Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing (original) (raw)

• Topalian, S. L. et al. Safety, activity, and immune correlates of anti–PD-1 antibody in cancer. N. Engl. J. Med. 366, 2443–2454 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Brahmer, J. R. et al. Safety and activity of anti–PD-L1 antibody in patients with advanced cancer. N. Engl. J. Med. 366, 2455–2465 (2012).
  Article PubMed PubMed Central CAS Google Scholar
• Hellmann, M. D. et al. Nivolumab plus ipilimumab as first-line treatment for advanced non-small-cell lung cancer (CheckMate 012): results of an open-label, phase 1, multicohort study. Lancet Oncol. 18, 31–41 (2017).
  Article PubMed CAS Google Scholar
• Tumeh, P. C. et al. PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature 515, 568–571 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Rizvi, N. A. et al. Mutational landscape determines sensitivity to PD-1 blockade in non–small cell lung cancer. Science 348, 124–128 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Huang, A. C. et al. T-cell invigoration to tumour burden ratio associated with anti-PD-1 response. Nature 545, 60–65 (2017).
  Article PubMed PubMed Central CAS Google Scholar
• Herbst, R. S., Heymach, J. V. & Lippman, S. M. Lung cancer. N. Engl. J. Med. 359, 1367–1380 (2008).
  Article PubMed CAS Google Scholar
• The Cancer Genome Atlas Research Network. Comprehensive molecular profiling of lung adenocarcinoma. Nature 511, 543–550 (2014).
  Article PubMed Central CAS Google Scholar
• Topalian, S. L., Taube, J. M., Anders, R. A. & Pardoll, D. M. Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat. Rev. Cancer 16, 275–287 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• van der Maaten, L. & Hinton, G. Visualizing data using t-SNE. J. Mach. Learn. Res. 9, 2579–2605 (2008).
  Google Scholar
• Rodriguez, A. & Laio, A. Clustering by fast search and find of density peaks. Science 344, 1492–1496 (2014).
  Article PubMed CAS Google Scholar
• Hidalgo, L. G., Einecke, G., Allanach, K. & Halloran, P. F. The transcriptome of human cytotoxic T cells: similarities and disparities among allostimulated CD4+CTL, CD8+CTL and NK cells. Am. J. Transplant. 8, 627–636 (2008).
  Article PubMed CAS Google Scholar
• Wherry, E. J. & Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 15, 486–499 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Spitzer, M. H. et al. Systemic immunity is required for effective cancer immunotherapy. Cell 168, 487–502.e15 (2017).
  Article PubMed PubMed Central CAS Google Scholar
• Gerlach, C. et al. The chemokine receptor CX3CR1 defines three antigen-experienced CD8 T cell subsets with distinct roles in immune surveillance and homeostasis. Immunity 45, 1270–1284 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Szabo, S. J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655–669 (2000).
  Article PubMed CAS Google Scholar
• Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381–386 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Tirosh, I. et al. Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Danaher, P. et al. Gene expression markers of tumor infiltrating leukocytes. bioRxiv https://doi.org/10.1101/068940 (2016).
• Zheng, C. et al. Landscape of infiltrating T cells in liver cancer revealed by single-cell sequencing. Cell 169, 1342–1356.e16 (2017).
  Article PubMed CAS Google Scholar
• Crawford, A. et al. Molecular and transcriptional basis of CD4+ T cell dysfunction during chronic infection. Immunity 40, 289–302 (2014).
  Article PubMed PubMed Central CAS Google Scholar
• Ganesan, A.-P. et al. Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer. Nat. Immunol. 18, 940–950 (2017).
  Article PubMed PubMed Central CAS Google Scholar
• Newman, A. M. et al. Robust enumeration of cell subsets from tissue expression profiles. Nat. Methods 12, 453–457 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Plitas, G. et al. Regulatory T cells exhibit distinct features in human breast cancer. Immunity 45, 1122–1134 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• De Simone, M. et al. Transcriptional landscape of human tissue lymphocytes unveils uniqueness of tumor-infiltrating T regulatory cells. Immunity 45, 1135–1147 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Bacher, P. et al. Regulatory T cell specificity directs tolerance versus allergy against aeroantigens in humans. Cell 167, 1067–1078.e16 (2016).
  Article PubMed CAS Google Scholar
• Grinberg-Bleyer, Y. et al. NF-κB c-Rel is crucial for the regulatory T cell immune checkpoint in cancer. Cell 170, 1096–1108.e13 (2017).
  Article PubMed CAS PubMed Central Google Scholar
• Wei, S. C. et al. Distinct cellular mechanisms underlie anti-CTLA-4 and anti-PD-1 checkpoint blockade. Cell 170, 1120–1133.e17 (2017).
  Article PubMed CAS PubMed Central Google Scholar
• Pauken, K. E. et al. Epigenetic stability of exhausted T cells limits durability of reinvigoration by PD-1 blockade. Science 354, 1160–1165 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Sen, D. R. et al. The epigenetic landscape of T cell exhaustion. Science 354, 1165–1169 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).
  Article PubMed PubMed Central CAS Google Scholar
• Ruitenberg, J. J., Mulder, C. B., Maino, V. C., Landay, A. L. & Ghanekar, S. A. VACUTAINER® CPTTM and Ficoll density gradient separation perform equivalently in maintaining the quality and function of PBMC from HIV seropositive blood samples. BMC Immunol. 7, 11 (2006).
  Article PubMed PubMed Central CAS Google Scholar
• Sallusto, F., Lenig, D., Förster, R., Lipp, M. & Lanzavecchia, A. Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401, 708–712 (1999).
  Article PubMed CAS Google Scholar
• Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014).
  Article PubMed CAS Google Scholar
• Wu, T. D. & Nacu, S. Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformatics 26, 873–881 (2010).
  Article PubMed PubMed Central CAS Google Scholar
• L. Lun, A. T., Bach, K. & Marioni, J. C. Pooling across cells to normalize single-cell RNA sequencing data with many zero counts. Genome Biol. 17, 75 (2016).
  Article PubMed Central CAS Google Scholar
• Stubbington, M. J. T. et al. T cell fate and clonality inference from single-cell transcriptomes. Nat. Methods 13, 329–332 (2016).
  Article PubMed PubMed Central CAS Google Scholar
• Reantragoon, R. et al. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210, 2305–2320 (2013).
  Article PubMed PubMed Central CAS Google Scholar
• Brennan, P. J., Brigl, M. & Brenner, M. B. Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat. Rev. Immunol. 13, 101–117 (2013).
  Article PubMed CAS Google Scholar
• Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47–e47 (2015).
  Article PubMed PubMed Central CAS Google Scholar
• Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci 102, 15545–15550 (2005).
  Article PubMed CAS Google Scholar
• Murtagh, F. & Legendre, P. Ward’s hierarchical agglomerative clustering method: which algorithms implement Ward’s criterion?. J. Classif. 31, 274–295 (2014).
  Article Google Scholar