Interactions between cancer cells and immune cells drive transitions to mesenchymal-like states in glioblastoma

Cancer Cell - Tập 39 - Trang 779-792.e11 - 2021
Toshiro Hara1,2,3,4, Rony Chanoch-Myers5, Nathan D. Mathewson3,6, Chad Myskiw4, Lyla Atta7, Lillian Bussema1,2,3, Stephen W. Eichhorn8,9, Alissa C. Greenwald5, Gabriela S. Kinker5,10, Christopher Rodman1, L. Nicolas Gonzalez Castro1,2,3,11, Hiroaki Wakimoto12, Orit Rozenblatt-Rosen2,3, Xiaowei Zhuang8,9, Jean Fan7, Tony Hunter4, Inder M. Verma4, Kai W. Wucherpfennig3,6, Aviv Regev2,3,13, Mario L. Suvà1,2,3
1Department of Pathology and Center for Cancer Research, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
2Klarman Cell Observatory, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
3Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
4Laboratory of Genetics, Salk Institute for Biological Studies, La Jolla, CA 92037, USA
5Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot 761001, Israel
6Department of Cancer Immunology and Virology, Department of Microbiology and Immunobiology, Department of Neurology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, MA 02215, USA
7Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD 21218 USA
8Howard Hughes Medical Institute, Harvard University, Cambridge, MA 02138, USA
9Department of Chemistry and Chemical Biology, Department of Physics, Harvard University, Cambridge, MA 02138, USA
10Department of Physiology, Institute of Bioscience, University of Sao Paulo, Sao Paulo, Brazil
11Department of Neurology and Center for Neuro-Oncology, Brigham and Women’s - Dana-Farber Cancer Center and Harvard Medical School, Boston, MA 02115, USA
12Department of Neurosurgery, Massachusetts General Hospital and Harvard Medical School, Boston, MA 02114, USA
13Howard Hughes Medical Institute, Koch Institute for Integrative Cancer Research, Department of Biology, MIT, Cambridge, MA 02139, USA

Tài liệu tham khảo

Beyer, 2012, High-resolution transcriptome of human macrophages, PLoS One, 7, e45466, 10.1371/journal.pone.0045466 Bhat, 2013, Mesenchymal differentiation mediated by NF-kappaB promotes radiation resistance in glioblastoma, Cancer Cell, 24, 331, 10.1016/j.ccr.2013.08.001 Bhat, 2011, The transcriptional coactivator TAZ regulates mesenchymal differentiation in malignant glioma, Genes Dev., 25, 2594, 10.1101/gad.176800.111 Butowski, 2016, Orally administered colony stimulating factor 1 receptor inhibitor PLX3397 in recurrent glioblastoma: an Ivy Foundation Early Phase Clinical Trials Consortium phase II study, Neuro Oncol., 18, 557, 10.1093/neuonc/nov245 Carro, 2010, The transcriptional network for mesenchymal transformation of brain tumours, Nature, 463, 318, 10.1038/nature08712 Chen, 2015, RNA imaging. Spatially resolved, highly multiplexed RNA profiling in single cells, Science, 348, aaa6090, 10.1126/science.aaa6090 Cosset, 2017, Glut3 addiction is a druggable vulnerability for a molecularly defined subpopulation of glioblastoma, Cancer Cell, 32, 856, 10.1016/j.ccell.2017.10.016 de Souza, 2018, A distinct DNA methylation shift in a subset of glioma CpG island methylator phenotypes during tumor recurrence, Cell Rep., 23, 637, 10.1016/j.celrep.2018.03.107 Filbin, 2018, Developmental and oncogenic programs in H3K27M gliomas dissected by single-cell RNA-seq, Science, 360, 331, 10.1126/science.aao4750 Friedmann-Morvinski, 2012, Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice, Science, 338, 1080, 10.1126/science.1226929 Furnari, 2015, Heterogeneity of epidermal growth factor receptor signalling networks in glioblastoma, Nat. Rev. Cancer, 15, 302, 10.1038/nrc3918 Gabrusiewicz, 2016, Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype, JCI Insight, 1, e85841, 10.1172/jci.insight.85841 Geirsdottir, 2019, Cross-species single-cell analysis reveals divergence of the primate microglia program, Cell, 179, 1609, 10.1016/j.cell.2019.11.010 Gilbert, 2014, A randomized trial of bevacizumab for newly diagnosed glioblastoma, New Engl. J. Med., 370, 699, 10.1056/NEJMoa1308573 Grabowski, 2020, Immune suppression in gliomas, J. Neurooncol., 151, 3, 10.1007/s11060-020-03483-y Hara, 2019, Modeling gliomas using two recombinases, Cancer Res., 79, 3983, 10.1158/0008-5472.CAN-19-0717 Jahani-Asl, 2016, Control of glioblastoma tumorigenesis by feed-forward cytokine signaling, Nat. Neurosci., 19, 798, 10.1038/nn.4295 Jones, 2018, Recent insights into targeting the IL-6 cytokine family in inflammatory diseases and cancer, Nat. Rev. Immunol., 18, 773, 10.1038/s41577-018-0066-7 Junk, 2017, Oncostatin M promotes cancer cell plasticity through cooperative STAT3-SMAD3 signaling, Oncogene, 36, 4001, 10.1038/onc.2017.33 Kinker, 2020, Pan-cancer single cell RNA-seq uncovers recurring programs of cellular heterogeneity, bioRxiv, 807552 Koga, 2019, When less is more: gaining power through gene rearrangement of amplified EGFR, Oncotarget, 10, 2116, 10.18632/oncotarget.26786 Korsunsky, 2019, Fast, sensitive and accurate integration of single-cell data with Harmony, Nat. Methods, 16, 1289, 10.1038/s41592-019-0619-0 Kucia-Tran, 2016, Overexpression of the oncostatin-M receptor in cervical squamous cell carcinoma is associated with epithelial-mesenchymal transition and poor overall survival, Br. J. Cancer, 115, 212, 10.1038/bjc.2016.199 Li, 2011, RSEM: accurate transcript quantification from RNA-seq data with or without a reference genome, BMC Bioinformatics, 12, 323, 10.1186/1471-2105-12-323 Li, 2017, Classifying Drosophila olfactory projection neuron subtypes by single-cell RNA sequencing, Cell, 171, 1206, 10.1016/j.cell.2017.10.019 Li, 2019, Developmental heterogeneity of microglia and brain myeloid cells revealed by deep single-cell RNA sequencing, Neuron, 101, 207, 10.1016/j.neuron.2018.12.006 Louis, 2016 Mantovani, 2017, Tumour-associated macrophages as treatment targets in oncology, Nat. Rev. Clin. Oncol., 14, 399, 10.1038/nrclinonc.2016.217 Mariathasan, 2018, TGFbeta attenuates tumour response to PD-L1 blockade by contributing to exclusion of T cells, Nature, 554, 544, 10.1038/nature25501 Masuda, 2019, Spatial and temporal heterogeneity of mouse and human microglia at single-cell resolution, Nature, 566, 388, 10.1038/s41586-019-0924-x Mathewson, 2021, Inhibitory CD161 receptor identified in glioma-infiltrating T cells by single-cell analysis, Cell, 184, 1281, 10.1016/j.cell.2021.01.022 Moffitt, 2018, Molecular, spatial, and functional single-cell profiling of the hypothalamic preoptic region, Science, 362, eaau5324, 10.1126/science.aau5324 Moffitt, 2016, High-performance multiplexed fluorescence in situ hybridization in culture and tissue with matrix imprinting and clearing, Proc. Natl. Acad. Sci. U S A, 113, 14456, 10.1073/pnas.1617699113 Neftel, 2019, An integrative model of cellular states, plasticity, and genetics for glioblastoma, Cell, 178, 1, 10.1016/j.cell.2019.06.024 Ozawa, 2014, Most human non-GCIMP glioblastoma subtypes evolve from a common proneural-like precursor glioma, Cancer Cell, 26, 288, 10.1016/j.ccr.2014.06.005 Patel, 2014, Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma, Science, 344, 1396, 10.1126/science.1254257 Picelli, 2014, Full-length RNA-seq from single cells using Smart-seq2, Nat. Protoc., 9, 171, 10.1038/nprot.2014.006 Puram, 2017, Single-cell transcriptomic analysis of primary and metastatic tumor ecosystems in head and neck cancer, Cell, 171, 1611, 10.1016/j.cell.2017.10.044 Ramilowski, 2015, A draft network of ligand-receptor-mediated multicellular signalling in human, Nat. Commun., 6, 7866, 10.1038/ncomms8866 Rapoport, 2015, NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma, Nat. Med., 21, 914, 10.1038/nm.3910 Robbins, 2008, Single and dual amino acid substitutions in TCR CDRs can enhance antigen-specific T cell functions, J. Immunol., 180, 6116, 10.4049/jimmunol.180.9.6116 Rodig, 2018, MHC proteins confer differential sensitivity to CTLA-4 and PD-1 blockade in untreated metastatic melanoma, Sci. Transl. Med., 10, eaar3342, 10.1126/scitranslmed.aar3342 Rooj, 2017, microRNA-mediated dynamic bidirectional shift between the subclasses of glioblastoma stem-like cells, Cell Rep., 19, 2026, 10.1016/j.celrep.2017.05.040 Saha, 2017, Macrophage polarization contributes to glioblastoma eradication by combination immunovirotherapy and immune checkpoint blockade, Cancer Cell, 32, 253, 10.1016/j.ccell.2017.07.006 Shibue, 2017, EMT, CSCs, and drug resistance: the mechanistic link and clinical implications, Nat. Rev. Clin. Oncol., 14, 611, 10.1038/nrclinonc.2017.44 Smigiel, 2017, Potent EMT and CSC phenotypes are induced by oncostatin-M in pancreatic cancer, Mol. Cancer Res., 15, 478, 10.1158/1541-7786.MCR-16-0337 Sottoriva, 2013, Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics, Proc. Natl. Acad. Sci. U S A, 110, 4009, 10.1073/pnas.1219747110 Stupp, 2005, Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma, New Engl. J. Med., 352, 987, 10.1056/NEJMoa043330 Tanay, 2017, Scaling single-cell genomics from phenomenology to mechanism, Nature, 541, 331, 10.1038/nature21350 Terry, 2017, New insights into the role of EMT in tumor immune escape, Mol. Oncol., 11, 824, 10.1002/1878-0261.12093 Tirosh, 2019, Deciphering human tumor biology by single-cell expression profiling, Annu. Rev. Cancer Biol., 3, 151, 10.1146/annurev-cancerbio-030518-055609 Tirosh, 2016, Single-cell RNA-seq supports a developmental hierarchy in human oligodendroglioma, Nature, 539, 309, 10.1038/nature20123 Venteicher, 2017, Decoupling genetics, lineages, and microenvironment in IDH-mutant gliomas by single-cell RNA-seq, Science, 355, eaai8478, 10.1126/science.aai8478 Verhaak, 2010, Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1, Cancer Cell, 17, 98, 10.1016/j.ccr.2009.12.020 Wakimoto, 2012, Maintenance of primary tumor phenotype and genotype in glioblastoma stem cells, Neuro-Oncology, 14, 132, 10.1093/neuonc/nor195 Wang, 2017, Tumor evolution of glioma-intrinsic gene expression subtypes associates with immunological changes in the microenvironment, Cancer Cell, 32, 42, 10.1016/j.ccell.2017.06.003 Wen, 2020, Glioblastoma in adults: a Society for Neuro-Oncology (SNO) and European Society of Neuro-Oncology (EANO) consensus review on current management and future directions, Neuro-Oncology, 22, 1073, 10.1093/neuonc/noaa106 West, 2017, Oncostatin M drives intestinal inflammation and predicts response to tumor necrosis factor-neutralizing therapy in patients with inflammatory bowel disease, Nat. Med., 23, 579, 10.1038/nm.4307 Xia, 2019, Spatial transcriptome profiling by MERFISH reveals subcellular RNA compartmentalization and cell cycle-dependent gene expression, Proc. Natl. Acad. Sci. U S A, 116, 19490, 10.1073/pnas.1912459116 Zhao, 2019, Immune and genomic correlates of response to anti-PD-1 immunotherapy in glioblastoma, Nat. Med., 25, 462, 10.1038/s41591-019-0349-y Zhong, 2018, A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex, Nature, 555, 524, 10.1038/nature25980
Thông tin
Thông tin xuất bản

Cancer Cell

Tập 39

779-792.e11

Thông tin tác giả