep-learning-based segmentation, revealed variability in the composition of tumor-immune populations across individuals, reconciled by overall immune infiltration and enriched co-occurrence of immune subpopulations and checkpoint expression. Spatial enrichment analysis showed immune mixed and compartmentalized tumors, coinciding with expression of PD1, PD-L1, and IDO in a cell-type- and location-specific manner. Ordered immune structures along the tumor-immune border were associated with compartmentalization and linked to survival. These data demonstrate organization in the tumor-immune microenvironment that is structured in cellular composition, spatial arrangement, and regulatory-protein expression and provide a framework to apply multiplexed imaging to immune oncology.

Keywords: Breast Cancer; Checkpoint; Imaging; MIBI; Mass spectrometry; Multiplexed Ion Beam Imaging; Proteomics; Systems Biology; Tumor Immunology; Tumor Microenvironment.

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The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications.
Yuanyuan Zhang, Zemin Zhang.
Cell Mol Immunol, 2020 Jul 03; 17(8). PMID: 32612154    Free PMC article.
Prognostic Value of Immune-Related Genes in the Tumor Microenvironment of Bladder Cancer.
Faping Li, Haolin Teng, +5 authors, Honglan Zhou.
Front Oncol, 2020 Aug 28; 10. PMID: 32850407    Free PMC article.
Systems biology approaches to measure and model phenotypic heterogeneity in cancer.
Aaron S Meyer, Laura M Heiser.
Curr Opin Syst Biol, 2020 Aug 31; 17. PMID: 32864511    Free PMC article.
Tissue Imaging by Mass Spectrometry: A Practical Guide for the Medicinal Chemist.
Robert W Johnson, Nari Talaty.
ACS Med Chem Lett, 2019 Feb 21; 10(2). PMID: 30783497    Free PMC article.
State-of-the-Art of Profiling Immune Contexture in the Era of Multiplexed Staining and Digital Analysis to Study Paraffin Tumor Tissues.
Edwin Roger Parra, Alejandro Francisco-Cruz, Ignacio Ivan Wistuba.
Cancers (Basel), 2019 Feb 23; 11(2). PMID: 30791580    Free PMC article.
Human Tumor-Infiltrating Dendritic Cells: From in Situ Visualization to High-Dimensional Analyses.
Margaux Hubert, Elisa Gobbini, +2 authors, Jenny Valladeau-Guilemond.
Cancers (Basel), 2019 Aug 02; 11(8). PMID: 31366174    Free PMC article.
Coordinated Cellular Neighborhoods Orchestrate Antitumoral Immunity at the Colorectal Cancer Invasive Front.
Christian M Schürch, Salil S Bhate, +11 authors, Garry P Nolan.
Cell, 2020 Aug 09; 182(5). PMID: 32763154    Free PMC article.
Integrated analysis of immune-related genes in endometrial carcinoma.
Yiru Wang, Yunduo Liu, +7 authors, Hang Yin.
Cancer Cell Int, 2020 Oct 08; 20. PMID: 33024415    Free PMC article.
Concepts of extracellular matrix remodelling in tumour progression and metastasis.
Juliane Winkler, Abisola Abisoye-Ogunniyan, Kevin J Metcalf, Zena Werb.
Nat Commun, 2020 Oct 11; 11(1). PMID: 33037194    Free PMC article.
Neoadjuvant Immune-Checkpoint Blockade in Triple-Negative Breast Cancer: Current Evidence and Literature-Based Meta-Analysis of Randomized Trials.
Daniele Marinelli, Marco Mazzotta, +14 authors, Patrizia Vici.
Cancers (Basel), 2020 Sep 10; 12(9). PMID: 32899209    Free PMC article.
Reconstruction of cell spatial organization from single-cell RNA sequencing data based on ligand-receptor mediated self-assembly.
Xianwen Ren, Guojie Zhong, +3 authors, Zemin Zhang.
Cell Res, 2020 Jun 17; 30(9). PMID: 32541867    Free PMC article.
LifeTime and improving European healthcare through cell-based interceptive medicine.
Nikolaus Rajewsky, Geneviève Almouzni, +48 authors, LifeTime Community Working Groups.
Nature, 2020 Sep 08; 587(7834). PMID: 32894860    Free PMC article.
The immune phenotype of tongue squamous cell carcinoma predicts early relapse and poor prognosis.
Giuseppe Troiano, Corrado Rubini, +6 authors, Marco Mascitti.
Cancer Med, 2020 Oct 14; 9(22). PMID: 33047888    Free PMC article.
Breast Cancer Heterogeneity and Response to Novel Therapeutics.
Mariona Baliu-Piqué, Atanasio Pandiella, Alberto Ocana.
Cancers (Basel), 2020 Nov 11; 12(11). PMID: 33167363    Free PMC article.
An immunogenic NSCLC microenvironment is associated with favorable survival in lung adenocarcinoma.
Kevin B Givechian, Chad Garner, +3 authors, Patrick Soon-Shiong.
Oncotarget, 2019 Apr 09; 10(19). PMID: 30956762    Free PMC article.
Deep learning for cellular image analysis.
Erick Moen, Dylan Bannon, +3 authors, David Van Valen.
Nat Methods, 2019 May 28; 16(12). PMID: 31133758
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IL-6 and IL-8 secreted by tumour cells impair the function of NK cells via the STAT3 pathway in oesophageal squamous cell carcinoma.
Jian Wu, Feng-Xia Gao, +9 authors, Tian-Yang Dai.
J Exp Clin Cancer Res, 2019 Jul 22; 38(1). PMID: 31324197    Free PMC article.
SITC cancer immunotherapy resource document: a compass in the land of biomarker discovery.
Siwen Hu-Lieskovan, Srabani Bhaumik, +14 authors, Holden T Maecker.
J Immunother Cancer, 2020 Dec 04; 8(2). PMID: 33268350    Free PMC article.
Channel Embedding for Informative Protein Identification from Highly Multiplexed Images.
Salma Abdel Magid, Won-Dong Jang, +4 authors, Hanspeter Pfister.
Med Image Comput Comput Assist Interv, 2020 Dec 08; 12265. PMID: 33283211    Free PMC article.
A single cell atlas of the human liver tumor microenvironment.
Hassan Massalha, Keren Bahar Halpern, +9 authors, Shalev Itzkovitz.
Mol Syst Biol, 2020 Dec 18; 16(12). PMID: 33332768    Free PMC article.
Single-Cell Spatial Analysis of Tumor and Immune Microenvironment on Whole-Slide Image Reveals Hepatocellular Carcinoma Subtypes.
Haiyue Wang, Yuming Jiang, +3 authors, Ruijiang Li.
Cancers (Basel), 2020 Dec 03; 12(12). PMID: 33260561    Free PMC article.
A quantitative analysis of the interplay of environment, neighborhood, and cell state in 3D spheroids.
Vito Rt Zanotelli, Matthias Leutenegger, +3 authors, Bernd Bodenmiller.
Mol Syst Biol, 2020 Dec 29; 16(12). PMID: 33369114    Free PMC article.
MAL2 drives immune evasion in breast cancer by suppressing tumor antigen presentation.
Yuanzhang Fang, Lifei Wang, +18 authors, Xinna Zhang.
J Clin Invest, 2020 Sep 30; 131(1). PMID: 32990678    Free PMC article.
PPP2R2B downregulation is associated with immune evasion and predicts poor clinical outcomes in triple-negative breast cancer.
Zheng Li, Yaming Li, Xiaolong Wang, Qifeng Yang.
Cancer Cell Int, 2021 Jan 08; 21(1). PMID: 33407498    Free PMC article.
Host tissue determinants of tumour immunity.
Hélène Salmon, Romain Remark, Sacha Gnjatic, Miriam Merad.
Nat Rev Cancer, 2019 Mar 15; 19(4). PMID: 30867580    Free PMC article.
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Cellular sociology regulates the hierarchical spatial patterning and organization of cells in organisms.
Shambavi Ganesh, Beliz Utebay, Jeremy Heit, Ahmet F Coskun.
Open Biol, 2020 Dec 16; 10(12). PMID: 33321061    Free PMC article.
The Impact of Immunofunctional Phenotyping on the Malfunction of the Cancer Immunity Cycle in Breast Cancer.
Takashi Takeshita, Toshihiko Torigoe, +3 authors, Kazuaki Takabe.
Cancers (Basel), 2021 Jan 06; 13(1). PMID: 33396390    Free PMC article.
Tumour heterogeneity and the evolutionary trade-offs of cancer.
Jean Hausser, Uri Alon.
Nat Rev Cancer, 2020 Feb 26; 20(4). PMID: 32094544
A High-Dimensional Window into the Micro-Environment of Triple Negative Breast Cancer.
Iris Nederlof, Hugo M Horlings, Christina Curtis, Marleen Kok.
Cancers (Basel), 2021 Jan 21; 13(2). PMID: 33467084    Free PMC article.
NF2 mutation status and tumor mutational burden correlate with immune cell infiltration in meningiomas.
John W Rutland, Corey M Gill, +10 authors, Mary Fowkes.
Cancer Immunol Immunother, 2020 Jul 15; 70(1). PMID: 32661686
Nanoscopic subcellular imaging enabled by ion beam tomography.
Ahmet F Coskun, Guojun Han, +8 authors, Garry P Nolan.
Nat Commun, 2021 Feb 06; 12(1). PMID: 33542220    Free PMC article.
Dissecting cellular crosstalk by sequencing physically interacting cells.
Amir Giladi, Merav Cohen, +11 authors, Ido Amit.
Nat Biotechnol, 2020 Mar 11; 38(5). PMID: 32152598
Targeted Chinese Medicine Delivery by A New Family of Biodegradable Pseudo-Protein Nanoparticles for Treating Triple-Negative Breast Cancer: In Vitro and In Vivo Study.
Hiu Yee Kwan, Qinghua Xu, +2 authors, Chih-Chang Chu.
Front Oncol, 2021 Feb 09; 10. PMID: 33552972    Free PMC article.
Single-cell metabolic profiling of human cytotoxic T cells.
Felix J Hartmann, Dunja Mrdjen, +12 authors, Sean C Bendall.
Nat Biotechnol, 2020 Sep 02; 39(2). PMID: 32868913    Free PMC article.
Single-Cell Virtual Cytometer allows user-friendly and versatile analysis and visualization of multimodal single cell RNAseq datasets.
Frédéric Pont, Marie Tosolini, +7 authors, Jean-Jacques Fournié.
NAR Genom Bioinform, 2021 Feb 13; 2(2). PMID: 33575582    Free PMC article.

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Immune cell infiltrates as prognostic biomarkers in pancreatic ductal adenocarcinoma: a systematic review and meta-analysis.
Andrew J McGuigan, Helen G Coleman, +4 authors, Richard C Turkington.
J Pathol Clin Res, 2021 Jan 23; 7(2). PMID: 33481339    Free PMC article.
Expansion sequencing: Spatially precise in situ transcriptomics in intact biological systems.
Shahar Alon, Daniel R Goodwin, +40 authors, Edward S Boyden.
Science, 2021 Jan 30; 371(6528). PMID: 33509999    Free PMC article.
Identification of distinct immune landscapes using an automated nine-color multiplex immunofluorescence staining panel and image analysis in paraffin tumor tissues.
Edwin R Parra, Jie Zhai, +12 authors, Cara Haymaker.
Sci Rep, 2021 Feb 27; 11(1). PMID: 33633208    Free PMC article.
Giotto: a toolbox for integrative analysis and visualization of spatial expression data.
Ruben Dries, Qian Zhu, +11 authors, Guo-Cheng Yuan.
Genome Biol, 2021 Mar 10; 22(1). PMID: 33685491    Free PMC article.
Profiles of immune cell infiltration and immune-related genes in the tumor microenvironment of esophageal squamous cell carcinoma.
Mingdi Liu, Faping Li, +5 authors, Zhixiang Xu.
BMC Med Genomics, 2021 Mar 12; 14(1). PMID: 33691689    Free PMC article.
Immune Checkpoint Inhibitors in Triple Negative Breast Cancer Treatment: Promising Future Prospects.
Remy Thomas, Ghaneya Al-Khadairi, Julie Decock.
Front Oncol, 2021 Mar 16; 10. PMID: 33718107    Free PMC article.
Genetic and non-genetic clonal diversity in cancer evolution.
James R M Black, Nicholas McGranahan.
Nat Rev Cancer, 2021 Mar 18; 21(6). PMID: 33727690
Neutrophil dynamics in the tumor microenvironment.
Amanda J McFarlane, Frédéric Fercoq, Seth B Coffelt, Leo M Carlin.
J Clin Invest, 2021 Mar 16; 131(6). PMID: 33720040    Free PMC article.
Leveraging microenvironmental synthetic lethalities to treat cancer.
Kevin J Metcalf, Alaa Alazzeh, Zena Werb, Valerie M Weaver.
J Clin Invest, 2021 Mar 16; 131(6). PMID: 33720045    Free PMC article.
Curcumin inhibits the growth of liver cancer by impairing myeloid-derived suppressor cells in murine tumor tissues.
Sha Tian, Liu Liao, +5 authors, Xuefei Tian.
Oncol Lett, 2021 Mar 19; 21(4). PMID: 33732362    Free PMC article.
TRIPODD: a Novel Fluorescence Imaging Platform for In Situ Quantification of Drug Distribution and Therapeutic Response.
Nathan P McMahon, Allison Solanki, +5 authors, Summer L Gibbs.
Mol Imaging Biol, 2021 Mar 23;. PMID: 33751366
Unraveling the cartography of the cancer ecosystem.
Roy Rabbie, Doreen Lau, Richard M White, David J Adams.
Genome Biol, 2021 Mar 26; 22(1). PMID: 33761966    Free PMC article.
Landscapes of cellular phenotypic diversity in breast cancer xenografts and their impact on drug response.
Dimitra Georgopoulou, Maurizio Callari, +21 authors, Carlos Caldas.
Nat Commun, 2021 Apr 02; 12(1). PMID: 33790302    Free PMC article.
Genetic and Non-Genetic Mechanisms Underlying Cancer Evolution.
Yelyzaveta Shlyakhtina, Katherine L Moran, Maximiliano M Portal.
Cancers (Basel), 2021 Apr 04; 13(6). PMID: 33803675    Free PMC article.
High-dimensional immunotyping of tumors grown in obese and non-obese mice.
Cara E Wogsland, Hilde E Lien, +5 authors, Nils Halberg.
Dis Model Mech, 2021 Mar 04; 14(4). PMID: 33653826    Free PMC article.
Spatially Resolved Mass Spectrometry at the Single Cell: Recent Innovations in Proteomics and Metabolomics.
Michael J Taylor, Jessica K Lukowski, Christopher R Anderton.
J Am Soc Mass Spectrom, 2021 Mar 04; 32(4). PMID: 33656885    Free PMC article.
Cytomapper: an R/bioconductor package for visualisation of highly multiplexed imaging data.
Nils Eling, Nicolas Damond, Tobias Hoch, Bernd Bodenmiller.
Bioinformatics, 2020 Dec 29;. PMID: 33367748    Free PMC article.
Unraveling Heterogeneity of Tumor Cells and Microenvironment and Its Clinical Implications for Triple Negative Breast Cancer.
Ke Jiang, Mengting Dong, Chunyang Li, Jiayu Sheng.
Front Oncol, 2021 Apr 16; 11. PMID: 33854958    Free PMC article.
Tumor microenvironment as a therapeutic target in cancer.
Yi Xiao, Dihua Yu.
Pharmacol Ther, 2020 Dec 02; 221. PMID: 33259885    Free PMC article.
CD244+ polymorphonuclear myeloid‑derived suppressor cells reflect the status of peritoneal dissemination in a colon cancer mouse model.
Yutaka Sugita, Kimihiro Yamashita, +12 authors, Yoshihiro Kakeji.
Oncol Rep, 2021 Apr 29; 45(6). PMID: 33907826    Free PMC article.
Using the R Package Spatstat to Assess Inhibitory Effects of Microregional Hypoxia on the Infiltration of Cancers of the Head and Neck Region by Cytotoxic T Lymphocytes.
Justus Kaufmann, Christophe A N Biscio, +4 authors, Arnulf Mayer.
Cancers (Basel), 2021 May 01; 13(8). PMID: 33923522    Free PMC article.
MAUI (MBI Analysis User Interface)-An image processing pipeline for Multiplexed Mass Based Imaging.
Alex Baranski, Idan Milo, +4 authors, Leeat Keren.
PLoS Comput Biol, 2021 Apr 20; 17(4). PMID: 33872301    Free PMC article.
Spatial clustering of CD68+ tumor associated macrophages with tumor cells is associated with worse overall survival in metastatic clear cell renal cell carcinoma.
Nicholas H Chakiryan, Gregory J Kimmel, +16 authors, Brandon J Manley.
PLoS One, 2021 Apr 22; 16(4). PMID: 33882057    Free PMC article.
Apolipoprotein B Is Associated With the Microenvironment of Cholangiocarcinoma.
Xiaofeng Xu, Diyu Chen, +7 authors, Jian Wu.
Front Oncol, 2021 May 07; 11. PMID: 33954113    Free PMC article.
Targeting inflammation in atherosclerosis - from experimental insights to the clinic.
Oliver Soehnlein, Peter Libby.
Nat Rev Drug Discov, 2021 May 13;. PMID: 33976384    Free PMC article.
Macrophage Biology and Mechanisms of Immune Suppression in Breast Cancer.
Anita K Mehta, Sapana Kadel, +2 authors, Jennifer L Guerriero.
Front Immunol, 2021 May 11; 12. PMID: 33968034    Free PMC article.
Triple-negative breast cancer: new treatment strategies in the era of precision medicine.
Song-Yang Wu, Hai Wang, Zhi-Ming Shao, Yi-Zhou Jiang.
Sci China Life Sci, 2020 Aug 18; 64(3). PMID: 32803712
Geospatial immune variability illuminates differential evolution of lung adenocarcinoma.
Khalid AbdulJabbar, Shan E Ahmed Raza, +21 authors, Yinyin Yuan.
Nat Med, 2020 May 29; 26(7). PMID: 32461698    Free PMC article.
Immune cell composition and functional marker dynamics from multiplexed immunohistochemistry to predict response to neoadjuvant chemotherapy in the WSG-ADAPT-TN trial.
Monika Graeser, Friedrich Feuerhake, +19 authors, Nadia Harbeck.
J Immunother Cancer, 2021 May 09; 9(5). PMID: 33963012    Free PMC article.
Breast cancer dormancy: need for clinically relevant models to address current gaps in knowledge.
Grace G Bushnell, Abhijeet P Deshmukh, +6 authors, Max S Wicha.
NPJ Breast Cancer, 2021 May 30; 7(1). PMID: 34050189    Free PMC article.
Biological explorations with nanoscale secondary ion mass spectrometry.
Frank Gyngard, Matthew L Steinhauser.
J Anal At Spectrom, 2019 Aug 01; 34(8). PMID: 34054180    Free PMC article.
Exploiting a New Approach to Destroy the Barrier of Tumor Microenvironment: Nano-Architecture Delivery Systems.
Yanting Sun, Yuling Li, Shuo Shi, Chunyan Dong.
Molecules, 2021 Jun 03; 26(9). PMID: 34062992    Free PMC article.
Phenotypic Heterogeneity of Triple-Negative Breast Cancer Mediated by Epithelial-Mesenchymal Plasticity.
Barbora Kvokačková, Ján Remšík, Mohit Kumar Jolly, Karel Souček.
Cancers (Basel), 2021 Jun 03; 13(9). PMID: 34063254    Free PMC article.
Highly Multiplexed Phenotyping of Immunoregulatory Proteins in the Tumor Microenvironment by CODEX Tissue Imaging.
Darci Phillips, Christian M Schürch, +3 authors, Sizun Jiang.
Front Immunol, 2021 Jun 08; 12. PMID: 34093591    Free PMC article.