CD103+CD8+ TRM Cells Accumulate in Tumors of Anti-PD-1-Responder Lung Cancer Patients and Are Tumor-Reactive Lymphocytes Enriched with Tc17

Cell Reports Medicine - Tập 1 - Trang 100127 - 2020
Stéphanie Corgnac1, Ines Malenica1, Laura Mezquita2, Edouard Auclin3, Elodie Voilin1, Jamila Kacher1, Heloise Halse1, Laetitia Grynszpan1, Nicolas Signolle4, Thibault Dayris5, Marine Leclerc1, Nathalie Droin5, Vincent de Montpréville1,6, Olaf Mercier6, Pierre Validire7, Jean-Yves Scoazec5, Christophe Massard8, Salem Chouaib1, David Planchard2, Julien Adam1
1INSERM UMR 1186, Integrative Tumor Immunology and Immunotherapy, Gustave Roussy, Faculté de Médecine, Université Paris-Sud, Université Paris-Saclay, 94805 Villejuif, France
2Department of Cancer Medicine, Gustave Roussy, Institut d’Oncologie Thoracique, Gustave Roussy, Université Paris-Saclay, 94805 Villejuif, France
3Gastrointestinal and Medical Oncology Department, Hôpital Européen Georges Pompidou, Paris, France
4INSERM Unit U981, Department of Experimental Pathology, Gustave Roussy, Université Paris-Sud, Université Paris-Saclay, 94805 Villejuif, France
5Department of Biology and Medical Pathology, Gustave Roussy, 94805 Villejuif, France
6Hôpital Marie-Lannelongue, Service d’Anatomie Pathologique, 92350 Le-Plessis-Robinson, France
7Institut Mutualiste Montsouris, Service d’Anatomie Pathologique, 75014 Paris, France
8Drug Development Department, Gustave Roussy, Université Paris-Saclay, 94805 Villejuif, France

Tài liệu tham khảo

Tumeh, 2014, PD-1 blockade induces responses by inhibiting adaptive immune resistance, Nature, 515, 568, 10.1038/nature13954 McGranahan, 2016, Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade, Science, 351, 1463, 10.1126/science.aaf1490 Webb, 2014, Tumor-infiltrating lymphocytes expressing the tissue resident memory marker CD103 are associated with increased survival in high-grade serous ovarian cancer, Clin. Cancer Res., 20, 434, 10.1158/1078-0432.CCR-13-1877 Djenidi, 2015, CD8+CD103+ tumor-infiltrating lymphocytes are tumor-specific tissue-resident memory T cells and a prognostic factor for survival in lung cancer patients, J. Immunol., 194, 3475, 10.4049/jimmunol.1402711 Ganesan, 2017, Tissue-resident memory features are linked to the magnitude of cytotoxic T cell responses in human lung cancer, Nat. Immunol., 18, 940, 10.1038/ni.3775 Nizard, 2017, Induction of resident memory T cells enhances the efficacy of cancer vaccine, Nat. Commun., 8, 15221, 10.1038/ncomms15221 Savas, 2018, Single-cell profiling of breast cancer T cells reveals a tissue-resident memory subset associated with improved prognosis, Nat. Med., 24, 986, 10.1038/s41591-018-0078-7 Clarke, 2019, Single-cell transcriptomic analysis of tissue-resident memory T cells in human lung cancer, J. Exp. Med., 216, 2128, 10.1084/jem.20190249 Mackay, 2012, Long-lived epithelial immunity by tissue-resident memory T (TRM) cells in the absence of persisting local antigen presentation, Proc. Natl. Acad. Sci. USA, 109, 7037, 10.1073/pnas.1202288109 Hofmann, 2011, E-cadherin promotes accumulation of a unique memory CD8 T-cell population in murine salivary glands, Proc. Natl. Acad. Sci. USA, 108, 16741, 10.1073/pnas.1107200108 Ray, 2004, The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection, Immunity, 20, 167, 10.1016/S1074-7613(04)00021-4 McNamara, 2017, Up-regulation of LFA-1 allows liver-resident memory T cells to patrol and remain in the hepatic sinusoids, Sci. Immunol., 2, eaaj1996, 10.1126/sciimmunol.aaj1996 Mackay, 2016, Hobit and Blimp1 instruct a universal transcriptional program of tissue residency in lymphocytes, Science, 352, 459, 10.1126/science.aad2035 Hombrink, 2016, Programs for the persistence, vigilance and control of human CD8+ lung-resident memory T cells, Nat. Immunol., 17, 1467, 10.1038/ni.3589 Milner, 2017, Runx3 programs CD8+ T cell residency in non-lymphoid tissues and tumours, Nature, 552, 253, 10.1038/nature24993 Le Floc’h, 2007, Alpha E beta 7 integrin interaction with E-cadherin promotes antitumor CTL activity by triggering lytic granule polarization and exocytosis, J. Exp. Med., 204, 559, 10.1084/jem.20061524 Anikeeva, 2005, Distinct role of lymphocyte function-associated antigen-1 in mediating effective cytolytic activity by cytotoxic T lymphocytes, Proc. Natl. Acad. Sci. USA, 102, 6437, 10.1073/pnas.0502467102 Johnston, 2014, The immunoreceptor TIGIT regulates antitumor and antiviral CD8(+) T cell effector function, Cancer Cell, 26, 923, 10.1016/j.ccell.2014.10.018 Guo, 2018, Global characterization of T cells in non-small-cell lung cancer by single-cell sequencing, Nat. Med., 24, 978, 10.1038/s41591-018-0045-3 Duhen, 2018, Co-expression of CD39 and CD103 identifies tumor-reactive CD8 T cells in human solid tumors, Nat. Commun., 9, 2724, 10.1038/s41467-018-05072-0 Parkhurst, 2017, Isolation of T-Cell Receptors Specifically Reactive with Mutated Tumor-Associated Antigens from Tumor-Infiltrating Lymphocytes Based on CD137 Expression, Clin. Cancer Res., 23, 2491, 10.1158/1078-0432.CCR-16-2680 Gros, 2014, PD-1 identifies the patient-specific CD8+ tumor-reactive repertoire infiltrating human tumors, J. Clin. Invest., 124, 2246, 10.1172/JCI73639 Takada, 2011, Kruppel-like factor 2 is required for trafficking but not quiescence in postactivated T cells, J. Immunol., 186, 775, 10.4049/jimmunol.1000094 Skon, 2013, Transcriptional downregulation of S1pr1 is required for the establishment of resident memory CD8+ T cells, Nat. Immunol., 14, 1285, 10.1038/ni.2745 Cepek, 1994, Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin, Nature, 372, 190, 10.1038/372190a0 Shiow, 2006, CD69 acts downstream of interferon-alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs, Nature, 440, 540, 10.1038/nature04606 Simoni, 2018, Bystander CD8+ T cells are abundant and phenotypically distinct in human tumour infiltrates, Nature, 557, 575, 10.1038/s41586-018-0130-2 Scott, 2019, TOX is a critical regulator of tumour-specific T cell differentiation, Nature, 571, 270, 10.1038/s41586-019-1324-y Mackay, 2015, Cutting edge: CD69 interference with sphingosine-1-phosphate receptor function regulates peripheral T cell retention, J. Immunol., 194, 2059, 10.4049/jimmunol.1402256 Guan, 2018, ZEB1, ZEB2, and the miR-200 family form a counterregulatory network to regulate CD8+ T cell fates, J. Exp. Med., 215, 1153, 10.1084/jem.20171352 Quintana, 2012, Aiolos promotes TH17 differentiation by directly silencing Il2 expression, Nat. Immunol., 13, 770, 10.1038/ni.2363 Li, 2019, Dysfunctional CD8 T Cells Form a Proliferative, Dynamically Regulated Compartment within Human Melanoma, Cell, 176, 775, 10.1016/j.cell.2018.11.043 Willinger, 2006, Human naive CD8 T cells down-regulate expression of the WNT pathway transcription factors lymphoid enhancer binding factor 1 and transcription factor 7 (T cell factor-1) following antigen encounter in vitro and in vivo, J. Immunol., 176, 1439, 10.4049/jimmunol.176.3.1439 Brummelman, 2018, High-dimensional single cell analysis identifies stem-like cytotoxic CD8+ T cells infiltrating human tumors, J. Exp. Med., 215, 2520, 10.1084/jem.20180684 Im, 2016, Defining CD8+ T cells that provide the proliferative burst after PD-1 therapy, Nature, 537, 417, 10.1038/nature19330 Sade-Feldman, 2018, Defining T Cell States Associated with Response to Checkpoint Immunotherapy in Melanoma, Cell, 175, 998, 10.1016/j.cell.2018.10.038 Kurtulus, 2019, Checkpoint Blockade Immunotherapy Induces Dynamic Changes in PD-1(-)CD8(+) Tumor-Infiltrating T Cells, Immunity, 50, 181, 10.1016/j.immuni.2018.11.014 Miller, 2019, Subsets of exhausted CD8+ T cells differentially mediate tumor control and respond to checkpoint blockade, Nat. Immunol., 20, 326, 10.1038/s41590-019-0312-6 Siddiqui, 2019, Intratumoral Tcf1(+)PD-1(+)CD8(+) T Cells with Stem-like Properties Promote Tumor Control in Response to Vaccination and Checkpoint Blockade Immunotherapy, Immunity, 50, 195, 10.1016/j.immuni.2018.12.021 Yost, 2019, Clonal replacement of tumor-specific T cells following PD-1 blockade, Nat. Med., 25, 1251, 10.1038/s41591-019-0522-3 Mielke, 2019, TCF-1 limits the formation of Tc17 cells via repression of the MAF-RORγt axis, J. Exp. Med., 216, 1682, 10.1084/jem.20181778 Cheuk, 2017, CD49a Expression Defines Tissue-Resident CD8+ T Cells Poised for Cytotoxic Function in Human Skin, Immunity, 46, 287, 10.1016/j.immuni.2017.01.009 Ichiyama, 2011, Transcription factor Smad-independent T helper 17 cell induction by transforming-growth factor-β is mediated by suppression of eomesodermin, Immunity, 34, 741, 10.1016/j.immuni.2011.02.021 Tajima, 2011, IL-17/IFN-γ double producing CD8+ T (Tc17/IFN-γ) cells: a novel cytotoxic T-cell subset converted from Tc17 cells by IL-12, Int. Immunol., 23, 751, 10.1093/intimm/dxr086 Piet, 2011, CD8+ T cells with an intraepithelial phenotype upregulate cytotoxic function upon influenza infection in human lung, J. Clin. Invest., 121, 2254, 10.1172/JCI44675 Woodberry, 2005, Alpha E beta 7 (CD103) expression identifies a highly active, tonsil-resident effector-memory CTL population, J. Immunol., 175, 4355, 10.4049/jimmunol.175.7.4355 Webb, 2010, Profound elevation of CD8+ T cells expressing the intraepithelial lymphocyte marker CD103 (alphaE/beta7 Integrin) in high-grade serous ovarian cancer, Gynecol. Oncol., 118, 228, 10.1016/j.ygyno.2010.05.016 Franciszkiewicz, 2009, Intratumoral induction of CD103 triggers tumor-specific CTL function and CCR5-dependent T-cell retention, Cancer Res., 69, 6249, 10.1158/0008-5472.CAN-08-3571 Edwards, 2018, CD103+ Tumor-Resident CD8+ T Cells Are Associated with Improved Survival in Immunotherapy-Naïve Melanoma Patients and Expand Significantly During Anti-PD-1 Treatment, Clin. Cancer Res., 24, 3036, 10.1158/1078-0432.CCR-17-2257 El-Asady, 2005, TGF-beta-dependent CD103 expression by CD8(+) T cells promotes selective destruction of the host intestinal epithelium during graft-versus-host disease, J. Exp. Med., 201, 1647, 10.1084/jem.20041044 Wang, 2015, CD103+ Tumor Infiltrating Lymphocytes Predict a Favorable Prognosis in Urothelial Cell Carcinoma of the Bladder, J. Urol., 194, 556 Franciszkiewicz, 2013, CD103 or LFA-1 engagement at the immune synapse between cytotoxic T cells and tumor cells promotes maturation and regulates T-cell effector functions, Cancer Res., 73, 617, 10.1158/0008-5472.CAN-12-2569 Boutet, 2016, TGFβ Signaling Intersects with CD103 Integrin Signaling to Promote T-Lymphocyte Accumulation and Antitumor Activity in the Lung Tumor Microenvironment, Cancer Res., 76, 1757, 10.1158/0008-5472.CAN-15-1545 Pascutti, 2019, Peripheral and systemic antigens elicit an expandable pool of resident memory CD8(+) T cells in the bone marrow, Eur. J. Immunol., 49, 853, 10.1002/eji.201848003 Patro, 2017, Salmon provides fast and bias-aware quantification of transcript expression, Nat. Methods, 14, 417, 10.1038/nmeth.4197 Pimentel, 2017, Differential analysis of RNA-seq incorporating quantification uncertainty, Nat. Methods, 14, 687, 10.1038/nmeth.4324 Yu, 2012, clusterProfiler: an R package for comparing biological themes among gene clusters, OMICS, 16, 284, 10.1089/omi.2011.0118 Bolotin, 2015, MiXCR: software for comprehensive adaptive immunity profiling, Nat. Methods, 12, 380, 10.1038/nmeth.3364 Hothorn, 2003, On the Exact Distribution of Maximally Selected Rank Statistics, Comput. Stat. Data Anal., 43, 121, 10.1016/S0167-9473(02)00225-6